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Beer G. Vertebrate Zoology. (1922)

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XIV The development of Lepus (the Rabbit)

Fertilisation

The egg is very small, and contains very little yolk. It is surrounded by a vitelline membrane secreted by itself, and by a secondary membrane formed from the follicle-cells, the zona pellucida. The follicle-cells are several layers thick surrounding each egg-cell, which however they do not ﬁt closely. There is a large space inside the follicle ﬁlled with ﬁuid and bathing the egg, which gives the characteristic appearance of the Graaﬁan follicle, typical of mammals. One polar body is extruded in the ovary, the second is extruded after fertilisation. _

Ovulation is the process of release of the egg from the ovary, and is usually brought about during a period of “heat” or oestrus as a result of the action of the follicle-stimulating hormone of the pituitary. Other mammals, including the rabbit, only ovulate after the stimulus of copulation. The follicle vacated by the egg becomes ﬁlled by the great increase in size of the follicular cells and by the ingrowth of connective tissue and blood-vessels, and becomes a corpus lutcum under the influence of the luteinising hormone of the pituitary. Should the egg just ovulated be fertilised, the corpus luteum becomes an important structure, functioning as a gland of internal secretion producing the hormone progesterone, and among its functions are the following: it stimulates the uterus to hypertrophy and undergo “progestational proliferation" as a result of which the uterine glands secrete nutritive material for the embryo before it becomes ﬁxed to the wall of the uterus; it prepares for the reception and ﬁxation of the embryo; and it renders the muscles of the uterus insensitive to the osytocic hormone of the pituitary and other stimuli which would cause them to contract prematurely and produce abortion. The corpus luteum disappears at the end of the period of gestation, but if no pregnancy has ensued it disappears soon after ovulation.

During copulation sperms are introduced into the vagina, and they make their way up through the uteri to the oviducts, near the top of which they meet and fertilisc the egg. Fertilisation is therefore internal, as in the chick.

CLEAVAGE. Cleavage is total and gives rise to a ball of cells, or "

morula. A cavity appears within it, and it soon becomes differentiated 194 ' DEVELOPMENI or LBPUS 195

into an outer layer and an inner mass of cells." The former is . the trophoblast, and the whole structure is known as a blastocyst. . IMPLANTATION. The blastocyst travels down the oviduct and eventually ﬁnds itself in the cavity of the uterus where it ingests through its trophoblast the nutritive substances secreted by the uterine glands. The lining of the uterus has on its mesometrial side (see p. 238) a pair of prominent folds, which project into the cavity

Figure 108. Lepus: early stages in the development of the rabbit. (After Assheton.)

A, two-cell stage, enclosed by the zona pellucida (zr); B, morula (m) stage; C, blastocyst showing the dllferentiation into the trophoblast (t) and the inner mass (im); D, the inner mass has become the embryonic plate and IS dilferentiated into eetodemt (er) and endodcrm (en); E, the trophoblast overlying the embryonic plate—the cells of Rauber (cR)-—disappear; F, after the disappearance of the trophoblast over the embryonic plate; G, transverse section through the primitive streak (pr). c, ccelom; me, mesoderm.

or lumen of the uterus. To these, the blastocyst becomes attached by

_ means of its trophoblast. This process is called implantation. In the

rabbit where the blastocyst remains in the cavity of the uterus, the type of implantation is termed central. In other mammals including man, the blastocyst bores its way into the uterine wall, a’ type of implantation termed interstitial.

FORMATION or THE EMBRYO. The blastocyst enlarges and expands in the cavity of the uterus. The cells of the inner mass 196 TBMBRYOLOGICAL rvrns

become arranged in the form of a ﬂattened disc, immediately beneath the trophoblast. This disc is known as the embryonic plate.

At the same time, the inner mass gives rise to a layer of cells which grow as an epithelium lining the inner surface of the trophoblast. This layer is endoderm (also called the “lower layer”), and the cavity which it encloses represents the yolk-sac of the chick. Here, however, there is no yolk, and the yolk-sac is consequently empty.

The cells of the trophoblast immediately overlying the embryonic plate (the cells of Rauber) disappear, and the embryonic plate thus

M

grams shon ing the formation of the amnion in the rabbit. (From Jenkinson, after van Beneden.)

The C11l'llL‘l' stage is on the left: the later stage on the right. Since the cells of Rauher have disappeared, the embryo 18 at the surface of the blastocyst until the amnion has formed. all, allantols; arr, region of the trophoblast where the allantoie placenta will he formed; c, extra-etnbryontc euclom; e, embryo; ham, head amniotic fold; arr, region of the trophoblast where the omphaloidean placenta is formett: st, sinus terminalis (blood-vessel) of the area vasculosa; mm, tall tunmottc fold. _t-s, yoll-t-sate.

Figure 109. Din

‘J comes to the surface of the trophoblast. A primitive streak is formed in the centre of the embryonic plate, and, as in the chick, it proliferates mesodermal cells to each side, and forms the notochord in the middle line as it retreats towards the hind end of the embryo. Neural folds rise up and enclose the neural tube, and the embryo becomes folded up from the surrounding tissue by the head-fold and tail-fold. In this way, the gut begins to be formed, and, as in the chick, anterior and posterior intestinal portals arise (see p. 181).

The amnion arises by the upgrowth of folds at the edge of the embryonic plate. The hinder amniotic fold develops faster than that DEVELOPMENT or LBPU8 "197

in front, and when these folds meet, the embryo is no longer at the

surface of the trophoblast, but folded away within it. The embryo is then enclosed in the amniotic cavity, just as in the chick, and the trophoblast of the rabbit corresponds to the chorion of the chick,

Figure 110. Diagram showing the relations of the embryonic membranes and placenta of the rabbit, as seen in an idealised transverse section of the uterus. (From Jenlunson, after Duval and van Beneden.)

all, allantois; c, extra-embryonic _ca:lom; ep, epithelium of the uterus; Iu, cavity of the uterus; m. mcsometrium; arr, omphaloidean trophoblast; pl, placenta (allantoic); pr am, proammon; ys, yolk-sac. the relations of which are identical (see p. 178). It may be mentioned that in some other mammals such as the mouse the amnion is not formed quite in this way, but arises precociously, even before the

embryo (see p. 219). The rabbit has been chosen for description here 198 * I aunnvonootcu. ‘nu-as

because its development is so easily comparable with that of the

\ _\ ll

71 " €chick. The mesoderm splits into somatic and splanchnic layers with the

ccelomic cavity between them. The splanchnic layer overlies the

yolk-sac. The somatic layer grows up round the amnion and separates the latter from the trophoblast.

An area vasculosa develops in the wall of the yolk-sac, and the blood-vessels so formed extend as far as the sinus terminalis. The lower wall of the yolk-sac is not vascularised. In some mammals this lower wall of the yolk-sac with its overlying trophoblast persists for some time, and absorbs nourishment from the walls of the uterus. In the rabbit, however, this “omphaloidean” region of the trophoblast together with the lower wall of the yolk-sac disappears, and the cavity of the yolk-sac is then openly continuous with that of the lumen of the uterus. This disappearing part of the blastocyst contained neither blood-vessels nor mesoderm.

PLACENTA. Meanwhile, the upper part of the trophoblast which is in contact with the wall of the uterus on the mesometric side becomes much thicker and hollowed out by the formation of a number of lacuna: into which the trophoblast projects countless ﬁnger-like processes called pseudo-villi. The outer surface of the pseudo-villi loses its cell-boundaries forming a syncytium (or plasmodi-trophoblast). The more basal part of the trophoblast, between the syncytium and the mesoderm, retains its cell-boundaries (and is called the cyto-trophoblast). The allantois grows out from the region of the hind-gut and brings with it a covering layer of mesoderm and blood-vessels. The mesoderm covering the allantois fuses with the mesoderm underlying the cyto-trophoblast, and the allantoic bloodvessels make their way into the pseudo-villi. In this way the placenta is formed, and since it is related to the allantois, it is called an “allantoic placenta". The placenta is an organ which places the mother and embryo in physiological communication, for the interchange of substances. The epithelium of the wall of the uterus disappears where the trophoblast touches it, with the result that the trophoblast is in contact with the subepithelial tissues and bloodvessels of the uterine wall. The blood from these maternal vessels bathes the surface of the trophoblast and fills the lacuna: so that the pseudo-villi are immersed in maternal blood. This type of placenta is called hatmo-chorial. The blood of mother and embryo are never in direct communication.

The capillaries of the allantois branch in the substance of the pseudo-villi, and the blood which they contain is separated from the maternal blood only by the lining of the capillaries and the surface of the trophoblast. Across these membranes which constitute the _DEVELO_l_’MBN'l‘ “or LEPU§.- 199

placental barrier, substances are passed by diﬁusion. The maternal blood supplies not only oxygen but food—substances which may require to be digested by enzymes and broken down into simpler compounds, for the placental barrier is impassable to substances of high molecular weight. In the contrary direction the embryonic blood brings carbon dioxide and excretory products which are passed on into the maternal circulation. The placenta therefore functions as a respiratory, nutritive, and excretory organ. At the same time, a certain amount of nutriment is obtained from the glands of the uterus, and is either ingested phagocytically by the trophoblast or absorbed into the blood-vessels of the yolk-sac (the cavity of which

Figure 111. Section through a part of the haemo-chorial allantoic placenta of the rabbit.

The maternal tissue is on the right, the embryonic tissue on the left. They can often be distinguished by the fact that the red blood-corpuscles of the embryonic blood have not yet lost their nucleus. a, allantois; ct, cyto-trophoblast; eb, embryonic blood-vessels; cg, embryonic glycogen layer; I, lacuna: in the trophoblast and ﬁlled with maternal blood; mb. maternal blood-vessels; mg, maternal glycogen layer; st, syncytium or plasmodi-trophoblast; uv, umbilical vein. opens freely into that of the uterus). But the functions of the placenta do not end there, for it also serves as a store of food material for the developing embryo. In particular, glycogen is accumulated in the placenta at early stages before the embryo has a liver of its own; when the latter develops, the gycogen content of the placenta decreases. The placenta also secretes a hormone which controls and preserves the continuance of the pregnancy.

The vascular system of the embryo rabbit resembles that of the chick, but the posterior cardinals persist as the azygos and hemiazygos veins. The blood from the placenta arrives in the umbilical veins, of which the right disappears and the left runs into the ductus

venosus and so to the right auricle. As in the chick, the septum 200 H i éyaunnvorocrcxs types, between the auricles in the heart is perforated, and the oxygenated

. blood from the placenta can get through to the left auricle, left ventricle, and so to the carotids and brain, which requires the

purest blood in the body. The pulmonary artery connects with the aorta on the left side by the ductus arteriosus, so that the remainder of the venous blood in the right auricle passes through the right ventricle, pulmonary artery, and ductus arteriosus to the aorta below the place where the carotids come oil", and does not have to go through the lungs. The ductus arteriosus degenerates and the perforation of the interauricular septum is closed at birth when the lungs begin to function. The right systemic arch disappears.

A feature of great interest for the respiration of the intra-uterine embryo is the fact that the haemoglobin of the embryonic red blood corpuscles is different from that of the adult in having a greater affinity for oxygen. Indeed, it is obvious that the embryonic blood in the placenta must be able to take up oxygen at an oxygen-tension at which the maternal blood parts with it.

As in lower forms, the fore-gut and the hind-gut remain blind for a long time. In these regions the endoderm becomes apposed to the overlying ectoderm forming the oral plate and cloacal plate respectively. Perforation of these gives rise to the mouth and cloaca, which latter is divided into anus and urino-genital aperture. The bladder forms from the base of the allantois.

The urino-genital ducts develop much as in the chick, except that the right oviduct persists, and the testis descends into the scrotum.

From the fact that the perforation of the mouth does not occur at the extreme front end, but in the centre of the oral membrane, a small pocket is formed morphologically in front of the mouth. This is the so-called preoral gut. In a similar way, a post-anal gut is left after perforation of the anus.

In the region of the pharynx, the gill-pouches arise as outpushings from the gut to the ectoderm. They do not, however, become perforated.

Several structures enter into the formation of the diaphragm. The transverse septum moxcs backwards a considerable distance during development, and it is followed in its course by the phrenic nerve. The transverse septum forms the ventral portion of the diaphragm, and the wall which separates the pericardium from that part of the perivisceral cavity into which the lungs extend. The dorsal portion of the diaphragm separates this pleural corlom from the abdominal cavity behind, and it is formed by the growth of the mesenteries associated with the liver (which enlarges), kidneys, lungs, and gut.

As the placenta and the embryo increase in size, the uterus becomes enlarged to accommodate them. This is effected by a great , nnvanormanr or Laws . 201

increase in the‘ size’ of the smooth miiscle-cellsiiof which the wall of the uterus is composed, without any increase in their number.

When the period of gestation is accomplished, the amnion breaks and the embryo is expelled by the contractions of the muscular walls of the uterus. The umbilical cord is torn. The placenta also becomes detached from the wall of the uterus, and, together with clots of blood and debris, is expelled as the after-birth. 4."

HAIR. The development of hair starts by a thickening of the deeper layer of the epidermis, and its downgrowth into the dermis

Figure 112. Sections through the skin of mammalian embryos showing stages in the development of the hairs.

A, early stage showing the ectodennal inpushing (er) and the concentration of

the mesoderm to form a papilla (mp?; B, the ectoderm forms a follicle (f) inside

which the hair (/2) is developing; C, ate stage after the hair has erupted from the surface. apm, arrector plli muscle; sg, sebaceous gland.

forming a little cylinder. At its base a papilla is formed, and just above this, the epidermal cells proliferate and give rise to the shaft of the hair. This elongates as more material is added to it from beneath, and it ﬁnally emerges from the follicle and grows freely out. The centre of the hairshaft is composed of the medulla; surrounding thistis the cortex, and round this again is the cuticle. The outer wall of the follicle forms a sheath round the base of the hair, and the following layers can be made out in it. In contact with the cuticle of the hair is the cuticle of the sheath, and next outside that are Huxley’: 202 WEMBRYOLOGICAL nrras

layer. Healers myegﬁrmd the ‘inain epidermal layer of the sheath. ,,S1g»rt'ounding this again is the dermal sheath of the follicle. The epidermis of the wall of the follicle gives rise to little pouches which become the sebaceous glands. Some mesenchyme cells outside the ‘follicle become differentiated into smooth muscle-ﬁbres; they gain

, attachment to the wall of the follicle and become the arrector ﬁniuscles of the hair.

LITERATURE

BONNET, R. Lehrbuch der Entwicklungsgeschichte. Parey, Berlin, 1920.

CORNER, G. W. Hormones in Human Reproduction. Princeton University Press, 1946.

HAMMOND, J., and MARSHALL, F. H. A. Reproduction in the Rabbit. Oliver and Boyd, Edinburgh, 1925.

Ji!NK1l;§t;N, J. W. Vertebrate Embryology. Oxford, at the Clarendon Press, I .

KELUCOIT, W. E. Chordate Development. Henry Holt, New York, 1913.

PRENTISS, C. W., and AREY, L. B. A Laboratory Manual and T ext-book of Embryology. Saunders Co., Philadelphia and London, 1922.

PART III

COMPARATIVE ZOOLOGY OF CHORDATES

OUTLINE CLASSIFICATION or THE MAIN (moves or cnonmrn ANIMALS, SHOWING rue MEANING AND VALUE or me COMPREHENSIVE reams EMPLOYED. FOR comnere CLASSIFICATION, see p. 418.

-9‘

(Most of the extinct groups have been omitted.)

Phylum. CHORDATA. Animals with gill-slits, notochord, dorsal tubular nerve-cord, and post-anal tail.

Subphylum. HEMICHORDATA. Very lowly forms with

gill-slits and tubular nerve cord but no proper notochord, e.g.

Balanoglossus.

Subphylum. PROTOCHORDATA. Without a specialised head or skull.

Class. unocuononu. Degenerate forms with

a notochord only in the tail of the larva, e.g. Ascidia.

Class. CEPHALOCHORDATA. Primitive forms with the notochord extending the whole length of the body, e.g. Amphioxus.

Subphylum. CRANIATA. With a specialised head and skull, paired eyes, ears and noses, heart and ccelomostomic kidneys.

Division. ANAMNIA. Without an amnion. Breathing by gills at some stage of life if not altogether.

Branch and Class. CYCLOSTOMATA. With a round sucking

mouth, no Jaws or paired ﬁns, e.g. Petromyzon (lamprey), Myxine

(hag).

Branch. GNATHOSTOMATA. With biting jaws, stomach, paired ﬁns or limbs Wolfﬁan and Mttllerian ducts.

Grade. PISCES (nsu). With paired ﬁns. 203 204 ‘ com-Attanva zoonoav or cnonnnss

Class. 2* ’ Order.

‘ Order.

Class.

Subclass. Subclass.

Class.

Order.

Order. Order. Order. Division.

Class.

Subdivision.

Order.

CHONDRICHTHYES. With cartilaginous skeleton only.

SELACHH. Gills uncovered, hyastylic or amphistylic, e.g. Scyllium, sharks and rays.

HOLOCEPHALI. Pscud-autostylic, e.g. Chimera.

osrarcurmnas. With bony skeleton, lung or air-bladder.

TELEOSTOMI. With air-bladder. hyostylic, e.g. Gadus (cod).

DIPNOI. Lung used for breathing, e.g. Ceratodus.

A M P HI am . With an aquatic gill-breathing larval stage followed by a terrestrial air-breathing adult.

LABYRINTHODONTIA (or STEGOCEPHALIA). Primitive extinct forms with a complete rooﬁng to the skull, e.g. Eogyrinus.

URODELA. With a tail in the adult, e.g. Triturus (newt).

ANURA. Without a tail in the adult, c.g. Rana (frog).

(3 YM N or H IONA . Limblcss, e.g. Icl1rlz_roplu's.

AMMOTA. Embryo develops on land inside an amnion.

RFPFILIA. Body covered with horny scales, cold-blooded.

SAUROPSIDA. Reptiles related to the birds.

(IHELONIA. Body enclosed in a

carapace, e.g. T estudo (tortoises and turtles).

RHYNCHOCEPHALIA. Primitive forms, e.g. Sphenodon.

LACERTILIA. Quadrate loose, e.g. .’.ac¢'rra (lizard).

ormom. Both halves of lower jaw loose, e.g. Vipera (snakes).

CROCODILIA. Heart 4-chambered. e.g. C racodilus. OUTLINE .cLAssrrrcA'rroN 205

Subdivision. ~ _ msnorsrna. Reptiles related to the‘ mammals. “

Class. M/ES (sums). With feathers, warmblooded.

Subclass. PALEOGNATHIB. With a large prevomer, e.g. Struthio (ostrich).

Subclass. NEOGNATHIE. With a small prevomer, e.g. Calumba (pigeon), Gallus (fowl).

Class. MAMMALIA. Mammary glands, hair, diaphragm, warm-blooded.

Grade and Subclass. MONOTREMATA. With a cloaca, e.g. Ornirlzorhynchus (duck-billedplatypus). .

Grade. DITREMATA. Anus and urinogenital apertures separate.

Subclass. MARSUPIALIA. With marsupial pouch, e.g. Peramcles.

Subclass. PLACENTALIA. Well-formed allantoic placenta, e.g. Lepus (rabbit).

Note. VERTEBRATA may be used as roughly synonymous with CRANIATA. TETRAPODA includes AMPHIBIA and AMNIOTA. CHAPTER XV

THE BLASTOPORE

. THE blastopore is one of the most important structures in development, for as a result of the processes which are entailed in its formation the fundamental architecture of the future embryo is laid down. Further, experimental investigations have shown that the region of the dorsal lip of the blastopore (which is the ﬁrst part of

_the blastopore to develop) is responsible for inducing the formation

of the neural tube out of the overlying ectoderm, and determining the place of formation of various organs. The blastopore itself introduces the ﬁrst differentiation (after the establishment of the axis of the egg in the ovary, and of the plane of bilateral symmetry by the point of entrance of the sperm) in that it converts the singlelayered hollow ball (blastula) into the double-layered bowl (gastrula). In those animals where the relation of the sperm’s entrance point to the blastopore is known (amphibia). it is found that the dorsal lip of the blastopore arises opposite the sperm-entrance point, and marks the dorsal side of the future embryo.

I n Amp/u'o.x'us where there is little yolk, the rim of the blastopore is formed as the result of simple invagination of the vegetative hemisphere into the animal hemisphere. Thereafter the rim of the blastopore stretches backwards and the embryo increases in length. In Craniates. the quantity of yolk present prevents simple invagination, and the rim of the blastopore arises either as the result of overgrowth (epiboly) accompanied by invagination or some form of ingrowth, or by means of the formation of a primitive streak which bears no relation to the enclosure of the yolk. There is an increasing tendency for the imagination to become reduced as the quantity of yolk increases, and the yolk ceases to become encircled in the process of closure of the blastopore. At the same time. the endoderm appears early (one might say out of its turn), and the aperture of the blastopore becomes virtual.

In the development of the dogftsh, the egg contains so much yolk that cleavage is incomplete or meroblastic, and a disc of cells or blastoderm is formed lying on the top of the yolk. Now the important point to notice is that all round the edge of this blastoderm, cells are growing over the yolk and tucking-in underneath the upper layer

of the blastoderm to form endoderm. In fact, the edge of the blasto206 rrus BLASTOPORB .297

derrn is the “bf the blastopore, and mesederm-"cells are ail-;o1.* proliferated from it. The embryo forms in front of the posterior”

edge of the blastoderm, which is the dorsal lip of the blastopore, and does not wait for the blastopore to close. Indeed, this takes a long time, for the anterior edge of the blastoderm has to grow a long way down and back under the yolk before it comes up underneath and opposite the dorsal lip to form the ventral lip of the blastopore.

a£:=vl

Figure ll3..Views of a developing embryo of a dogﬁsh. (After Jenkinson.)

A from above; B, C, and D from the left side. The lips of the blastopore are formed from the edge of the blastoderm. ae, anterior edge of the blastoderm; dl,"c‘lorsa| lip of the blastopore; e, embryo; vl, ventral lip of the blastopore; y, yo .

The edge of the blastoderm in the dogﬁsh corresponds to the edge of the pigmented cells of the animal hemisphere in the frog, and this is the place where the overgrowing lip which is the rim of the blastopore arises in the frog also. All round the rim of the blastopore, the ectoderm, mesoderm, and endoderm are in contact. In the case of the frog, the blastopore starts a little below the equator of the spherical embryo, and as it grows down to latitudes nearer the 208 .coMrAt1uvr1ve zoonoev or CHORDATBS

- vegetative pole, the diameter of the blastopore naturally decreases.

Any given point on the rim of the blastopore grows straight down along a meridional line towards the vegetative pole; but as the diameter of the blastopore decreases, any two given points on the rim at the start will ﬁnd themselves closer together at the ﬁnish of gastrulation. This process is called conﬂuence. In the case of the dogﬁsh, the diameter of the blastopore (edge of the blastoderm) has to increase considerably until it has grown down and passed the equator of the yolk, whereupon it decreases again.

It is characteristic of these lower vertebrates (ﬁsh, frog, and newts) that the rim of the blastopore arises along the margin separating the protoplasmically-rich cells of the animal hemisphere from the cells rich in yolk (or the undivided yolk) of the vegetative

Figure 114. Viewsot‘ the blastoderm of Hypogeop/u's, one of the Gymnaphiona showing the origin and closure of the blastopore. (From Jenkinson, after the brothers Sarasin.)

The anterior edge of the blastoclerni here does not become the ventral lip of the blastopore. vp, yolk-cells seen through the blastopore.

hemisphere: i.c., the edge of the blastoderm is the rim of the blastopore. Also, in the closure of the blastopore, the yolk becomes enclosed by the growth of the anterior part of this margin which becomes the ventral lip of the blastopore.

This is, however, not the case in the higher forms (reptiles, birds, and mammals), in which there is a primitive streak. In order to understand the evolution of the primitive streak from the simple blastopore of the lower vertebrates, it is necessary to consider the condition in the Cymnophiona. which is more or less intermediate. The quantity of yolk in the Gymnophionean egg brings about the formation of a blastoderm. The posterior edge of this blastoderm grows back over the yolk and tucks cells in beneath itself‘, like the dorsal lip of the blastopore which it is. Overgrowth also takes place at each side of the dorsal lip, and the blastopore becomes crescentie. Eventually the two horns of the crescent meet and the blastopore is then a closed circle. But the anterior edge of the blastoderm has not THE BLASTOPORB v 209

moved, it has not grown round underneath the yolk, and it takes no‘ share whatever in the formation of the blastopore. At the same time it is to be noticed that the blastopore is a real aperture, through which the yolk can be seen from the outside. The cavity which communicates with the exterior through the blastopore is, of course, the archenteron, and the lining of this cavity is the endoderm, formed by the activity of the edge of the blastopore.

In the reptiles, yolk is abundant, and cleavage leads to the formation of a blastoderm. At a place which marks the posterior end of the future embryo, cells are proliferated under the blastoderm, forming a lower layer between the blastoderm and the yolk. This lower layer is really the endoderm, which has been formed precociously, probably serving the function of digesting the large quantity of yolk. A dorsal lip of a blastopore arises (not at the extreme hind edge of the blastoderm, but well within its margin) as a rim beneath which cells become tucked in and passed forwards beneath the blastoderm and above the lower layer. The rim of the blastopore extends to the sides, and so the lateral lips come into being. Eventually the lateral lips extend backwards, and lie parallel to one another. The blastopore is now slit-like, and resembles a primitive streak. The lateral lips of the blastopore join postcriorly, and the blastopore is then closed. The cells which get tucked in by the lips of the blastopore line a cavity which is the archenteron, so that here as in ﬁsh, frogs, newts, and Gymnophiona, the blastopore is a real aperture. The archenteron extends far forwards as the result of invagination, and its roof in the middle line becomes the notochord; on each side the roof becomes mesoderm. The ﬂoor of the archenteron fuses with the underlying lower layer and then disappears, so that the blastopore leads right down through the archenteron to the surface of the yolk. The walls of the deﬁnitive alimentary canal are formed from the lower layer, which is endoderm formed really before the blastopore proper can be said to exist.

The conditions in the reptile lead on easily to those which obtain in birds. Here, again, the endoderm is formed precociously as a lower layer split oil" from the underside of the superﬁcial layer of the blastoderm. The blastopore, however, never is a real aperture, because its lateral lips are fused together all along their length forming the primitive streak which arises in the middle of the blastoderm, not at its edge. The dorsal lip is the primitive knot beneath which a solid strand of cells is tucked in to form the notochord. As the primitive streak moves backwards over the blastoderm, ‘it pays in a stream of cells into the hinder end of the notochord and gives oﬁ‘ mesoderm to each side. In the bird, therefore, the blastopore is closed from the start, and its aperture is represented only by the

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4'?

depression of the primitive pit just behind the primitive knot, and .4,‘ by the primitive groove which runs along the centre of the primitive . streak. The bird '5 blastoporc begins where that of the frog leaves

210 ghCOM1’A_!lAT!VE ZQOLOGY or cnonmrns

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Figure ll5. L0ngltUt.iill£l.i sections through the blastoderm of a reptile, showing the origin of the blustopore. (From Jenkinson, after Will.)

A-E. sttccessiu: stages. A. precocious origin of the endoderm or lower layer (pd). which is in eoiit.iet with the upper latyer of the blastoderrn at pp; B, origin of the lilztstopore. dl. dorsal lip of the bhtstopore (cf. Fig. 89); C, invagination at the hlatstopoie to form the iii'<.lienteroii; the lower layer forms a continuous mcnihrtine sepiiiuted from the yolk by the suhgerminnl cavity (sgc); mesv, mesoderin formed from the lip of the bltistopore; D, the arehenteron (arch) extends it long w.i_\ fomuitls beneittlt the upper ltiyer of the blastoderm; yp. yolk-plug (cf. Hg. 75); [5, fusion of the Hour of the ztrehenteron with the underlying region of the lower i£i)t‘f, and their subsequent dlS£lppCt1l'i1I1Ct3, so that the nrchentcron eoiiiiuunieutcs with the subgermimtl cavity.

off, for in the hitter it vi ill be remembered that the blastopore which was spherical becomes oval, and its lateral lips become apposed to one another, forming what is in fact at short primitive streak. In the bird, there is invagiiiation in spite of the blastopore being closed. THE nusroroas 211

but there is no archenteron, and the viiaﬂs of‘ the aliiiientary canal A

are derived (as in reptiles) from the lower layer.

In mammals, the embryo develops from a primitive streak which develops in the middle of the embryonic shield. In some cases the blastopore is a real aperture, or in other words, the primitive pit sinks down and opens into an archenteron beneath the superﬁcial layer of the ﬂoor of the amniotic cavity (corresponding to the blastoderm). In others, the blastopore is reduced. The primitive streak and archenteron give rise to the notochord and mesoderm, and the endoderm is formed from the lower layer.

In reptiles, birds, and mammals, therefore, the blastopore either closes or arises already closed without the yolk becoming enclosed; for the anterior edges of the blastoderm do not grow down round the yolk to form any part of the rim of the blastopore.

Arnphioxus. Frog. Reptile. l Bird. Placental Mammal. ....__...._—_......... c... .- r f ......i ._- -- _- ..-. - _.. ...._.._. .. .. ' _._........_.......... Yolk Very little. Little. Much. Very much. None. Condition of Yolk at start Enclosed. Enclosed. Not enclosed. Notenclosed. . Blastopore Open. Open. Open. Closed from Sometime: start. open. Gastrulation Invagination. Overgrowth Primitive Primitive Primitive and invagi- streak and streak and streak and nation. invagination. invagination. invngination. Gut formed from Wall of Wall of Lower layer. Lower layer. Lower layer. archenteron. . archenteron. Q I I

It remains to say a few words about the germ-layers which are brought into position as a result of the formation of the blastopore and primitive streak. The apparent regularity with which corresponding structures appeared to arise from the same germ-layer in different animals led to the formulation of the germ-layer theory which sought to make this correspondence absolute and inevitable. It is now realised, however, that the segregation of the germ-layers does not involve the determination of the fate of the various layers, and many cases are known where organs are formed from the “wrong” germ-layers. The signiﬁcance of the germ-layers is that they represent an essential embryonic manceuvre in marshalling the material out of which the embryo will be built. They need not and sometimes do not correspond in different animals.

Nevertheless, the correspondence of the germ-layers is suﬂicient to impart to them some value in the systematisation of the description of development in different forms.

ECTODERM gives rise to:

Epidermis, with horny scales, horny “teeth”, caruncles, feathers, hair, horns, hooves, nails, sweat-glands, nasal epithelium, 212' ' ‘COMPAQRATIVE zoowov or euonmrrns

lateral-line organs, bar vesicles, lens, placodes, enamel, stomodaeum and proctodmum;

Neural tube, with eye-cups, ventral nerve-roots, sympathetic ganglia, adrenal medulla, pituitary body;

Neural crest which gives rise to: dorsal-root ganglia, pigment cells, ectomesenchyme, cartilages of visceral arches, dermal bones of jaws, odontoblasts, teeth, (7) denticles;

Nephridia;

Amnion and chorion (trophoblast).

MESODIERM gives rise to:

Myotomes and segmental muscles, lateral plate and visceral muscles;

Coelomic epithelium, somatopleur and splanchnopleur, extraembryonic cualom;

Gonads and genital ducts, Wolliian and Miillerian, uterus, kidney tubules, ureter;

Sclcrotomes, mcsenchyme and connective tissue, cartilages (other than visceral arch), bones ('3 other than dermal bones of jaws), bony scales and [in rays;

Blood and blood—vcssels. heart, veins, arteries, lymph glands, lymphatics;

Adrenal cortex.

r2NnoDr.a M gives rise to:

Gut with salivary glands, visceral pouches, thymus, thyroid, pharynx, larynx, lungs, stomach, pancreas, liver, gallbladder and bile-duct, intestine, urinary bladder;

Yolk-sac and allantois.

NOTOC‘.HORD is a structure on its own.

LITERATURE

ma Bush, 0. R. The diﬂ‘ercntiation of neural crest cells into visceral cartilages and odontoblasts in Amblystoma and a re-examination of the germ-layer theory. Pr0('e£'tl'l'ngs of the Royal Society, B. Vol. 134, 1947.

JENKINSON, J. W. Vertebrate Embr_voIog_r. Oxford, at the Clarendon Press, 1913. CHAPTER XVI THE EMBRYONIC MEMBRANES

THE YOLK-SAC. In those forms in which the quantity of yolk contained in the egg is large, the embryo is formed from a blastoderm on the surface of the yolk and does not wait for the latter to be enclosed. So it comes about that the yolk is not situated within the embryo, as, for example, it is in the frog; indeed, in the chick it would be manifestly impossible. In the heavily-yolked forms, then, the yolk is outside the embryo, and it becomes surrounded by a layer of cells which are endodermal and continuous with those of the gut-wall inside the embryo. The yolk then ﬁnds itself inside a “yolksac”, which may be regarded as temporarily extra-embryonic gut. This sac carries a layer of mesoderm outside its (endodermal) wall, and blood-vessels passing between the mesoderm and cndoderm absorb the yolk (which has been digested) and convey it into the embryo. Chief among these vessels are the vitelline arteries and veins. Indeed, in most groups of vertebrates the wall of the yolk-sac is the site of origin of the blood in the form of blood-islands.

In the ﬁsh, the function of the yolk-sac circulation is not only to convey digested yolk, but also to oxygenate the blood in its many capillaries, at the early stages of development before the gills have become functional.

The yolk-sac reaches the height of its development in reptiles and birds; and in the Monotremcs where, although mammals are oviparous, yolk is present and the yolk-sac is large. What yolk there is in the egg of the Marsupials is extruded, and the egg of the Placental mammals contains no yolk. Nevertheless, in both the last-mentioned groups a yolk-sac is present although it contains no yolk.

In several groups of vertebrates, the yolk-sac may come to bear interesting relations to the wall of the oviduct, with which it is in contact if the egg is not laid but undergoes development within the body of the mother. The blood-vessels of the yolk-sac are in these cases able to absorb substances from the circulation of the mother (by diffusion), and such an organ of physiological communication between mother and embryo is a placenta. It is necessary to'specify the organ which forms the placenta, and a placenta derived from the yolk-sac is called an omphaloidean placenta, as in the Selachian

Mustelus. 213 214 . ». comntttartve ZOOLOGY or cnonpares 1

As development‘ proceeds, and the quantity of yolk is reduced,

! the size of the yolk-sac decreases and ﬁnally it is withdrawn into the body through the umbilical stalk.

THE CHORION. In ﬁshes and Amphibia the whole of the egg

pbecomes converted into the embryo. In reptiles, birds and mammals, j on the other hand, only a portion of the living matter formed out W of the egg gives rise to the embryo; the remainder goes into the

production of the embryonic membranes. The outermost of these is the chorion. In reptiles and birds the chorion is formed as a result

' of the upgrowth and fusion of the amniotic folds (see below), and

represents the whole of the upper layer of the blastoderm other than that which goes to form the embryo and the amnion. It is to the inner surface of the chorion that the yolk-sac and allantois become apposed.

In mammals the chorion arises ready-made as the trophoblast,_

which invests the blastocyst from the start. It is, however, customary in mammalian embryology only to give the trophoblast the term chorion when it is underlain by the outer mesodermal layer of the extra-embryonic coelom, the mesoderm covering the yolk-sac, or the mesoderm covering the allantois. Where the blood-vessels of the yolk-sac form a placenta, it is known as a ehorio-omphaloidean placenta, as in the reptile C'h(1Ic't'dcs; it is the chief nutritive organ in the embryonic development of the Marsupials except Perameles, and in the “l’lacental" mammals it arises early and disappears later. Where the blood-vessels of the allantois form a placenta, it is known as a chorio-allantoic placenta. as in Peranmles and all “Placental” mammals: often abbreviated to allantoie placenta. Tm: Al.l.ANTOlS. The allantois occurs in reptiles, birds, and mammals. and attains its greatest dctelopment in the latter. It develops as an outgrowth from the hind part of the gut, and is an endodermal sac covered with mesoderm in which blood-vessels run. In amphibia it is represented by the (allantoic) bladder. In reptiles, birds, and Monotremes, the allantois functions as a respiratory and excretory organ. for which it is well titted since the excretory ducts open into its base, and its distal portion is spread out close beneath the chorion and the porous shell. In the reptile Chalcides, the Marsupial1’mnm'Ie.s', and the Placental mammals, the allantois enters into relations with the chorion and so with the wall of the oviduct (or uterus) and forms the allantoic placenta. Its function is then nutritive as well as respiratory and excretory. It is easy to see how this may have occurred in evolution by the retention of the egg within the oviduct and the disappearance of the shell. It is necessary to mention this last proviso because in sortie forms the egg is not laid; it undergoes development in the oviduct but does not lose the _ W'rH_§ amniuronre Maynnanns r ,. 3 215,

shell. This condition, which occurs“ in :the Viper, is called ovoviviparous.

In the Placental mammals, the allantois relieves the yolk-sac in‘

the formation of the placenta, and the higher the order of mammals the earlier does this happen. Indeed, in the highest of all, the Primates (including man), the mesoderm of the allantoie stalk appears frpm the beginning (the “body-stalk”), and the endodermal allantois grows into it later. In these animals the allantoic blood-vessels (the

Figure ll6. Diagram of the relations of the embryonic membranes in the human embryo. (From Jenkinson, after Graf Spec.)

A, the embryo, developed in the ﬂoor of its amniotic cavity (arm), is attached to the trophoblast by the mesodermal body-stalk (bst), into which the allantois 15 beginning to grow; bu, blood-vessels round the wall of the yolk-sac (ys). B, transverse section through the body-stalk in the plane indicated showing allantois and blood-vessels. umbilical arteries and veins) are ready at a very early stage to transport to and from the embryo, which increases the efficiency of the placenta. The blood-vessels of the allantois are usually covered by the outermost layer of extra-embryonic ectoderm, the chorion in reptiles and birds, and the trophoblast in mammals.

THE ALLANTOIC PLACENTA. The blood ofthe mother and that of the embryo are never in direct communication. The passage of foodstuffs, excretory and respiratory substances must therefore take place by diffusion through the membranes. The efficiency of the

placenta is conditioned by the area of mutual contact between the .216 'coMMttA'rrva zoonoer or cnonnuas

maternal iand embryonic circulations, and by the thickness and

‘number of the intervening membranes. The area of contact can be

increased by throwing the surfaces of the maternal and embryonic tissues into folds; and the intervening membranes can be decreased by removal or erosion of certain of the layers of the uterus. Four grades of structure and corresponding eﬂiciency can be seen in the mammals, which will now be taken in order.

(i) The embryonic and maternal surfaces are ﬂat and unfolded; the area of contact is therefore small. However, the trophoblast becomes syncytial in its outermost layer, and this fuses with the

Figure 117. Section through a part of the allantoic placenta of Peramelesz embryonic tissue on the left, maternal on the right. (After Hill.)

11, allantois; ob, embryonic blood-vessels; em, embryonic mesoderm; mb,

maternal blood-vessels; mc, matemal connective tissue; ue, uterine epithelium (which has become syncyual). fused with the syncytial layer of the embryonic trophoblast.

uterine epithelium which also becomes syncytial. Substances therefore have to pass through the wall of the maternal capillaries, through the combined syncytium of the uterine epithelium and trophoblast, across the intervening space and through the wall of the embryonic capillaries. This type of placenta occurs in Perameles, the only Marsupial to possess an allantoic placenta at all. It was probably present in the ancestors of the Marsupials, and has been lost in the other living Marsupials.

(ii) The epithelio-chorial type. The embryonic and maternal tissues are thrown into folds; embryonic “fingers” or villi ﬁtting into corresponding crypts in the uterine wall. In the pig, villi are distributed all over the trophnblast. The uterine epithelium persists. Substances therefore must diffuse through the wall of the maternal THE BMBRYONIC MEMBRANES ,217

capillaries, connective tissue, uterine epithelium, trophoblast, and the wall of the embryonic capillaries. Curiously enough, this type of placenta is found not only in certain Ungulates but also in the Inseetivore Scalopus and in the Lemurs.

(iii) The syndesmo-chorial type. This is similar to the epitheliochorial type except that the maternal epithelium is eroded and the embryonic tissues are in contact with the connective tissue of the uterine wall. In the cow the villi are grouped together in clumps forming cotyledons.

Figure 118. Section through a part of the epitheho-chorial allantoic placenta of the pig; embryonic tissue to the left, maternal to the right.

The trophoblast (r) is produced into villi (v), which ﬁt loosely into crypts (c) in the uterine wall, the epithelium of which (ue) persists; al, allantois; ch, embryonic blood-vessel; ec, embryonic connective tissue; mb, maternal bloodvessel; mr, maternal connective tissue; ug, glands in the wall of the uterus.

(iv) The endothelio-chorial type. The uterine epithelium is eroded and the underlying maternal connective tissue is invaded by the developing villi of the trophoblast, so that the latter comes into contact with the endothelial walls of the maternal capillaries. Substances have only to pass through the wall of the maternal capillaries, the trophoblast, and the wall of the embryonic capillaries in’ order to diffuse through the placental barrier. This type of placenta occurs in carnivora (cat and dog), and is restricted to a zone of the

trophoblast, whence its name zonary. 8t 218 ,COMPARATIVE zoonomr or cnonnarns

., ",,(,v‘j The haemo-ehorial type. The epithelium of’ the uterus is removed, but the underlying connective tissue is not invaded as in the carnivores; instead the trophoblast is very much thickened and then hollowed out here and there to form lacunae. The remaining projections from the trophoblast are called pseudovilli to distinguish them from the true villi which are deﬁnite outgrowths. The maternal blood-vessels are “tapped” by the very thorough erosion of the uterine wall, and the blood ﬂows out of them and into the lacuna: in the trophoblast. The pseudovilli are therefore bathed in the blood of the mother, and the substances have only to pass through the trophoblast and the wall of the embryonic capillaries to enter into

Figure ll9. Section through a part of the endothelio-chorial allantoic placenta of the cat; embryonic tissue to the left, maternal to the right.

Letters as Figure H8.

the embryonic circulation. This is the highest type of placenta, and it is found in Rodents. lnsectixores, Cheiroptera, and Primates other than Lcmurs, i.c.. in the rabbit. mouse, but. shrew, hedgehog, mole, Tar.s'iu.v. monkey. ape. and ma n. This ty pe of placenta occupies a discshaped region of the lrophoblast. whence its name discoidal (Fig. lll).

At birth, the allantois and placenta are nipped oﬁ‘ from the embryo; and the placenta separates from the uterus, and is expelled as the “after-birth“. In the carnix ores (type iv) this entails a certain

amount of loss of maternal tissue; in the others the mother only‘

loses blood. in Pcrantcles, on the other hand, the placenta is absorbed by the uterus.

It must be remembered that as well as being an organ of exchange between mother and embryo, the placenta functions during early .r_ria emnnlvomc nrnstennnas , . 3:3,219

stages of development as a regulator bf metabolism of substances such as glycogen. Later on, this function is taken on by the liver of " the embryo.

The placenta also secretes a gonadotropic hormone which, at least in some mammals, plays an important part in preventing premature cessation of the pregnancy.

Tl-IE AMNION. The amnion is found only in reptiles, birds, and mammals. All these animals differ from the ﬁsh and amphibia in that the eggs are laid on dry land and not in water. The amnion is formed by folds of the extra-embryonic ectodcrm and underlying mesoderm which rise up on all sides of the embryo and meet above it. The inner layer so formed enclosing the amniotic cavity is the amnion proper; the outer layer is the chorion. In the reptiles and the Monotremes, the fusion of the folds above the embryo is not complete, so that the amniotic cavity is not quite closed. In the birds, the amniotic cavity is closed, but it opens again later (at the seroamniotic connexion).

In the mammals, there are two principal types of amnion-formation. In the one type, of which the rabbit is characteristic, the embryonic plate comes to the surface of the blastocyst by the disappearance of the overlying trophoblast (cells of Rauber), and the amniotic folds rise up on each side of the embryo from the edge of the embryonic plate. This method of formation ofthe amnion is very similar to that which holds in birds; the chorion of the latter corresponds to the trophoblast of the mammals. The only difference is the fact that the trophoblast in the mammal formed a complete investment at the earliest stage.

In the other type, of which the mouse is an example, the amnion arises as a cavity hollowed out in the inner mass of cells, within the trophoblast. This method is called amnion-formation with entypy of the germ. In this case, there are no amniotic folds, and the trophoblast (which forms a complete investment, as in the rabbit) does not become interrupted by any disappearance of Rauber’s cells. When the amniotic cavity is formed in the mouse or man, the embryo becomes differentiated on its ﬂoor. The mouse and man therefore start from a condition which the reptiles do not reach until a fairly late stage of development, when the amniotic folds have been formed.

The amniotic cavity contains ﬂuid, and this enables the embryo to develop in a fluid medium, although its egg was not laid in water.

It is interesting to note how in the higher vertebrates certain processes take place as if they were abbreviations of the conditions which prevail in lower vertebrates. To start with, the primitive streak which is the beginning in higher vertebrates, represents a stage which 220,3‘ *CQlilPAM1'lVE ZOOLOGY or caononrss

the lower vertebrates only reach after the blastopore’ has formed, , and become closed by the apposition ol'_ its lateral lips. Similarly, the

mammal with a hollowed-out amniotic cavity within the trophoblast starts from a condition which the reptiles and birds reach after the upgrowth and fusion of the amniotic folds. Not only this, but in such mammals the amniotic cavity arises ﬁrst and the embryo forms in its ﬂoor; whereas in the reptiles and birds the embryo forms first and the amniotic folds arise afterwards. This process of “shortcircuiting” and telescoping of developmental processes reaches its climax in the Primates, where the body-stalk develops ﬁrst and the allantois grows into it later. In lower mammals as well as in reptiles and birds, the allantois grows out from the hind-gut at a fairly late stage. In the Primates, the conditions are as if everything were ﬁrst got ready for the embryo, after which it makes its appearance. This is not without interest in connexion with the superior organisation and differentiation of the highest mammals, for this superiority in construction is dependent on a prolonged and intense period of embryonic development, when the elﬁciency of the embryonic membranes and placenta is of the utmost importance.

LITERATURE

HILL, J. P. The developmental history of the Primates. Philosophical Trart.s'ttt'tions' of the Royal Society, B. Vol. 221, I932.

JENKINs0N, J. W. Vertebrate Embryology. Oxford, at the Clarendon Press, l9l 3.

MossMAN, H. W. (‘omparativc Morphogenesis of the Fetal Membranes. Contributions to Ernbryolog_t-, Vol. 26, Carnegie Institution of Washington. 1937.

MOSSMAN, H. W. The epithelto-chorial placenta of an American mole, Scalopus aqaaticus. Proceerlings of the Zoological Society of London, B. Vol. l09, I939.

Wusttss, ll. C. A review of placentation among reptiles. Proceedings of the Zoological Society of Lomlon, 1935. CHAPTER XVII THE SKIN, AND ITS DERIVATIVES

T HE skin forms the outermost layer of the body, and its functions are protective, excretory, and sensory; for all information which the animal receives concerning the outer world must come through the skin. Correlated with these functions, it is found that the constituents of the skin may undergo various modiﬁcations.

The skin is formed of an outer ectodermal layer, the epidermis, and an inner mesodermal layer, the dermis. In Amphioxus the epidermis is only one-cell thick (as in most invertebrates); while in all Craniates it is several layers of cells in thickness. Of these, the innermost form the stratum germinativum (or stratum Malpighi) which constantly produces new cells, while the outermost layers tend to become horny forming the stratum corneum. As the cells become horny the protoplasm within them dies. and they become worn away by friction with the environment and replaced from the stratum germinativum. In many reptiles and amphibia, it is common for the superﬁcial layer of the epidermis (overlying the horny scales) to be sloughed off all at once and replaced.

The epidermis may be ciliated in early stages of development in the lower forms, such as Amphiaxus and the frog tadpole.

The epidermis covering the eye becomes very thin and transparent forming the conjunctiva. Sensory cells are present in the stratum germinativum, and it will be remembered that the sensory epithelium of the nose, of the eye, the ear, the lens and the placodes which contribute nerve-cells to the cranial ganglia, are all formed from the epidermis.

The skin excretes by means of glands which may be composed of single cells or many cells. Examples of the latter are to be found in the mammary, sebaceous, and sweat-glands of the mammals. These glands arise in the epidermis and project inwards into the underlying dermis. In some animals the glands may be modiﬁed into poisonglands; and in deep-sea ﬁsh they may produce a luminous secretion.

In the embryos of some Teleost ﬁsh and some Amphibia, the skin of the snout secretes a “hatching enzyme” which digests the overlying egg-membrane and enables the embryo to hatch.

The epidermis may be modiﬁed into a variety of structures such

as horny scales (comeoscutes) which are present in reptiles, birds 221 222 , coumtisrrva .zooLocv or ,caonns’ras

(chieﬂy on the feet) and mammals (allover the body of the Pangolin, "-at the base of the tail of the rat). The epidermis also gives rise to -Heathers which are characteristic of birds (see p. 190); hairs which are ' 3..~.0haracteristie of mammals (see p. 201); the termination of the digits;

which may take the form of claws, nails, or hoofs; and the horny«

“covering of the beak in tortoises and birds. The “homs” of cattle t are formed of a layer of epidermal horn overlying a central dermal bony core. The horn of the rhinoceros is made of fused hair. Special epidermal structures on the edge of the mouth of Petromyzon, frog tadpoles, and ()rniI/zorlzynchus, give rise to the so-called “horny teeth”, which have nothing to do with true teeth. Somewhat similar is the horny projection or caruncle on the upper jaw or snout of embryos of Sphcnodon, Crocodilia, Chelonia, birds, and Monotremes, by means of which the embryo cracks the shell and hatches. Lastly, the epidermis produces the cap of enamel which forms at covering to the dcntine of denticles and true teeth.

Hairs and feathers are commonly moulted at intervals and replaced.

The dermis forms the leathery layer of the skin. It contains bloodvessels which serve to supply the cells of the epidermis as well as those of the dermis, and especially the papillae at the bases of hairs and feathers, and the glands. ln amphibia this dermal circulation also serves respiratory purposes, and in the mammals it forms part of the mechanism for regulating the heat of the body. In amphibia the dermis is separated front the underlying muscles by lymph-spaces, but in higher forms the skin is ﬁrmly attached to the muscles by connective tissue. In higher forms, special muscles arise in connexion with the dermis. Some of them are attached to scales, feathers, or ,hair-follicles. which they mmc. It is by the contraction of these (smooth) muscles in mammals that hair is made to “stand on end”, and the puckering of the skin round the hair-follicles gives rise to the condition known as “chicken-skin".

In addition to these dermal muscles. there are in the higher forms, and especially in the mammals, sets of muscles beneath the skin and which move the skin as a whole. The panniculus carnosus muscles are in the region of the trunk and they serve to shake the skin. (They are of somatic origin.) In the head and neck regions the platysma muscles (of \ isceral origin) move certain parts of the skin such as the lips, eyebrows. and ears. ln man. these are the muscles of expression. The smooth dermal muscles are innervated by sympathetic ﬁbres,

the panniculus carnosus by ventral nerve-roots, and the platysma 5

by the facial nerve. Just as the cells of the epidermis seem to be prone to the production

. of horn and horn—like structures, so the cells of the dermis seem to_

him ‘ A

ma sum, syn lTS~l)‘1El_l.I: YAT_IVE~:§ 1 “ 223

run to the formation of bone and dentine. Dentine is the substance ‘ of which denticles and teeth are formed, under the epidermal cap of enamel. The bone produced in the dermis takes the form of dermal ,7 or membrane-bone, bony scales, or ﬁn-rays (lepidotrichia). In ~r»

Selachii the dermis forms dentine but no bone.

Dermal bones are widely distributed over the body in forms above the Selachii. They play an important part in the formation of the skull, and of the pectoral girdle. In some animals, the body may be entirely covered by an armour of bony plates, as in the Labyrinthodonts, or the armadilloes. These bony plates are osteoscutes, and remnants of them are to be found in the carapace and the ventral shield (or plastron) of the tortoise, and in the so-called abdominal ribs or gastralia of Sp/zenodon, crocodile, Plesiosaurs, lchthyosaurs, Pterosaurs, and Archtwpteryx (see Fig. 160). Osteoscutes are also present in Gymnophiona, lizards, and crocodiles.

In the ﬁsh, the dermal bones come into relation with the overlying denticles, forming complex scales. In the Osteolepidoti and primitive (extinct) Dipnoi, the denticles have fused together forming a layer of “cosmin”, and this is attached to the underlying bony plate, which forms the so-called “isopedin” layer. This is the “cosmoid” scale.

In the primitive (extinct) sturgeons (the Palaeoniscoidea) and in Polypterus, the layer of cosmin is not only covered by bone underneath (the isopedin), but also on top, the superﬁcial layer of bone being called the ganoin. This type of scale is called palaconiscoid. In Lepidosteus the structure of the scale is similar, but the layer of cosmin has disappeared, and the scale consists simply of a layer of ganoin overlying a layer of isopcdin. This is the lepidosteoid type of scale. The palzeoniscoid and lepidosteoid scales are ofcourse beneath the epidermis since the layer of ganoin (bone) is a dermal structure. The epidermis overlying these scales may possess true denticles. It is also worth noticing that the structure of the dermal bones and of the dermal ﬁn—rays (lepidotrichia) in a given animal tends to be identical with that of the scales.

In the higher bony ﬁsh or Tcleosts, the scales lose the layer of ganoin. The scales form in the dermis, but the bone—cells become lost and the scales are very thin. It is obvious that these dermal scales together with the dermal scales of Gymnophiona and lizards (osteoscutes) must not be regarded as having anything in common with the epidermal scales (corneoscutes) of higher forms. Dermal scales are retained throughout life; epidermal scales and, denticles are shed.

Other examples of dermal ossiﬁcations are to be found in the bone (as corneum) which forms the core of the “horn” of cattle, and which becomes attached to the frontal bone of the skull. Similar 224 coumnsrrve zoonoev or cnonmrss

‘little bones form the knobs on the head of the giraffe, while large

bony structures in this position give rise to the antlers of deer. Antlers are restricted to the males, they may be forked, and they are ished every year. The size of the antler often bears an interesting relation to the size of the body (see p. 413). Horns, on the other hand,

Figure 1220. Sections through the skin of Scyllium embryos, showing the

mode of development of the placoid scales or denticles at successive stages [mm A to E.

d, dentine; e. eetoderrn; or. modified ectoderm cells which produce the enamel; en, enamel; ‘rn, mesoderm; o, odontoblasts, cells which produce the dentine; pt, pulp-cavity.

may be present in both sexes. and, except in Antilacapra (the American prong-buck), they are neither forked nor shed.

Lastly, when dealing with the skin, mention must be made of colour. Pigment-cells may occur in the epidermal and the dermal layers of the skin. in some cases, the pigment-cells are capable of y rue sxm, AND we ueruvarrves 225

altering the distribution of their pigment, with the result that the animal may change colour (as, for example, the frog, or the charmleon). Pigment may also be present in feathers and in hair, but in these structures the texture of the surface may also produce eﬁects of colour without any pigment being there.

LITERATURE

GOODRICH, E. S. Vertebrata Craniata, Cyclostomes and Fislres. Black, London, 1909. CHAPTER XVIII

THE TEETH

TEETH and the dentieles (or placoid scales) of the dogﬁsh are identical in that they consist essentially of a hollow cone of dentine, inside which is a pulp-cavity, and outside which is a layer of enamel. The dentine is formed from odontoblasts in the skin, and the enamel is produced from the overlying ectoderm. In the Amphibia, at least, it has been shown that the odontoblasts are ectomesenchyme cells derived from the neural crest. The denticle or tooth is formed below the surface of the skin, and is subsequently erupted through it. In the dogﬁsh the denticles are not restricted to the borders of the mouth, but occur all over the surface of the body. In a few bony ﬁsh such as Polypterus, Lepidosteus, and catﬁsh, denticles also occur over the surface of the body; but in the remainder, and all higher vertebrates, teeth are restricted to the mouth. In addition to those on the premaxilla. maxilla, and dentary. teeth may be carried by the prevomer, parasphenoid, palatine, pterygoid and splenial in lower vertebrates; in the bony ﬁsh teeth may even be carried on the branchial arches. In Selachians, the teeth are loosely attached to the underlying skeleton by connective tissue. In bony ﬁsh, they are ﬁrmly ﬁxed on to the underlying bone by “cement”. a modiﬁed form of bone, which is absorbed when the tooth is shed. ln some cases the teeth may be hinged. in higher forms the bone grows round the base of the teeth. which thus come to lie in grooves (pleurodont) or sockets (thecodontl. ln Sphenodon and C’/zamzrleo the teeth are fused on to the edge of the bone (acrodont condition) and are not replaced.

The teeth of Osteolepidoti and of the earliest amphibia are peculiar in that their walls are throw it into folds, giving a characteristic appearance when seen in section, and which is responsible for the term I.abyrinthodontia which is applied to the earliest amphibia. In snakes the teeth may be grooved or ex en hollow and converted into poison—t'angs. The poisonous secretion passes in the groove or tube and is inserted as with a hypodermic needle into the tissues of the prey.

Living Chelonia have no teeth, but they were present in the primitive fossil T riussoc/iel_v.v. The same applies to birds, which are toothless today, but which originally possessed teeth, as is shown by

the fossil Arc}m'opter,v.v and others. » 226 rue ream 221,

The teeth of mammals and of those extinct reptiles ‘which were on ' the mammalian line of descent differ from those of other vertebrates

in that they are not all similar, but differ in shape in the various ‘iii.

regions of the mouth. This condition is called heterodont, as opposed to the homodont condition when the teeth are all similar.

Figure l2l. Transverse sections through the lower jaw of mammalian embryos showing the development of the teeth.

A, early stage, the dental lamina (d!) has grown in from the ectoderm; B, a tooth-gem: has been fomted on the dental lamina, the cells of Which (cctodermal) produce the enamel (e); beneath the enamel the odontoblasts produce dcntine (dn). C, the development of the tirst or mrlk-tooth (mt) IS nearing completion; beneath it the dental lamina has formed another tooth—germ which will produce a permanent tooth (pt); the dcntary bone (:1) encloses the teeth in a socket. fm, ﬂoor of the mouth; I, lip; Mr, Meckel‘s cartilage; mp, odontoblast papilla; pc, pulp-cavity; r, tongue. (Cf. Method of development of the denticle, hg. 120.)

The most anterior teeth are the incisors, and (except in some Marsupials) they are never more than three in number on each side in each jaw. In the upper jaw they are carried on the prcmaxilla. Next come the canines, the premolars, and the molars. The molars diifer from the premolars in that there is only one set of them, whereas the premolars are represented by a lacteal or “milk” «£228 commuunva ZOOLOGY or CHORDATES

dentition followed by a permanent set which replaces them. In a few mammals, such as the toothed whales, the teeth are all similar, but this is a secondary and degenerate condition.

Another diﬂerence between the teeth of mammals and those of other vertebrates lies in the fact that they arise in two sets, or, in other words, they are replaced once only (except for the molars which are not replaced at all). Other vertebrates have perpetual replacement of teeth as and when the existing ones wear out. The mammalian condition is called diphyodont, that of other vertebrates polyphyodont. However, it is probable that the two sets of teeth of the mammal are not to be regarded as simply an abridgement and reduction of the many sets of teeth of, say, the crocodile, for the

Figure I212. The origin of teeth in the dogﬁsh.

A, inner side of one half of the upper jaw, showing the rows of reserve teeth: B, section through the lowerjaw; the smallest teeth are the most recently formed. Me, Mecltelis cartilage.

following reason. The ectoderm, which sinks down beneath the surface of the skin of the mouth to produce the enamel, forms a long band extending parallel to the edge of the jaw, known as the dental lamina. The rudiments of the teeth appear on the outer side of the dental lamina in two families; one from the middle of the side of the lamina, and the other from its base. The teeth formed by one family of rudiments grow up and are intercalated between the teeth formed by the other family. When, in the crocodile, for example, a tooth has been f ormcd. another tooth arises beneath it from the same rudiment, and this second tooth will exentually push out and replace the ﬁrst. But any given tooth is only replaced by a tooth belonging to its own family, and which has arisen from the same part of the dental lamina. In the mammal there are the same two families of tooth-rudiments, but each rudiment gives rise to one tooth only. Further, owing to the reduction in size of the jaw. there is not room for both families of teeth at the same time. One family appears first, and gives rise to rna ream 229

the lacteal or “milk” dentition. Later on, the other family appears and forms the permanent dentition which pushes out and replaces the lacteal teeth. In the mammal, therefore, a replacement is effected by a tooth of one family displacing a tooth of the other family; in

Figure 123. Diagrams showing the relation of the mammalian to other modes of tooth-succession. (After Bolk.)

A, diagrammatic view of the outer side of the dental lamina (c/I) of the lower jaw, showing the alternation between tooth-genns at the side (5) and at the base (b) of the dental lamina. B, diagrammatic representation of tooth-replacement in reptiles; the teeth formed from the tooth-germs at the side of the dental lamina are shaded: those formed from the tooth-germs at the base of the dental lamina are white; the tooth-genus produce several teeth, which replace other teeth formed originally from the same tooth-germ as themselves. C, diagrammatic representation of tooth-replacement in mammals; each tooth-germ produces one tooth only, and the teeth formed from the tooth-germs at the base of the dental lamina replace those formed from the tooth germs at the side of the

dental lamina. e, ectoderm.

the other vertebrates replacement is brought about by the displacement of a tooth by another tooth belonging to the same family. It is probable that the molars belong to the permanent family, the corresponding lacteal teeth having been suppressed.

The Marsupials have a peculiar mode of reproduction in that the young are born very early and in a very undeveloped condition230 , COMPARATIVE ZOOLOGY or cnorrparas

‘F: ‘IN’ a ‘ h ‘ 0 . They are attached to the nipples of the mother and continue their “development in her pouch, or marsupium. During this period no

‘teeth are required, and it is found that in Marsupials the 1ﬂCtC3.1'..

-dentition is reduced; in fact only one tooth (the third premolar) ism‘

replaced. That this is a secondary reduction is proved by the fact

‘that in extinct forms replacement took place in more of the teeth.

There is another point of interest in the teeth of the Marsupials, which refers to the fact that they are the only mammals in which

more than three incisors are found on each side. The probable ex- .

planation is that in this region of the mouth, the teeth of one family are not replaced by the teeth of the other, but that both families of teeth are erupted together, the members of the two families intercalated as in the crocodile. Behind the canine, however, the families of teeth replace one another as in other mammals. The marsupials,

then, are intermediate between the reptiles (simultaneous presence .

of teeth of both families all over the jaw with complete intercalation) and the higher mammals (no intercalation of teeth of the two families).

The primitive shape of the molar teeth in the mammal is threecusped or tritubereular in the upper jaw, while those of the lower jaw have three cusps and a posterior “heel” or talonid, and are called tuberculo-sectorial. The three cusps of the upper teeth form a triangle or "trigon", with the apex pointing inwards; the three cusps of the lower teeth form a “trigonid”, with the apex pointing outwards. They arc so arranged by this means that the teeth of the upper and those of the lower jaw ﬁt into and work against one another. This type of molar was evolved from the primitive reptilian type in which each tooth had but one cusp. The original cusp is represented by the outer cusp of the trigonid in the lower molars, while in the upper molars the original cusp has been split into two and is represented by the two lateral cusps of the trigon. The remaining cusps and the talonid were subsequently developed in relation to the “ﬁt" of the teeth on one another. The number and arrangement of the cusps may be much modiﬁed in the different groups, but the primitive forms of most groups of mammals have molars of this tritubercular and tubcrculo-sectorial type.

When the cusps remain separate as in the pig, the tooth is called bunodont. In other forms, the cusps may be joined to one another by ridges running at right angles to the length of the jaw, as in the tapir (lophodont condition). In others. again, the cusps are splayed out to form crescents running in the line of the length of the jaw, as in the camels (selcnodont condition).

It is characteristic of mammalian molars to have divided roots or

“fangs". ‘run rear}: 231

Figure 124. Types of teeth (the different teeth are not drawn to the same scale).

A, longitudinal section through a human molar, showing: c, cement (here restricted to the base of the tooth); d, dentine; 9, enamel; pc, pulp-cavity; r, roots or fangs; such a tooth is short and low in the crown, and conforms to the type called brachyodorit. B, longitudinal section through a premolar of the horse; cement, dcntine and enamel all enter into the composition of the crown of the tooth, and as the hardness of these substances differs, they are worn away to different extents; such a tooth is long and high in the crown, and conforms to the type called hypsodont. C, longitudinal section through the incisor of a rabbit, showing the open ("rootless”) pulp-cavity or pC!'5lbtCl”lt pulp (pp). D, view of the crown of an upper molar of a pig, showing the separate cusps characteristic of bunodont teeth. E, crown of an unworn, F, crown of a worn lower molar of a camel, showing the crescent-shaped ridges joining the cusps, characteristic of selenodont teeth. G, crown of an unworn, H, crown of a worn lower molar of a tapir, showing the transverse ridges joining the cusps, characteristic of lophodont teeth. I, inner side view of a tritubercular (upper) molar, in relation to J, a tuberculo-scctorial (lower) molar; r, talonid. K, diagram of the relative positions of the cusps of tritubercular molars (dotted lines) of the upper jaw, and tuberculo-sectorial molars (full lines) of the lower jaw; an, anterior side; an, outer side. L, simple peg-like tooth of a reptile. 232 conrsrtartve zoonoov or cnonbxrss

Normally, a tooth grows to a certain size (not very big), and after that the pulp-cavity becomes almost closed at the base. Such a tooth may have one or more “roots” or fangs, and when these have "formed, the tooth ceases growing. This is the brachyodont type, the name being derived from the fact that the teeth are comparatively short. and as a rule their possessors do not make use of them for grinding hard materials. Where the diet consists of resistant material which requires grinding, and in other cases where the teeth are subjected to hard wear, the pulp-cavity remains widely open at the base,‘

and the teeth are capable of continuous growth. These teeth are described as being “rootless", or possessing persistent pulps, and from the fact that they are usually long, this condition is known as hypsodont. Examples of hypsodont teeth are to be found in the premolars and molars of the horse, the incisors of the rabbit, the incisors (tusks) of the elephant, and the canines of the boar, to mention only a few.

In the carnivores (cats and dogs) one tooth in each jaw on each side becomes enlarged and modiﬁed for tearing ﬂesh, forming the so-called carnassial tooth. It is the last premolar (4th) in the upper jaw and the first molar in the lower jaw. Other carnivores (bears and seals) do not have the carnassial tooth well developed.

In addition to dcntine and enamel, it is common for the teeth of mammals to have a complete or partial covering of bone which is called “ccmcnt". This may be restricted to the roots of the teeth, as in man, or it may form a complete covering over the crown before the tooth is erupted, as in ungulates. After the tooth has been erupted and projects above the gums, it is subjected to wear, and its different constituents become worn away according to their softness. The hardest substance is the enamel, and next comes the dentine, and lastly the cement which is the softest. The result of the unequal wear in teeth like those of the elephant or of some rodents is that the crown is not smooth but becomes ridged like a file, and such teeth are as ellicicnt as mill-stones grinding against one another.

In some of the lidentates (sloths and armadilloes) the teeth have no enamel, while in others (ant-eaters) and in some whales there are no teeth at all.

in the embryos of Lacertilia, Ophidia, and Monotremes it is usual to ﬁnd that the foremost two teeth or a single tooth of the upper jaw are precociously formed, enlarged, and directed forwards so that they project beyond the mouth and can pierce the embryonic membranes and the shell, thereby enabling the embryo to hatch. Such “egg-teeth” are not to be confused with the epidermal caruncles found in other forms. Both are present in Monotremes.

There is no difliculty in tracing the teeth of vertebrates back to the rue ream ‘ . 233

denticles of the Selachians, and of some of the Ostracoderms. It has been suggestw that denticles also gave rise to dermal bone by fusing together. This is very improbable. Denticles are composed not of bone but of dentine, which differs from bone in that the cells which secrete it do not remain in it but migrate out. Denticles are often found attached to true scales or dennal bones, but these are developed independently from the denticles.

It can be said that the dermal bones and scales develop in relation to the denticles, but not from them.

The so-called teeth of Petromyzon, of Ornithorhynchus, and of the tadpole of the frog are epidermal horny structures, and have nothing whatever in common with the true teeth.

LITERATURE

Bout, L. Odontological Essays, Journal of Anatomy Vol. 55, 1921; Vol. 56, 1922; and Vol. 57, 1922.

MUMMERY, J. H. The Microscopic Anatomy of the Teeth. Henry Frowde and Hodder & Stoughton, London, l9l9.

TOMBS, C. S. A Manual of Dental Anatomy, Human and Comparative. Churchill, London, 1898. CHAPTER XIX

THE CCELOM AND MESODERM

J .

t

IN Amphioxus and all Craniates the most dorsal mesoderm is seg:-"ii

mented into somites. These each contain a portion of coelomic cavity

r

called myoccel, which persists in Amphioxus, but becomes obliterated '

in higher forms. The median wall of the myocoel is thickened and produces the myotome: a plate of muscle with striated ﬁbres, innervated by somatic ellerent ﬁbres (voluntary) through the ventral’

nerve-roots. The outer layer of ccelomic epithelium lateral to the myoccel gives rise to the dermatome or cutis-layer, beneath the skin. On the median side, the myotome also produces the sclerotome. In Ampliioxzzs this is in the form of a hollow outgrowth, but in higher forms it is composed of mesenchyme. It gives rise in Craniates to the

basidorsal and basiventral elements which go to make up the vertebral column.

The dorsal segmented portion of the mesodenn is known as the vertebral plate. The more ventral portion of the mesoderm arises segmentally in .-imp/u'm'us, each segment separated from the ones in front and behind by septa. These septa, however, break down, and the ventral coclomic cavity or splanchnocoel is continuous from end to end of the animal. This condition arises from the ﬁrst in the Craniates, where the mesoderm in this region, known as the lateral plate, is not segmented. The outer wall of the splanchnocoal becomes applied to the body-wall. and the inner wall covers the gut-wall. The separation between right and left splanchnocoel usually breaks down ventrally. but persists dorsally as the mesentery which suspends the gut. The muscles which the coelomic epithelium of the splanchnoeoel produces are smooth, intoluntary, and innervated by the autonomic nervous system, except for those which are situated in the anterior region of the body, in connexion with the gill-slits. The gillslits pierce through from the gut to the outside in the region of the lateral plate; between the gill-slits, in the visceral arches, the lateralplate mesoderm gives rise to the muscles WlllCl1 move the arches, including the jaws. These muscles are striated and voluntary, but they are not myotomic, and they are innervated by visceral eﬂerent ﬁbres through the dorsal roots of the cranial nerves.

Between the myocoels and the splanehnoccels there are typically

little hollow stalks, through which at early stages the cavities of the”

234 ‘ THE craters A‘ND MBSOQBRM 235 latter can communicate with those of the former. They are segmental

in arrangement. In Amphiaxus, these regions of the ccelom represent “

the future gonads, and are called the gonotomes with their cavities the gonoccels. In the Craniates, they are called the nephrotomes (or intermediate cell-masses); the cavities (communications between the myoccels and the splanchnoctel) are the nephrocoels, and they give rise to the tubules of the kidneys and associated structures, eventually losing connexion both with myocoels and splanchnoccel.

In Amphioxus the splanchnoctrl is continuous from end to end of the body as in the Ammocoete, for the transverse septum in which the ductus Cuvieri crosses over from the body-wall to the gut-wall is not large. In Selachians. the transverse septum separates an anterior pericardial cavity from a posterior peritoneal or perivisceral cavity, leaving only very small communications between them in the form of the pericardio-peritoneal canals. In higher forms the separation between pericardial and perivisceral cavities is complete. Beginning in the Dipnoi, the pericardium becomes thin-walled and projects backwards into the perivisceral cavity.

All viscera are morphologically outside the ctelomic cavity and only suspended in it by a bag of coelomic epithelium which forms a double membrane or mesentery. So the gut is suspended by the dorsal mesentery from the roof of the perivisceral cavity, and between the two membranes composing it there pass the arteries from the dorsal aorta to the gut. The gut and liver are connected by the lesser omentu m, through which the bile-duct runs from the liver to the anterior portion of the intestine. The lungs in amphibia are of course covered over by ctrlomic epithelium (pleura) which is continuous with the ordinary lining of the perivisceral cavity round the stalk of the lungs. in some reptiles, the ccelomic epithelium covering the lung is also attached to the roof of the perivisceral cavity forming the accessory mesentery, and attached to the liver below by the pulmohepatic ligaments. On each side of the dorsal mesentery therefore there is a recess, the pulmo-hepatic recess, bounded on the median side by the dorsal mesentery and stomach, laterally by the accessory mesentery and pulmo-hepatic ligament, and below by the liver. Owing to the curvature of the stomach and the return of the anterior portion of the intestine to form the loop of the duodenum, the pulmo-hepatic recess of the right side comes to form a pocket, the omental cavity. This pocket communicates with the general perivisceral cavity by an opening the front edge of which is formed by the hind border of the accessory mesentery and pulmo-hepatic ligament. Along this edge runs the inferior vena cava. The hind edge of the opening is formed from the dorsal mesentery and

t lesser omentum and along the latter run the bile-d uct, the portal vein 236 C,OMPAlA'['IVB zoomar or cnonnnns

and the hepatic artery. The opening is the primitive foramen of Winslow.

In the birds, the conditions start similarly with regard to the accessory mesentcries and the pulmo-hepatic ligaments, but the latter in addition are connected to the side wall of the perivisceral cavity. In this manner the oblique septa are formed, which separate a pair of dorso-lateral pleural cavities (into which the lungs project) from

Figure I25. 'I‘rans\erse section throu_gh the trunk of an embryo of Lac-erta, showing the relations of the ctnlom.

_ am, accessory mcsentcry: da, dorsal aorta; rim, dorsal mesentery; ﬂ, falciform ligament; g, gut; 1. liver; In. lung; In, lesser omcntum; n, notochord; nc, nervecord; phi, pulmo-hepatic ligament; phr, pulmo-hepatic recess.

the perivisceral cavity. The latter is further obstructed by the posthepatic septum which connects the gizzard to the ﬂoor of the cavity.

The mammals are cliaracterised by the presence of the diaphragm. This is formed partly from the transverse septum which separates the pericardial cavity from the rest, and partly from cuelomic epithelium in connexion with the mesentery and the folds in which the kidneys hang down from the roof of the perivisceral cavity. By THE CCELOM AND MBSODERM 237

this means the pleural cavities (already separated from the pericardial by the transverse septum) are separated from the remainder of the perivisceral cavity. But it is important to note that the pleural cavities of the mammal are formed in an altogether different manner from those of birds.

Figure 126. Transverse section through the trunk of a bird showing the relations of the caelom.

as, air—sac; as, oblique septum; pc, pleural cavity; v, vertebra; other letters as Fig. 125.

Anterior to the diaphragm in mammals therefore there are three ctelomic spaces: the pericardial and the two pleural cavities. The diaphragm contains striped myotomic muscles innervated by the phrenic nerves. Originally the heart and the transverse septum were far forward in the body in the region of the neck, from the spinal nerves of which the phrenic nerve arises. Later in development the 238 ‘ ,COMP._KRATlVB ZOOLOGY or cuonnarns

“heart. and transverse septum bwome shifted backwards, with the

‘result that the phrenic nerves have long courses to run from their

‘origin in the neck to the diaphragm. The diaphragm is pierced by the

gut, aorta, and the inferior vena cava. , In many mammals, the dorsal mesentery supporting the stomach ‘from the roof of the perivisceral cavity becomes drawn out into a

‘double sheet of ccelomic epithelium, which overlaps the transverse colon of the large intestine on the ventral side. Eventually this sheet ,

may fuse with the mesentery suspending the large intestine (mesocolon). This extension, which is called the great omentum, brings about an increase in size of the omental sac, on the wall of which fat is often deposited.

The Miillerian ducts or oviducts and the uterus are suspended by mesenteries, called mesometria, and which are of interest in determining the relation of the implanted blastocyst to the walls of the uterus. The mesentery supporting the testis is called the mesorchium, that supporting the ovary the mesovarium.

Ccelomic cavities are always lined by mesodermal tissue. In Amplu'o.x'u.r, the ecelomic cavities of the somites, when they arise, are in open communication with the gut, and are hence known as entere00:18. In higher forms. the co.-lomic cavities appear as splits in the mesoderm, without communicating with the gut. These cavities are known as sclrimctels. The method of origin is not of much importance, but it is important to realise that all cavities which arise, either as subdivisions of. or outgrowths from, enteroctrls and schizoccels, are ctt:lomic. So the cavities of the pericardium, of the kidneytubules, of the Wolllian and Miillcrian ducts, of the gonads in Amplu'oxu.t~, are coelomic. On the other hand, no cavity is ctnlomic which does not arise in this way. The cm itics of the blood-vessels are not cu.-lomie. although their walls are composed of mesodermal tissue. Cavities lined by tissue other than mesoderm, such as those of the atrium of .-tmpIu'uxu.r. nerve-tube, nephridia, amnion, gut, or blastoctrl, are, of course. not co:lomie.

The coelomic cavities originally probably opened to the outside in each segment for the purpose of freeing the germ-cells. Something like this happens in Ant]!/t1'u.\‘u.$‘, where also the left anterior headcavity opens into the preoral pit. Rarely, in higher forms, the cavities of the prcmandibular somites may open into the hypophysis. Comparable “proboscis pores“ (see p. 311) occur in Balarzoglossus and its allies, ‘and in the Echinodermata. In the Craniata, the splanchnocml may communicate with the outside, through the genital pores via the cloaca as In Pcfromyzori. through the abdominal pores as in

Scyllium, or through the Miillerian ducts. Mention must be made of the fact that in some cases the electric THE CCBLOH AND Miisonsnu 239 difference tafpoteiitial which ‘always accompanies muscular activity has been specially increased, with the result that some muscles have been converted into “electric organs”. It is interesting to notice that

Figure 127. Longitudinal scction_through the trunk of a mammalian embryo, showing the relations of the ceelom and viscera.

a, anus; au, auricle of heart; [2, bladder (continuous with allantois); bd, bileduct; d, diaphragm; 9, liver; gb, gall-bladder; i‘, intestine; In, lung; m, metanephric kidney; _ae, oesophagus; p, pancreas; pl, pleural ecelomie cavity; pn, penis; pr, pericardial ccnlomic cavity; r, rectum; sc, spinal cord; sm, sternum ; sp, perivisceral splanehnocml; st, stomach; i, tail; ta, truneus arteriosus; (Ii, thyroid; rm, thymus; tr, trachea; Is, testis; u, ureter; uo, opening of urethra; v, ventricle of heart; vc, vertebral column; vd, vas deferens.

while in Raia it is the somatic (myotornic) muscles in the region of the tail that have become thus modiﬁed, in T orpcdo it is the visceral

muscles derived from the visceral arches. The first three pairs of somites (in the Craniates) are small and 240 .COMPARATlVB ZOOLOGY or crronnxrss

ﬁve rise to the extrinsic eye-muscles. From the fact that they are situated in front of the car, they are known as prootic somites, and their development is described in Chapter XXVIII. The myotomes which are produced from the next posterior (or metotic) somites are divided by the gill-slits into dorsal and ventral portions, the latter portion forming the hypoglossal muscles.

In Amphioxus, each myotome is a plate of muscle extending from near the middorsal to the midventral line, on one side of the body. When seen from the side, each myotome is bent into the shape of a V with the apex pointing forwards. The Silurian fossil Jamoytius showed a similar condition of the myotomes. In Petromyzan, the myotomes behind the region of the gill-slits are like those of Amphioxus; only the septa are slightly more bent so that each myotome seen from the side is in the form of a W. In ﬁsh and all higher forms, however, each myotome behind the gill-slits is divided into two by a horizontal partition or septum. It is in this septum that the “true” or dorsal ribs are formed. The myotomes are then represented by dorsal or epaxonic, and by ventral or hypaxonic muscles.

The muscles of the fins in Craniates are formed from “musclebuds”, which are nipped off from the myotomes.

In the T etrapods, the epaxonic muscles are much reduced, while the hypaxonic muscles assume greater importance. The muscles of the paired ﬁns and limbs are derived from the hypaxonic portions of the myotomes. Apart from the latter, the great development of which in T etrapods is connected with the greater strength necessary for locomotion on dry land, the hypaxonic portions of the myotomes also give rise to the intcrcostal muscles in the thorax, and the muscles of the abdominal wall.

The simple segmental arrangement of the myotomes which is so characteristic of Amp/u'0.\'zJs and lower Craniates tends to be obscured and lost in the Tetrapods.

With regard to the dermal musculature, the muscles attached to the hair—folliclcs (arrectores pili‘) are smooth and innervated by sympathetic fibres. The panniculus carnosus muscles are derived from the striped muscles of the trunk and are therefore innervated by ventral nerves. The platysma muscles, and the muscles of expression are derived from the striped muscles of the 2nd visceral arch. and consequently are innerxatcd by the facial nerve.

LITERATURE

NIAURER. F. Die lintwrcltlung dcs Musltclsystems und der elektrischen Organe. I1:-rtm',e’s Homlbm-I: der verg. und exp. Entwicklungslehre der Wfrbt'Irwrc. Part 3. Fischer, Jena, 1906.

VAN WIJHE, J. W. Ueber die rllcm2:/ermsegnieme und die Emwicklung der Nerven des Selaclrierkopjes. de Waal, Groningen, 1915. CHAPTER xx THE SKULL

THE skull consists of the protective case round the brain (neurocranium) and of the skeletal supports of the jaws (splanchnocranium). It is formed in all chordates from Petromyzon upwards (whence the name Craniate) and is always cartilaginous at ﬁrst. In Cyclostomes and Selachians the skull remains cartilaginous throughout life, but in other forms this cartilaginous chondrocranium becomes more or less thoroughly replaced by cartilage-bone, and membrane-bones are added to it. The chrondrocrania of the various vertebrates may be compared with one another on the one hand, and on the other, the bony skulls may similarly be compared.

CARTILAGINOUS SKULL. The typical structure of the ehondrocranium may now be considered. The floor of the neurocranium is formed of paired trabecula: in front (enclosing the hypophysial fenestra between them) and of paired parachordals (on each side of the notochord) behind. The auditory capsules are firmly anchored on to the parachordals on each side. Behind the auditory capsules the paired occipital arches rise up from the parachordals, and become attached to the hind part of the auditory capsule. In so doing they enclose a fenestra (metotica) through which the glossopharyngeal and vagus nerves and the internal jugular vein pass. In front of the auditory capsule paired pillars rise up from the parachordals and join on to the orbital cartilages. The latter form the sides of the brain-case in front of the auditory capsules, and the pillars just mentioned are the pila: antoticze. The pila antotica joins the front part of the auditory capsule of its own side, and in so doing encloses the trigeminal, facial, and abduccns nerves in a fenestra prootica. In front of the pila antotica the optic, oculomotor, and trochlear nerves, and the pituitary vein pass.

The olfactory or nasal capsules are formed at the front of the skull. They are separated from one another by the inter-nasal septum formed from the trabecula: which anteriorly join together in the middle line. The nasal capsule is separated from the orbit of its side by the lamina orbito-nasalis, which reaches from the trabecula to the orbital cartilage. The roof is often very incomplete, and may be formed only in front and behind. That part of the roof which connects the two auditory capsules is called the tectum synoticum.

9—v.z. 241 242 comunnxvn ZOOLDGY on cuonnuns The relations of the trabecula: are of importance, for the hypophysial fenestra which they enclose between them also serves for the

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admission of the internal carotid arteries to the brain-case. In those cases where the trabecula: are wide apart from one another, as in the frog, the skull is said to be platytrabic (or platybasic); in others, such as the trout. the trabeculze are close to one another and fuse in the middle line, and this condition is called tropitrabic (or tropibasic). The splanchnocranium consists of the pterygo-quadrate of the mu sxuu. 243

upper jaw, Meckel’s cartilage of the lower jaw, the hyomandibula and ceratohyal in the hyoid arch, and the cartilages of the branchial arches.

D dbll btp Od

Figure 129. Diagram of a schematic chondrocranium seen from the left side, and showing the relations of the car-tilages to the principal nerves and blood-vessels.

This diagram does not represent any particular form, but shows the type on which nearly all skulls are built. abn, abducens nerve; ac, auditory capsu e; at, ala temporalis; btp, basal process; hf, hyomandibular facial nerve; Ir, internal carotid artery; jv, jugular vein; Ion. lamina orbitonasalis; o, occipital arch; oa, orbital artery; ac, olfactory capsule; ocn, oculomotor nerve; oln, olfactory nerve; an, optic nerve; op, otic process; pa, ascending process; pf, palatine facial nerve; pp, prla antotrca; pq, pterygo-quadrate; pv, pituitary vein; rop, profundus ophthalmicus nerve; to, trabecula; vn, vagus nerve.

One of the most important features of a skull is the method by which the splanchnocranium is attached to the neurocranium. The hyomandibula is always ﬁrmly attached to the auditory capsule, but with regard to the jaws, there are three types of attachment:

Amphistylic, as in the dogfrsh Hexanchus, and in Cladoselache. Here the upper jaw has an otic process which abuts against the

auditory capsule, and in addition the hyomandibula serves to sling the upper jaw from the neurocranium.

Hyostylic, as in Scyllium. The upper jaw nowhere touches the auditory capsule, and is suspended by the hyomandibula and by ligaments.

Autostylic, as in Ceratodus and higher vertebrates. The hyomandibula takes no share in the suspension of the upper jaw, which is attached to the neurocranium by its own processes.

The processes of attachment of the upper jaw in autostylic skulls are typically three in number. The otic process abuts against the auditory capsule, and lies in front of the main branch of the facial The autostylic vertebrates above Ceratodus are terrestrial animals

may or may not join, and lies between the ophthalmic (V1) and the maxillary (V2) branches of the trigeminal nerves.

Figure 130. The relations of the splanchnocranium to the neurocranium.

A, Hexanchus, amphistylic. B D, chondrocraniurn of the shrew, illustrating the mammalian type. V1 V2, maxillary branch of trigeminal nerve; V3, mandibular branch of trigeminal nerve; Vllp, facial nerve; VIM, hyomandibular facial nerve. ac, auditory capsule; ap, temporalis; bp, basal process; ch (articular); Me, Meekel's cartilage

Scyllmm, hyostylic. C, chondrocranium of Ceratodus, autostylic. profundus (ophthalmic) nervepalatine ascending process; at, ala hm, hyomandibula; 1', incus (quadrate); m, malleus

otic protwss; pq, pterygo-quadrate; sp, stvloid process.

ing process rises up on the outside of the pila antotica with which it

ceratohyal °

nerve; the basal process abuts against the ﬂoor of the neurocranium, and lies above and in front of the palatine nerve (facial);

the ascendCOMPARATIVE ZOOLOGY OP CI-IORDATES

244 ran SKULL 245

which no longer use the gill-slits for respiratory purposes in the adult. So the spiracular cleft gives rise to the tympanic cavity and Eustachian tube, and the hyomandibula becomes the columella auris.

This description of the typical chondrocranium can be applied to

Figure 131. Osteolepisz dorsal view of skull showing lateral-line canals. It is probable that the bones here conventionally labelled n, f, pa, and ppa, should read f; pa, ppa, and es respectively.

Explanation of lettering for Figs. 131 to 149:

al, alisphenoid; art, articular; bo, basioccipital; bpp, basiptcrygoid process; bs, basisphcnoid; c, canine; d, dentary; en, extemal nostril; co, exoccipttal; ep, epiptcrygoid; cs, extrascapular; f, frontal; fm, foramen magnum; 1', incisor; it, intertemporal; j, jugal; I, lachrymal; ls, lEllCl‘0.‘-.phCl'l0ld; m, maxilla; mp, mastoid process; n, nasal; o, orbit; ac, occipital condyle; rm, OUC notch; 00, opisthotic; op, opercular; as, orbitosphenoid; p4, fourth premolar; pa, parietal; pe, periotic; pf, postfrontal; pi, pineal foramcn; pl, palannc: pm, prcmaxilla; pa, postorbital; pop, preopercular; pp, paroccipital process; ppa, postpanctal; pr, prootlc; pr;f, prefrontal; ps, parasphenoicl; psp, prcsphenoid; pt, ptcrygoid; pv, prcvomer; q, quadrate; qj, quadratojugal; s, squamosal; sm, septomaxilla; sn spiracular notch; so, supraoccipital; st, supratcmporal; r, tabular; tb, tympanic bulla; tp, transpalatinc; v, vomer.

most groups of vertebrates. In the mammals an important modiﬁcation occurs in that the ascending process comes to lie between the maxillary (V2) and mandibular (V 3) branches of the trigeminal nerve, and it is usually known as the ala temporalis.

BONY SKULL. Attention may now be turned to the bony skull. The replacing or cartilage-bones are fairly constant throughout the vertebrate series. In the neurocranium they surround the brain, the 24.6 comrsnuxva zoonoev or cnonnnas

olfactory and ‘auditory capsules; while in the splanchnoeranium they form the main skeletal supports. The dermal or membranebones form a covering just beneath the skin, and in certain regions they line the mouth-cavity. The external covering of membranebones is primitively complete, as in Osteolepid ﬁsh, and several of them are traversed by the canals of the lateral-line system. In these forms, the only openings in the roof of the skull are the orbits, the chinks through which the spiracles opened, and the median pineal

pm

P0

Sort.ppaLP‘1'7St ‘ll

Figure 132. Stegocephalia (Loxmmna): dorsal view of a skull, showing the course of the lateral-line canals. (Drawn from a cast.)

foramcn which in fish is now held to lie between the parietal bones. In the higher bony fish or Teleostei, it is common to ﬁnd that some of the rectus eye-muscles pass back into a tunnel beneath the brainease; the so-called eye-muscle-canal or myodome.

In the most primitive amphibia, the membrane-bones also make a complete covering to the skull, for which reason these animals are called Stegocephalia. Many of these bones can be identiﬁed with those of Osteolepid ﬁsh because they are grooved by the lateral-line ‘ran sxuu. 247

system. The only openings in the roof of the skull in the Stagecephalia are the nostrils, the orbits, and the median pineal foramen which in these animals lies between the parietal bones. The spiracles are, of course, closed in land-vertebrates, but the position of their former openings is indicated by a notch in the hind border of the roof on each side.

In land-vertebrates the skull and vertebral column are separated by a joint, which allows the head to move. The articular facets belonging to the skull which take part in this joint are the condyles. In Stegocephalia there are three such condyles, formed by the two exoccipitals and the basioccipital. In higher forms, as will be seen,

pm

QR

L ll prf ‘ '“

PP‘

Figure 133. Seymouria: dorsal view of a skull. (Drawn from a cast.)

the number of condyles may be reduced to one or to two, according as to whether the exoccipitals or the basioccipital (respectively) drop out of sharing in the joint.

In the most primitive reptiles such as Seymouria, the covering of dermal bones is complete, and differs from the condition of the Stegocephalia only in that there are no grooves for lateral-line canals. As the nature of the roof of the skull is of the greatest importance in regard to classiﬁcation in the reptiles, it is necessary to consider a few of the relations which the membrane-bones bear to underlying structures. The more median membrane-bones, such as the nasals, frontals, and parietals, overlie the brain-case directly, and form its 248

COMPARATIVE ZOOLOGY OF CHORDATES

Figure 134. Left side of a skull of a Chelonian Figure 135. Skull of a Chelonian (7_"estudo) in which_the (Chelone) with a complete temporal roof. temP0T3l T_00f has b<?€ﬂ emafglﬂated fmm behind. thus exposing the auditory capsule.

roof. But the more lateral membranebones of the skullroof, such as the post-orbital, supratemporal, and squamosal lie over the auditory capsules. The auditory capsule, formed by the prootic and opisthotic (cartilage-) bones lies deep beneath the surface of the skull, with the result that between it and the overlying membrane-bones of the skull-roof there is a space. This space is the temporal cavity; it is continuous in front with the orbit or eyeball-space, and posteriorly the temporal cavity opens on the hind face of the skull by the post-temporal fossa. It must be remembered that the word “cavity” is here used to denote a space which is not occupied by bone; it is, however, not hollow, but ﬁlled by the muscles of mastication which actuate the lower jaw. Below, the temporal cavity opens on to the palatine surface of the skull, in front of the auditory capsule, and through this opening the above-mentioned muscles pass. The roof run sxuu. 249

of the temporal region typically has three borders: an anterior border which is also the hind border of the orbit; a lower border, reaching from the maxilla to the quadrate; and a posterior border which is also the upper border of the post-temporal fossa.

The most primitive reptiles or Cotylosaurs, of which Seymouria is an example, are characterised by skulls of this type, in which the temporal cavity is completely roofed over; a condition inherited from the Stegocephalian ancestors.

In the Chelonia probably the skull was primitively of this kind also, and Clzelone is a good example of a skull with a temporal cavity completely roofed over, opening behind by a post-temporal l‘ossa.* In other forms of tortoises and turtles, however, the roof over the temporal cavity becomes reduced by a process known as emargination. The skull-roof becomes as it were eaten away from the edge, and this reduction may affect the hind border or the lower border of the roof of the temporal region, or both. When reduction by emargination has taken place, the prootic and opisthotic bones of the auditory capsule become visible from the dorsal side of the skull. It is important to notice that in emargination there is no perforation of the skull-roof.

It is common to ﬁnd the Cotylosaurs and the Chelonia grouped together as Anapsida, since they have skulls completely roofed-over or sometimes emarginated, but never perforated as regards the roof by apertures other than the orbits and nostrils. These forms usually have three condyles.

The remaining vertebrates are characterised by the fact that the roof of the skull in the temporal region has been perforated. with the result that windows are formed, completely surrounded by bone, and opening into the temporal cavity. A window of this kind is called a temporal fossa or vacuity, and it enables the muscles of mastication to become enlarged. Through the window the auditory capsule is visible. It must be clearly understood that a temporal fossa is only a perforation in the roof of the temporal cavity; it is not an opening into the brain-case.

Some reptiles have a single temporal fossa on each side. Others have a pair on each side, for which reason they are called the Diapsida. The Diapsida have a superior and an inferior temporal fossa, and these fossa: are separated from the orbit by the postorbital bar (usually formed by the post-frontal and post-orbital bones); they are separated from the post-temporal fossa by the postI

“" It should be mentioned that some authorities prefer to regard the complete rooﬁng of Chelone as secondarily developed. This is immaterial for the present purpose, which aims only at pointing out the typical relations of the temporal region of the skull.

9‘ Figure 136. Skull of a Cotylosaur (Captorhinus), Anapsid type, with the complete temporal roof.

Figure 137. Skull of Ichthyosaurus, Parapsid type, with the temporal roof perforated by a superior temporal fossa. Figure 138. Skull of Varanus, Parapsid type with the lower temporal bar emarginated from below.

Figure 139. Skull of Sphenodon, Diapsid type with the temporal roof perforated by an upper and a lower temporal fossa.

COMPARATIVE ZOOLOGY OF CHORDATES rm: sxuu. 251

temporal bar (supratemporal and squamosal bones); and they are separated from one another by the superior temporal bar (postorbital and squamosal bones). The superior temporal fossa is bordered above by the parietal bone; the inferior temporal fossa is bordered below by the inferior temporal bar (jugal, quadrato-jugal, and squamosal bones).

The Diapsida include the Rhynchocephalia of which Sphenodon is an example, the Crocodilia, the Dinosauria, the Pterosauria, and the birds. In the latter, however, the post-orbital and temporal bars have been broken, with the result that the temporal fossw can no longer be clearly recognised. It can nevertheless be seen that the bird's skull must have been derived from a Diapsid type which had the typical two temporal fossae. In the primitive crocodiles, in the Pterosaurs, Dinosaurs, and birds, there is also a prelachrymal fossa on each side, between the orbit and the nostril. The condyle is usually single in the Diapsida.

The remaining reptiles have a single temporal fossa on each side,

C“ P L L]

Figure 140. Skull of a bird (C'r)lumba).

but whereas in some this would seem to be the superior temporal fossa, in others it represents the inferior temporal fossa of Diapsida.

Forms with a single inferior temporal fossa on each side are called Synapsida, including the Theromorph reptiles and the mammals. The inferior temporal fossa is primitively bounded above by the post-orbital and squamosal bones. In the higher forms, however, it often happens that the post-orbital and squamosal bones no longer touch one another. The result of this is that the inferior temporal fossa now extends up between them and is bordered above by the parietal bone. From the mere fact that it touches the parietal it must not be mistaken for a superior temporal fossa. This enlarged type of inferior temporal fossa is present in the higher Theromorph 252

reptiles, and in the mammals. A fossa of this type is also found in the Sauropterygia, or Plesiosaurs. Here again, although the fossa is bordered by the parietal, it is probably an inferior temporal fossa which has extended in the manner just described. For this reason,

COMPARATIVE ZOOLOGY OF CHORDATBS

Figure l4l. Skull of a primitiye Theromorph reptile (ll/Iycterosaurus), Synapsid type, with the temporal roof perforated by an inferior temporal fossa.

Figure I42. Skull of a late Theromorph reptile (Cynognathus), Synapsid type, with an inferior temporal fossa which has extended upwards and is bordered by the parietal owing to the separation of the post-frontal from the squamosal. (Drawn from a cast.)

Figure 143. Skull of a dog.

Figure 144. Skull of a Primate (Chimpanzee), showing the complete separation of the

the Sauropterygia are usually classed as Synaptosauria, close to the Synapsida. Synapsida usually have two condyles.

The Parapsida have a single superior temporal fossa on each side, lying above the post-orbital and squamosal bones, and the supratemporal bone appears to have been retained. To this group belong

orbit from the temporal fossa. -ma sxuu. 253

the Iehthyosaurs and the Squamata, which latter consist of the Lacertilia and Ophidia. In the Laeertilia, the bar beneath the lateral temporal fossa has been much reduced by emargination from below.‘ The result of this is that there is very little rooﬁng left over the temporal region, and the quadrate, which still retains the otic process abutting against the paroccipital process of the auditory capsule (see p. 87), becomes uncovered and loose. The quadrate is therefore capable of movement relatively to the squamosal and to the braincase. This condition, which is called streptostylic, is associated with the fact that the upper jaw can move relatively to the brain-case, which arrangement enables the animal to open its mouth with a gape wider than would otherwise be possible.

An extreme case of the streptostylic condition is found in the Ophidia or snakes. Here the post-orbital bar and the temporal bar are completely broken down, so that the temporal region is uncovered. The quadrate has lost its connexion with the auditory capsule, and is only indirectly articulated with it by the intermediary of the squamosal. When a snake opens its mouth the lower jaw drops and the quadrate moves forward. This movement of the quadrate is imparted to the pterygoid and transpalatine bones, which, moving forward in their turn, cause the maxilla and associated bones to rotate upwards. In some snakes such as the viper, this process of rotation of the maxilla is especially interesting, for the maxilla carries the long teeth which are modiﬁed into poison-fangs. When the mouth is open these poison-fangs are made to project forwards out of the mouth ready for “striking”; whereas in the normal position of rest with the jaws closed the fangs extend back parallel to and beneath the roof of the mouth.

Streptostylic skulls are also found in the birds, and especially in the parrots. Here the upper beak is freely movable relatively to the brain-case. Some of the Dinosaurs also had streptostylic skulls.

When the quadrate is ﬁxed, and the upper jaw is incapable of separate movement (as in Splzenodon, crocodiles, and mammals, for instance), the skull is described as monimostylic.

In many Theromorph reptiles, as in mammals, it is common for the post-orbital bar to disappear, and the temporal fossa then becomes confluent with the orbit. In Ornithorhynclzus, for example, the temporal fossa has extended upwards in the manner described above in other Synapsida, and its upper border is formed by the parietal. It is bounded behind by the squamosal, below by the squamosal and jugal (forming the zygomatic arch), and in front it has no border since it is continent with the orbit. Behind, the

"_ Some authorities prefer to regard the Lacertilia as derived from Diapsida which have lost the inferior temporal bar. 254 COMPARATIVE zoonoav or CHORDATES

temporal fossa of Ornithorhyncus communicates with a small posttemporal fossa between the squamosal and the auditory capsule (periotic bone) and which opens on the hind face of the skull. This is the last appearance of the post-temporal fossa, for in higher mammals it is obliterated, as, for instance, in the dog.

Figure 145. Left side view of the skull of a snake (puff adder) showing

the streptostylic condition of the jaws. A, with the mouth closed; B, with the mouth open.

In the higher Primates including man, the post-orbital bar not only persists but actually extends inwards, forming a complete partition between the orbit and the temporal fossa. It may be mentioned that the alisphenoid bone of the mammal is an ossiﬁcation of the ala temporalis, which corresponds roughly to the ascending process of the pterygo-quadrate of the reptile. The mammalian alisphenoid therefore represents the reptilian epipterygoid, both ran SKULL 255

being really parts of the splanchnocranium. It follows that the socalled “alisphenoids" of ﬁsh, reptiles, and birds, which are ossi. iications of the primitive wall of the brain-case, have nothing in common with the mammalian alisphenoid. Their proper name is laterosphenoid. In birds as in mammals, the brain has undergone great development and enlargement, and so it happens that in the bony skull certain bones come to form part of the wall of the braincase although primitively they had nothing to do with it. This applies to the mammalian alisphenoid, and to the squamosal in birds and mammals.

Primitive forms have a large number of bones on the palatal surface of the skull. The pterygoids. of which the ﬁsh have three on each side, become more and more reduced in the higher forms. The transpalatine of amphibia and reptiles corresponds to the ectopterygoid of the ﬁsh, and it disappears in birds and mammals. In the

Figure 146. Hind view of the skull Figure 147. Hind view of the skull

of Chelone, showing the rela- of Ornithorhynchus, showing the tions of the post-temporal fossa small post-temporal fossa, indi(through which an arrow is cated by an arrow.

passed into the orbit).

Tetrapods the pterygoid is a membrane-bone, underlying the pterygo-quadrate cartilage.

The articulation of the pterygoid with the basipterygoid process of the basisphenoid, as for instance in Varanus, corresponds roughly to the connexion between the pterygo-quadrate cartilage and the brain-case by the basal process.

In crocodiles, some Theromorph reptiles and in mammals, the maxilla‘. and palatines have shelf-like extensions which meet in the middle line beneath the original roof of the mouth. These shelves are the false palate, and between it and the original roof of the mouth (formed by the vomer and mesethmoid bones) is the nasal passage leading from the external nostrils to the secondary choanae. The prevomers of the lower vertebrates are represented by the 256 comnnurva zoonoov or cnonmurss

“dumb-bell-shaped bone" of Ornithorhynchus. The mammalian vomer represents the anterior part of the parasphenoid of lower forms.

In the lower jaw, Meckel’s cartilage ossiﬁes as the articular, and dermal bones are formed round it. In the lower vertebrates these dermal bones are numerous, consisting in the Stegocephalia, for instance, of the dentary, angular, supra-angular, splenial, and three coronoid bones. The number of these bones becomes reduced in

Figtire I48. Palatal view of a skull Figure 149. Palatal view of a skull of l m'mm.t'. of a dog, showing the false palate. An arrow is passed through the nasal passage.

higher forms. The two halves of the lowerjaw in snakes are separate, and their front ends can he moved wide apart. This allows the mouth to be opened very wide indeed. so that the snake is capable of swallowing relatively enormous prey. In some Laeertilia such as Varanus and in the extinct Mosasauria, there is a joint on each side of the lower jaw. These joints enable the space between the two halves of the lower jaw to be widened, and large prey to be swallowed.

In crocodiles, and in the fossil bird Arcluzopteryx, the lower jaw ma sxuu. 257

is characterised by being pierced by a foramen on each side. Among the Dinosauria, the Predentata are peculiar in possessing a predentary bone, the most anterior in the lower jaw. The lower jaw of the Marsupials is characterised by the fact that the lower edge of the hindmost region of each half is bent inwards, forming the “inﬂected angles”.

In all mammals the lower jaw is peculiar in consisting of a single bone: the dentary. Very interesting stages in the reduction in number of bones are found in the Theromorph reptiles. Cynognathus has a large dentary, while the articular, angular, supra-angular, prearticular, coronoid, and splenial are small. The dentary develops an uprising coronoid process which touches the squamosal, and so takes on the function of articulating the lower on to the upper

Figure 150. Side views of the lower jaws of A, Varanus; B, a dog.

The mammalian lower jaw contains only one home; the dentary. an, angular; ar, articular; c, coronoid; d, dentary; ml, ﬁrst molar; par, supra-angular.

jaw. At the same time the original quadrate-articular articulation (which is present in all lower forms) falls into disuse, and the quadrate becomes small and loose. The next stage is that of the mammals, of which the dog may be taken as an example; and since here the lower jaw consists of the dentary alone, the question arises as to what has happened to the other bones. The quadrate and articular have been intercalated between the columella auris and the tympanic membrane, thus forming part of the chain of three auditory ossicles which is characteristic of mammals. The columella auris ( or hyomandibula), pierced by the stapedial artery, comes to look like a stirrup and is hence called the stapes; the quadrate is now called the incus, and the articular becomes known as the malleus. At the same time the angular becomes converted into the tympanic bulla (also peculiar to mammals) and the supra-angular is represented by 258 COMPARATIVE ZOOLOGY or CHORDATBS ,,

the proeessus Folﬁi; the remaining bones of the Theromorph reptiles have disappeared. It is a striking fact that the mammalian ear is associated with bones which in the ancestors served to form the articulation between the upper and lower jaws. The remarkable change of function which these bones have undergone is, however, less remarkable than would appear at ﬁrst sight, for their essential feature is that they remain articulated to one another, and so are able to transmit the vibrations of sound. The columella auris is pierced by an artery and resembles the stapes in certain lizards and

Figure l5l. Diagrammatic views showing the transition from the reptilian to the mammalian method of articulation of the lower Jaw: A, reptile; B, mammal.

a, angular; art, articular; ca, columella auris; d, dentary; t‘, incus (quadrate); m, malleus (articular); Mr, Mecl-tel’s cartilage: pr, processus Folii (supra-angular); q, quadrate; s, squamosal; sa, supra—angular; st, stapes (columella auris); t, tyrnpanic (angular).

Gymnophiona, and in the latter group of animals it may be connected with the quadrate. There is therefore no radical innovation in the fact that the incus articulates with the stapes. The most remarkable feature of this change is the fact that it was effected without functional discontinuity. There was never a time when, the quadrate and articular having been drawn away into the service of the ear, the lower jaw had no articulation with the upper, because, before this happened. the dentary had already established connexion with the squamosal. This new squamoso-dentary method of articulation, which is peculiar to mammals, was in working order before the quadrate and articular underwent their modification.

LITERATURE

DE BEER, G. R. The Development of the Vertebrate Skull. Clarendon Press, Oxford, 1937. 1943.

THE SKULL

GAUPP. 3- D10 Eﬂtwicldung des Kopfskelettes. Hmiﬁbucli der I/erg, and Exp. Entwickelungslelire der Wi'rbelti'ere. Part 3. Fischer, Jena, 1906.

GOODRICH, E. S. Vertebrata Craniata. Cyclostomes and Fishes. Black, London, 1909.

GREGORY, W. K. Present Status of the Problem of the Origin of the Tetrapoda. Annals of the New York Academy of Sciences. Vol. 26. 1915.

HUXLEY, T. H. Contributions to Morphology. Ichthyopsida. On Ceratodus forsteri. Proceedings of the Zoological Society of London, 1876.

WESTOLL, T. S. The origin of the Tetrapods. Biological Reviews. Vol. 18.

259

WtLLis'roN, S. R. The Osteology of the Reptiles. Harvard Univ. Press, 1925.

Part of Skeleton.

Skull i l

Neuro-_

cranium

Splancliiiocranium

TABLE OF VERTEBRATE BONES

-—u.-jj—.——.-_—-I

M embrane-bones.

Nasal Frontal Parietal Post—l'rontal=- part of Splienotic Lachrymal Sub-orbitals Post-orbital Intertempornl ==- part of pterotic? Supratemporal Squamosal Post-parietal Tabulare Extrnscapular Prevomer Parasphenoid Vomer= part of Parasphenoid Basitemgoral-= part of Parasp enoid Septoniexillary

Premaxille

M axilla

1 until Quadrato-jugal Ectopterygoid -- transpalatine Endopterygoid Pterygoid = Endopterygoid?

Dentary

Predentary

Angular - Ty-mpanie Supra-angular -= Processus Folii

Coronoids

Splemal Briinchiostegnl rays Preopercular Opercular Subopercular

l nteropercular

u-—-1-o— -i

Cartilage- (and tendon-) bones.

Basioccipital Basisphenoid

Presphenoid Exoccipitiil Supraoccipital

Pe_ri'otic

Prootic Opisthotle Epiotic

Mesethinoid Laterosphenoid

Orbitosphenoid Turbinals

Quadrate- lncus

Metapterygpid Epipterygoid

Alisphenoid Articular - M alleus Hyom andibula -- Columella auris - Stitpea

Symplectic

Epihyal

Ceratohyiil Hypohyal

Interhyal

Biisihyal Pharyngobranchiel Epibranchial Ceratobrenchiiil

- Hypobranchial

Biisibranchial

Bones of mixed origin.

-.——-—.:_n--.— :1

Prefrontal

Splienotic Pterotie

Paintine

—-—:

—-u———--—u—Cartiln e from which t e cartilage-bone. or part of the mixed bone ossiﬁes.

Basal plate (Pariichordal) Basal plate (Pnrachordnl) Trabecular plate Occipitel arch Tectum synoticum

Auditory capsule Auditory capsule Post-temporal tendon Trnbecula: internasal septum. and nasal capsule Pila nntotiea Orbital Turbinals

Lamina orbitei naselis Auditory capsule

Auditory capsule

Pterygo-quadrnte Pterygo-quiidrate Proccasus ascendens

Ala temporalis Mecke-l's

Hyoid arch

Briuichinl arch I

Pterygo-quadrate

.... .-i --nu--—--niunnusu-i

_—--. -(Continued on page 260). 260 COMPARATIVE ZOOLOGY or CHORDATES

TABLE or VERTBRATE BONES—caurlnued

Pm of smaum M°mbrma_bom_ i Cm.ila¢o- (iuid tendon-) iCmil_age from which tlio

bones. . Cartilage-bones unify. i Axial uliuletuu Neural arch Buidoml (Vertebral Column, Hcmul arch Biisiveiitrul etc.) Hypoceiitrum Buiventral Plcuioccutruin lnterdorinl and interve_nti'al Radial: Radial: Ribs Costals Appendiculiir skeleton (Limbs. Girdli-ii, and Stemum) l Post-temporal scapula

lJpl'8lCic'l1lhl'UIl1 Corucoid d Scapulo-coracoid

ostc cii rum Precorucoi Cleiihrum llumerus Humerus Cliivicle Radius Radius I Uliia Ulna V Radial:-=Sciiphoid

i lntennedium -w Lunar lilnare - Cunciform

I grrsszztzg. cm

rapezoi I ‘lsjlagrlium nci onn

. Meuiciiimls Metacarpuls Plialanges Phuliingcs

l llium llium lschium lschium

E Pubia Pubis

A Fpipubicm Mﬂfsupldi pipubic

iemur emur Tibia Tibia Fibula Fibula HTlbllliG _ v==Aslral iFn:.l.:!‘ll1'lCdluE'l gains’ I u are- ii ciincum

' ('cntriile== Nuvicular T lindocuiieifoim mm

b iglcsocuiifiifciriii

-ciocuiic orm ' Cuboid l Metatarsal: Mctauirsals l Riidiiils Radials ! Iytemum Siemum

Socsiinioids and patella Tendon:

Dcriiiiil Ilieluliin Liipiduiricliiri i 4 0§le0SCul¢S ' (iustriiliii ‘ CHAPTER XXI

THE VERTEBRAL COLUMN, RIBS, AND STERNUM

THE primitive skeletal stiffening of the body is the notochord. In Amphioxus, this extends to the extreme anterior end of the body; in Petramyzon it does not reach further forwards than the region of the infundibulum, but in this position it persists throughout life. In the remaining vertebrates, the notochord usually disappears in the skull region.

Surrounding the notochord are two sheaths, the so-called elastica interna and the elastica externa. These are of importance in some forms in connexion with the formation of the vertebral column.

Amphioxus has no structures comparable to vertebrae, but they appear ﬁrst in Petromyzon in the form of little paired pegs or struts on each side of the nerve-cord, rising up from the notochord. There are two pairs of these pegs to each segment as a rule. The notochord in Petromyzon is continuous and unconstricted, a primitive feature.

A properly formed vertebral column appears first in the Selachii. Each vertebra is composed of a neural arch formed from a pair of basidorsals, and a pair of basiventrals which in the region of the tail form a hzemal arch. Between them, the basidorsals and basiventrals form the body of the vertebra or centrum, which constricts the notochord and usually obliterates it altogether except between one centrum and the next. Alternating with the basidorsals are the interdorsals, and in some, interventrals are present. The basidorsals and basiventrals perforate the elastica externa and cartilage-cells invade the notochordal sheath. Such centra are called chordal, and they occur in the Selachii, in the sturgeons and in the Dipnoi. In all other forms the vertebra arise outside the notochord and do not invade its sheath. These are called perichordal vertebrae.

The vertebra of the higher bony ﬁsh are compact bony structures obliterating the notochord. Amia is interesting with regard to its vertebral column, for in the region of the tail there are what look like vertebrae with neural and hzemal arches alternating with vertebra: without. Those vertebra: with the neural and hazmal arches are the basidorsals and basiventrals; those without are the interdorsals and interventrals. The neural arches are always formed from basidorsals

and the hzemal arches from basiventrals. 261 262 COMPARATIVE zooroov or cnonmrras

The vertebra are formed from the sclerotome, which is segmented.

The anterior part of the sclerotome in each segment gives rise to the interdorsals and interventrals, while the posterior part produces the

basidorsals and basiventrals. Later it is found that the basidorsals and basiventrals of one segment fuse on to the interdorsals and interventrals of the next posterior segment. The vertebrae are therefore intersegmental in position, which enables the myotomes, which of course are intrasegmental, to be attached to two vertebra.

The most posterior haamal arches are enlarged to form the hypurals which support the ventral lobe of the tail-ﬁn.

Figure 152. Transverse sections through the developing vertebral column of Sm‘!/imn embryos.

A, early stage; B, late stage (in the regron of the tail). bd, basidorsal; by, basiventral; ca. caudal artery; cv, caudal vcm; ec, elastnca externa: ha, hemal arch; hs, ha-mal spine; n, notochord; na, neural arch; nc, nerve-cord; ns, neural spine.

In the most primitive amphibia, the Embolomeri of the Labyrinthodonts, the vertebrae have neural arches and two centra. The anterior centrum of each vertebra is formed from the basiventrals and is called the hypocentrum; the posterior centrum is formed from the interdorsals and interventrals, and is called the pleurocentrum. While in the later amphibia the hypocentrum has been enlarged and the pleurocentrum reduced. in the reptiles, birds, and mammals the opposite has occurred, and the vertebrae of these animals have centra which correspond to pleurocentra. In consequence of this, the htemal arches in amphibia are always attached to the centra themselves; whereas in the amniota. when they occur (mostly in the tail-region), VERTBBRAL COLUMN, runs, AND sraauuu 263 the hzemal arches are attached to separate little elements called

intercentra which represent the hypocentra. These intercentra and ‘

hamal arches in the amniotes are called “chevron-bones"; they are never found in the amphibia. Primitive reptiles like Seymouria and Sphenodon have a complete set of intercentra all the way along the vertebral column, and some primitive mammals (hedgehog; mole) have intercentra in the lumbar region.

The transverse processes are lateral extensions of the vertebrae

bd d "d

n.3.l.dn_

Figure 153. Origin of the vertebral column, A, in Scylliumg B, diagram showing the relations of the vertebral elements to the nerves; C, the vertebral column in the tail-region of Amia; D, the vertebral column

in the Embolomcrous Stegocephalia.

dr, dorsal nerve-root; hc, hypoccntrum; id, interdorsal; iv, intervcntral; m, myotome; pc, pleurocentrum; vr, ventral nerve—root. Other letters as Fig. 152.

from the base of the neural arches. The dorsal (or tubercular) head of the ribs is attached to the transverse process, and in all landvertebrates except the most primitive Stegocephalian amphibia (such as Eogyrinus) the transverse processes of at least one vertebra are attached to the ilia of the pelvic girdle forming the sacrum. The sacrum is of course not formed in animals which do not possess hind limbs.

The first vertebra in amphibia is modiﬁed to carry the head, and the vertebral column (which in ﬁsh is divisible only into trunk- and 264 COMPARATIVE ZOOLOGY or cnonnuss

tail-regions) is now divisible into regions corresponding to neck, thorax, sacrum, and tail. In the amniotes the ﬁrst vertebra (the atlas) becomes detached from its centrum, which becomes attached to the second vertebra or axis, and forms its odontoid peg. There are therefore two vertebra: specially modiﬁed in connexion with the neck,

hc’ PC

Figure 154. Vertebral columns of A. a bony ﬁsh (runny); B, crocodile (in the tall-region); C‘, Splzcnodan (trunk region).

r, centrum; ch. chevron-bone; ha. hzemal arch; I_2c, hypocentrum; na, neural arch; pr, pleurocentrum; p:,, prczygapophysts; r, nb; rp, transverse process.

and a variable number of normal cervical vertebrze which differ from the thoracic in that their ribs are short and do not reach the sternum. The vertebra: between the thoracic (whose ribs reach the sternum) and the sacral are the lumbar. In primitive forms the sacrum aﬂ‘ects only one vertebra, to the ribs or transverse processes of which the vaarennan COLUMN, rues, AND STERNUM 265

ilia are attached. In higher forms, and especially in birds, there are several sacral vertebrae.

The vertebra: of land-animals bear facets by means of which they articulate with one another, and so enable the vertebral column to bend with considerable ﬂexibility without diminishing its strength. These facets are the pre-and post-zygapophyses. In some groups such as the lizard and snakes, additional facets may be developed. The faces of the centra are either ﬁat or slightly concave or convex, but in the birds a special saddle-like shape has been developed, which allows of very great ﬂexibility.

In the mammals, the number of cervical vertebrae is seven in all

3'12 E/_..m. la,’ Wt: .,_,,,:. OP by I ‘

hi

P3 T11

Figure 155. View of the anterior region of the vertebral column of the crocodile seen from the left side.

c2, centrum of the 2nd or axis vertebra; hl, hypocentrum of the 1st or atlas vertebra; nl, neural arch of the lst or atlas vertebia: n2, neural arch of the 2nd or axis vertebra; rip. odontoid peg, or pleuroeentrum of the atlas vertebra which has become attached to the axis vertebra; pa, proatlas; rl, 2, 3, ribs of the lst to 3rd vertebrae; v3, 4, 3rd and 4th vertebrae.

species with only three exceptions. These are the Edentates Bradypus which has nine, and a species of Cholaepus which has six or seven, and the Sirenian Manatus which has six.

Ribs are extensions of the basiventrals, and they may be of two kinds. Those which pass just on the outside of the splanchnocarlic cavity are pleural or ventral ribs, and they occur in Dipnoi. “True” or dorsal ribs pass in the horizontal septum which separates the rnyotomes into dorsal and ventral portions, and they occur in 266 COMPARATIVE ZOOLOGY or CHORDATES

Selachii and in the Tetrapods. Both kinds of ribs are present in Palyjiterus and some Teleosts. ' In the land-vertebrates, the ribs primitively articulate with the

vertebrae by a broad head which touches the centrum and the neural ‘

arch. These holocephalous ribs as they are termed are present in Labyrinthodonts, Cotylosauria, and Sphenodon. Later, that portion of the head which touches the centrum (capitulum) became distinct from that which abuts against the transverse process (tuberculum), by the reduction of the intervening part of the head. In this way, the typical double-headed or dichocephalous ribs arose. Between the two heads of the rib and the vertebra there is a canal through which

Figure 156. Dingramshowing the relations of dorsal (“true") and ventral ribs, as seen in transverse section.

c, centrurn of vertebra; co, cu:lom_; dr, dorsal rib; e, epaxonic muscles; g, gut; Ii, hypaxomc muscles; ns, neural spine; vr, ventral rib.

the vertebral artery passes; and this vertebrarterial canal is conspicuous in the cervical vertebra: on to which the cervical ribs are usually fused.

In many forms. the articular heads of the ribs are degenerate and either the capitulum or the tuberculum may be lost. This secondary single-headed condition must be distinguished from the primitive holocephalous type.

In the Chelonia, the ribs are expanded into broad flat plates which touch one another and are fused to the dermal bones (osteoscutes) to form the carapace. In Splzenodon, crocodiles and in birds the ribs bear uncinate processes. which extend backwards and overlap the next posterior rib. In many cases, the ribs are in two portions: a dorsal or vertebral. and a ventral or sternal portion. The hindmost ribs do not usually reach the sternum, and they are known as venrsanu coumn, runs, AND STBRNUM 267

ﬂoating ribs. Primitively, alltthe vertebrae as far back as the middle of the tail bore ribs. In higher forms they do not extend behind the sacrum.

'I'he sternum ﬁrst appears in Amphibia. It arises from paired rudiments of cartilage which may become replaced by cartilage-bone. In the Amphibia which are alive today, the sternum has no connexion with the ribs. The sternum in the Amniotes is however connected with the ribs, and this was probably the condition in the Stegocephalia also. The sternum is also usually in contact with the coracoids and clavicles. In the mammals, the sternum is often broken into a number of pieces or sternebrae. In the birds (with the exception of the Struthiones: ostrich and its allies) the sternum bears a median projection forming the “keel” or carina to which the ﬂight muscles are attached. Analogous but not homologous keels are developed on the sterna of Pterosaurs and bats.

Overlying the sternum on the ventral side there is in many forms a dermal bone, the interclavicle. It is present in the Stegocephalia but has been lost in the living amphibia. Among the reptiles, it is present in all except the snakes. In birds it is apparently absent, unless it is represented by the keel of the sternum. Only the Monotremes preserve the intcrclavicle among the mammals.

LITERATURE

GOODPJCH, E. S. Studies in the Structure and development of Vertebrates. Macmillan, London, 1930. CHAPTER xxu FINS AND LIMBS

THE most primitive chordates relied for their locomotion on the myotomes of the body-wall, which, by contraction on one side and relaxation on the opposite side of the body, can produce the sinuous bendings which pass like waves down the length of the body and propel the organism along. Amphioxu: is in this condition.

Improvement of methods of locomotion is connected with the formation of extensions of the body in the shape of ﬁns. The earliest of these to arise were apparently those which lie in the middle line of the dorsal and ventral surfaces: the so-called median ﬁns. In A mphioxus they are f oreshadowed, but in Petromyzon well-developed median ﬁns are present, supported by cartilaginous radials provided with radial muscles at their base on each side. Fish likewise have median ﬁns, and these show an advance over the conditions in Petromyzon in that the web of the ﬁn is supported by dermal ﬁn-rays in addition to the cartilaginous radials. These ﬁn-rays are horny (ceratotrichia) in the Selachians; bony and jointed (lepidotrichia) in the Teleostomes, and in the Dipnoi they are ﬁbrous and jointed (eamptotrichia). The median ﬁns of the amphibia have neither cartilaginous radials nor dermal ﬁn-rays at all. and in some of them the ﬁns develop and regress according to the season and the breeding period.

In the ﬁsh, in addition to the median ﬁns there appear the two pairs of "paired" ﬁns: a pectoral pair and a pelvic pair.

The method of origin of median ﬁns and paired ﬁns is very similar. In each case a longitudinal fold of skin appears, and into it little “muscle-buds" make their way, having been formed from the rnyotomcs and separated off from them. Cartilaginous radials then appear, and on each side of these, the dermal ﬁn-rays. The ﬁns contain structures derived from several segments of the body, and this is reflected in the number of radial muscles, cartilaginous radials, dermal ﬁn-rays and nerves which the ﬁn contains.

In the most primitive forms, and in early stages of development of other forms. it is common to ﬁnd that the median ﬁns are continuous and form one fold which extends down the dorsal side, round the tail and forwards again on the ventral side. The presence of a

number of separate and discontinuous median ﬁns in many ﬁsh is ~ 253 r-‘ms AND turns :59

therefore probably due to the subdivision of an originally continuous ﬁn.

If the median ﬁn was primitively continuous, it is possible that the paired ﬁns also were originally continuous folds on each side of the body, and that they became subsequently divided into pectoral and pelvic sections. Indeed, this appears to have been the condition in the Silurian fossil Jamoytius. The fact that in some ﬁsh such as Scyllium, there is in early stages of development a continuous series of muscle-buds given oil‘ from all the segments of the trunk would thereby receive an explanation. Later on during development the muscle-buds between the positions of the pectoral and pelvic ﬁns come to nothing.

The most primitive paired ﬁns known are probably those of the

Figure 157. The pectoral ﬁn of Cladoselac/ze, showing the radials (r) projecting parallel to one another and perpendicular to the side of the body (b). (Drawn from a cast.)

fossil Cladoselache, in which they are triangular flaps with the apex pointing outwards and the broad base attached to the side wall of the body. The radials are more or less parallel to one another and stick out at right angles to the side of the body. It is important to notice that the radials are scarcely concentrated at all at their base; in fact the base is the broadest part of the ﬁn. In the body-wall there are some basal cartilages with which the bases of the radials articulate.

The next step in the evolution of the ﬁns was probably the concentration of the radials at the base of the fin. The result of this was that the stalk attaching the ﬁn to the side of the body became narrow, and the ﬁn became free to move in a greater variety of manners. The arrangement of the radials was now in the shape of a fan as in the Osteolepidoti, and the ﬁn itself was in the form of a blunt paddle. The centremost radials formed what may be called the axis 270 COMPARATIVE zoonoov or cnoaones

of the ﬁn, but this is not well marked in primitive forms in which the ﬁn is short. ‘ ,

By a lengthening of the axis a pointed laurel-leaf-shaped ﬁn is arrived at, like that of Ceratadus (the so-called archipterygium). This type of ﬁn is also present in the fossil Pleuracanthus, where it would seem to have evolved independently from that of Ceratodus. The skeleton of the paired ﬁns of the primitive fossil Dipnoi resembles that of the Osteolepidoti.

On the other hand, by a shortening of the axis and reduction of

the radials, the web of the ﬁn comes to be supported mostly by the dermal ﬁn-rays, and this is the condition of the higher bony ﬁsh.

Figure 158. Comparison between the tin of Srmripterus, A, and a pentadactyl limb, B. (A after Gregory.)

r, carpals; co, coracoid: Ii, humerus; mc, metaearpals; p, phalanges; r, radius; ra. radials; s, scapula; u. ulna; w, web of the ﬁn, supported by lepidotrichia. The (in of Sam'I'pIerus IS an example of the blunt paddle-shaped type of ﬁn.

The pectoral and pelvic girdles must have arisen in accordance with the need for a ﬁrm point of attachment of the ﬁns in the wall of the body. The radials at the base of the ﬁn have fused together and grown inwards, and in so doing they may enclose in foramina the nerves supplying the ﬁn. In the pectoral girdle it is usual to ﬁnd a dorsal scapular and a ventral coracoid element; the pelvic girdle is not so well developed. These girdles lie in the body-wall and are not primitively connected with any other part of skeleton.

In the bony ﬁsh, the scapula, coracoid and pelvis ossify as cartilagebones, and in addition. a number of dermal bones arise in connexion with the pectoral girdle. In a primitive bony ﬁsh like Polypterus, these dermal bones are the clavicle, cleithrum, supra-cleithrum, and rms AND Lines 271

the post-stemporal which is attached to the hind part of the skull. This girdle, which is composed of dermal bones, may be called the clavicular girdle, to distinguish it from the other grdle, formed of cartilage or cartilage-bones, to which the term scapular girdle may be applied. The clavicle is present in the sturgeon (Acipenser), but in all higher ﬁsh it is lost. It may seem curious that the pelvic girdle never has any additions of dermal bones to the cartilage-bones of which it is composed. The explanation is that the dermal pectoral girdle originally had no connexion with the pectoral ﬁns. It provides a ﬁrm attachment for the muscles of the body-wall just behind the

Figure 159. The forelimb of Splzenodon: an example of a typical pentadactyl limb with a primitive carpus.

The ﬁgures indicate the ordinal numbers of the digits. c, carpals of the distal row, which are ﬁve in number; ce, centralia; h, humerus; 1', inter-medium; mc, metacarpal; p, phalanges; ps, pisifonn; r, radius; ra, radiale; u, ulna; ul, ulnare.

gill-slits in those forms (the bony ﬁsh) in which the gill-slits are highly developed. The gill-slits occupy a region of perforation and weakness, and they prevent the main mass of the lateral body-wall muscles from becoming attached to the skull. The dermal pectoral girdle, which itself is attached to the skull, gives these muscles something solid to work from. The joining of the scapular and clavicular pectoral girdles is due to the fact that both are situated close behind the gill-slits. Since there are no gill-slits or other source of weakness near the pelvic girdle, the latter has no dermal elements added to it.

From the nature of the water in which they live, the ﬁns of ﬁsh are necessarily more or less like paddles. But it is from such paddles 272 COMPARATIVE ZOOLOGY or caoanuas

(or ichthyopterygia) that the ﬁve-digited or pentadaetyl limb (eheiropterygium) of the Tetrapods or land-vertebrates was evolved. It is interesting to inquire into the question as to which type of tin most probably gave rise to the limb. The most convenient startingpoint is the blunt lobate ﬁn of the Osteolepidoti (and primitive Dipnoi) with a single large radial at its base, and an increasing number of radials arranged fanwise running to the outer border of the ﬁn. In such a form as Sauripterus (one of the Osteolepidoti) the single basal radial of the pectoral ﬁn may perhaps be held to represent the humerus, and the next two correspond to the radius and ulna of the terrestrial fore-limb. In a general way the next radials represent the carpals and metacarpals.

The earliest limbs probably had more than ﬁve ﬁngers, and the

Figure 160. Ventral view of the abdominal ribs or gastralta, and pectoral girdle of Splzenodorr.

cl, clavicle; co. coracoid; g, gastralia; gr, glenoid cavity; ic, inter-clavicle; r, ribs (true); 5, scapula.

number of rows of radials in the distal part of the ﬁns of Sauriprerus is greater than live. But if the pectoral tin of Sauripterus be compared with the arm of a primitive amphibian like Eryops, it is easy to see how the structure of the latter could be derived from that of the former. The evolution of the live-digited, or pentadactyl limb is an adaptation to locomotion on land. During this transformation, the limb-girdles must have become better developed, for an animal in air is relatively heavier than in the water, and the limbs are subjected to greater strains and stresses. At the same time, the girdles of the earliest land-vertebrates closely resemble those of their aquatic ancestors. So in Eogyrinus (fossil Amphibian of the Carboniferous period), the clavicular pectoral girdle is represented by the clavicle, cleithrum, supra-cleithrum and post-temporal, which latter is PINS AND Lines 273

attached to the hind end of the skull, just as in bony ﬁsh. To these is added a median ventral interclavicle. As in all Tetrapods, the scapula (cartilage-bone of scapular girdle) rests on, but is not attached to, the ribs. The pelvic girdle of Eogyrinus is interesting in that the ilium rests on the ribs without fusing with them to form a sacrum. In this respect, the pectoral and pelvic girdles are similar, but in higher forms the ilium becomes ﬁrmly attached to one or more sacral vertebrae. In addition to the ilium, the pelvic girdle contains the pubis and ischium.

In the earliest land-vertebrates, the function of the limbs was not to support the body of the animal but to row it along while its ventral surface rested on the ground. Such movement must have been slow, and improvement came in the reptiles, in which the limbs

Figure 161. Ventral view of the pectoral girdle of Ornitliorhyncluw. cc, epicoracoid (or precoracoid). Other letters as Figure 160.

lift the body off the ground. In them, there was no friction to be overcome between the body and the ground, and the higher the body was lifted, the longer the limbs, the longer the stride and the faster was the pace. In the reptiles the clavicular pectoral girdle is reduced to the clavicle and interclavicle (the cleithrum persists only in some primitive forms), while the scapular girdle usually consists of a dorsal scapula and a ventral coracoid. In the Theromorph reptiles the scapular girdle may have two ventral elements, the coracoid and precoracoid. In the pelvic girdle the ilium becomes attached to the sacral vertebrae, and the ischio-pubic foramen appears between the pubis and ischium. In some Dinosaurs a post-pubis is present, extending back beneath the ischium. In Chelonia, the pectoral and pelvic girdles have a peculiar position in that they lie inside the ribs,

instead of outside them as in other forms. In birds, the pubis rotates '. lo-‘V.z. l'\ wt‘

.| a

ll. » ﬁn" r\‘|\|

274 comammve ZOOLOGY or cnonmtras

baclrwards and domes to lie parallel to and beneath the ' , with which it may to a certain extent fuse. , . ‘ In mammals, the coracoid, precoracoid, and interclavicle

' retained only in the Monotremes. The pelvic girdle of Monotremeé;

‘-Hv,“and of Marsupials is characterised by the presence of a pair of‘

' 1 i 1'1‘,

‘epipubic bones, which support the ventral body-wall. The clavicle‘ istfg

‘ often missing in the higher mammals, and especially those which i

i‘ I

use their limbs for fast running. So the clavicle is absent in the horse,

\ «' l .-... “JD?

Figure 162. Diagrams illustrating the evolution of the limbs of Tetrapods.

A and 13, views of the early stage when the limbs stick out laterally and the ventral surface of the body rests on the ground. C and D, later stage, when the body is lifted oh" the ground. the forearm and shank being vertical, and the limbs projecting to the side. E and F, late stage, when the hind-limb is rotated forwards from the aoetabulum, and the fore-limb rotated backwards from the glenoid cavity; but the hand points forwards and the radius and ulna are crossed.

and it is much reduced in the dog. In the more primitive forms, and those which are specialised for tree-climbing and digging, the clavicle is usually present.

The limbs themselves show interesting modiﬁcations. In the earliest Tetrapods, the limbs stuck straight out at right angles to the side of the body. When the ventral surface of the body became lifted oil‘ the ground, the upper arm and thigh stuck straight out laterally and‘ horizontally; at the elbow and knee there was a right-angle bend, so that the forearm and shank descended vertically to the ground. “ hand and foot extended horizontally away from the body.

~ .

. ‘ 1 runs AND Lmns , i l _ M 275 tlie.wrist"and ankle, therewas another right-angle so‘ that the I ‘rk:

l ‘-J

5

W In the mammals, starting from the condition just described. the“ limbs have undergone a rotation. The hind-limbs have been rotated forwards, so that the thigh runs forwards from the hip-girdle, and parallel with the side of the body, the shank runs downwards, and the foot points forwards again. In the fore-limb, however, the upper arm has been rotated backwards parallel with the side of the body, and the forearm runs downwards. But the hand would point back»wards if the fore-limb had undergone a simple rotation similar to that of the hind-limb (though in the opposite direction). As a matter of fact, the hand points forwards. and this is brought about by a rotation of the wrist through 180° about a vertical axis which coincides with the forearm. So it happens that the forearm is twisted, and the radius runs from the outer side of the elbow to the inner side of the wrist, passing in front of the ulna. which runs from the inner side of the elbow to the outer side of the wrist. This is the typical position (ofpronation) in mammals; most Primates, including man, however, are able to uncross the radius and ulna and so turn the palm of the hand upwards (supination).

It is impossible to go into all the types of limb-structure, but it is interesting to consider the adaptations of limbs to the three great media, viz. to locomotion on land, in the air, and in water.

The ﬁngers and toes of land-living vertebrates above the amphibia end in horny claws which may be modiﬁed into nails or hoofs. When the whole surface of the hand or foot is applied to the ground, as in the human foot, the animal is said to be plantigrade. Other animals,‘ like the dog, rest only the under surface of the ﬁngers and toes on the ground, while the palm of the hand and sole of the foot take no share in bearing the animal’s weight. This is the digitigrade condition. Others again, such as the horse and cow, which rest only on the end joints of the ﬁngers and toes, are unguligrade. The latter form part of the order Ungulata.

The limbs of the horse are specialised for rapid movement on hard ground. Only the 3rd digit is retained, and its extremity is expanded and surrounded by the nail which gives rise to the hoof. The other digits have disappeared, leaving only small vestiges of the metacarpals and metatarsals (of the 2nd and 4th digits) in the form of “splint-bones”. The fossil ancestors of the horse show different stages in this process of reduction of the number of digits, and lead back to normal pentadactyl animals. These odd-toed Ungulates are called Perissodactyls. Curiously enough, a parallel process of reduction in number of digits, and of formation of hoofs consisting of a single digit, went on in a group of animals (all now extinct) quite 276 . COMPARATIVE zoonoov or CI-IORDATBS

independently of the horses: the Thoatheria. This is a very remarkable case of convergence in evolution. ‘

In the “cloven-hoofed” Ungulates or Artiodactyls, the hoof is formed from the end joints of digits 3 and 4, as in cattle, where the mctacarpals and metatarsals of the two digits fuse.

Figure l63. Convergence in the adaptation oflimbs for ﬂight, A, in birds; B, Pterodactyls; C, bats.

cm, carpo—metaearpus; h, humerus; mc, metacarpal ; p, phalanx; r, radius; u, ulna.

Among mammals, limbs with a primitive type of structure are those of the Primates, which preserve all the ﬁve digits. In most Primates, the first digit (thumb or big toe) is capable of touching any or all the remaining digits, i.e., is opposable. This structure enables

’ . ems AND turns 277 the limbito grasp objects ﬁrinly. Apes have this power in feet as well

as, hands, while man only preserves the capacity to oppose the first

digit in his hands. , Three separate and independent groups of vertebrates have ome adapted to life in the air, by the modiﬁcation of the forelimbs into wings. These are the extinct Pterosauria (“ﬂying reptiles"), the birds and the bats. In the Pterosauria, the fourth digit of the hand was enormously elongated, and a web of skin was stretched between it and the side of the body, extending back to the hind-limbs and tail. The bird's wing is built on an altogether different principle, for the wing-surface is made up of a number of feathers inserted on the

‘gﬂ B 00

§ (33000

Figure 164. Convergence in the adaptation of limbs for swimming, in, A lchthyosaurs; B, Plesiosaurs; C, birds (pypnguin); D, mammals (dolphin).

hand and forearm. The skeleton of the fore-limb of the bird shows a reduction in number of digits to three, and the claws at the end of the digits have disappeared except in the young of some birds, such as the ostrich and the Hoatzin. The primitive fossil bird Archwapteryx had well-developed claws.

The wing of the bat is diﬂerent, again, for in it the 2nd, 3rd, 4th, and 5th digits of the hand are much elongated, and support a web of skin which stretches out from the side of the body.

The three types of wings just described form another interesting example of convergent evolution on the part of unrelated animals, but the most striking example is that furnished by the limbs of those land-vertebrates which have subsequently returned to an aquatic mode of life and become adapted to it. The adaptation takes the form of a modiﬁcation of the limbs into ﬂippers or paddles, which 278,_ .,.t‘_:oMrA,tts'r1va. zootocv or V cuonosras ,,

’ supcrﬁctall‘ ‘ 5' may cbme to resemble the «Sr butWh1¢h' 'i i bir;t;ray

their descent from the pentadactyl structure of the laﬁd-vertebratefsivi iimb in their internal structure. This adaptation has taken place at 3,

1 ~lea;st nine separate times, in independent groups. Three of these

3: ‘mammals: the whales, the Sirenia, and the seals. Among the birds, g ..the penguins have modiﬁed the wing into a paddle. In the reptiles, . ',.the turtles (Chelonia), lchthyosaurs, Plesiosaurs, Mosasaurs,

Thalattosuchia, and Thalattosaurs all show the same modiﬁcation of the limbs into paddles, and in several fossils it is possible to trace

' ‘the evolution from normal pentadactyl limbs.

In the more highly modiﬁed of these paddle-like limbs (as in the

‘ whales, for example), it is common to ﬁnd that the number of

phalanges is increased (a condition known as hyperphalangy). In + the broad paddles of Ichthyosaurs, the number of rows of phalanges exceeds ﬁve, producing the condition called hyperdactyly.

The 5th metatarsal bone is an object of interest. Normally this bone is straight, as in the amphibia, the most primitive reptiles (Cotylosauria), the Theromorph and allied reptiles and the mammals. In other groups of reptiles, however, it is peculiar in being hookshaped, and the possessors of this modiﬁed type of 5th metatarsal are: Sphenodon, lizards, tortoises, crocodiles, Dinosaurs, and Pterosaurs. It is worthy of note that these groups all have characters in common in the structure of the heart or of the skull, and are regarded as belonging to the great Sauropsidan branch of the reptiles which culminates in the birds. It is probable that the hook-shaped metatarsal is characteristic of this group, and distinguishes it from the other main stem of reptiles (Theropsida) which evolved in the direction of mammals. The evidence from the 5th metatarsal ﬁts in

~ with that obtained from other sources.

Mention must be made of those animals which have lost their limbs. They have totally disappeared in some of the eels. Among the amphibia, the pelvic limbs and girdle have been lost in the Sirenida, and the worm-like Gymnophiona have lost all the limbs and girdles. Coming to the reptiles, the snakes have lost the girdles and the

pectoral limbs altogether, while only very small vestiges of the pelvic limbs remain. Several families of lizards have independently assumed

‘ the snake-like form by loss of the limbs, such as the slow-worm . (Anguis), some of the Scincidm and the Amphisbanidaz. These

forms furnish an interesting example of convergent evolution.

Among mammals the pelvic girdle and limbs vanish almost completely in the whales (Cetacea) and Sirenia. Cioonmcii, E. S. Vertebmra Craniara, Cyclostames and ﬁsher. Black;-’

ﬁwnmcn, E. S. On the Classiﬁcation of the Reptilia. Proceedings of the

A , . rxynsannyprups y_.,2'/9 ‘t 3 7LITERATURE~ ‘ " ' ’

Al I “J,

London, 1909. ~ 3:

Royal Society, Ser. B, vol. 89, 1916. W

GREGORY, W. K. Present Status of the Problem of the Origin of the

Tetrapoda. Annals of the New York Academy of Sc':'em'es, vol. 26, 1915.

WATSON, D. M. S. The Evolution of the Tctrapod Shoulder Girdle and Forelimb. Journal of Anatomy, vol. 52, 1917.

--——. The Evolution and Origin of the Amphibia. Philosophical Transactions of The Royal Society, Ser. B, vol. 214, 1926. cnxpran xxm THE TAIL

AN extension of the body behind the anus, containing all the chief tissues of the body, is a structure characteristic of chordate animals.

Its original function was to assist the animal in swimming, for it‘

contains myotomes and a portion of the notochord, and so is able to take part in the undulatory movements from side to side which propel the animal forwards through the water. The area of the tail is commonly increased by the formation of a ﬁn in the middle line, in the lower chordates. In Amphioxus, the ﬁn is not very large, but it extends symmetrically from the middorsal and midventral lines of the tail, and tapers to a point behind. This primitive type of tail is called diphycercal. It is present also in the Cyclostomes, where it is supported by cartilaginous radials, and in early stages of develop

ment of other forms.

In Selachians the tail is asymmetrical, for the vertebral column is bent slightly dorsally, and the dorsal (epichordal) lobe of the caudal ﬁn is reduced while the ventral (hypochordal) lobe is increased. The ventral lobe is supported by the elongated hamal arches of the vertebral column, known as the hypurals, and not by separate radials. This type of ﬁn is called heterocercal. In addition to the Selachii, it is present in the sturgeon, the Osteolepidoti and the fossil Dipnoi.

In the higher bony ﬁsh (Tcleosts) the dorsal lobe of the caudal ﬁn is further reduced and the ventral lobe enlarged, with the result that the tail presents an externally symmetrical (usually forked) appearance. Internally. however, the skeleton reveals the fact that this homocercal type of tail is derived from the heterocercal, and the axis can be seen to bend up at the tip. It is found also that during development the homoeercal tail passes through a heterocercal stage.

In other forms the tail tapers symmetrically to a point, and so comes to resemble the diphycercal type. This secondarily simpliﬁed type of tail (shown by Mucrurus, for example) is called gephyrocereal. and is the result of reduction from the heterocercal or homocereal condition. The tail-ﬁn of Gadus is peculiar, for it is merged with the hind portions of the median dorsal and ventral ﬁns. Such

a tail is called pseudocaudal. 280 ‘ma TAIL 231

In Ceratadus, the tail seems to be diphycercal (and the;-gfom primitive), because its ventral lobe is supported by separate radials, and not by hypurals. There is, however, doubt about this, because many of the fossil Dipnoi had heterocercal tails, and if it can be proved that Ceratadus is descended from them, the structure of its tail must be gephyrocercal.

In amphibia, the tail-ﬁns are present in the larval stages, which live in water; but they disappear when the animals come out on land, to grow again in some during the water sojourn of the breeding season. In the Anura (frogs and toads) the tail disappears altogether in the adult terrestrial form; in the Urodeles (newts) it persists as a more or less tubular structure. In the Gymnophiona there is scarcely any tail at all, for the anus is almost at the hind extremity

Figure 165. Skeleton of the tail of the salmon, showing the homocercal pattern of tail-ﬁn characteristic of most Teleost ﬁsh.

Note the up-turned vertebral column. ii, hypurals; I, lepidotrichia; v, vertebra.

of the animal. In land-animals, the tail ceases to have the function which it exercised in the water, and it is often consequently much reduced. Instead of being a posterior prolongation of the body, it has the appearance of being merely an appendage, and it is of use to the animal in the maintenance of its balance, as a covering for the anus and genitalia, and in some cases as a fly-whisk.

Lizards have an interesting modification in that the vertebrae of the tail are cleft transversely, and it is at these points that the tail can be detached from the rest of the body. This faculty (autotomy) is of service to the animal in enabling it to escape from its enemies.

The primitive birds had long tails, with separate vertebrae, as is shown by Arclueopteryx. In living birds the caudal vertebra: are fused together to form the pygostyle, and the tail is itself much reduced. The so-called tail of birds consists of the tail-feathers.

10"‘ 282 .coMr4;nAr1va ZOOLOGY or cnonnaras 1 W

In sonic such as the sea-horse, the chameleon and the American monkeys, the tail is prehensile and capable of ' grasping 1;

' ‘ ‘ ‘ “F

' It is common to ﬁnd that in those vertebrates which have returned

to the water the tail is well developed and expanded into ﬁns,"§5

While superﬁcially not unlike the tails and caudal ﬁns of ﬁsh, they a‘

show in their structure fundamental differences. So in Ichthyosaurus; "‘ the vertebral column passes back into the ventral lobe of the ﬁn; in‘ the whales the two lobes of the caudal ﬁn are not dorsal and ventra but right and left, for the tail is expanded horizontally. In the apes and man the external tail has disappeared altogetherﬂ;

LITERATURE

BARRINGTON, E. J. W. The structure and development of the tail in the

plaice and the cod. Quarterly Journal of Microscopical Science, Vol. 79, 1937. CHAPTER XXIV

THE VASCULAR SYSTEM

THE vascular system is remarkably uniform in its main features in all chordates. It consists essentially of four longitudinal vessels running along the whole length of the animal. Of these, one runs under the gut in the gut-wall (subintestinal vessel); the other three run in the body-wall, and are the dorsal aorta and the paired cardinal veins respectively. The subintestinal vessel connects with the dorsal aorta at the anterior end of the animal by a number of paired vessels which run up round the gut on each side passing in between the gillslits. The anterior prolongations of the dorsal aorta (which is paired in the anterior region) are the internal carotids. Farther back the dorsal aorta gives off small vessels in each septum (between the segments) to the tissues of the body-wall, and other vessels which

pass down the mesentery supporting the gut to supply the gut-wall. .

The blood in the gut-wall is collected up into the subintestinal vessel and is led forwards again. On the way, it breaks up into capillaries again in a glandular diverticulum of the gut—-—the liver—and deposits much of the digested and absorbed material which it has picked up in the posterior region of the gut (intestine). In this way a hepatic portal system is formed. The blood in the body-wall makes its way to the cardinal veins, and from them it crosses the cnelomic cavity between the body-wall and the gut-wall by the ductus Cuvieri (or superior vena cava), running in the transverse septum, to the subintestinal vein. This is the fundamental type on which the peripheral vessels are arranged in all ehordates, and the details in the various groups can be considered under the headings, veins, heart, and

arteries. It may be remembered that arteries are vessels leading blood‘,

away from the heart, and veins lead blood towards the heart, whatever be the kind of blood which they contain. Further, arterial blood is rich in oxygen, and venous blood poor in oxygen, whatever may be the nature of the vessel which contains it. Actually, the purest arterial blood in the body is in a vein (pulmonary), and the foulest venous blood is in an artery (also pulmonary).

THE VEINS. The description given above applies to the venous system of Amp/rioxus. In the Craniates, the presence of mesodermal

kidneys (pronephros and mesonephros), lying in the track of the 283 Figure 166a. Diagrammatic representation of

the heart and aortic arches of A, a ﬁsh; B, an amphibian; C, a lizard.

284

COMPARATIVE ZOOLOGY OF CHORDATES ms vascuun system 235

and forwards

dc, ductus caroticus; I, lung;

At, left aurtele: Isa, left systemic arch; lvcs, left superior vena wva; pa, pulmonary arch; ra, right auricle; rsa, right systemic arch; rrcs. right superior vena cava: sv, sinus venosus; at,

I

v, ventricle; vci, inferior vena cava.

hes. ca, cmliac artery; da, dorsal aorta

'5 ««(«««(g i ~ — -2‘;-~.‘ , ‘. 'r r. 'r '1" I,‘ :r ‘—.,~_‘‘'-..‘ -2

»»t=t/   . Ea

«aural? '- ‘ ‘t -at -‘I ' ‘-3:‘ «maul (1 “ ' -g I‘ ,' .1 ' E U E-'. ‘-2 " ' ~ "=3 ‘\'u .'.o “ ‘ ' :6 (((l((l(((§ - l(4(((u(f&.t.....¢uu.. ‘ LL} g \

rd

U)

Lso that the observer is looking from the ventral side back into the ventricle

Figure l66b. Diagrammatie representation of the heart and aortic arches of D, a crocodile; E, a bird; and F, a mammal. _ The heart _is represented as cut across, _ [[110 the auncles and the bases of the truncus and arterial are 286 comraaurva ZOOLOGY or cnoanaras

pmterior cardinal irbins, brings about the formation of a portal. system. The anterior cardinal veins give rise to the jugulars,‘ and in’ the Gnathostomes there are veins returning blood from the ﬁns or

‘limbs. Those from the anterior limbs are the subclavian veins which ~

run into the ductus Cuvieri; those from the hind-limbs are the pelvic» veins which run into the renal portals and into the lateral abdominal‘ veins. The two latter veins often join in the middle line on the ventral

side and give rise to the anterior abdominal vein of Ceratodus and .

higher forms. In the amniotes the lateral abdominal veins receive

‘ the blood from the allantois in the embryonic stages of development.

Beginning in the Dipnoi, there is another connexion between the circulation of the body-wall and that of the gut-wall, apart from the superior vena: cava. This is the inferior vena cava. Pulmonary veins are present in Polyplerus, Dipnoi, and Tetrapods, returning blood from the lungs to the heart. In the amniotes the renal portal veins’ tend to diminish owing to the fact that the functional kidney of the adult is no longer a mesoncphros but a metanephros, and in the bi ds and mammals there is no renal portal system.

THE HEA RT. In Amplzioxus there is no specialised heart in which the blood is pumped forwards, but, apart from the specialised bulbils, the whole vascular system is contractile and propels the blood along. Beginning in the Cyclostomes, there is a deﬁnite portion of the subintestinal vein in front of the liver and behind the gill-slits which is set apart as a muscular pump, and forms the heart. The veins from the liver and the ductus Cuvieri are received by a sinus venosus, which in turn leads into a thin-walled auricle. The latter passes the blood on to the thick-walled muscular ventricle, by which it is propelled into the anterior portion of the subintestinal vessel which is called the ventral aorta. The arteries are surrounded by smooth muscle, but the musculature of the heart is peculiar and unique in that it shows a number of cross-striations and its ﬁbres branch. The openings between the various subdivisions of the heart are guarded by valves which prevent a return ﬂow.

In Sc'yIh'um the ventricle is produced forwards into a muscular and contractile conus, which contains several rows of valves. In front of this, the base of the ventral aorta is swollen into a noncontractile bulbus. (The walls of the conus contain heart-muscle, those of the bulbus smooth muscle.) In the higher bony ﬁsh the conus tends to disappear while the bulbus enlarges. Amia is primitive in showing a fairly large conus with three rows of valves. In the Dipnoi, the valves of the conus are well developed. and they give rise to a spiral septum which almost or quite divides the conus into two. These same forms are further very interesting in that the ventral‘ aorta is very much shortened up into a truncus (instead of extending THE VASCULAR SYSTEM 287

forwards ‘all the way beneath the gills as in Scyliium), and also because in Ceratadus there is a beginning of the subdivision of the

auricle into two, with the pulmonary veins running into the left ‘ subdivision. ‘ , In the frog, the heart is not unlike that of Ceratodus, except that,

the auricles are completely divided into two, and that the spiral

septum in the conus and truncus is better developed, dividing a pulmonary channel (leading to the pulmonary arches) from an aortic channel (leading to the aortic and carotid arches).

In the water-breathing forms, the heart is always full of venous deoxygenated blood, while in air-breathing forms there is always a double stream of blood in the heart. One of these streams is arterial and oxygenated, and the other venous and deoxygenated. Since in the frog there is only one ventricle, and both the arterial blood from the left auricle and the venous blood from the tight auricle open into it, there is a mixture in the ventricle which is sorted out into the two channels in the truncus by the spiral septum and valves. In newts, the septum between the auricles tends to break down, as does the septum in the truncus. In the embryonic stages of amniotes the septum between the auricles remains incomplete also, until the time of hatching or birth, in connexion with functional details of the embryonic circulation.

The hearts in the amniotes fall into two classes, neither of which can be derived from the other, and which must have been separately evolved from the amphibian condition. The conus is reduced and incorporated in the wall of the ventricle, but while in one group which may be called Sauropsidan the truncus is split right down to the ventricle into three channels, in the other or Theropsidan group it is split into only two channels.

The three channels in the Sauropsida are the pulmonary, the right systemic, and the left systemic. The two latter cross over one another so that the right systemic springs from the left side of the ventricle, while the left systemic arises with the pulmonary from the right side of the ventricle. In the lizards, snakes. tortoises, and Sphenodon, the ventricle is still single, although there is a septum which divides it incompletely. The left auricle, as always, contains the arterial blood, most of which goes into the right systemic arch. In the crocodile, the interventricular septum is complete, but it is formed in such a way that while the right systemic arch gets all the arterial blood from the left auricle, the left systemic arch, together with the pulmonary, gets only venous blood from the right auricle. There is a small foramen (of Panizza) between the right and left systemic arches which allows a little interchange of blood. The condition in the bird is like that of the crocodile except that the left systemic arch has 288 couuurrve zoonoov or cnononss

been abolished altogether, which is not surprising, seeing that it could only distribute blood which is almost purely venous. In the bird, therefore, with its four-chambered heart, there is no mixture of arterial with venous blood; all the venous blood in the heart goes to the lungs and only to the lungs. In reptiles and birds, the carotidsi arise from the right systemic arch.

The two channels of the truncus in the Theropsida are the pulmonary and the single systemic aorta. These forms include the mammals, and the Theromorph reptiles, although the latter (fossils) are obviously only known from their skeleton. The heart is fourchambered, and the ventricle is completely divided into two, so that all the venous blood from the right auricle goes into the pulmonary arch, and all the arterial blood from the left auricle into the systemic aorta, and there is no mixture. It so happens that the aortic arch of the right side does not persist, and only the left one remains, but it is of the utmost importance to realise that the reason why there is a single systemic arch in the bird is totally different from that which is responsible for the single arch in the mammal. The structure of the heart in the amniotes shows that the reptiles contain two main lines of evolution (besides other less important lines), the one culminating in the birds and the other in the mammals. The sinus venosus disappears in the highest forms, birds and mammals, and is represented by the so-called sino-auricular node. This structure is of great functional importance, for it acts as the pace-maker to the heart. It is here that the contraction originates, which contraction then becomes taken up by the other parts of the heart, and constitutes its “beat”. in birds and mammals the superior and inferior caval veins open direct into the right auricle. The sino-auricular valves give rise in the mammals to the Eustachian and Thebesian valves. The right auriculo-ventricular valve is muscular in birds. -.....»'

TH13 ARTIERIES. In the fish typically, each of the visceral arches has an afferent branchial artery leading from the ventral aorta to the gills. and an etlerent branchial artery connecting the gills to the lateral dorsal aorta. The vessels in the mandibular arch become reduced. The general arrangement of these vessels is necessitated by the presence of the visceral clefts. which make it impossible for the vessels to reach the dorsal side of the gut from the ventral side except by passing in the visceral arches between the clefts. Since gill-slits or pouches are present in the embryos of all chordates, the same reason accounts for the arrangement of the arterial arches in the higher forms. In the air-breathing vertebrates, the gills are reduced and there is a continuous vessel in each visceral arch running from the truncus arteriosus (ventral aorta) to the lateral dorsal aorta.~’ln Salamandra all the vessels in the 3rd to 6th visceral arches persist. ms VASCULAR srsram 239

The 3rd becomes the carotid, the 4th and 5th become systemies, and the 6th is the pulmonary. All these arterial arches place the truncus in communication with the lateral dorsal aorta. The lateral dorsal aorta are, however, interrupted between the dorsal ends of the 3rd and the 4th arterial arches; i.e., there is no ductus caroticus. The conditions in Triton are similar except that the 5th arterial arch has completely disappeared. In Lacerta (as in all higher forms) the 3rd arch persists as the carotid, the 4th as the systemic, and the 6th as the pulmonary. In Lacerta, the connexion between the dorsal ends of the arteries of the 3rd and 4th arches persists, forming the ductus caroticus. The lateral dorsal aorta is here accordingly uninterrupted. The ductus caroticus is absent in the adult of higher forms. The connexion between the pulmonary arch and the lateral dorsal aorta is the ductus arteriosus. This connexion is important in the embryonic stages of Amniotes. It enables the blood from the right side of the ventricle (or the right ventricle, if it is separated oil‘) to reach the lateral dorsal aorta through the pulmonary arteries. instead of going to the lungs. At these early stages of development the lungs are not yet open. In the adult amniote, the ductus arteriosus usually degenerates into a ligament, as. for example. in the mammal (on the left side), or disappears. It persists, however, in some turtles, and their case is interesting. for they are in the habit of diving, and during the submerged period the lungs are not working. The blood in the pulmonary artery can then escape into the general circulation without going through the lungs. The ductus arteriosus is also called

the ductus Botalli. In the frog, there is neither ductus caroticus nor ductus arteriosus

in the adult.

In the Sauropsidan reptiles, the right and left systemic arteries of the 4th arch are separate right down to the base of the truncus. The left one of these arches is absent in the bird. The subelavian arteries come off from the right systemic arch in lizards (dorsal type of subclavian); in Chelonia, crocodiles, and birds, the subclavian arteries are given off from the earotids (ventral type).

In the mammal, the right and left arteries of the 4th (systemic) arch differ from those of the Sauropsidan reptiles in that the aorta is undivided, instead of being split to its base. The artery on the right side does not reach round to the dorsal aorta; it is given the name of innominate artery, and it leads to the right carotid and subclavian arteries. That on the left side forms the so-called aorta, gives off the left carotid and subclavian arteries, and continues back as the dorsal aorta. It is connected with the pulmonary arch by the ductus arteriosus as already mentioned.

The internal carotid arteries are the anterior prolongations of the 290 COMPARATIVE zooroov or CHORDATES

lateral dorsal‘ aorta, and they enter the skull by passing ug between the trabeculaa, close to the pituitary body. The external carotids are

the anterior prolongations of the ventral aorta, on each side of the.

thyroid.

The proximal ends of the arteries and veins are joined at the heart;

The distal ends of the arteries are connected with those of the veins

by the capillaries, so that the whole vascular system is a closed one. ' When a vein starts from capillaries and breaks down into other i

capillaries again before reaching the heart, it is known as a portal vein. The hepatic portal vein occurs in all chordates, the renal portal appears in the Cyclostomes and disappears in the amniotes.

The blood of Amphiaxus is colourless, but in all higher forms, haemoglobin, a respiratory pigment, is present in corpuscles, which become known as “red blood-corpuscles”. In the adult mammal, these corpuscles are peculiar in being non-nucleated. In forms with enclosed embryonic development (e.g. Mammals) the embryonic haemoglobin differs in its affinity for oxygen from that of the adult. (See p. 200.) The white eorpuscles of the blood play an important part in the defence of the organism against invasion by foreign bodies. In the embryo, the blood arises from blood-islands, between the mesoderm and the endoderm in the region of the yolk. In the adult, blood-corpuscles are formed in the marrow of the bones, and in the lymphatic organs. The blood is under pressure in the arteries and capillaries, owing to the contraction of the smooth muscle surrbunding the former and of the Rouget-cells which compose the walls of the latter.

l..YMl‘HATl(“S. Attention may now be turned to the lymphatic system. In addition to the blood-vessels, the body contains a system of vessels, channels, and spaces in which lymph circulates, forming the lymphatic system. it is in communication with the coalomic cavity. Lymph is blood-plasma and white corpuscles which exude from the capillaries and bathe all the tissues of the body, supplying them with nutritive products. From the tissues, the lymph (which may thus be regarded as blood minus the red blood-corpuscles) is gathered up into thin-walled channels, called the lymphatics. These start from blind ends and eventually join the veins, in particular the subelavians, the left of which receives the main lymphatic trunk which is known as the thoracic duct. In the amphibia the space between the skin and the muscles of the body-wall is occupied by lymph, and in certain regions "lymph-hearts" are present, with muscular walls, which propel the lymph along. These lymph-hearts are lacking in mammals. Lymphatic vessels are present in the wall of the intestine, and are known as lacteals, for they absorb the fatty products of digestion, and the milk-like emulsion which they contain rm: VASCULAR system 291

gipes them a white appearance. Here and there along the lymphatics, lymph glands are formed. To these belong the spleen (which first

appears in the Selachii), the tonsils (derived from the 2nd pair of visceral pouches), and Peyer’s patches along the intestine in the

mammals.

LITERATURE

BARCLAY, A. E., FRANKLIN, K. 1., and Pmcmnn, M. M. L. Tire fa.-ml circulation. Blackwell, Oxford, 1945.

GOODRICH, E. S. Vertebrata Cranium, C yclostomes and Fishes. Black, London, 1909.

GOODRICH, E. S. On the Classiﬁcation of the Reptilia. Proceedings of the Royal Society, Ser. B, vol. 89. 1916. cnxprsn xxv THE RESPIRATORY SYSTEM

ALL chordates have a closed vascular system and haemoglobin as a convenient transporter of oxygen. Their respiratory systems involve structures in which blood-vessels are brought into close contact with the surrounding medium (water or air) with as little intervening tissue and as great an exposed surface as possible. The former requirement is met by the very thin nature of the epithelium covering the blood-vessels, and the latter by reducing the size of the blood-vessels to capillaries, which therefore have a large surface compared with their volume.

The respiration of embryos within their membranes is effected by various means, such as the circulation of the yolk-sac or of the allantois, as has been described in connexion with the development of the frog, chick, and rabbit.

After the embryonic stage has been passed, chordates breathe either by gills, or by gills and lungs (sometimes assisted by the skin), or by lungs alone.

Gills are groups of capillaries in the walls of the gill-slits, through which water passes out from the pharynx. In Amp/zioxus the current of water is caused by the action of the cilia on the under side of the oral hood and in the gill-slits themselves. Fish breathe in the following manner: the gill-slits are shut and the floor of the mouth is lowered. which causes water to enter the mouth. The mouth is then closed, its floor is raised, and the water escapes through the gill-slits. When Cyclostomes are feeding, they are firmly attached to their prey by their mouth and the sucker surrounding it. They cannot therefore take in water through the mouth, and the gill-pouches are modilied into sacs which pump water in and out again. In the larva of some fish (Polyprerus, Lepitlosiren), and in those of amphibia, external gills may be developed in the form of tuft-like structures projecting out from the body into the water, and which enable the blood to be oxygenated before the gill-slits are pierced. The larval amphibia afterwards develop ordinary gills on the outer faces of the gill-arches, and their respiration is like that of the fish. In all these cases the respiratory movements are brought about by means of the contraction of visceral muscles, innervated by dorsal cranial nerveroots, and controlled by a centre in the medulla oblongata. 292 THE RESPIRATORY SYSTEM 293

The ﬁrst visceral cleft was originally as in Acanthades a functional respiratory slit like the gill-slits behind it. In hving forms, the ﬁr-st visceral cleft is reduced to a small aperture or spiracle in Selachii, Polypterus, and Acipenser; but in all other forms it is closed. There may be a spiracular gill, which is called a pseudobranch because its capillaries receive blood which has already been oxygenated in the next posterior (true) gill. In the Tetrapods the cavity of the spiracular cleft gives rise to the tympanic cavity and Eustachian tube.

The rays are Selachii adapted for living on the sea-bottom, and they are of a flattened shape, with the gill-slits on the under side. The spiracle is on the upper side, and serves to admit water into the pharynx. In the Selachii, the gill-slits are uncovered, but in the bony ﬁsh (Dipnoi and Teleostomes) they are covered over and protected by an operculum. An analogous operculum develops in the larva of the frog, and it may be remembered that in Amp/zioxus the gill-slits are protected by being enclosed in the atrial cavity.

The gill-sacs of Petromyzon all open independently to the exterior, whereas those of M yxine have a single joint opening on each side.

The number of gill-slits in Amp/zioxus is large (up to 180). In Selachii, not counting the spiracle, it is ﬁve, except in Ileptanclms which has seven, and Hexanc/ms and Pliutrema which have six. _Five is also the number in bony ﬁsh except Eurypharynx which has six. It is important to remember that gill-slits or pouches are present in early stages of development of all chordatcs up to and including mammals, and that they play a part in the disposition of the arterial arches although they cease to function as respiratory organs. Their walls also contribute to the formation of the thymus and parathyroid glands.

The adult Amphibia (or most of them, i.e., those which have not lost their lungs) and all higher vertebrates breathe by lungs. (The use of the skin as a breathing organ in Amphibia is made possible by the fact that their skin is moist and uncovered.)

Lungs are also present in some ﬁsh. In P0lypt(’ru.s‘, there is a trachea leading out from the ventral side of the oesophagus, and forking into two lungs. The cavity of these lungs is divided into small spaces or “cells”, which has the result of increasing the internal surface. Such lungs are called cellular, and they are supplied with blood by pulmonary arteries, i.e., branches from the last (6th) pair of branchial arterial arches. From them, blood returns (to near the sinus venosus) by paired pulmonary veins. In the Dipnoi, there are paired lungs in Protopterus and Lepidosiren, but a single one only in Ceratodus. Their relations are similar to those of Polypzcrur, except that the lungs, together with the pulmonary arteries and veins, have been displaced to a dorsal position by passing round the right side 294 COMPARATIVE zoowov or cuounxras

of the (esophagus. In Ceratodus the pulmonary veins open into the left side of the auricle. Lungs were almost certainly present in the Osteolepidoti. These animals lived or live in fresh water in which the oxygen-content is low (owing to desiccation and accumulation of decomposing organic debris), and branchial respiration is supplemented by the intake of bubbles of air through the mouth. Indeed, Protopterus is able to withstand periods of drought when the swamps

» in which it lives dry up, by burying itself in the mud and breathing ‘ by its lungs. The lungs of higher vertebrates are easily derived from

those of the ﬁsh just described. It is possible that the lungs represent a pair of gill-pouches behind the remainder, and which ceased to open to the exterior. They are formed from the endoderm and communicate with the alimentary canal, and they preserve their bloodsupply from the vessel of the last branchial arch.

In the higher bony ﬁsh, the lung is single and modiﬁed. In the primitive form Amia, it is still supplied with blood from the last branchial artery and its walls are cellular, but in all the rest it derives blood from the emliae artery and dorsal aorta, and its walls are not adapted for the diffusion of gases through them, except in a restricted vascular area. In some forms it remains connected with the alimentary canal by an open tube, but in others it is completely “shut off (in the adult condition). In these higher bony ﬁsh, the lung no longer functions as a respiratory organ, but it has become a hydrostatic organ. The quantity of gas which it contains is regulated by the vascular area just referred to (where oxygen may be passed from the blood into it or vice versa), and the ﬁsh is able to adapt its speciﬁc gravity to that of the depth of the water at which it is swimming. it is therefore able to maintain its depth without muscular effort. In these forms it is no longer a lung, but an air-bladder or swimbladder. ln some Teleosts, such as the catﬁsh (Amiurus), the swimbladder enters into relations with the auditory vesicle, and is connected with it by a chain of small bones called the Weberian ossicles, which are derived from the first three vertebrae. In some other Teleosts, the swim-bladder disappears in the adult, and these are often found to be bottom-living forms, which live at a more or less constant depth.

Strange as it may seem, therefore, it is probable that the lungs were evolved while the vertebrates were still in the water, and that they gave rise to the swim-bladder by specialisation.

It is now necessary to turn to the relations which the olfactory organs bear to the respiratory system. In the Selachii and the higher bony fish, the nasal sacs have no connexion with the mouth, but this is not the case in the most primitive bony ﬁsh. In Osteolepis and in the Dipnoi there are external nostrils on the snout, and they lead to THE RESPIRATORY svsrau 295

internal nostrils which open into the mouth-cavity. This condition is also present in all the Tetrapods. In these forms, therefore, the olfactory organs are subservient to the respiratory system in that

they enable the respiratory medium (water or air) to enter the mouth»

cavity without having to pass through the mouth itself. It may be remembered that in Petromy.-on the nostril is single and conﬂuent with the opening of the hypophysial sac. The same is true of M yxine, but here the hypophysial sac opens into the alimentary canal. This connexion between nose and gut is, however, quite different from that of the other forms just mentioned, and was independently acquired.

The amphibia when adult breathe air into their lungs, but the mechanism for doing so is similar to that which the ﬁsh use for breathing with their gills. The ﬂoor of the mouth is lowered and air is taken into the mouth cavity. The mouth and nostrils are then closed, and the ﬂoor of the mouth raised, which forces the air down the throat and larynx into the lungs.

The method of respiration in the amniotes is more cfﬁcient. The volume of the lungs is increased by the expansion of the thoracic box, and this is accomplished by movements of the ribs (assisted in the mammals by movements of the diaphragm). The muscles concerned in these movements are somatic and innervated by ventral nerveroots of the neck and thorax. The tortoises, whose ribs are, of course, ﬁxed to the carapace which surrounds them, replenish the air in their lungs by movements of the neck, arms, and legs.

The lungs of Polypterus, Dipnoi, and amphibia are more or less hollow sacs. In reptiles the internal surface of the lungs is increased by foldings of the walls, with the result that the lungs can no longer be described as simple hollow sacs. In birds and mammals, this process has been carried still further, and the lungs are spongy masses of tissue penetrated by innumerable small air-spaces. In mammals, the internal surface-area of the lungs may be thirty times that of the external surface of the body.

The lungs of the chameeleon are of interest in that they are produced into a number of blind diverticula or air-sacs. These air-sacs reach their highest degree of development in the birds, in which they may occupy a large volume. Air is led into the air-sacs from the bronchi passing straight through the lungs, and it then passes back into the lungs where it oxygenates the blood, and out again through the trachea. The efiiciency of this mechanism lies in the fact that there is a through-draught right through the lungs. All the air can be renewed, whereas in other forms, the lungs are blind sacs and there is always a certain amount of stale residual air at the bottom of them which cannot be renewed. The efficiency of the respiratory system 296 compxnxrrvn ZOOLOGY or cnonoxrss

has played a large part in the evolution of the birds, which require a high rate of metabolism in order- to perform the very arduous muscular exertion of maintaining the body in the air during ﬂight.

Attention may now be turned to two modiﬁcations which may occur in connexion with the respiratory system. The ﬁrst concerns

the formation of the false palate. This structure is a secondary roof '

to the mouth, closing over the original internal nostrils, and enclosing the nasal passage as far back as the secondary choana. The secondary choana is opposite the glottis (the opening through which the pharynx communicates with the larynx and trachea, and so with the lungs), and the whole structure is an adaptation enabling the animal to breathe and yet have its mouth full of food or water at the same time. It is especially developed in aquatic forms such as the crocodile and the whale, but it is characteristic of the higher Theromorph reptiles and mammals in general. In the whales the glottis carpi

be pushed right up into the secondary choana, thus making a closed ' communication between the external nostrils (above the surface of the water) and the lungs, without running the risk of water entering‘ the latter from the mouth. In the higher vertebrates, and especially

those which frequent deep waters, the windpipe or trachea is prevented from collapsing by rings of cartilage or bone.

The fact that respiration in terrestrial vertebrates involves the pumping of air in and out of the body has been made use of in connexion with the production of sound. Bands of connective tissue stretch across the cavity of the larynx, and can be thrown into vibration by the passage of the air. These bands are the vocal cords. In the male frog there are vocal sacs at the corners of the mouth, and these become distended with air when the animal “croaks” and act as resonators. ,

The larynx and its vocal cords are the organ of voice-production in the mammal. and the pitch of the sounds can be controlled by the tension of the cords and the laryngeal muscles. The false palate acts as a resonator. In the birds there is a special organ called the syrinx situated at the fork where the trachea divides into the two bronchi, and it is to the vibrations of this that the song of birds is due.

It is interesting to note that the power of producing vocal sounds has evolved parallel with the capacity for appreciating them, or in other words, the differentiation of the cochlear part of the ear.

LlTl.':RATURE GOOIJRICH, S. Vt’r'r¢'br'um Cranium. (.')'cl0sIcm1es and Fi.she.s'. Black, London. 1909.

OPPEL, A. Atmungsapparat: Lelubucli der Wrgleiclienden Mikroskopischen Anatomic der Wirbc'Itiere. Part 6. Fischer. Jena, 1905. CHAPTER XXVI THE ALIMENTARY SYSTEM

THE alimentary system comprises the tube which leads from mouth to anus, together with the glands attached to it which aid in the processes of digestion. There is a slight invagination of the ectoderm at the mouth and anus, forming the stomodzeum and the proctodzeum; but the remainder, which forms by far the larger part of the alimentary system, is formed exclusively from the endoderm. In addition to the digestive glands, the alimentary canal has a number of derivatives which have been considered in connexion with other organ-systems. So the gill-pouches and the larynx and lungs belong to the respiratory system: the allantoic bladder forms part at‘ the excretory system; while the thyroid gland, which in Gnathostomes and adult Cyclostomes is one of the endocrine organs, helon gs to the alimentary systems in Amplriowrs and the larval Cyclostome (Ammoctete).

The primitive method of obtaining food is by the creation of a current of water towards the mouth by means of cilia. This is the case in Amphioxus, the Ascidians, and the Ammocozte larva of Cyclostomes. Here the endostyle is accessory to the alimentary system in that it ensures that the particles of food reach the intestine instead of being lost with the current of water llowing out through the gill-slits. The method of feeding by means of a sucking mouth and a rasping tongue which is characteristic of the Cyclostomes. is secondary and specialised. In all the Cinathostomes, the most anterior visceral arches, between the mouth and the lirst visceral cleft, become modified and adapted for seizing food, and give rise to the jaws. This method enables food of larger size to be obtained than is possible by the ciliary method, and the Gnathostomes were thereby able to evolve to greater size. In these forms also, the jaws are garnished with teeth, and the nature and shape of the teeth varies with the kind of diet. Not only do teeth assist in seizing prey, but in the higher forms they serve to grind it up small, which is an aid to the processes of digestion. In the higher vertebrates, the tongue may also be used for obtaining food as in the case of the chamteleon, and it assists in the process of swallowing.

In the primitive forms the alimentary canal or gut runs straight

from mouth to anus, as in Amplzioxus and the Cyclostomes. In these 297 298 comrnnarrvs ZOOLOGY or crronosras

two foiimsi the litiing of the gut is ciliated, but in higher forms the eiliation is restricted to certain anterior regions, and in them the food:

- is propelled along by peristaltic action of the smooth muscle infthd ‘

‘*5

" gut-wall.

Beginning in the Selachians, a special part of the gut is modiﬁed J.

ml as a receptacle in which bulky food (capture of which is made” ‘‘ “possible by the jaw method of feeding) is treated with digestive

juices secreted by its walls, and in which absorption does not take

place. This is the stomach, and in all Gnathostomes it is an enlarged. region of the gut, kinked to the left side of the body, and situated between the non-digestive supply-tube or (esophagus and the absorbent intestine. The intestine of the Gnathostomes is greater in length than the space which contains it, with the result that it is more or less coiled. In the higher forms the intestine is very considerably longer than the body itself. The effect of this is to increase the surface of absorption. A modiﬁcation which serves the same function is the spiral valve in the intestine, which is feebly developed in Petromyzon and well developed in the Selachians. The spiral valve is also present in Cerarodus and in a few primitive bony ﬁsh (Teleostomes), but it is lost in all higher forms. A peculiarity of the stomach of the higher bony ﬁsh (Teleostei) is the development of a number of blind outgrowths (pyloric eaeca) from the hinder end of the stomach. The wall of the intestine is well supplied with blood-vessels belonging to the hepatic portal system, and with lymphatic vessels or “lacteals”.

The oesophagus in birds is modiﬁed and enlarged into a crop or temporary storage place. The stomach is divided into two regions. The first of these, the proventriculus, has soft walls provided with glands. Next comes a hard-walled gizzard, in which the food is crushed with the help of stones, for the bird has no teeth and so cannot perform this function in the mouth.

In mammals, the stomach is simple except in a group of the Ungulates called the Ruminants, where it is divided into several parts. These animals “chew the cud”, and their stomach is modiﬁed

' in consequence. The food (grass) is swallowed down (without being masticated) into the anterior divisions of the stomach composed of the paunch or rumen, and the “honey-comb” or reticulum. When the animal ceases feeding. the food is brought up to the mouth again and thoroughly chewed and salivatcd. It then redescends to the other divisions of the stomach, termed the maniplies and the abomasum. The latter has glandular walls, and secretes digestive juice.

The region between the intestine and the anus is short and straight “ in the lower forms, and is called the rectum. It is usually marked oﬁ‘ from the intestine by the development of a constriction, the ileucolic sphincter, and by one or two blind diverticula or caeca. In the ran Atmauranr srsrnu 299

Tetrapods 'reg'on between the intestine and the ~

longer and coiled, and it becomes possible to distinguish a’ so-called

large intestine (on account of its diameter) or colon which is coiled, ‘

from the terminal straight rectum. The intestine proper is then called the small intestine. The large intestine is concerned with the absorption of water from the non-digested remains of the food, a function of importance for animals which inhabit dry land.

The cacum in mammals may be very large, as in the rabbit, and this condition is common in herbivorous animals. The caecum contains a colony of bacteria whose function it is to attack the cellulose of the food and to digest it. In other forms the caecum is reduced, and may be represented only by its tip, the vermiform appendix, as in man.

The anus primitively opens to the outside in conjunction with the urino-genital ducts, forming a cloaca. This condition is departed from in the higher bony"ﬁsh (Teleostomes) and in the higher mammals or Ditremata (Marsupials and Placentals), in which the alimentary and urino-genital systems open separately to the exterior.

The first special digestive gland to appear is the mid-gut diverticulum, which is present in Amphioxus. It may correspond with the intestinal diverticula found in the Ammocoete larva of certain Cyclostomes. The proteolytic enzymes of Amphioxus and Cyclostomes are of the tryptic type, functioning in an alkaline medium. It is not until the Fish stage, with a stomach, is reached that acid and peptic enzymes appear. The acid probably played an important part in killing the prey, dissolving its skeleton, and rendering it aseptic.

It was in the Cyclostomes that the liver ﬁrst appeared; in higher forms the increasingly important function of the bile being to neutralize the acid of the gastric secretions and thereby enabling tryptic digestion to continue, the tryptic enzymes being secreted by a recognisable pancreas.

Salivary glands are lacking from the lower water-livin g chordata, as is readily understood when it is remembered that a current of water is constantly sweeping through the mouth to the gill-slits. Salivary glands make their appearance in the Amphibia. In the snakes, some of the salivary glands may be modified into poison-glands.

The control of secretion in the higher vertebrates is subject both to nervous impulses passing through the autonomic nervous system, and to hormones (e.g., secretin).

LITERATURE

. BARRINGTON, E. J. W. Gastric digestion in the lower vertebrates. Biological

Reviews, vol. 17, Cambridge, 1942. '

OPPEL, A. Der Magen, Schlund und Darm, Mundhiihle, Bauchspcicheldrtise und Leber. Lehrbuch der Vergleichenden mikroskopischen Anatomic der Wirbeltiere, Parts 1, 2, and 3. Fischer, Jena. 1395CHAPTER xxvu THE EXCRETORY AND REPRODUCTIVE SYSTEMS

Amphioxus is unique among chordate animals in possessing true nephridia. These organs are situated above the gill-slits, their solenocytes project into the lateral dorsal ccelomic cavities, and their external openings lead into the atrial cavity. The gonads of Amphioxus are segmental, and situated at the ventral ends of the original rnyoetelic cavities. The germ-cells of each segment make their way independently to the exterior (actually into the atrial cavity) by pores in the body-wall.

It is possible that the region of the ccelom, which in all higher Cltordates is concerned with the formation of the excretory organs, corresponds to that region which in Amplzioxus forms the gonads.

Originally there must have been a continuous row of little tubes on each side of the body. leading out of the splanchnoccel into a duct which collected from them all, and opened to the outside at or near the anus. These little tubes represent the original connexion between the myoctel and the splanchnocosl (the nephrocael, in the intermediate cell-mass), and consequently they are segmental in arrangement: one tubule on each side to each segment. Such an arrangement has been called an archinephros, and the duct the archinephric duct. and this condition is almost f ullilled in the Cyclestome Brlt=Ilosronta. Here a continuous row of tubules is formed, but an intermediate section of them disappears. thus separating an anterior batch —the pronephros-——from a more posterior set—the mesonephros. ln other forms the pronephros appears first, and the duct which is formed by the backward growth of the ends of the tubules is the pronephric duct. The pronephros is the functional larval kidney in the lower vertebrates, and the pronephric duct grows back to the cloaea without waiting for the mesonephric tubules to develop. When these form, they ﬁnd the pronephric duct ready-made to receive them. After receiving the mesonephric tubules the pronephric duct becomes known as the mesonephric duct, and the pronephros degenerates (except in the bony ﬁsh Fierasjfer and Gobiesox). The functional kidney in the adult ﬁsh or amphibian is the mesonephros.

The cavity of each tubule (pronephric or mesonephric) becomes

shut oil‘ from the splanchnoccel, although the opening of the 300 nrs axcnaronr AND REPRODUCTIVE systems 301

tubule into the splanchnoccel (the ciliated funnel or erzlomostome) may persist (as in Selachians and amphibia) on the median side of the occlusion. The cavity of the tubule now becomes known as a Bowman’s capsule, and its wall is indented by capillaries from the dorsal aorta and leading to the posterior cardinal vein, forming the glomerulus. Bowman’s capsule and the glomerulus together form a Malpighian corpuscle. Primitively, these corpuscles are segmentally arranged, and this condition is retained in Myxine. In other forms the number of Malpighian corpuscles is greatly increased by the formation of others by budding.

Essentially, the glomerulus is an adaptation to life in fresh water, in which, the water being hypotonie to the body-ﬂuids of the animal, there is constant ingress of water by osmosis. The excess water is got rid of by ﬁltration from the blood in the glomeruli to the Bowman’s capsules and so to the exterior. At the same time, during the passage of this ﬁltrate down the tubules, certain substances (salts and sugars) are reabsorbed and returned to the blood.

In ﬁshes and amphibia the nitrogenous excretory products are usually ammonia or urea, both of which are easily soluble in water. The glomerular system is therefore well adapted to carryout the excretory function as well as adjusting the water-balance.

In the Cyclostomes, the germ-cells in the two sexes are shed into the coelomic cavity, and make their way to the exterior by a pair of pores at the base of the mesonephric ducts. In all higher forms the sperms are never shed into the ccelom, but led by vasa efferentia to the vas deferens, primitively passing through the tubules of the mesonephros. The vasa efferentia are the coclomic funnels leading into the tubules, and the mesonephric duct forms the vas deferens or Wolfﬁan duct. In addition, on each side there is another duct, in the embryo. This is the Miillerian duct or oviduct, which develops in the females but becomes reduced in the males. The Miillerian duct in the Selachians arises by splitting oil" from the Woltlian duct, but in other forms it grows back independently from its opening into the ca:lom (the ovidueal funnel or Fallopian tube) in front, to the cloaca behind. The eggs are then shed into the cu.-lom whence they enter the oviducts, whereas the sperms pass down a duct which serves for them as well as for the evacuation of urine from the kidney. Thus, while the Cyclostome has a single kidney-duct on each side in both sexes, and the germ-cells do not pass through it, in the ﬁsh and amphibia typically the females have two ducts on each side. One of these is the Wolﬂian duct evacuating the urine, the other is the Miillerian duet leading out the eggs. In the males of fish and amphibia the Wolﬂian duct evacuates both urine and sperms; the Miillerian duct is reduced, and in the Selachian is 4“

302 , .

n"‘D

om; by the funnel and the sperm-sacs. This

also represented in the frog and newt.

,cosr;vAnA'rrvs ZOOLOGY .or_ CI-IORDATBS condition is

i In several different groups of ﬁsh and amphibia, this arrangement ._is slightly altered by the separation of a part of the Woliﬁan duct

conveying the sperms (vas deferens) from another part which drains

the kidney (mesonephric ureter, not a true ureter). By this means, the sperms avoid going through the excretory part of the kidney, and this condition is found in the Dipnoan Protopterus, Polypterus, the Teleosts, and in such toads as Alytes, in all of which it has been independently developed. In Scyllium, it will be remembered that

. only the hinder part of the mesonephros is excretory in function,

and the sperms pass through the anterior part.

In Lepidosteus and many Teleosts, the caalomic wall surrounds the ovary forming a sac which joins on to the oviduct. In this manner the ovary is completely shut off from the ccelomic cavity, and consequently the eggs are not shed into it, but led directly to the exterior?

In the amniotes, the functional kidney in the adult is the meta» nephros, and the metanephric duct or ureter is an outgrowth from the Wolfﬁan duct. The Wolfﬁan duct is therefore spared the function of

” evacuating urine, and it persists only in the male, where it functions

solely as a vas defcrens for the sperm. The mesonephric tubules form the epididymis. The Miillerian duet disappears in the male, and the Wolflian duct disappears in the female. The Mtillerian duct persists in the female as the oviduct. In the adult bird, only the left ovary and oviduct persist.

The tubules of the metanephros in birds and mammals have a special segment, the loop of Henle, where water is absorbed from the ﬁltrate that has passed through the glomeruli with the result that a concentrated hypertonic urine is formed. This is an adaptation to life on dry land and to the necessity for conservation of water. The nitrogenous excretory product in mammals is urea: in most reptiles and in birds it is uric acid, and in these forms the excretory ducts lead into a cloaca, common with the end of the rectum. As the latter organ also has the function of reabsorbing water, the urine in these animals when ejected is almost solid.

Except in the M onotremes. the base of the oviduct in the mammals becomes specialised to form the uterus, in which the embryos undergo development. According as to whether the bases of the two oviducts remain separate or become fused together the uterus may be double or single.

Another peculiarity of the mammalian reproductive system is the fact that in the male the testes usually leave their position in the roof of the abdominal cavity, and descend into scrotal sacs (see

p.125). THE E1fECR§TQRY_AND RBIEQKODUCTIVB SXSTBMS ‘ 303

'l=

While clasp'ers" or vorgdns are present“ in the males of;

s; ‘ ral ﬁsh, the amphibia lack them (except the Gymnophiona), and? fertilisation has to take place in water since the sperm require a " ﬂuid medium. In Anura the eggs and sperm are shed together into '

the water. In the newts, as a rule, the male lays a packet of sperm, and then gives a display of “courtship” in front of the female to

stimulate her to pick up the packet with her pelvic limbs and place I

it in her cloaca. During the breeding season the male has specially developed secondary sexual (epigamic) characters, such as the crest and the colour of the belly, which assist in the courtship activities.

In the amniotes, fertilisation is internal, and the sperms are introduced into the cloaca of the female by the copulatory organ or penis of the male. In this way, the amniotes are independent of water for fertilisation.

A feature of considerable interest is the increase in care of the young after they are hatched, by the parents. This increases in the higher groups of vertebrates, and all stages can be found in the evolution of the family, from the condition of Amplzioxus where fertilisation takes place in the sea water outside the parents which are in no way concerned with the development of the young, to that of man. This evolution has involved the development and perfection of characters of behaviour as well as those of structure. The ﬁrst step in this direction is usually the habit of protecting the eggs until the young hatch. In several species of ﬁsh, the eggs are laid in holes or in nests specially prepared by the parents, and the male remains on guard. This habit is resorted to by Protopterus and Lepidosiren among the Dipnoi, by Amia, several catfish, and the stickleback, only to mention a few. In some of these cases there are interesting adaptations for ensuring a sufficient supply of oxygen to the eggs. So in Lepidosiren, the pelvic ﬁn of the male becomes modiﬁed into a tuft-like organ well supplied with blood, from which oxygen diffuses out into the water. In some catﬁsh, the eggs are carried about by the parent (usually the male), and so are continually exposed to fresh sea water. Ichthyophys (Gymnophiona) coils itself round its eggs in a burrow, as do some snakes such as the python. Several Anura lay their eggs in nests specially prepared; others make living nests of themselves. In Pipa the eggs are placed on the female‘s back, where they sink into pits and undergo development; the male Rhinoderma carries the eggs in large vocal sacs; I1 ylambates carries the eggs in its mouth. Alytes is peculiar in that pairing takes place on land, and the eggs, which are tied together by strings of slime, are carried about by the male, wound round his legs. When the young are about to hatch, the male takes them to the water and abandons them. In some forms (e.g. Salamandra, Vipera) the eggs hatch while CHAPTER xxvut THE HEAD AND NECK

THE structure of the head in an adult vertebrate animal is somewhat complicated, and bears little resemblance to the simpler segmented nature of the trunk-region. The segmentation is obscured, addechi,‘ to which there is the complication introduced by the presence of ' the special paired sense-organs (nose, eye, and ear) and of the gill-‘ slits. The somites do not all form straightforward myotomes as in" the trunk, but give rise to the eye-muscles; and lastly, it is diﬂicult to recognise the segmental nerves because the dorsal and ventral nerve-roots remain separate. Nevertheless, the head is built strictly on a segmental plan, and it is easy to unravel its structure by considering early stages of development.

The embryo of the dogﬁsh, for example, passes through a stage in which the mesoderm on each side of the body is segmented "into a complete row of somites, from the front to the hind end of the body. There is no ditlerence between the somites of the future headregion and those of the trunk, and they grade insensibly into one another. The lst somitc is, however, peculiar in that it is connected with its fellow of the opposite side by a strand of mesoderm-cells which passes in front of the tip of the notochord. Such a connexion would be impossible between somites situated farther posteriorly, because the notochord separates those of one side from those of the other. The lst somite is called the premandibular somitc, and it is innervated by a ventral nerve-root: the oculomotor. The 2nd somitc is rather larger than the others; it is called the mandibular somitc and is innervated by the trochlear nerve. The 3rd somite is the hyoid somitc. and it is innervated by the abducens. These ﬁrst three somites will become dillerentiated into the extrinsic eyemuscles, and they all lie in front of the auditory vesicle, for which reason they are called the prootic somites.

The 4th somite is the lst of the metotic somites, and it is similar to the ones following it. It and the 5th somitc in the dogﬁsh eventually disappear, being squashed underneath the large developing auditory sac, and they either do not have, or do not retain, any ventral nerveroots. In Perramyzcm, however, no somites are lost, and the 4th becomes the most anterior of the myotomes of the body. In the dogfish, it is the 6th somitc which gives rise to the most anterior

myotome of the body. 306 i _ W ‘ ‘run new item user: .3 307 It is now‘ necessary to turn to the relations whichthe dorsal nerveroots bear to the somites. Above the premandibular somite, the

cells of the neural crest group together to form the ganglion of the ophthalmicus profundus nerve. This nerve is very small’ in adult:}. Scylliwn, but it is large in Squalus, and it is the dorsal root of the 1st segment, corresponding to the oculomotor.

Above the mandibular somite is the ganglion of the trigeminal nerve which is the dorsal root of the 2nd segment, corresponding to the trochlear. The hyoid somite lies under the ganglion of the facial nerve, which is accordingly the dorsal root of the 3rd segment,

gl

Figure 167. Reconstruction of the head of a dogﬁsh embryo, showing the segmentation.

9!

III. oculomotor; IV, trochlcar; V, trigeminal; VI, abducens; VII, facial; IX, glossopharyngeal; X, vagus; nerves; as, auditory sac; gl to g3, first to third gill-slits; hm, hypoglossal muscles; lm, hypoglussal nerve; op, ophthalmicus profundus nerve; s, spiracle; .51 to .98, first to eighth somite; sn, spinal nerve; the arrows show the position of the posterior limit of the neurocranium: P, in Petromyzon; Se, in Scyllium; Sq, in Squalus.

corresponding to the abducens. It is possible, therefore, to recognise three prootic segments.

The glossopharyngeal nerve is the dorsal root of the 4th segment, overlying the 4th somite. The vagus represents parts of four dorsal roots joined together, and it corresponds to the 5th to 8th segments. The ventral roots of the 4th and 5th segments, which disappear in the dogﬁsh, are present in Petromyzon. The ventral roots of the 6th and following segments are present in the dogﬁsh, innervating the anterior myotomes, and contributing to the hypoglossal nerve which accompanies the growth downwards and forwards of portions of the myotomes to form the hypoglossal muscles.

So far, then, the only difference between the head and trunkregions is that in the former the dorsal and ventral nerve-roots 308 ’ _co1t§_ArtA'r1vs ZOOLOGY or cr_roamrrss,« _ remain distinct ‘from one another, and that in the three prootio

.1‘ somites the ganglia of the dorsal roots lie outside the little somites, ‘

.« instead of median to them as in the trunk. , It is now time to turn to the gill-slits, which arise as out-growths from the pharynx on each side, and connect with the ectoderm. The gill-slits are formed at a level below that of the somites, in the region of the lateral plate, or unsegmented mesoderm. The connexion of ' the endoderm of the pharynx with the ectoderm in the formation of the gill-slits necessarily obliterates the mesoderm in places and

conﬁnes it to the bars between the gill-slits. These are the gill-bails -“

(gill-arches, or visceral arches). The remnants of the splanchnoomlic cavity in this region are restricted to the cavities in the gill-bars (as in the primary gill-bars of Amphioxus). ‘

Now, down each of these gill-bars or visceral arches there passes a large branch of a dorsal nerve-root. The most anterior visceral slit is the spiracle, and separating it from the mouth is the mandibular arch (or lst visceral arch) down which the trigeminal nerve passes. Between the spiraclc and the 2nd visceral slit (1 st gill-slit) is the hyoid arch (or 2nd visceral arch), and down this there passes the facial nerve. In a similar way, the glossopharyngeal nerve passes down the 3rd visceral arch, behind the lst gill-slit; and a branch of“the vagus runs down each of the 4th, 5th, 6th, and 7th visceral

,arches.

Since the dorsal nerve-roots are segmental in arrangement, the visceral arches are segmental also, for they correspond. This means that the spiraclc and gill-slits are intersegmental in arrangement. It must be remembered, however, that this segmental arrangement of the visceral arches is not the same thing as the primary and fundamental segmentation of the somites, because the visceral arches lie in the lateral-plate mesoderm (not in the segmented vertebral plate). The cavities enclosed in the mesoderm of the visceral arches are really part of the originally continuous splanchnocotl, and not myocoelic cavities. This is important, for it explains why the muscles to which the mesoderm of the visceral arches gives rise are innervated by dorsal and not ventral nerve-roots, although they are striped and voluntary. Ventral nerve-roots only innervate somatic striped muscles derived from the segmented myotomes of the vertebral plate. Muscles formed from the visceral mesoderm (inner wall of the splanchnoco.-lic cavity) in the region behind the gill-slits are of course the smooth muscles of the gut, innervated by the autonomic system. That the muscles of the visceral arches should differ from these latter in being striped and voluntary is due to the fact that, unlike them, they are attached to skeletal structures. These skeletal structures support the jaws and the branchial arches, and their ran nun we tract; . , 309

movements are involved in the processes of biting and breathing, . which are related to the outside world. Smooth muscles are only related to the events which go on inside the animal.

Since the visceral arches correspond to the segmentation of the body, the structures in them correspond also. These consist of the skeletal elements just mentioned. and of the blood-vessels which run up round the gut from the ventral to the dorsal aorta. So Mecke1’s cartilage and the quadrate correspond to the trigeminal nerve and the 2nd segment, and the hyomandibula and ceratohyal correspond to the facial nerve and the 3rd segment. The blood-vessels in these two arches disappear in the higher vertebrates, but that in the 3rd visceral arch corresponding to the glossopharyngeal nerve and the 4th segment of the body becomes the carotid. Similarly, the systemic blood-vessel corresponds to the 4th visceral arch (Sth segment of the body) down which the first branch of the vagus nerve runs. The pulmonary artery corresponds to the 6th visceral arch (7th segment of the body) down which the 3rd branch of the vagus runs.

The segmentation of the head is now clear, and it may be asked how many segments of the body does the head occupy? Before this can be answered it is necessary to be clear as to whether “the head" is to be regarded as everything in front of the hindmost part of the skull (occipital arch), or whether it extends as far back as the gillslits. In point of fact, it is necessary to distinguish between the dorsal or “neural head”, and the ventral or “visceral head”, for they differ in extent. The hindmost region of the neural head is indicated by the position of the occipital arch of the skull, that of the visceral head by the position of the last visceral arch. It is interesting to ﬁnd that the number of segments in either kind of “head” varies in different animals. The neural head of Petromyzon occupies 4 segments, that of Scyllizmz 7, that of Squalus 9, that of Amphibia 6, that of Amniotes probably 9. Similarly, the number of segments in the visceral head varies from 10 in Petromyzon to 8 in Scyllium, 9 in Hexanchus, and 10 in Heptanchus, while the number is reduced in land-vertebrates

._which no longer breathe by gills. In the formation of the neural

head, more and more segments of the trunk are incorporated during evolution. The occipital arch is therefore not formed by the same segment in different groups of vertebrates, but this fact does not affect the homology of the occipital arches. This structure has a representative in the common ancestor of Craniates, whatever segment of the body it may be in. In the more primitive forms the neural head is short, and the occipital arch becomes displaced backwards. The primitive extent of the visceral head is probably about 10 segments, for not only is this the number in Petromyzon and in the primitive Selachian Heptanchus (both of which have 8 visceral slits, Txmxorunsamntunrnwznﬁnm. ._

Derivagive 0} ‘ Ventral nerve - Dorsal nerve root. IOIIIIIC. } FOOL I i } E

Segment.

w-——._7 :——u— 4.: _-j J

Oculomotor (IID. '

I or premandihular.

Rectum superior, Intemus. inferior. Oblnquus inferior.

Ophthalmicus ‘ profundus (V I).

5-M3-In-but-:1-In-I .. 3.. .. ..,...—...— ..-pn-—

2 or man- -bkbhquus supermr. . Trochlcar (IV). Trigeminal (V 2 & dibular. _ _ 1 . 3).

. Abducens (VI) _,

1st or . mandabular. _

—.-—

Rectus exlernus.

,-—

Facial (VI!) :1: . 2nd or Aud1tor1.(\.'lII). ( hwond.

3 or hyoxd

. _....u-mu. .u..-. .. ... u

. Disappears except ‘ In Perram) :on. '

3rd

Glossophary ngeal (IX). *

._....._-. —._...—

5. . D_1sappears except 1 4th. ; ln Petramyzon '

and Amphxbua.

Vagus. ls! branch (X 1) (sup. larynzeal).

ls! myotome of Sqllrum (hypoglossal muscles).

1. 2:1 myotome Dmo. (hypoglossal F muscles). '

Part of Hypoglossal (XII).

Vague. 2nd branch (X 2).

5th.

——-.

4-. 4-.‘

p—___._. n...p—-._... -.....-—. u—.. .Vagus 3rd branch (X 3).

(Spmal Accessory, XI).

6th.

lst.

«mi-—

. Quadrate (incus), I‘ Meckcrs car': tilage (malleus). ‘ Hyomandibula Ceratohyal (columella, _ stapes) stylmd process, hyoid lesser cornu.

ls! phar) ngo—,

hypo-branchmls (hyoid greater cornu).

Znd duto (am. tbyroxd cart).

93rd ditto (post' thyro1dcart.).

I 4th ditto.

epi-, cerato-, &.

..

Mandibular vessel.

I I Hyoxd vessel. i I I I

lst.

‘ Carotid arch.

3rd.

j,.::|

Systemic arch.

- 4th.

J -— 5th. 4th. I Pulmonary arch, P ductus arterioﬁ SIJS.

_u—

l l Ditto. 5 Vagus 4th branch (X 4) (rec. larynI SC?”(Spmal Accessory. XI).

.1. —n—j:. J-nu.‘ _:——~.——-—8. 3rd myolome

(hypozbssal muscles).

L - —-.._‘._. --u .:—_-jj

«junc

--jinn-g... uv

' sm.

‘ sm ditto.

r 60: .

2nd.

3rd.

5m.

32% 535:

2'."

,_con’g—

Oeci . of frog.

Occip.

nrdlof

'vAn.mvn zoomcv or cnomnyrns 1 , rash nun, AND‘ NBQK‘ . ,; 311 ,

although. feiromiiioa one), but Amphioicus in its development , I passes ‘through a‘ stage (the so-called “critical stage”) when it has ‘it 8 pairs of symmetrically arranged gill-slits. ’ '*‘ " ‘ ‘-.:"

The relations and destinies of the three prootic scnﬁtes are con-ti“

stant in all vertebrates above the Cyclostomes (in which the eyes are degenerate), and they may now be considered. n . In the first place, it is interesting to note that the 1st or pre- J mandibular somites correspond to the anterior head-cavities or anterior gut-diverticula of Amphioxus, and that the front ends of all chordates correspond. Just as in Amphioxus the anterior head-cavity

‘(of the left side) opens into an ectodermal pit (the preoral pit), so in

Selachians (Torpedo) the premandibular somites open into an ectodermal inpushing (the hypophysis), and this connexion between premandibular somites and hypophysis also occurs in some reptiles" and birds. The hypophysis is therefore probably homologous with‘ the preoral pit of Amphioxus. This connexion between a mesodermal pouch and the ectoderm is similar to that which occurs in Balancglossus and the larvae of Echinoderms, forming the so-called “waterpores” and “proboscis-pores”. (It may be mentioned that the socalled “anterior head-cavities” of some Seluchians are merely parts _ of the premandibular somites, and have no segmental value.)

The morphological anterior end of the body in Craniates is a point near the middle of the mesodermal strand connecting the premandibular somites with one another. Just behind this point is the front end of the notochord, and the preoral gut; just in front of it the hypophysis grows in from the superﬁcial ectoderm, and just above it is the floor of the fore-brain near the optic chiasma and the point of closure of the neuropore. This morphologically anterior point of the animal is represented in many skulls near the dorsum sellae, which lies immediately behind the pituitary body. That part of the head which lies in front of this is the result of secondary forward growth.

In the conversion of the prootic somites into the eye-muscles in

,thc clogﬁsh, for example, the walls of the somites become thickened

by the formation of muscle-ﬁbres, and the contained coelomic cavity is obliterated. The premandibular somite wraps round the optic nerve from behind, and becomes divided into four pieces. The two dorsal portions are the internal and superior recti muscles, the two ventral portions are the inferior oblique and the” inferior rectus muscles. The mandibular somite grows forwards above the pre~ mandibular and gives rise to the superior oblique; and the hyoid somite, also growing forwards, becomes attached to the posterior part of the eyeball, forming the external rectus muscle.

In higher vertebrates, the prootic somites are not always separately 3124 .COIﬂ’ARA‘l'IVB ZOOLOGY or cnonmrns

~ recognisable aslsuch, and in these cases the eye-muscles appear to jarise from masses of mesenchymatous mesoderm-cells. In others, , the manner of “development is the same as that described for the xlogﬁsh. .

rosVi I

Figure 168. Rcconstructions showing stages in the conversions of the first three somnes into the extrinsic eye-muscles in a dogﬁsh.

A to E, successive stages. ab, abducens: cxr, external rectus muscle; f, facial nerve; lzy, hyoid or 3rd somite; inf:-, inferior rcctus muscle; inob, inferior oblique muscle; inr, internal rcclus muscle; m, mandibular or 2nd sonute; oc, oculomotor nerve; upn, optic nerve; p, profundus ophthulmicus nerve; pa, trochlear nerve; pm, premandibular or lslson1ite;ros I/and VII, superﬁcial ophthalmic branches of trigeminal and facial nerve; suob, superior oblique muscle; sur, superior rectus muscle; ll‘, trigeminal nerve.

In the lower vertebrates, the head has no greater mobility than any other part of the body; indeed, in several bony ﬁsh it has none, for the back of the skull is connected with the pectoral girdle by a chain of bones. The neck has not yet evolved in these animals. The neck is a region of flexibility which enables the head to be moved without moving the body. This is made possible by the specialisation of the most anterior vertebrae. In reptiles. the differentiation of the

rosV ,?"‘.~ me new also use: 3 313

ﬁrst two mar; into the atlas and axis ‘appeaxsfane the head is. ‘

then able to hinge on the transverse axis (as in signing “yes” . and

on the longitudinal axis (as in signing “no"). Movement of the head ', to the side is effected by the ﬂexibility of the next posterior vertebrae. :

the ribs of which do not get attached to the sternum. In this way,

the cervical vertebrae differ from the thoracic. When the neck is very‘

long and capable of extensive twisting, it is common to ﬁnd vertebrarterial canals, formed between the centra and the ribs fused on to them. These canals protect the artery from being kinked when the neck is twisted. In mammals, the neck contains seven vertebrae, except in three species only (see p. 265).

L I T E R A T U R E DE BEER, G. R. The Development of the Vertebrate Skull, Clarendon Press, Oxford, 1937.

Goomucu, E. S. “Proboscis Pores" in Craniatc Vertebrates. Quarterly Journal of Microscopical Sct'cnce, Vol. 62, 1917.

—— On the development of the Segments of the Head in Scyllium. Quarterly Journal of Microscopical Sc't'tmce, Vol. 63, 1918.

VAN WIJHE, J. W. Ueber (lie Mesodc-rmsegmerzte und die Erttwlcklung der Nerven des Selacltie:-kopfe.s'. de Waal, Groningen, 1915. bﬂﬂr 151$ ALIA

TTHE FUNCTIONAL DIVISIONS OF THE NERVOUS.

SYSTEM

IT is usual to describe and to refer to a nerve with regard to the ~

Tsegment of the body in which it ﬁnds itself. So one may speak of the

facial (7th) nerve, or of the 2nd spinal nerve, and designate by these terms well-marked structures, visible by dissection. Nerves are composed of ﬁbres formed of long ﬁlaments (or axons) which are produced by cells (neurons), the “bodies” and nuclei of which are situated in the brain and spinal cord, or in the swellings on certain ‘nerves called ganglia. But all the ﬁbres of any given segmental nerve do not serve the same function. The function of a nerve is to conduct impulses. I f the conduction is towards the brain and spinal cord (which together are called the central nervous system) from sense-organs, the ﬁbres are called afferent or sensory. If the conduction is from the central nervous system outwards towards muscles or glands, the ﬁbres are called efferent or motor. Senseorgans may be of many different kinds and appreciate various sorts of stimuli, such as light, sound, pressure, vibration, pain, etc., but from the fact that they do receive these stimuli they are called receptors. On the other hand, muscles and glands are structures which “do something", and are consequently called eﬂectors.

A large part of the life of an animal is taken up with adjusting itself to different conditions, and these conditions may be of two kinds. There is the outside world with which the animal keeps in touch by means of its receptors at or near the skin: eyes, ears, lateral-line organs, and the skin itself. These are the exteroceptors. The movements which the animal makes in response to the outside world are largely locomotory, and brought about by the muscles of the body-wall and limbs. These muscles are striated and voluntary. In order that such movements may be properly co-ordinated, the animal must have some information (unconscious, of course) of the existing state of its muscles, tendons. and joints. This is supplied by sense-organs which are situated in these structures, and are called proprioceptors.

At the same time. there is a “world” within the animal and sensations arise from stimuli which start from organs such as the stomach, "T

intestine, or bladder, and the functions connected with them. The; 314 7 FU,Nl(;TlON‘itL Divisions or run NERVOUS svsrm 315 sense-organs of ‘taste largely of use in connexion witli"what5is

about to enter the alimentary canal, and they alsobelong‘ here. "T sense-organs are called interoceptors. The reactions to these stimulia”

4 take the form of secretions on the part of glands, and contractions"

of the muscles of the alimentary canal, bladder, arteries, or oviduct.;.

i

Such muscle_s are always smooth and involuntary. ‘ ‘1

Figure 169. Diagrammatic transverse section through the trunk of a vertebrate showing the relations of the nerve—roots, sympathetic ganglia, and the functional components.

ama, anterior mesenteric artery; amg, anterior mesenteric ganglion; da, dorsal aorta: dr, dorsal nerve-root; g, gut; in, notochord; rr, ramus communicans; sg, spinal ganglion: sm, somatic motor region of grey matter; ss, somatic sensory region; sy, sympathetic ganglion; vm, visceral motor region; vr, ventral nerveroot; vs, visceral sensory region.

It is possible, therefore, to make out four main divisions of the nerves according to their function:

those which convey sensory impulses from the outside world, somatic sensory, or afferent;

those which convey sensory impulses from the inner world, visceral sensory, or afferent;

those which convey motor impulses to the smooth muscles of the viscera, visceral motor, or efferent;

those which convey motor impulses to the striped muscles of the body-wall and limbs, somatic motor, or efferent.

Each of these functional systems is called a component, and as the same components can be found in several different nerves, it is interesting to study the nerves according to the components which 316 . couransrrva ZOOLOGY or cnonnaras they contain. In this way a classiﬁcation of nerves is obtained, which,

as it were, runs at right angles to the classiﬁcation according to the

- segment of the body in which they lie. Further, the different components occupy special parts of the central nervous system, and the,

»~ evolution of the latter, and especially of‘ the brain, has been largely

«controlled by the positions and relations of these “centres”. . — In an ordinary spinal nerve of any vertebrate above the Cyclo‘- stomes, there are two roots: one dorsal and one ventral, and they join to form a mixed nerve. The mixed nerve also sends a branch

(ramus communicans) to a sympathetic ganglion. Now, the dorsal

, root is made of ﬁbres of afferent (sensory) neurons, and the ventral

root is composed of efferent (motor) ones. Accompanying the anatomical division into dorsal and ventral roots, there is therefore an important physiological distinction.

The cell-bodies of the afferent neurons are situated in the ganglion which is always present on the dorsal root in all chordates above

1 Amphioxus. This means that the receptor cell itself does not convey

the impulse to the central nervous system, this function being served by the afferent neuron of the ganglion of the dorsal root. To some extent in Amplzioxus, and in the nose of all vertebrates, on the other hand, the primitive condition characteristic of many invertebrates persists: that is, the receptor sensory cell itself produces an axon which runs into the central nervous system and conveys the impulse thither. There is, therefore, no ganglion on the dorsal root of the nerves of AmpIu'o.rus, nor on the olfactory nerve in any vertebrate.

After running into the central nervous system through the dorsal root, the afferent ﬁbres terminate and make synaptic Connexions with other neurons. Now the neurons in the spinal cord have their cell-bodies in the grey matter which is central, while the surrounding white matter is made up of the axons (ﬁbres) which pass up and down the cord to higher or lower levels. The grey matter of the cord can be separated into four longitudinal regions on each side. The most dorsal strip is where the ﬁbres of somatic afferent neurons terminate. Beneath this is the place where the visceral afferent neurons end. Under this again is the region which contains the cell-bodies of the efferent visceral neurons; and lastly the most ventral part of the grey matter contains the cell-bodies of the efferent somatic neurons. Thus the dorsal half of the spinal cord is related to afferent and the ventral half to "efferent ﬁbres. As will be seen later, this arrangement is also the fundamental plan on which the brain is built.

The axons of‘ the efferent neurons run out of the spinal cord through the ventral root. The somatic efferent neurons go straight to the striated voluntary muscles of the body-wall and to the muscles of the limbs (or ﬁns), and end in them. All muscles which runcrronat, nrvrsroxss on use heavens srsratu 317

are innervated direct in this way by ventral rduts are somatic.‘ striated, voluntary muscles derived from the segmented myotomes. On the other hand, the visceral efferent ﬁbres leave the mixed nerve.” by the ramus communicans, and end in the sympathetic ganglia,‘ There they make synaptic connexions with other neurons which run

‘to the smooth muscles of the viscera and form the sympathetic

(autonomic) nervous system. The sympathetic system will be dealt with in greater detail below, but it may be noticed now that the visceral efferent ﬁbres belonging to this system never run all the way to the smooth muscle or gland. There is always another neuron intercalated in the circuit, and carrying the impulses on from the sympathetic ganglion. The muscles so innervated are never striated, voluntary not derived from the segmented myotomes.

The ramus communicans serves not only for the passage of the visceral efferent ﬁbres, but also for the visceral afferent ﬁbres, which then continue to the spinal cord through the dorsal root.

In the region of the head, a slight complication is introduced’ owing to the development of special sense-organs, and to the fact that the anterior region of the alimentary canal is modiﬁed in connexion with the jaws and gill-arches. There is further the fact that the dorsal and ventral nerve-roots of the cranial segments remain separated and do not join to form a mixed nerve.

The various nerve-components in the head can conveniently be studied in the dogﬁsh. Leaving aside for the moment the very specialised visual and olfactory organs, the somatic afferent system is divided into two owing to the development of the lateral-line system.

There is, therefore, a general somatic afferent system which receives impulses from simple sense-organs in the skin corresponding to those in the region of the trunk and spinal nerves. This com~ ponent is present in the trigcminal, glossopharyngeal, and vagus, and their ﬁbres end in the dorsal portion of the medulla oblongata in a region which may be called the “skin-brain”.

The special somatic afferent system is concerned with the lateralline organs and the special member of these which is the car. This component is present in the facial (superﬁcial ophthalmic, buccal and hyomandibular branches), auditory, glossopharyngeal and vagus, and its centre is also in the dorsal part of the medulla oblongata. So great is the number of ﬁbres which end in this way, that the neurons in the medulla with which the afferent ﬁbres make connexion are also multiplied. The result is that this region, which may be called the “ear-brain”, bulges out, forming the tuberculurn acusticum. The special somatic afferent system is also called the lateralis system, and arises in relation to the dorso-lateral placodes

of the 7th, 9th, and 10th cranial nerves (see p. 164). 318 COMPARATIVE zoonoer or CHORDATBS

pigopri  ive organs are innervated by ‘nerves which (tum,
‘t-;l1ead)'i'pn in to t "e brain through most of the cranial nerves, including’

-the oculomotor, trochlear, and abducens. The car, as an organ of

.,;,balance, can also be considered as belonging to the proprioceptive ‘

organs. "

The visceral alierent ﬁbres collect impulses from the mucous

surface of the pharynx, mouth, and “other viscera, and from the taster:

."..|i;I5i'."'.» H it I ‘H53

I

Figure 170. Dingrammatic representation of the component systems of the nerves of a doglish (based on Herrick and Johnston).

A, general somatic sensory (extcroceptivc); B, special somatic sensory (from lateral-line organs and car); C, visceral sensory (in the trunk-region the nerves pass through the sympathetic chain); D, special visceral motor (to the striated visceral muscles of the visceral arches); E, visceral motor (autonomic); F, somatic motor; Ci, see p. 319. The cranial nerves are indicated by Roman ﬁgures: sp, spinal nerves; sy, sympathetic chain. The regions of the brain and spinal cord which are related to the various component systems are shaded.

sense-organs. in fish, the taste sense-organs are not conﬁned to the mouth, but may be found all over the surface of the body. The aﬂerent visceral ﬁbres run in the branches of the facial, glossepharyngeal, and vagus from the pharynx and from the anterior and posterior faces of the gill-slits. In the brain they converge in the medulla oblongata in the visceral lobe or “taste-brain”, beneath the centres for the somatic allerent system. The visceral afferent system is also called the communis system. The fibres innervating the senseorgans of taste are sometimes regarded as forming the special 1" FUNCTIONAL prvtsious or THE NERVOUS system 319

visceral afferent system,‘ and they arise in relation to the epibranehial .placodes (see p.‘ 164). ‘ - ~ *' “ . ,.. ‘The visceral eﬁerent system is complicated by the fact that the ‘anterior end of the alimentary canal enters into‘ relations with the“ outside world. Its opening, the mouth, is bounded by thejaws which 3 are under voluntary control, and so enable the animal to aim at its“ prey and bite it. In connexion with this, it is found that the muscles which actuate the jaws are striated and voluntary, although they are visceral in origin. The muscles attached to the gill-arches and which 1 perform respiratory movements are likewise striated. But although voluntary and striated, these jaw and gill-arch muscles are not innervated by ventral roots, for they are not derived from segmented I myotomes. Instead, they are innervated direct by fibres of the special eﬁerent visceral system which run in the branches of the trigeminal,

facial, glossopharyngeal, and vagus, that pass down behind the

Figure 170, G. The proprioceptive fibres of the general somatic sensory component.

mouth, spiracle, and the several gill-slits respectively. In higher vertebrates, a portion of the ﬁbres of the vagus become grouped together more posteriorly, and form the spinal accessory or llth nerve.

The general efferent visceral system innervates smooth muscles and glands, and forms part of the autonomic (para-sympathetic) system. The ﬁbres run through the oculomotor, facial, glossapharyngeal, and vagus nerves. The centre of origin of the visceral efferent neurons is for the most part in the medulla oblongata, beneath the visceral lobe.

The somatic efferent system is concerned with the innervation of striated voluntary muscles derived from the segmented myotomes. In the head these are represented by the muscles which move the eyeballs, and the hypoglossal muscles. This component is, therefore, to be found in the oculomotor, trochlear, abducens, and hypoglossal nerves. The centres of the oculomotor and troehlear are in the mid-brain, those of the abducens and hypoglossal are in the

--it medulla oblongata.

‘ft 320 coufrnturtva zoonoov on cnonoaras . ,qtr“'

It may benogced that the arrangement in the medulla oblongata

‘of the centres doncerned witlri-the various components is similar in.

a general way to that which holds in the spinal cord. The medulla is ' I the least specialised portion of the brain.

The eyes themselves are part of the brain, and therefore the optic

nerve is not an ordinary nerve. Its ﬁbres are strictly intra-cerebral . throughout their course. They run through the optic chiasma and

end in the roof of the mid-brain, which is enlarged to form the optic lobes, or “eye-brain”.

The nasal sacs are lined by sensory epithelium, the cells of

produce axons growing back into the end-brain. The latter becomes enlarged to form the olfactory lobes or “nose-brain”.

Expressed in tabular form, the component nerve-systems are as follows.'—

SOMATIC. AFFLRIENT. General. Exteroceptors. Proprioceptors Ear Special. Lateral-line organs ' nrrannnr. To myotomic striated muscles. VISCERAL. AFFERI-INT. g:‘»;1I:i‘aces}Inter0ceptors. lilil-'ERhN'l'. General. Autonomic, to smooth muscles and glands. (Sympathetic and

Parasympathetic.) Special. To visceral striated muscles. OPTIC. Retina. OLFACTORY. Nasal epithelium. LITERATURE

HERRICK, C. Junsow. An Itttr0duc'tt'(m to Neurology. Saunders Co., Philadelphia and London, 1922.

JOHNSTON, J. B. The’ Nt’rvou.s' System of Vertebrates. John Murray, London, 1907.

KAPPERS. C. V. A. Anatomic compare'e du Systéme Nerveux. Bohn and Masson, l laarlem and Paris, 1947. cnxr-ran xxx THE BRAIN, AND COMPARATIVE BEHAVIOUR

Tl-IE brain is the anterior region of the spinal cord. modiﬁed, specialised, and enlarged in connexion with the development of special sense-organs in the anterior region of the body. That these sense-organs should be accumulated here rather than elsewhere is due to the fact that chordate animals are bilaterally symmetrical and move along a deﬁnite axis with one end constantly leading. This end is the ﬁrst to come into contact with new surroundings, information concerning which is of the highest value to the animal. _ ,

In order to understand the evolution of the spinal cord and brain, it is necessary to consider what is known as a reﬂex are. An afferent ﬁbre brings an impulse from a receptor, and if this aﬂ‘erent ﬁbre were to connect with only one efl‘erent ﬁbre going to a particular muscle, whenever the receptor was stimulated the response would be the contraction of this muscle. Nothing else in the way of response would be possible. But actually the afferent ﬁbre when it has run into the brain or spinal cord makes a large number of connexions with other neurons. Some of these may be efferent neurons and connected with various effectors; others may be neurons which carry the impulse to other parts of the spinal cord or brain: the so-called association-neurons. By this means a receptor can be connected up with several effectors, or one effector may be stimulated by impulses coming from several different receptors. This possibility of one efferent neuron being used by impulses coming from several afferent neurons, as a “final common path” for their reflex circuits, is of the greatest importance. The efiiciency and economy of using what may be called interchangeable standard units (the neurons) capable of an inﬁnite variety of combinations is one of the main factors of the success of the higher vertebrates. An animal possessing this type of nervous system can make many kinds of response, and indeed by suitable connexions and adjustments there is no limit to the number of combinations which may be formed between receptors and effectors. These adjustments are made in the central nervous system, and they are its function, just as that of a telephone exchange is to make adjustments between calling and answering subscribers. The key to the whole system is the neuron, which is not rigidly fused on

to any other cell, but which can make synaptic connexions with a 321 322 coitrxnxriva ZOOLOGY or cnonnnas

aeiitwhumbaﬁhf other cells and‘ pass impulses on to them; New connexions can be made, and new kinds of response can be evolved;

which become “conditioned” reﬂexes, or habits. —v - ~

Tl

,5-are made are called centres, and they lie in the grey matter. When the

.‘ m The places in the central nervous system where these aditustme

1 skin of a dog is stimulated by a small irritation, the recep or in the,

skin sends an impulse through an afferent neuron which runs into the spinal cord by the dorsal root. This neuron makes a synaptic,

connexion with an association-neuron in the grey matter of the;

Figure 171. Transverse SCCUOHS through the end-brains of, A, dogﬁsh; B, frog; C, Chelonian (reptile); and D, shrew (mammal).

Showing the development of the cerebral hemispheres and lateral ventricles, and the development of nerve-cells at the surface, forming a cortex.

spinal cord. The ﬁbre of this association-neuron runs down the spinal cord in the white matter to the segment of the body where the hind leg is situated. There it makes a synaptic connexion with an efferent neuron (in the grey matter) which passes out through the ventral root to the muscle of the leg. The result of the stimulus is a jerk or“\‘scratch" on the part of the leg. This reﬂex arc illustrates the fact that‘*the function of the spinal cord is twofold. It contains a number of \rellex adjustment-centres (in the grey matter), and it conducts impulses up or down the cord to different levels (in the white matter). -ran nnxm, AND CpMP‘A%Ag'lvB aanxvroun 323

In the brain there are the primary cpntres. connected with the diﬂ‘er‘ent functional systems of components. These are the “skinbrain”, “ear-brain”, “taste-brain" (in the medulla oblongata), “eye-brain” (in the mid-brain) and the “nose-brain” ' the fore-ii brain). Each of these is a centre where impulses ar received of a particular type (from a particular component-system), and where adjustments are made with association and eﬁ‘erent neurons so as to complete the reﬂex circuit. ,

Now if these primary centres are marked off in the brain of a dogﬁsh, it is found that except for the cerebellum they occupy nearly the whole of the brain. Those regions of the brain which conform to the organisation of the spinal cord are called the “segmental apparatus” or “brain-stem”, and are to be distinguished from the additions in the shape of the cerebellum and in higher forms the cerebral cortex, which are “suprasegmental" structures. '

The various centres of the brain of the ﬁsh are mainly concerned with their own functional component-system; there is not much “team-work” between the different centres. The result is that the behaviour of ﬁsh largely takes the form of reﬂex responses to stimuli of certain kinds without much ability for variation or modiﬁcation by experience. When any particular sensory system is very highly developed, the corresponding centre in the brain is enlarged. So in the carps, which are well supplied with taste-organs, the medulla oblongata is enlarged owing to the expansion of the visceral lobe. This expansion is due to the increase in number of neurons in the centre, parallel with the increased number of afferent ﬁbres coming from the numerous receptors. In the catﬁsh, the lateral-line system and the “ear-brain” are well developed.

A certain amount of correlation exists between the primary centres. For example, in the catﬁsh the “skin-brain” is connected with the “taste-brain”, so that food may be recognised by touch and by taste, and these two types of sensation co-operate in producing those movements which lead to feeding. In other words, the reﬂex arc can pass from one functional component system to the other.

But this interrelation and team-work between primary centres is best brought about by special correlation-centres, which are not related to any single primary centre but to several. The history of the development and evolution of these correlation-centres really makes up the evolution of the brain in vertebrates.

In the ﬁsh, the correlation-centres are not well developed, with the exception of the cerebellum. The cerebellum lies on the dorsal side of the medulla, and from its position its conncxions are mostly with the neighbouring centres: “ear-brain” and “eye-brain”. The earbrain is concerned with the balance of the animal as reported from 324 cotrrsnxrrvs gootoor or cnoamn-as

theisemicircular canals, and the eyes report its position relatively to external objects. At the same time, ﬁbres of the general somatic

. system run to the cerebellum and convey impulses of tactile sensations, and of the state of the muscles and joints of the body (proprioceptive). As a result of the commingling of these impulses, the cerebellum comes to be an organ for the regulation of the posture of the body and of bodily movements. It keeps the muscles in “tone”, and as a whole regulates the execution of reﬂexes. It may, in a sense, be compared with the steam steering gear of a ship, which smoothly carries out the directions of the man at the wheel; and it has been called the head of the proprioceptive system. In bony ﬁsh, the cerebellum is enlarged to form the so-called valvula which projects forwards beneath the roof of the mid-brain. In most amphibia and all higher vertebrates the lateral-line system is lost except for the ear, and the cochlea or organ of hearing is better developed. This alTects the cerebellum to some extent. In mammals, two new features arise, the superﬁcial cerebellar cortex and the pons Varolii. These develop in connexion with the cerebral cortex.

Apart from the cerebellum, the correlation-centres are mostly concerned with responses to the outside world. In the ﬁsh there are correlation-centres of this kind in the fore-brain and the mid-brain, but the most important are those which become evolved above the evolutionary stage of the ﬁsh, and which are situated in the sides of the between-brain (thalamus), the floor of the end-brain (corpus striatum), and the roof of the end-brain (cerebral cortex).

It is characteristic of these higher centres of correlation that they are more or less isolated from the primary sensory centres; in other words, the correlation-centres are not monopolised by any single sensory system. in much the same way, if the government of a nation sat in the ordinary town-hall of one of its cities, much of its business would be taken up or inﬂuenced by local municipal matters, and it would be less able to deal with business affecting not the city but the nation as a whole.

The thalamus is related by ﬁbres to most of the sensory centres, and it is among other things the centre where impulses are analysed into pleasurable and painful. As such, it is of great importance, for a negative reaction to danger and a positive reaction to food and to a mate go far to ensure the perpetuation of the species. Consequently the thalamus has great survival value in evolution.

The corpus striatum reaches a great development in birds, in which it is responsible for the correlation of the many and varied reactions and movements which form part of the instinctive behaviour. Instinct in birds is highly developed, and its hereditary ran BRAIN, ANi5 coursnartva nemwtoun 325

nature is due to the fact that the reﬂex arcs and association’-neurons in the thalamus and corpus striatutn conform to a certain pattern which is the result of development. This also accounts for the fact

\‘

I’///'///'

Figure 172. Dorsal views of the brains of A, Pclromyzon; B, Scyllium; C, Gadus; D, Ceratodus; E, Triton; F, Laccrta; G, Columba; and H, sheep. (Not all drawn to the same scale.)

c, cerebellum; ch, cerebral hemisphere; f, ﬂocculus; lib, hind-brain; mb, midbram; ol, olfactory lobe; an, olfactory nerve; op, optic lobe; or, olfactory tract; 1:. pineal; v, vermis.

that instincts are speciﬁc, that is, they occur in all members of a species, just as they all have kidneys or livers. But because instinct is determined by the hereditary pattern of the neurons, such behaviour is not easily modiﬁed to meet unusual circumstances. A 326 cosrrxnxrrvs ZOOLOGY 1 or cnonoxrss

'.r ' .. ‘if . .

good example of such shortcomings is to be found in the meadow _ pipit, a bird which is parasitised by the cuckoo. In the pipit’s nest-the ,3 cuckoo lays an egg, which hatches into a young cuckoo. This ;young ‘gﬁparasite proceeds to eject the young pipits from the nest. ‘It Efobserved on one occasion that the young pipit so ejected remained

just outside the nest, under the mother-bird’s nose, where it

1 ‘helpless and squeaking. It never occurred to the mother-bird to p,‘

f‘ it back in the nest under her, and so the young one died. The sittig,§"

tion was novel and had not presented itself to the bird before,’and'

it could not rise to the occasion. The necessary correlation of neurons‘ could not be made; and if it could, the bird would probably not have been able to act on the experience of a similar previous occasion. The corpus striatum is not well adapted for such powers of individual adaptability, though it is very suitable for ready-made correlations which make the species as a whole well adapted to a particular routine of life. It is interesting to note that the behaviour of birds resembles that of insects in this respect, and that both the brain of the insect and the corpus striatum of birds are solid compact masses of neurons. For really effective and unusual correlations such an arrangement appears to be ill suited. The cerebral cortex which fulﬁls v .,this very function is shaped not as a solid mass, but as a layer of ’ "neurons, the number of which is augmented by increasing the area of the layer. The hollow tubular nerve-cord of vertebrates is very suitable for such an arrangement, and it is probable that its possession enabled vertebrates to evolve as they have done, while its absence from insects prevented them from progressing any further. The cerebral cortex is a layer of grey matter near the surface of the end-brain. It is scarcely represented in the ﬁsh, and in the amphibia most of the neurons remain in the primitive position for grey matter; that is, near the central cavity. Some neurons, however, appear towards the surface. At the same time, the end-brain has been evolving in another direction, in that the cerebral hemispheres are formed as outgrowths containing each a cavity (the lateral ventricles) communicating with that of the between-brain through the foramina of Monro. Cerebral hemispheres ﬁrst appear in the Dipnoi, and ‘it is possible that they are an adaptation to deﬁcient oxygen-supply: a matter of great importance. for the brain requires the purest arterial blood in the body. The formation of cerebral hemispheres increases the surface of the brain-tissue relatively to its volume, not only on the outside in contact with the vascular pia mater, but also on the inside which is bathed by the cerebro-spinal ﬂuid, itself oxygenated by the choroid plexus. The location of the neurons at the surface to form a cortex may also be an adaptation to oxygen requirements, for solid masses of neurons would require ‘rue BRAIN, ANDICOMPARATIVE BEHAVIOUR 327 large arteries to enter the brain, and thereare indications that the . pulse of large arteries is injurious to the delicate, ivorltings of the"? neurons. M

Another advantage of the cortex type of structure is that it allows ‘i’ of the arrangement of centres on its surface after the fashion of a"'°~ chequer board. The cortex deals with impulses from the outside, world, in animals with sense-organs sulﬁciently well developed to give them good representations of the relations of different objects and events in space. It is apparently necessary that these represents-" tions of objects in space should remain separate in the brain until ﬁnally co-ordinated. In the same way it would be impossible to judge . which of a number of threads was which, if they were all tangled up together in a ball. This analogy also introduces the fact that the function of the cerebral cortex is to receive the impulses which have already been sorted out in correlation-centres. and to judge which of many possible is the best response to make. The cortex introduces ’ hesitancy and arbitration into behaviour, which, on the level of the’ reﬂex arc, is immediate and determined.

Another factor to be borne in mind is that the cerebral cortex is principally concerned with impulses coming from the exteroceptors, and especially those which, like the eye, ear, and nose, can perceive. objects at a distance: the distance-receptors. Responses to stimuli which touch the animal usually (when successful) abolish the stimulus which evoked them. So the ﬂea tickling the dog on its skin evokes the scratch which incapacitates the ﬂea from tickling any more. Such a response is consummatory. If, however, an animal sees some of its food at a distance, the response which it makes to start with does not abolish the stimulus. It sets its limbs in motion towards the food; this is an anticipatory response, and the consummation is not complete until the food has been reached and eaten. Until this time, the food occupies the attention of the animal.

I n the reptiles, there are three sheets of superﬁcial grey matter in each cerebral hemisphere. The median sheet is the hippocampal and the lateral sheet the pyriform cortex. Both these regions are predominantly concerned with impulses coming from the nose; they are not really “impartial” arbitrators of behaviour. That the cerebral hemispheres should in early stages of evolution be largely under the inﬂuence of olfactory sensations follows from the proximity of the olfactory lobes, and from the fact that at these stages the vertebrates had recently emerged from life in water to dry land, for the nose is a more highly developed and eﬂicient organ in air than in water. Being at the most anterior end of the brain, it naturally took time in evolution before ﬁbres from all the correlation-centres farther back in the central nervous system reached them. Part of the middle sheet 328 cogarxnxrrve ZOOLOGY or cnonoxres in the eerebrﬁ hemispheres of the reptile appears to be the "fore. runner ‘of the true cerebral cortex, which reaches such a high development in the mammals. The hippocampal and pyriform cortex ‘are

«called arehipallium, to distinguish them from this neopallium in

which olfactory impulses do not predominate. ,

In the birds the cerebral cortex is less well developed than in th reptiles, and the corpus striatum with the attendant highly instinctive type of behaviour is specialised instead.

In the mammals, the cerebral cortex is developed out of proportion to the rest of the brain. In the higher mammals (but not in Monotremes or Marsupials) a special commissure is developed to link together the neopallium of the two hemispheres; this is the corpus callosum. The dorsal commissure of the reptiles, which links together the hippocampal archipallia, persists in the mammals as the hippocampal commissure.

The volume of the neopallium is increased in higher mammals without much increasing its thickness by throwing it into folds.

The various regions of the neopallium are connected with the other centres by projection-ﬁbres, and in addition, these regions are interconnected by association-ﬁbres. The number of possible combinations between the neurons is so large that it baffles the power of the mind to grasp it. As an example, one million neurons connected together in all possible ways in groups of two neurons each, gives a number of combinations with nearly three million ﬁgures in it. There are not far oil“ ten million neurons in the human cerebral cortex.

The neopallium is therefore well ﬁtted to correlate all the stimuli which the animal receives and to make delicately adjusted responses to them. It also serves as a storehouse for impressions which are collected during experience, and an animal which, in determining the response to be made to a set of stimuli, considers the results of experience, is said to show intelligent behaviour. Such an animal has the power of learning, which is not the same thing as the establishment of a habit. Habits can be formed in the lower simple correlationcentres, by means of neurons between certain afferent and certain eﬁerent neurons. The oftener an impulse passes along a reﬂex arc the easier does its passage become, with the result that the “habitual” response is given to a stimulus. Some habits so formed may be quite complicated, as when a piece of music is “learned by heart”. This learning is, however, not necessarily intelligent, because it often happens that when the musician breaks down he is unable to adapt himself to the immediate circumstances and continue, but has to start again at the beginning.

In a similar way animals can be trained to do tricks, or to thread the “Hampton Court” maze without going down any of the blind ms nmun, AND cosrranarrve asnsvxoun 329

alleys. If a rat be so trained as to “know” ainaze perfectly, and then be placed in a similar maze but with diﬂerent len hs of alleys and distances between the turnings, it will try to run ﬁt‘: it ran in the original maze, and turn where the turnings were in it,

distances which I

and in so doing it bumps into the walls of the new maze. Its learning t

was therefore not intelligent.

It is interesting to compare this case with that of a chimpanzee confronted with a novel situation. In order to reach food which was placed out of its reach, it hit suddenly on the idea of piling packingcases on one another and climbing up on them. There is a good deal of evidence to show that in order to “see" what to do in a set of circumstances, the ape must really see the goal and the object which it may use as an instrument, in the same ﬁeld of view at the same time. There is little doubt that the eyes have played an important part in the evolution of the brain: in man the number of afferent ﬁbres running in from the retina is greater than that running in from all the spinal nerves of one side put together.

The possession of a cerebral cortex and neopallium does not adapt the species to any particular set of environmental circumstances, but instead, it makes all the members of the species individually adaptable to a large variety of circumstances. This is one of the chief differences between the higher and lower vertebrates. All are well supplied with sense-organs, but the lower vertebrates can only make a small number of kinds of responses to the stimuli

which they receive. The higher vertebrates have much the same .

amount of information given them by their sense-organs, but they use it to much better advantage owing to the integrative and retentive properties of the neopallium. The intelligent being does not waste time on trial and error like the Protozoon Paramecium; the probable results of possible actions are weighed up in what must be called the mind, with the help of experience stored up as memory, and by means of thought, and the action when taken is intentional. Lastly. it must be noticed that the possession of such a mind and its physical basis the neopallium, confers an enormous advantage on its possessor, and has survival value in evolution.

LITERATURE

COGHILL, G. E. Anatomy and the problem of Behaviour, Cambridge, l929.

ELLIOT SMITH, G. Some Problems Relating to the Evolution of the Brain. The Lancet, 1910(1), pp. 1, 147, and 22!.

Hearucx, C. JUDsoN. Brains of Rats and Men. University of Chicago Press, 1926.

-—. Neurological Foundations of Animal Behaviour. Henry Holt & Co.. New York, 1924. 330 qgigrnnnvxvo zoonoov Jpn cuonnms

Koum, w. 175 Mentality of Apes. Kasai: Paul, London, 1925. Kumnnzcx, H. Voriesungen ﬁber dae Zentralnervensystem der Wirb’ei- em. Fischer, Join. 1927. 5,

gigsvxnniiuvoron, C. S. The Integrative Action of the Nervous System. Yal "* ‘University Press, 1920.

‘SMITH, E. M. The Investigation of Mind in Animals. Cambridge Univctéity

” Press, 1923. A

'1: F F. cnsrran xxxr THE AUTONOMIC NERVOUS SYSTEM

IT has been mentioned that the smooth muscles and glands of the body are innervated by ﬁbres of the general visceral efferent com-'‘ ponent system. It is characteristic of such ﬁbres that they do not reach all the way from the central nervous system to the eﬁ'ector in . question, but they make synaptic connexions with other neurons which carry the impulses on to the muscle or gland as the case may‘ i be. There are, therefore, two members in each efferent circuit of this kind: a connector neuron and an exciter neuron. The cell-body ofg, the exciter neuron may be in a sympathetic ganglion, or it may be"

by itself near the muscle which it innervates. In the former case,

the connector neuron is often called the preganglionic ﬁbre, and the exciter the postganglionic ﬁbre. lmpulses conveyed in this waythrough the visceral efferent system to smooth muscles and glands are involuntary, and the neurons and ganglia concerned in the conduction of these impulses form the autonomic or involuntary nervous system. It may be noticed that the autonomic system is essentially eﬁ'erent. Although the afferent visceral neurons run up from the viscera through the ramus communlcans, and accompany the efferent neurons, they conform to the type of the somatic aﬁerent ﬁbres in that their cell-bodies are in the ganglia on the dorsal roots, and that they stretch all the way from the sense-organ to the central nervous system. After separating off the autonomic nervous system, what is left is called the cerebro-spinal nervous system, including the brain, spinal cord, and the somatic ﬁbresystems.

The autonomic nervous system can be separated into two divisions, each of which works against the other. The visceral eﬁ"erent fibres which come out from the spinal cord in the neck, thorax, and lumbar

from the spinal cord in the sacral region, constitute the parasympathetic system. The word “sympathetic” is !sometimes loosely used as synonymous with “autonomic”, which introduces confusion. The sympathetic system may be called the “thoracicolumbar" outﬂow, and the parasympathetic system the “craniasacral outﬂow”. 331 332 _ cogrrnaarrva zoqaoov or cnonmras

The,»autoartiinic system may now be described in greater detail, in

a typical mammal, and commencing with its sympathetic constituent.

‘ The visceral elferent ﬁbres in the cervical, thoracic and lumbar regions, of me“ spinal cord run out through the ventral roots and .down the rami communicantes to the sympathetic ganglia situated on each side of the aorta. These ﬁbres are preganglionic or connectors, and their cell-bodies are in the grey matter of the spinal cord; they are surrounded by medullary sheaths and these rami communicantes are consequently white.

Some of the preganglionic ﬁbres stop in the sympathetic ganglion corresponding to the segment in which they emerge from the spinal cord; others continue to the next sympathetic ganglia in front or behind and end there. In this way, the sympathetic ganglia of each side become connected together forming the lateral sympathetic chains, and the ganglia on them are called the lateral ganglia. In the

,,region of the neck, several of these lateral ganglia join up close together, forming the large anterior and posterior cervical ganglia and the stellate ganglion.

Yet other preganglionic ﬁbres run out through the lateral ganglia, but do not stop there. Instead, they run on and end in groups of ganglia situated near the base of the coeliac, anterior and posterior mesenteric arteries. The most important of these ganglia, which are called collateral. are the anterior mesenteric and the posterior mesentcric ganglia. The long rami communicantes which connect these ganglia with the spinal nerves are the splanchnic nerves.

In the lateral and collateral sympathetic ganglia are the cell-bodies of the postganglionic or exciter neurons. These run out of the ganglia as non-medullated and therefore grey ﬁbres, to the muscles of the blood-vessels, heart. stomach, intestine, oviduct. bladder, and skin; and some of them run to the ciliary and iris muscles inside the eye. The postganglionic ﬁbres to the skin and some other structures reach their destination via the spinal nerves with which the sympathetic ganglia are re-connected by grey rami communicantes.

The effect of stimulation through the sympathetic system is to slacken the ordinary muscles surrounding the gut, but to tighten the sphincters, to tighten the heart and artery muscles, to tighten the muscles under the skin (which make hair stand “on end”), to tighten and slacken the muscles of the oviduct, to slacken the sphincter and tighten the radial muscles of the iris so that the pupil enlarges.

The structures enumerated above are also innervated by the parasympathetic system (except the muscles of the oviduct). The visceral branch of the vagus contains connector ﬁbres which run to exciter neurons situated on the lungs, heart, and the muscles of the gut as far as the end of the small intestine. In the region of the rue Autonomic tgpnvous svsrau . 333 intestine, the exeiter neurons lie between the inuscle lcoatsiof the

gut, forming the plexus of Auerbach. The remainder of the gut is

innervated by connector ﬁbres which leave the ‘spinal cord in the sacral region through the ventral nerve-roots, and form the pelvic nerve. These connector ﬁbres run to exciter neurons on the muscles of the large intestine, on the bladder, on the skin round the anus, and on the blood-vessels near the urethra.

The ciliary and iris eye-muscles receive innervation by means of connector ﬁbres which run in the oculomotor nerve to the ciliary ganglion. This ganglion contains the cell-bodies of the exciter neurons which run to the muscles in question in the eye. Two sets of autonomic connector ﬁbres run through the facial nerve. One goes down the palatine branch (“greater superﬁcial petrosal") to the sphenopalatine ganglion from which exciter neurons run to the lachrymal glands and the glands of the nose. The other set runs in the chords tympani (ramus mandibularis internus facialis of the dogﬁsh) to the submaxillary ganglion, whence exciter neurons run to the submaxillary salivary glands. Another set of connector ﬁbres runs out in the glossopharyngeal nerve through the lesser superﬁcial petrosal nerve to the otic ganglion, from which exciter neurons innervate the parotid salivary glands.

A very interesting feature of the connector ﬁbres of the parasympathetic autonomic nervous system is, that while those of the oculomotor (mid—brain outﬂow) and of the sacral outﬂow connect with the central nervous system through ventral nerve-roots, those of the facial, glossopharyngeal, and vagus (hind-brain outﬂow) run in dorsal nerve-roots.

The anatomy of the autonomic system in the head is slightly complicated. The anterior prolongation of the lateral sympathetic chain of the trunk continues forwards, accompanying the internal carotid artery as the internal carotid nerve. A branch of it (the deep petrosal) joins the palatine nerve (forming the Vidian nerve) and runs to the spheno-palatine ganglion. This ganglion is also connected to the maxillary branch of the trigeminal. Another sympathetic branch runs to the ciliary ganglion, which is also connected to the ophthalmic branch of the trigeminal. The sympathetic exciter neurons from the anterior cervical ganglion are thus able to make their way into the eye to the iris-muscles. The mandibular branch of the trigeminal connects with the chorda tympani and the submaxillary ganglion.

Further mention must be made of Auerbach‘s plexus, which lies between the circular and longitudinal coats of muscles on the intestine. The neurons which compose it are the exciters of the parasympathetic outﬂow through the vagus, and these neurons branch, 334 , _ coptranarzva zoqpoev orﬁcaoanafrns

the two axon"ﬁbres having different destinations. A mass of food in the intestine stimulates the muscles above it to contract, and those ‘_below it to slacken, thus causing peristaltic action. This is particularly interesting because peristalsis can occur when all the nerves to the “ intestine are out, which means that local reﬂex arcs are formcdpin f’_Auerbach’s plexus. Another plexus (Meissner’s), which lies within "the muscle-coats of the intestine, has an unknown function.

The effect of impulses travelling out through the parasympathetic

Ioutﬂows is to contract the ordinary muscles round the gut, but to slacken the sphincters, to slackcn the muscles of the heart and of the blood-vessels near the urethra (causing erection of the penis), to tighten the ciliary muscle and the sphincter of the iris, to slacken the radial muscles of the iris (which allows the pupil to be contracted, and to secrete saliva and tears). The antagonism between the effects of the sympathetic and parasympathetic systems is remarkable. It may be expressed as a table.

Ordinary muscles S hincters Radial muscles Sphincter of the gut. o the gut. Heart. of the iris. of the iris. SYMPATHETIC. Slackens. Tightens. Tightens. Tightens. Slackens.

PARASYMPATHETIC. Tightens. Slackens. Slackens. Slackens. Tightens.

It is also interesting to note that the action of the sympathetic system can partly be simulated by the injection of adrenalin, and that of the parasympathetic by injection of acetyl-cholin. The similar effects of adrenalin and the sympathetic are less surprising when it is remembered that the supra-renals and the medulla of the adrenal bodies are derived from cells similar to sympathetic neurons, and which like them have migrated out from the spinal cord.

The case of the gut is particularly interesting, because the ordinary muscles of its cent are antagonistic in their effects to those of the sphincters. It stands to reason that if the ordinary gut-musculature contracts and propels the contents of the gut along, contraction of the sphincters would prevent this movement of the contents. Now the parasympathetic system tightens the ordinary musculature and slackens the sphincters. and the sympathetic system contracts the sphincters and slackens the ordinary musculature. Further, the cellbodies of the neurons which tighten the sphincters and slacken the ordinary muscles are in the same ganglion (anterior or posterior mesenteric ganglion, according to the region of the gut). It is possible that it is one and the same neuron which produces two axon ﬁbres. one tightening the sphincters and the other slackening the ordinary muscles. This would provide an explanation of the co-ordination between antagonistic sets of muscles.

No autonomic system is known in Amphioxus. In Petromyzon neurons are found along the gut, connected with the vagus and Paras)/mpathetic cranial Sympathetic thoracico-lumbar Parasympathetic sacral

/if

I L -— a — E‘. I ‘C -q‘ I

Figure l73.—Diagram showir the relations of the autonom nervous system in a mamm (based on Gaskell).

The sympathetic (thoracic lumbar) outﬂow and parasymp thetic (cranial and sacral) outﬂoi are indicated. The connector ﬁbr are shown by broken lines, the exciter ﬁbres by full lines. III, oculomotor; V, anal sphincter; amg, anterior mesenteric ganglion; apm, dorsal aorta; Ii, heart: 1', intestine; iand c, iris and ciliary muscles; icg, _ gland; Ii‘, liver; In, lung; ag, otic ganglion; pn, pelvic nerve; r, rectum; sc, sympathetic nerve-chain; scg, anterior cervical ganglion; sg, S£llI\’E1l'}l’ glands; smg, submaxillary ganglion; sn, splanchnic nerves; spg, spheno-palatine ganglion; st. 5101333113 H. uterus. . r - trigcminai; VII, facinl; IX, glossopharyngeal; X, vagus, nerves; a, anus and arrector pili muscle; 45, bladder; br, brain; cg, C1lI@Iy ganglion; da, posterior cervical sympathetic ganglion; lg, lachrygnal

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THE A 336 , . coiuranartvs zooroov or CHORDATES probably 'witlii“pelvic” nerves. The parasympathetic system is therefore present. The sympathetic system is, on the other hand, not well developed, and imperfectly differentiated from the supra-renal

elements. Groups of these cells are found near the spinal nerves and the blood-vessels, but they are not joined together by sympathetic chains. Parallel with this poor development of the sympathegﬁ

‘component of the autonomic system in Petromyzon, it may

mentioned that that animal has no oviduct or bladder, andwtto smooth muscle under the skin. In the head the eyes are degenerate, and there are no salivary glands, and this is parallel with the absence of differentiated cranial autonomic ganglia. ln Selachians, the sympathetic ganglia are joined together by the longitudinal lateral chains, and the ciliary ganglion is present in the head ; but there are no grey rami communicantes. With the land-vertebrates the full development of the autonomic system appears.

It is not easy to see why the exciter neurons for smooth muscles and glands should migrate out of the central nervous system as they do, and take up positions outside it. It is also very remarkable that some of them should connect with the central nervous system through dorsal nerve-roots (hind-brain outﬂow of parasympathetic), while others should connect through ventral nerve-roots (rnid-brain and sacral outﬂow of parasympathetic and the entire sympathetic). In this connexion it may be noted that in Ampltioxus the smooth muscles of the body are innervated through the dorsal nerve-roots, while the ventral roots contain only ﬁbres belonging to the somatic system. The primitive course for fibres innervating smooth muscle, therefore, appears to be through the dorsal nerve-roots, and this primitive feature is retained in the case of the hind-brain (facial, glossopharyngeal and vagus) outﬂow of the parasympathetic system, but lost in all the rest.

LITERATURE GASKELL. W. H. The Involuntary Nervous System. Longmans, Green, London, 1920.

HILL. C. J. A Contribution to our Knowledge of the Enteric Plexuses. Pltlltlstlﬂlllctll Transactions of the Royal Society, B. Vol. 215, 1927.

LANGLEY, J. N. Autommzic Nervous .S'_vstem. Heﬂcr, London, l92l.

YOUNG, J. 2. The autonomic nervous system of Selachians. Quarterly Journal of Microscopical Science, Vol. 75, 1933. CHAPTER xxxn THE SENSE-ORGANS

THE EYE. With regard to the eyes, two points of interest present themselves. The ﬁrst concerns the method of accommodation of the eye for seeing objects at different distances, and the second relates to the capacity of some animals to see a single object with both eyes at the same time.

Accommodation is a simple optical problem concerning the focal length of the lens, the distance of the viewed object, and the distance between the lens and the retina. These three terms must be in relation according to the laws of optics if there is to be a clear image of the object on the retina. The first and the third term are within the animal, and are therefore variable, while the second, the distance of the object, is obviously external to the animal and not under its direct control. It is found that some animals accommodate by altering the distance between the lens and the retina, and others by altering the focal length of the lens itself.

Cyclostomes and Selachians may be left out of account, for their eyes can accommodate but little if at all. In the bony fish, the eye when at rest is accommodated for near vision. This fact is in relation to the optical nature of the medium in which they live, water, through which it is not possible to see very far. The lens is attached to the eye-cup by a retractor lentis muscle, and when this contracts, the lens is brought nearer to the retina, and the eye can then focus objects which are farther away. Land-vertebrates always have their eyes focused at rest for distant vision, which enables them the earlier to see their prey or their enemies. So, in amphibia, the lens is attached to the eye-cup by a protractor lentis muscle. By its contraction, the distance between the lens and the retina is increased, and the eye can then focus near objects.

In all the cases so far mentioned, the lens is a rigid body with a fixed and deﬁnite focal length, and which has to be moved bodily in order to accommodate the eye. In the remaining vertebrates, the lens is elastic and capable of varying its convexity and focal length. In reptiles, accommodation for near vision is brought about by contraction of the circular muscle of the iris, which has as its effect the increase in convexity of the lens, which thus tends to become spherical. In the birds, there is in addition a striated muscle called

12--V.Z. 337 338 cosrmaarrva ZOOLOGY or cnonmvras Craitipton’s ttittscle, contraction «of which decreases the diameter of

eyeball in "the neighbourhood of the junction between the cornea

objects to a focus on the retina.

and”th_e sclertitic. This causes the surface of the cornea to become

more convex,’ and assists the lens to bring rays of light from '

‘ The method of accommodation in the mammals differs from that

~ in other vertebrates. The lens is suspended by the suspensory ligament, which is kept tense by the elasticity of the lens trying to revert to the spherical shape. The suspensory ligament is attached to the ciliary process. The ciliary muscle is attached to the cornea in front and to the choroid behind, so that when it contracts, the choroid and ciliary process are brought forwards. This forwards movement of the ciliary process reduces the tension on the suspensory ligament, and the lens is allowed to become more spherical, which increases its refractive power and enables it to accommodate the eye to near objects. The change in focal length of the lens is therefore only indirectly due to the action of the ciliary muscle.

In some vertebrates, and especially those of nocturnal habits, the eyes do not accommodate for distance at all, which fact does not prevent them from enjoying good sight, as does the owl. In daylight, the pupil may be so contracted as to simulate a “pinhole” camera, in which accommodation is unnecessary.

In mammals the ciliary muscle is contracted by impulses passing in ﬁbres of the parasympathetic system through the oculomotor nerve and the ciliary ganglion. Other fibres following the same path constrict the pupil (contract the sphincter and relax the radial muscles of the iris). The pupil is dilated by impulses in ﬁbres coming from the sympathetic system of the neck.

In the lower vertebrates. the eyes are on each side of the head, and there is little, if any, overlap in the two ﬁelds of vision. In these forms, the decussation or crossing-over of the ﬁbres at the optic chiasma is complete: the ﬁbres from an eye run to the opposite side of the brain. In the higher vertebrates, on the other hand, it is common for the ﬁelds of vision of the two eyes to overlap considerably, and even to coincide. In these cases both eyes can be brought to bear on a single object, which enables the animal to estimate distance. This is of importance in arboreal animals which have to gauge the strength of their efforts in leaping from branch to branch. This binocular vision is present in the monkeys and man, in the owls, and to a varying extent in other animals.

The possession of binocular vision is a great advantage, but it robs the animal of vision over a large radius around it, which it would have if its eyes diverged widely on each side of the head. It is found as a rule that the more timid mammals have widely divergent 1-an sense-onosrss H 339

axes of vision, amounting to nearly two right angles in the‘ case of. the rabbit. The rabbit therefore can see objects almost everywhere” all round it; it uses its eyes qualitatively to warn it ‘of the approach“; of enemies. The axes of vision of the lion, on the other hand, are" almost parallel; it sacriﬁces a large ﬁeld of vision for the advantage 7of using its eyes quantitatively in estimating distance and spatial‘ relations. I ~ In mammals with binocular vision, it is important that the move-3 ments of the two eyes should be co-ordinated so that their axes of , vision remain more or less parallel with one another. In other animals each eye can be moved separately, and this faculty is ' extremely developed in Chamczleo. ’ The ﬁbres from the eyes of mammals such as the rabbit decussate almost completely at the optic chiasma. This is because the axes of ‘ vision of the two eyes diverge so widely that very little of the ﬁeld is seen simultaneously by both eyes. In the monkeys and man, on the other hand, the ﬁelds of vision of the two eyes overlap extensively, and the decussation of the ﬁbres is incomplete. Fibres from the lateral ' portion of the retina of each eye do not cross-over, but go to the same side of the brain. It is the ﬁbres from the median portions of the

retina: which cross-over and go to the opposite side of the brain. _.

The images of one object can therefore fall on corresponding points in the two retina:, and the ﬁbres from these corresponding points run to one and the same side of the brain. This is the basis for stereoscopic vision. In the higher primates and in man, the eyes have “corresponding points” of optimum sensitiveness (the macula lutea or “yellow spot"), in which the retina. is said to consist of cones only, with few if any rods.

In some teleost ﬁshes, reptiles, birds, and the higher primates, the eye can distinguish between different colours, and the evolution of colour-vision must have occurred independently in each group. It" is probable that colour-vision results from a differential action between the rods and the cones of the retina, and that when rods alone or cones alone are functioning there is no discrimination between colours. Rods contain rhodopsin or “visual purple", with maximum sensitivity to light of wave-length 507 my (between blue and green); cones contain iodopsin with maximum sensitivity to light of wave-length about 570 my (red).

‘ In some vertebrates the eyes have been lost. They are very degenerate in some of’ the Cyclostomes, which lead a semi-parasitic life, and in the Urodele Proteus, which inhabits the dark cavespf Carniola. Fish which live in the dark of the abyss of the ocean or in caves may be blind and eyeless, as, for example, Ipnops,_AmbIyop.s':'s, and Luczjfuga. Among mammals, the eyes are often reduced in forms 340 \ CGMPARATIVB zooroov or CHORDATES

which live in the dark in burrows underground. The common mole is an example, and a comparable but even more far-reaching reduction of the eyes has taken place independently *in the “marsupial mole” Notoryctes.

THE 1-1 NEAL. There is no doubt that the early vertebrates were capable of seeing by means of their pineal organs, through the pineal foramen in the root‘ of the skull, though possibly not ,,.oif forming an image. Among living forms, Petramyzon has two pineal organs; other forms have only one, which may represent the original right or left organ. The pineal is least degenerate in Sphenodon. It is in the form of a vesicle of which the upper wall forms the lens and the lower the retina, which is connected by nerve-ﬁbres with the brain. This retina is not “inverted”, as is that of the paired eyes. Surrounding the retina is pigment, and the organ is sensitive to light.

In birds and mammals there is no pineal foramen in the skull, and the pineal organ remains beneath the bone. It is reduced to a solid vestige and its function is changed from that of a visual organ to an organ of internal secretion or ductless gland.

LATERAI.-LINE ORGANS. Cyclostomes, ﬁsh and larval amphibia possess a system of sense-organs known as the lateral-line organs. The sensory cells are known as neuromasts, situated either in canals or in grooves. The neuromasts are sensitive to the direction of flow of the ﬂuid in the canals, and this is presumably of signiﬁcance for the ability possessed by ﬁshes to orientate themselves to the direction of ﬂow of water. The neuromasts are also very sensitive to lowfrequency vibrations in water, perception of which enables the animal to become aware of the presence of solid objects in water at a distance. The lateral-line organs are innervated by the special 1! somatic sensory components of the facial, glossopharyngeal and vagus nerves.

‘ THE EAR. The ear is essentially a specialised portion of the lateralline organ system, and the auditory nerve is a specialised branch of the special somatic sensory component of the facial nerve. The most primitive part of the ear is the utricular portion with its semicircular canals and ampullze. Myxine has one, and Petromyzon has two semicircular canals on each side. All other Craniates have three, in planes at right angles to each other. In the utriele and in the ampullte are the statolithic particles or otoliths which are supported on sensory cilia. Gravity makes these particles weigh on the cilia immediately beneath them, whatever the position of the animal, and so the animal is informed of its position with regard to the vertical according as to which of the cilia are so stimulated. The semicircular canals contain ﬂuid, the endolymph, as do all parts of the auditory sac. When the animal starts or ceases moving, a ﬂow of endolymph ms sansn-oncans _ 343

takes place in the semicircular canals, which resolve the direction of the movement into resultants in the three ‘planes of space in which they lie. While the otoliths in the utricle are static, the ampulla: of the semicircular canals are dynamic organs of balance. '

Hearing is the perception of mechanical vibrations of low frequency. Fish are capable of true hearing of sound (of a range of vibrations similar to that characteristic of man) by means of the saccule and lagena and its otolith. The acuteness of the power of hearing is greatly increased in the Cypriniform ﬁsh (e.g. Amiurus) where the swim-bladder is connected to the car by the Weberian ossicles, and in those Clupeiform ﬁsh (e.g. Mormyrus) in which diverticula of the swim-bladder come into contact with the car.

This sense becomes more important in the vertebrates which have left the water, and are therefore subject to vibrations in air. This is signiﬁcant because these animals are also the ﬁrst to emit real vocal sounds (although some ﬁshes can make noises). Since these animals are autostylic and no longer breathe by gills, the spiracular cleft and the hyomandibula are no longer needed to subservc their primitive functions; they give rise to the tympanic cavity (and Eustachian tube) and columella auris (stapes) respectively. The vibrations of air impinge on the tympanic membrane or ear-drum, and are conveyed by the columella auris across the tympanic cavity to the auditory capsule. The wall of the auditory capsule is imperforate in the ﬁsh and in the most primitive Stegoccphalia (Eogyrinus), but in the remaining vertebrates the auditory capsule has two openings in its wall. One of these is the fenestra ovalis which enables the vibrations to be imparted to the ﬂuid (perilymph) which bathes the auditory sac. The other is the fenestra rotunda; it is covered by a membrane which absorbs the vibrations in the perilymph and so brings them to an end.

That part of the auditory sac which is actually concerned with hearing is the cochlea, rudimentary in amphibia but well developed in the higher vertebrates. The vibrations of the perilymph are imparted to the endolymph within the cochlea, which in its turn stimulates the sensory cells. In mammals where the development of the ear is at its highest, the auditory ossicles are three in number: the malleus (formed from Meckel’s cartilage), the incus (representing the quadrate), and the stapes (the columella auris). The cochlea is long and coiled, and an external ear assists in collecting the air vibrations and, by comparison between the stimulation of the two cars, in ﬁnding the direction whence the sound comes.,A reﬁnement of this faculty enables bats to avoid objects when ﬂying in the dark. In ﬂight a bat emits a high-pitched sound of frequency about 0.05 megacycles per second. These sound waves are reflected from solid 342 COMPARATIVE ZOOLOGY OF CI-IORDATES

objects and picked’ up by the bat’s cars which, by stereophonic heating, give the bat power of audio-location so accurate that it is

able to avoidthe objects from which the sound-waves are reﬂected.

l ‘mu NOSE. The olfactory organ or nose contains an epithelium which is sensitive to very minute quantities of chemical substances, dissolved or suspended in water, or suspended in air. In Dipnoi and Tetrapods the nose has an open connexion with the mouth cavit , and so enters into the service of the respiratory system, enabhnjiigb to reach the lungs without opening the mouth. This connexion not exist in forms below the Dipnoi (except in Myxine, where the hypophysial sac opens into the gut).

TASTE-ORGANS. The nose is a distance-receptor, appreciating chemical substances from afar. Taste-organs, on the other hand, serve for appreciating substances in contact with the animal, and especially in connexion with the opening of the alimentary canal. Taste is a visceral sense, while smell is a somatic sense. While in most vertebrates the taste-organs are restricted to the mouth, in some ﬁsh, such as the catﬁsh, they are distributed over the surface of the body.

JACoBsoN’s ORGAN. Associated with the nose in land-vertebrates is a pair of pouches which constitute Jacobson’s, or the vomero-nasal organs. Their function is doubtful, but it is probably concerned with smelling the food in the mouth, with which they are in communication. In some forms, including man, J acobson’s organs disappear. In the snakes they are very highly developed, and the tips of the forked tongue enter their openings in the roof of the mouth.

Substances gathered on the tongue when protruded are thus placed in contact with the sense-organ.

LITERATURE VON BUDDENBROCK, W. Grmtdriss der vergleichertden Plzysiologie, Vol. 1. Borntracger, Berlin, 1924. VON Fluscn, K. The Sense of Hearing in Fish. Nature, Vol. 141, 1938.

HARTRIDGE, H. Acoustic Control in the Flight of Bats. Nature, Vol. 156, 1945.

Hemucx, C. Junson. An Introduction to Neurology. Saunders Co., Philadelphia and London, 1922.

SAND, A. The Mechanism of the Lateral Sense Organs of Fishes. Praeeediugs of the Royal Society, B. Vol. 123, 1937.

WILLMER, E. N. Some evolutionary aspects of Mammalian Colour Vision. Proceedings of the Lirmean Society of London, Vol. 161, 1949. CHAPTER XXXIII

THE DUCTLESS G LANDS

THE ductless glands, or endocrine organs, are a group of structures, remarkable no less for their function than for their mode of develop:

ment, and their evolutionary history. The method of pouring out a

secretion into the blood-stream instead of leading it away by a‘ duct, is secondary, and some glands which are now ductless doubtless‘

possessed ducts at earlier stages in evolution. Others, comprising the

majority of the endocrine organs, were originally not glands at all,‘ ._but structures which have become useless in the sense that their original function is not or cannot any longer be performed. They.

have become modiﬁed and their functions have changed in a remarkable manner. It is perhaps not without signiﬁcance that so many of the ductless glands should have such a history of structural and functional transformation. Another peculiarity which applies to several at least of these organs is that in development they arise from two separate rudiments, distinct in manner and place of origin, and even in the germ-layer from which they are formed.

The method of secreting into the blood-stream carries with it a property which cannot be possessed by glands secreting by means of deﬁnite ducts, for the latter can only communicate with deﬁnite and restricted spaces in the body, and the effects of such secretions must be only local. On the other hand, the blood circulates all over the body, carrying the endocrine secretions with it. These can therefore affect the body as a whole, and they are of immense importance both during development and during adult life in effecting correlations of the various parts with one another. The ductless glands act as a chemical mechanism of integration relying on the transportation of the stimulus (the secretions) through the vascular system; and this mechanism is complementary to that of nervous correlation and integration which involves not transportation of stimuli but conduction of impulses arising from stimuli along special paths, the nerves. “Secretin”, which is produced by the lining of the intestine and stimulates the pancreas to secrete, has been mentioned in Chapter XXVI. . _

THE THYROID. The thyroid was originally a longitudinal tract of ciliated and mucous-producing cells on the ﬂoor of the pharynx,

called the endostyle. The endostyle is typically represented in 343 344 cosrgansrrva ZOOLOGY or ononmrns Amphioxus (and in the Ascidians), wheregt is correlated with the

‘ ciliary method of feeding, and serves to make a moving “ﬂy paper", . on to which particles of food adhere and get carried safely back into

the intestine (along the hyperpharyngeal groove), instead of getting carried out through the gill-slits by the outgoing current of water

and lost. Such an endostyle is also present in the Ammocoete larva of Petromyzon. In the adult, however, it becomes closed off from the pharynx and sunk beneath it, and it gives rise to the vesicles of

the thyroid. In all Gnathostomes the thyroid arises in development ‘

from the ﬂoor of the pharynx, and in some Selachii its cells still show traces of ﬂagella. In the bony ﬁsh, the thyroid is not enclosed in a capsule of connective tissue, with the result that when it undergoes abnormal growth (goitre) it may become carcinomatous and give rise to a malignant cancer which invades the neighbouring tissues, including the bones. In the higher forms the thyroid is enclosed in a capsule. ,

The secretion of the thyroid increases the speed of the processes of metabolism in the body, and it has been said that it stands in the same relation to the body as the draught does to the ﬁre. It plays an important part in the metamorphosis of amphibia, by promoting the growth of the (previously invisibly determined) regions into the organs which distinguish the tadpole from the adult frog or newt.

THE PITUITARY. In all Craniates, the pituitary body is a composite organ formed from the hypophysis which grows in from the superﬁcial ectoderm of the front of the head, and the infundibulum which is a down-growth from the floor of the forebrain. In Myxine these two constituents remain separated by connective tissue, but in all the remaining animals they are intimately connected and fused. In the Tetrapods it is possible to distinguish four parts in the pituitary, of which three (the anterior, intermedia, and tuberalis) arise from the hypophysis, and one (the nervosa) arises from the infundibulum. The intermedia is always (except in M yxine) plastered on to the nervosa, and the two together form the neuro-intermediate lobe. This is separated from an anterior lobe (formed of the anterior part) by the hypophysial cleft which represents the original cavity of the hypophysial ingrowth, Rathke‘s pocket. In some animals, the hypophysial cleft becomes obliterated in the adult.

In evolution, the hypophysis appeared before the infundibulum, for in A mphioxus the latter is not represented, whereas the hypophysis is present in the form of the preoral pit. The preoral pit communicates with the (left) anterior head-cavity just as the hypophysis communicates with the premandibular somite in some Craniates (Torpedo). In the adult Amphioxus the preoral pit becomes absorbed in the oral hood and gives rise to the ciliated organ which produces rim oucrnsss GLANDS 345

a current of water towards the mouth. It: ‘later evoluﬁon it sank into the tissues and became a gland secreting by a duct into the mouth. This duct (which represents the open mouth of the cavity of ii Rathke’s pocket) is preserved in Polypterus, and Cyclostomes. In the latter, however, the duct has given rise to the large hypophysial sac which extends beneath the brain and has lost contact with the pituitary body. At the next stage in its evolution it must be imagined that the gland entered into relations with the infundibulum of the ' brain, and that it adopted the method of secreting into the blood-a stream.

The functions of the pituitary are many, and they are only very imperfectly known. It must suﬁice to say that among these functions are those of : promotion of growth, control of blood-pressure, causing contractions of the uterus, expanding the black pigment

Figure 174. The pituitary body of a cat, seen, A, ft om the left side; B, in longitudinal section.

_ al, anterior lobe; /rc, hypophysial cleft; ic, infundibular cavity; nil, neurointermedlate lobe; pa, pars anterior; pi, pars tntermcdia; pn, pars nervosa; pr, pars tuberalis; tc, ﬂoor ol‘ the brain.

cells in the skin of amphibia, stimulating; the follicles of the ovary, stimulating the conversion of a discharged follicle in mammals into a corpus luteum, and stimulating the mammary glands to secrete milk.

THE ADRENAL. Like the pituitary, the adrenal bodies of the Tetrapods are composite structures. They are made up of an external cortex derived from the (mcsodermal) coelomic epithelium, and a central medulla (chromafﬁne tissue, so-called from its staining reactions) derived from the (ectodermal) cells which have migrated out from the nerve-tube in connexion with the sympathetic nervecells. In the ﬁsh, these two components are quite separate. The cortex of the adrenal is in them represented by the inter-renal, which, as its name implies, is situated between the kidneys. The medulla is represented by a number of supra-renal bodies which lie on or near the sympathetic nerve-chains, on each side of the aorta; they are

12" 346 , cosrgxnxrrvs ZOOLOGY or cuoxnxrss roughly segmental in arrangement. In the Cyclostomes, the suprarenals are closﬂy associated with the ganglia of the _dorsal roots, » "but +the"inter-renals are not well known. '

Coming to the Tetrapods, the inter-renals and supra-renals are ‘i

‘What compact but form separate strips extending along the symr if

if. Ill n

‘,3=‘g§~»-rpathetic nerve-chains, from the kidney to the anterior region of the ‘thorax. The carotid gland, which is situated at the joint of the

internal and external carotid arteries, is one of these. ,

The secretion of the medullary portion of the adrenal (adrenalin) ~

has been synthetically prepared, but in spite of this fact, little is known of the functions of the gland, except that it produces effects

\

‘. mg ’I'hr":‘,7' £5 ‘

1 ’ ed together to form the adrenal bodies, but in the more primititre . ~

orrhs such as the newts, these still resemble the ﬁsh in that they are A

Ht I

tariff 4' Ii-‘~

similar to those due to stimulation through the sympathetic auto- ‘

nomic nervous system. The functions of the adrenal cortex appear to be related to the activity of the kidney and the maintenance of the

. water and salt balance.

THE THYMUS. The thymus ﬁrst appears in the fish as a series of paired upgrowths from the roof of the gill-slits. In the Selachians it is more or less segmental in its arrangement, but in higher forms the correspondence is lost, and the number of slits which contribute to it is reduced. It controls the formation of the shell, shell-membranes, and albumen in birds’ eggs but its functions are very obscure.

THE PARATHYROID. The name parathyroid is given to bodies which are usually situated close to or even in the thyroid, but which differ from the latter in their structure and method of development. They arise from the ventral regions of the 3rd and 4th visceral pouches in the Tetrapods, and are apparently absent in the ﬁsh. Their function is to regulate the calcium content of the blood.

THE PINEAL. The pineal eye has already been described in connexion with the sense-organs. In the higher vertebrates this structure degenerates and is transformed into a gland the functions of which are unknown.

THE PANCREAS. In addition to its function of producing enzymes for the purpose of digesting the food in the intestine, whither the enzymes are conducted by the pancreatic duct, the pancreas also functions as an organ of internal secretion. The tissue responsible for producing this internal secretion is that known as the islets of Langerhans. and its production is called insulin. The function of insulin is to store up glycogen in the liver, in which respect it is antagonised by the adrenalin. Diabetes is the result of faulty or non-functioning of the islets of Langerhans. Follicles of cells which secrete a hormone of the type of insulin are present in the wall of the mid-gut in Cyclostomes. In some Teleost ﬁsh, the endocrine rue ouérrass omvos , 347

islet-tissue may form little separaie and apart irom the ordinary panyneatic tissue, which secretes .the digestive pancreatic

~_yurcc. , . rns “PUBERTY” GLAND. The reproductive glands, ovary and =‘

i ‘testis, in the birds and mammals produce internal secretions which‘

are concerned with the development and maintenance. of the characters which distinguish one sex from the other. Since thesei“ secretions are essential for the proper sexual differentiation of the’

developing animals, the glands producing them have been called

“puberty” glands. The interstitial cells of the testis secrete testo-f sterone, the male hormone; the female hormone oestradiol is secreted

by the follicle cells of the ovary. THE CORPUS LUTEUM. The corpus luteum is the name given to what is really a temporary endocrine organ in the mammals. After

an egg has vacated its Graaﬁan follicle, the follicle undergoes changes ‘ resulting in the increase in size of the follicular cells, and the in-f

vasion of the follicle by connective tissue and blood-vessels. Should

the egg liberated not get fertilised, the corpus luteum soon disappears. »

Should fertilisation result, however, and the blastocyst become attached to the wall of the uterus, the corpus luteum persists and increases in size, until the end of pregnancy. During this time it produces a secretion, progesterone, the functions of which are to produce progestational proliferation of the uterus, and to render the uterine muscles insensitive to contractile stimulation.

LITERATURE

DE BEER, G. R. The Comparative Anatomy, Histology, and Development of the Pituitary Body. Oliver & Boyd, Edinburgh, 1926.

RIDDLE, 0. Internal Secretions in Evolution and Reproduction. The Scientiﬁc Monthly, Vol. 26, I928.

SWALE VINCENT. Internal Secretion and the Ductless Glands. Arnold, London, 1924 CHAPTER xxxrv REGULATORY MECHANISMS

ALL animals below the birds and mammals are what is usually called “cold-blooded”, or poikilothermous. Actually, these animals are not so much cold as dependent on the environmental temperature, which may be hot. It is a mistake to regard “cold-blooded” animals as necessarily cold, lethargic and sluggish, for in a tropical climate their temperature is high and they may be very active. Nevertheless, since the processes of life can only go on within a certain limited range of temperature, the fact that an animal is dependent on its environment for its temperature necessarily restricts the kinds of environments in which it is capable of living. Further, within the suitable habitat, the degree of activity of the animal will depend on the temperature. This inconstancy of thermal conditions is a serious bar to the further evolutionary progress of the poikilothermous animals.

The advantage which the birds and mammals have in being “warm-blooded” (homothermous) is not only the fact that the temperature at which their biological processes go on is high, but still more the fact that this temperature is constantly maintained, regardless of the temperature of the environment.

The processes of metabolism, and especially muscular activity, entail the production of heat. Some warm-blooded animals shiver when they are cold. and their muscles are then thrown into series of contractions. There is therefore a source of heat within the organism which tends to make the temperature rise. At the same time, heat is continually being lost by radiation from the surface of the animal. The maintenance of a constant temperature within the animal therefore depends on a regulation and balance of the amounts of heat produced and lost. Poi kilothermous animals have a temperature only slightly higher than that of the environment. Some seem to be able to raise their temperature slightly for a period by muscular contractions. such as the python when it is coiled round its eggs. But these animals have no means of combating really cold external temperatures, during which they must either hibernate or die. Within limits, the hotter the temperature, the better are the conditions for poikilothermous forms. Some lizards, however (Varanus, Uromastix),

when exposed to great heat, increase their rate of breathing very 348 REGULATORY uacmiuisms , , 349 .

considerably, and so resort to panting. Paiiting results in the lungs

getting rid of large quantities of water vapour, and as heat is absorbed‘ ~ in the conversion of water into vapour, panting means loss of heat I

also. Uromastix, which inhabits deserts, is dark in colour up to a

temperature of 41° C., but as th"e temperature rises above this point,_ it tends to become white. Since dark colours absorb heat and light‘

colours reﬁect it, Uromastix has a peculiar mechanism which tends roughly to regulate its intake of heat from the environment. This method, however, is quite different from that of homothermous animals, birds, and mammals. In the ﬁrst place, the homothermous animals have an external covering which is a bad conductor of heat; this takes the form of feathers in birds, hairs in terrestrial mammals, and oil or blubber in birds and mammals which lead an aquatic existence. The effect of such a layer is to minimise the loss of heat by radiation. Next, they have more eﬂicient respiratory and vascular systems, notably a four-chambered heart with complete separation of the arterial and venous circulations. In the Monotreme Echidna, the temperature is regulated by varying the amount of heat produced, but it has no method of varying the amount of heat which it loses. It has no sweat-glands, no increase in the amount of blood in the skin (vaso-dilatation), and it does not resort to panting. The heatproduction of Echidna varies according to the difference between its temperature and that of the environment. However, this regulation is not very eﬁicient, for if the environmental temperature varies from 35° to 5° C., the temperature of the animal will vary by about 10° C. Not only is the constancy of its temperature less than that of higher mammals, but the actual normal internal temperature is lower, being about 30° C. In cold weather, Echidna hibernates. lts protective covering of hair is poor, and, like a few other mammals (such as the marmot), it becomes almost poikilothermous. On the other hand, in hot weather when the temperature rises above 35° C., Echidna dies of apoplexy (unless it is zestivating, deep beneath the ground), for its only method of countering a rise in the environmental temperature is to reduce its own internal heat-production, and a point is reached below which it cannot reduce its metabolism and still live. _ The other Monotreme, 0rm'thorhynchu.s', has a slightly higher normal temperature, 32° C., and it keeps it a little more constant. Not only can it vary its heat-production, but it can also vary its loss of heat by means of evaporation of water from its sweatglands. « _ The higher mammals regulate their temperature almost entirely by controlling the heat-loss. This they do by three methods: by the evaporation of water from the sweat-glands, by the dilatation of the 350 ‘ cosrrnnnrvs ZOOLOGY or crronnnras

blood-vessels the skin, and by the acceleration of respiration or "panting”. The heat-production in these animals is not increased unless the external temperature drops considerably. The Marsupials

}:are intermediate between the Monotremes and the higher mammals‘

in the eiﬁciency of their temperature-regulations.

In birds, heat is lost by evaporation of water through the lungs and air-sacs.

The advantages accruing from the possession of a high and con- '.

I. stant internal temperature are very great. Not only does it allow of a higher rate of living, since chemical reactions are accelerated at ~

high temperatures, but it enables dilferentiations and specialisations to arise which would be wrecked if the speed of the metabolic processes (or in other words, the internal temperature) were not constant. Further, it enables the animals to inhabit climates in which poikilothermous forms either cannot live, or have to spend considerable time hibernating against the cold or aestivating against the heat. So it is found that the supreme and dominant animals in arctic regions are the birds and mammals, while in the tropics, reptiles can compete successfully with birds and mammals.

It is interesting to notice that during most of the period of incubation the embryo chick is poikilothermous. It is only shortly before hatching that it acquires the capacity of maintaining a uniform temperature. The same is true of new-born mice, which become homothermous by the tenth day after birth.

Another matter for which a regulatory mechanism has been evolved in the vertebrates is the osmotic pressure of the blood. The importance of maintaining a constant osmotic pressure of the blood lies in the fact that it entails constancy in the concentration of salts, or in other words a stable “internal environment”; and stability of conditions is essential for highly specialised and co-ordinated processes of life.

Of aquatic invertebrates it may in general be said that their bodyﬂuids have roughly the same osmotic pressure and the same percentage of salts as the water in which they live, and that these vary as the water varies. I n the fishes the salts in the blood are only about one-third as concentrated as in sea water, which means that the blood is markedly hypotonic to sea water and markedly hypertonic to fresh water, which entails fundamental diﬂiculties for the maintenance of a constant water-balance.

A Teleost in fresh water is exposed to the constant entry into its tissues of water by osmosis. This is minimised by the impermeability of the skin and the reduction of the permeable areas to the mucous membranes of the mouth and gut and the gills. The excess of water is then expelled by the glomerular kidney which excretes a copious nnouurorur MECHANISMS . 351

dilute urine. the essential salts and sugars havirif been reabsorbed

into the blood by the kidney‘ tubules. -7,. . .,,

A Teleost in sea water is exposed to the constant loss of water ii exosmosis. This is minimised by the reduction of the glomeruli so 9

that the kidneys only excrete a sparse urine, isotonic with the bloodf"

At the same time, sea water is drunk and the salts are got rid of the special “chloride-secreting” cells in the gills. In this way a supply , of pure water is obtainable from the sea.

Usually, T eleosts are restricted in their power of adaptation to one environment, either sea or fresh water: i.e., they are stenohaline. But in some, such as the eel or salmon, alternate use of both mechanisms allows them to adapt themselves to either medium, i.e., to be euryhaline.

A Selachian in sea water has the same concentration of salts in its blood as a Teleost but it has in addition about 2 per cent. of urea, which raises its blood to a level hypertonic to sea water. There is here therefore no diﬂiculty in obtaining pure water by endosmosis. The Selachian has no “chloride secreting” cells, and its glomerular kidney excretes a normal urine from which urea is reabsorbed by the tubules into the blood. ‘

A Selachian in fresh water has 0-6 per cent. of urea in its blood. which results in less endosmosis of water than if it had been 2 per cent., but it is nevertheless considerable and the excess of water is excreted as copious urine.

In the land-vertebrates, the osmotic pressure of the blood is regulated by the kidneys, which in birds and mammals excrete concentrated hypertonic urine (p. 302). Loss of water occurs through the lungs and, in mammals, the sweat-glands; it is minimised by reabsorption of water from the fences in the large intestine, and made good by drinking.

The relation between the quantities of oxygen and CO2 in the blood is regulated by the respiratory system, controlled by a centre in the brain. If the blood is rich in C02 the respiratory movements are accelerated, and conversely they are retarded if the quantity of CO2 is low. In this connexion it must be remembered that the respiratory movements of the ﬁsh and amphibia are effected by the muscles of the visceral arches. These are visceral muscles, innervated

._by visceral efferent ﬁbres in the dorsal cranial nerve-roots, and the

centre which controls them is in the visceral sensory lobe of the medulla oblongata. In the Selachian (Raia) it is perhaps better to

speak of several centres, one corresponding to each of the 7th, 9th,

and 10th cranial nerves. Each of these segmental centres in Rala has a degree of autonomy of its own, for if separated from the others by cutting across the medulla, it continues to regulate the 352 conrruurrva zoomov or cnonmrns muscular movements in the visceral arch or arches to which it is

connected. ‘ '~"~. ~

In the amniotes, however, the respiratory movements are effected

‘ by the intercostal muscles (moving the ribs) and the muscles of the

‘diaphragm. These are somatic (myotomic) muscles innervated by

“somatic efferent ﬁbres through ventral nerve-roots in the region of

the neck and trunk. Nevertheless, the “respiratory centre” is still in the medulla oblongata, in the primitive position which it occupied in the ﬁsh and amphibia, but it no longer shows the simple segmental arrangement. ”

Lastly, attention may be paid to two features which the higher vertebrates possess, and which, though not strictly regulatory (compensating) mechanisms, nevertheless serve to ensure maximum constancy of conditions. The ﬁrst of these is concerned with the fact that the ovary and testis in birds and mammals serve not only for the production of reproductive cells, but they also furnish a chemical secretion which evokes and maintains the development of the secondary sexual characters.

The other feature refers to the method of ossiﬁcation of certain cartilage-bones by means of a diaphysis and two epiphyses, which is characteristic of the mammals. This method enables the bones in question to function as supports and hinges, and at the same time to grow and enlarge so long as the diaphysis and the epiphyses remain separated by cartilage. But once the diaphysis becomes ﬁrmly united by bone with the epiphyses at each end of it, the growth of the bone as a whole ceases. The maximum size of such bones is therefore limited, as is that of the animal.

In several respects, therefore, the higher vertebrates differ from the lower. With the temperature, the osmotic pressure and the acidbase relations of the blood regulated and constant, the higher vertebrates are largely independent of the environment. Indeed, they have a constant internal climate and “environment” of their own, in which they live sheltered from external agencies, with, in mammals, a constant ﬁnal adult size.

The possession of this “internal environment" is not only one of the chief means of survival of the higher vertebrates, but it has also enabled them to become as specialised and perfected as they are.

LITERATURE

BALDWIN, E. An Introduction to Comparative Biochemistry. Cambridge University Press, 1937.

DAKIN, W. J. The Osmotic Concentration of the Blood of Fishes taken from Sea Water of naturally varying Concentration, and Variations in the Osmotic Concentration of the Blood and Ccelomic Fluids of nsouurronv MECHANISMS 353

Aquatic Animals, caused by Changes in the External Medium, Biochemical Journal, Vol. 3, 1908. " - . - ~

HALDANE, J. S. Respiration. Yale University Press, M22.

HIDE, I. H. Localisation of the Respiratory Centre in the Skate. Ameri¢'un\

Journal of Physiology, Vol. 10, 1904.

KEYS, A. The Mechanism of Adaptation to Varying Salinity in the,‘

Common Eel. Proceedings of the Royal Society, B. Vol. 112, 1933.

KREHL, L., und Sonrm-:23, F. Untersuchungen tlber die Wiirmeiikonomie der Poilcilothermen Wirbeltiere. Pﬂz2ger’s Archiv. f. :1. Gesammte Physiologic, Vol. 77, 1899.

MARTIN, C. J. Thermal Adjustments and Regulatory Exchange in Monotremes and Marsupials. Philosophical Transactions of the Royal Society, Ser. B, Vol. 195, 1903.

Scorr, G. G. A Physiological Study of the Changes in Mustelus Canis produced by Modiﬁcations in the Molecular Concentration of the

External Medium. Annals of the New York Academy of Sc-ieuce. Vol. 23, 1913. cnxprsa xxxv

Q BLOOD RELATIONSHIPS AMONG THE CHORDATES ' it

THE various species of animals differ not only in their structure, their method of development and their habits, but also in the chemical composition of their tissues. The most useful tissue to take in this connexion is the blood. Now, chemical methods are not sufficiently reﬁned to detect the difference between the bloods of two animals and to estimate the degree of similarity which they show. It is possible, however, to have recourse to biological methods by making use of the property which animals possess of developing immunity. If horse’s blood, for example, is injected into the vascular system of a rabbit, the rabbit will after a time produce a substance in its blood which reacts to horse’s blood, and precipitates it. This is the same principle as that used for preparing antitoxins for certain diseases. As to how the antitoxin or antiserum is produced, little is known, but it suﬂices for present purposes to realise that in the hypothetical case just described rabbit’s blood immunised against horse’s blood will always precipitate horse’s blood, to the extent of 100 per cent. This means that anti-horse serum, as it may be called, is speciﬁc against horse, and it is a matter of no importance what kind of animal has been used to produce the antiserum. But the speciﬁcity against horse is not quite exclusive. Anti-horse serum, as it may be called, will produce no effect whatever if mixed with, say, blood of a bird; but it will produce a slight precipitation with blood of pig, and still more with blood of ass. This means that the blood of horse is more similar to that of ass than to that of pig, as regards its chemical composition, and this is just what would be expected from a knowledge of the comparative anatomy and embryology, and from the palreontology regarding these three species.

The precipitin blood-tests therefore furnish a means for estimating the relative similarities between the bloods of different animals, and they are not only a biochemical proof of the theory of evolution, but also an index for classiﬁcation. '

The following are a few tables showing the relative aflinities between the bloods of a number of vertebrates:“

' From Nuttall.

354 noon nnnarronsarrs 355 Anti-human serum mixed with blood of’:--1-W I ‘

Man gives I ‘ 100» per cent. precipitation. Got an 64 ‘ as A no " Orang Outang ,, 42 » ,, ~ ~* ,, Baboon 29 | .. ..

Ox 4?, 9! 10 so ‘ ' » Sheep " .. 10 .. l ..

Deer so " 7 99 at Horse .. 2 .. .. Marsupial « .. 0 .. ..

These results show several interesting points. In the ﬁrst place, the

great similarity between the blood of man and that of the gorilla,

should dispel any doubt (should any be left) concerning the evolution of man from other mammals. The precipitation percentages show that human blood is more like that of the apes than that of the baboon. and more like the latter than the blood of animals like horse and deer. This ﬁts in perfectly with evidence derived from other sources. It is also interesting to note that two animals which are believed to be closely related to one another like ox and sheep, should show the same degree of dissimilarity to man. The relationship between sheep and ox can also be tested by immunising a rabbit to sheep blood.

Anti-sheep serum mixed with blood of :Sheep gives 100 per cent. precipitation. Ox ,, 75 ,, ,, Antelope ,, 67 ,, ,, Reindeer ,, 35 ,, ..

The relationship between sheep and ox is here shown to be close. Other experiments have revealed the Artiodactyla as the nearest relatives of Cetacea.

Some of the most interesting results are those which refer to the relative aﬁinities between the various groups of reptiles, and between them and the birds.

Anti-fowl egg serum mixed with blood of :— Crocodile gave a positive result (precipitation) in 50 per cent. of cases.

Chelonian ,, ,, ,, .. 40 n so Lacertilian ,, ,, ,, ,, 7 n H

,, ' ,, ,9 9) 6 " ”

These results show that the reptiles (alive now) nearest akin to the birds are the crocodiles, which again corroborates all the evidence from other sources. It further indicates that the crocodiles and turtles are more closely akin to one another than they are to the lizards and 356 COMPARATIVE ZOOLOGY or cnonnnss

snakes, which; again,“ are fairly closely allied to one another. This is further shown‘ by the following:

Anti-chelonian serum mixed with blood of:— Chelonian gave a positive result in 87 per cent. of cases.

CTOCOCHIE H as as as as Laceniiian as as 97 0 4' n n Ophidian 9! so so 6 or n

In the Urodeles, serological tests have shown that the neotenous forms Siren and Necturus are more closely reiated to Triturus than to Cryptobranchus, which means that they are not primitive but

" secondary.

Besides the precipitin tests, there are other methods of estimating the blood-relationships of vertebrates. For one thing, it is found that blood of any particular species has the power of destroying the blood-corpuscles of other species, to an extent varying with the remoteness of the relationship between them. Again, it is found that the degree of virulence with which an animal will suffer from a human disease varies with its degree of kinship to man. So syphilis attacks the chimpanzee more seriously than the orang, and the latter more than the baboon. Lastly, attention may be called to the so-called blood-groups, into which the human race is divided. There are four of these blood-groups, and they are due to two agglutinating substances, which may be absent, or one, or the other, or both may be present, in the blood of a man, and cause clotting when the blood is mixed with that of another incompatible group. Incidentally these groups are further interesting in that they are inherited by means of Mendelian factors, but their main interest from the present point of view lies in the fact that the blood-groups and agglutinating substances are also found in apes. Here, therefore, are deﬁnite biochemical characters which are shared by apes and man.

LITERATURE

BOYDEN, A. The relative position of the Cetacea . . . as indicated by prccipitin tests. Zoologica, New York, Vol. 35, 1950.

BOYDEN, A. & NOBLE, G. K. The relationships of some common Amphibia as determined by scrological study. American Museum Navitates, Nr. 606. 1933.

LANDSTEINER, K., and MILLER, C‘. P. Serological Studies on the Blood of ‘ the Primates. Journal of Experimental Medicine, Vol. 42, 1925.

NUITALL, G. H. F. Blood Immunity and Blood Relationship. Cambridge University Press, 1904. PART IV EVOLUTIONARY MORPHOLOGY

CHAPTER XXXVI

run BEARING OF PHYSICAL AND CLIMATIC FACTORS ON CHORDATES ,4»

To understand their evolution and life it is essential to consider animals in relation to their environment. Dining the time since chordate animals ﬁrst appeared, the environment has changed very considerably at one time or another. Of the most primitive forms there is no record preserved, for the simple reason that these animals did not possess structures capable of preservation by fossilisation. The earliest known vertebrates are from the Silurian period about 350 million years ago, and they were Acrania and “fish”. The earth was at this time covered with shallow seas containing coral-reefs which are indicative of a mild climate. In the ensuing Devonian period, about 300 million years ago, shallow lagoons and enclosed basins of fresh water were in abundance, and the land which had emerged enjoyed desert conditions with little rainfall. It is towards the end of this period that the ﬁrst land-vertebrates (Stegocephalian amphibia) appeared. The next or Carboniferous period, about 250 million years ago, was one of tropical climates, during which luxuriant forests covered the land. The trees had no rings of growth which fact proves that there were no seasons. True reptiles first appeared here. In the late Carboniferous and Permian period about 200 million years ago, the climate became colder as the continents rose and mountain chains were formed, resulting in an ice-age or glacial period. In the following Trias, about 190 million years ago, warm conditions returned, without seasonal variation. The earliest known mammals belong to this period. Warm conditions persisted throughout the Jurassic period, from 170 to 140 million years ago, in which the ﬁrst birds are found, but this period is pre-eminently the “age of reptiles”, not only on account of the number of dillerent types which ﬂourished, but also because of the gigantic size to which many of them grew. _ _

In the Cretaceous, about 100 million years ago, cold conditions

returned with seasonal variations. Mountain-building and glaciation 357 358 EVOLUTIONARY MORPHOLOGY

occurred in shame parts of the earth, the temperature of which was now considerﬁbly reduced. At ‘this time and perhaps for this reason the majority «of the reptiles which had ‘T hitherto been so successful went extinct and were superseded by . mammals as the dominant

‘animals. After this time, hot conditions set in again for the main

Z part “of the Tertiary era which began 70 million years ago, gradually

«diminishing towards its close when a fresh bout of mountain-building erected the Alps. Then, about 1 million years ago, followed the great Ice-Age, with its four episodes of glaciation and three interglacial periods. Mammals continued evolving during all this period, towards the end of which man appeared.

3, The most important early changes in the environment as far as

the vertebrates were concerned were the drying-up of the lagoons and estuaries in the Devonian, and the variations of temperature.

It is a characteristic feature of desiccated areas that the water expanses which they possess shrink to ponds, and the oxygen-content of the water decreases owing to the quantities of decomposing organic matter with which the ponds become ﬁlled. Under such circumstances it is obvious that ﬁsh which are provided with means of supplementing their branchial respiration would have a much greater chance of surviving, and the ﬁrst step in this direction was the habit of taking air into the pharynx when at the surface. At the present day, inhabitants of such waters show diverse adaptations, but by far the most important of these from the present point of view are the Dipnoi, with their lungs. There is little doubt that the ancestors of the Tetrapods encountered and mastered conditions of desiccation in fresh water, in the same way as the modern Dipnoi. There is the further danger that under these circumstances the water may dry up altogether, as it does in the case of the swamps in which Praroprerus lives, and then the possession of a means for pulmonary respiration is the only condition for survival.

1

Temperature may vary in several different ways, either in spaceor in time, or in both. So the tropics and the temperate and polar regions differ in temperature, as do day and night or summer ‘and winter.

Homothermous animals are largely independent of temperature variation in the outer environment since they live in a constant internal environment of their own. However, the outer environmental temperature has a bearing on their size. This follows readily from a consideration of the ratios of surface to volume at different sizes. The surface increases as the square, but the volume increases as the cube of the linear dimensions, so that there is relatively more surface in small animals than in large ones. The importance of this for homotherrnous animals is that the amount of internal heat piivsicst AND CLIMATIC FACTORS 359

produced (by metabolism) and lost (by radiation) varies relatively with the surface. So, of two dogs weighing 20 and 3} kg. respectively, the former will have a surface of 7,500 sq: cm.,’the latter 2,423 sq. cm.

For every kg. of dog, there is in the large dog 375 sq‘; cm.,_ and in the, small one 757 sq. cm. of surface, and the amount of heat given of,"

from the dogs per kg. is twice as high in the case oﬁthe small dog as in the ease of the large one. *

Small homothermous animals therefore radiate ‘relatively more heat from their surface than large animals, and this heat-loss has to be compensated by relatively more active metabolism and intake of

I ‘l

l l

n

\

I4

food. In spite of the fact that mammals and birds grind their food .

up small (in the mouth in mammals: in birds, in the gizzard) so.

that the processes of digestion are accelerated, a stage of smallness is reached when the animals have to spend all their time feeding. Shrews and humining-birds are of about this size. If they were smaller than this they would need to consume quantities of food which they would not have time to eat. Especially true is this of regions in which because of seasonal variation the days are short for a period in each year. The ratio of surface to volume therefore establishes a minimum limit of size for homothermous animals in a given outer environmental temperature. ,

In cold climates, such as prevail in polar regions, homothermous animals tend to be large. They proﬁt by their relatively small surface from which they lose heat, and also by the fact that they do not require to spend all their daylight eating as they would if their surface/volume ratios were large and they were small in size. On the other hand, tropical homothermous animals can afford to be small and to have large surface/volume ratios. The intensity of heat radiation is less than in polar regions because of the higher temperature of the air, and small size enables them to get rid of their heat. Also, there is ample food, and daylight to eat it in, to make up for the heat lost. Homothermous animals as small as humming-birds could not live in really cold climates.

It is worth noticing that fat, which is a poor conductor of heat, forms a layer underlying the skin in the animals inhabiting polar regions (seal, penguin), and so assists in minimising the amount of heat lost by radiation. When, on the other hand, fat is stored by

‘homothermous animals living in hot climates, it is not distributed

under the skin all over the body, where it would interfere with heatradiation, but it is localised and forms humps as in the camel or the

zebu. . _ Whereas homothermous animals tend to be large in polar. regions and small in the tropics, poikilothermous animals show precisely the

opposite tendency, and for the same reasons. The reptile depends

a‘ 360 , EVOLUTIONARY MORPHOLOGY

on the outer environment for its heat. In cold climates, when it is not hibernating, it is to its advantage to absorb as much as possible of what heat there is. This is assisted by a large surface/volume ratio, ‘and consequently a small size. Effectively, it is found that the ﬁsh, ‘amphibia, and reptiles inhabiting cold climates are smaller than their relatives living under warmer conditions. For in tropical climates, these animals can afford to be large. The giant frogs, turtles, lizards, snakes, and crocodiles of the tropics illustrate this point well. The huge size of the reptiles in the Jurassic period must have been made possible by the hot conditions which prevailed then.

It is further to be noticed that in tropical regions the poikilothermous animals can compete successfully with the homothermous; whereas in polar regions the homothermous animals dominate over the poikilothermous by reason of their constant internal temperature. It follows that if a region of high temperature, populated by poikilothermous and homothermous animals, were to undergo a reduction of temperature (as by greater elevation of the land above sea-level or the approach of an ice-age), the homothermous animals would survive, whereas the poikilothermous forms would be very likely to go extinct, especially if they were of large size. This may be what happened at the cold end of the warm secondary era (Trias to Cretaceous inclusive, the “age of reptiles”), when the reptiles all but went extinct, and were only survived by the present-day forms, which furnish a miserable sample of former richness of the reptilian fauna. At the same time, the homothermous birds and mammals survived, the latter to become the dominant animals.

It is seen, therefore, that certain of the greatest episodes in the history of the vertebrates, such as the evolution of the amphibia, may have been largely conditioned by climatic changes in the earth's crust. Other episodes were probably related to adaptations to more ﬁxed climatic conditions. Of these, two only will be mentioned here» The first concerns the evolution of the early ﬁsh. The original ancestors of the chordates must have been marine forms, but there are certain considerations which suggest that the evolution of the early chordates took place in fresh or estuarine water. The typical chordate method of locomotion by undulations of the body from side to side may be regarded as an adaptation to life in rivers in which there is a more or less constant ﬂow of water in a certain direction. The glomerular kidney is also an adaptation to life in fresh water (see p. 301).

The other episode concerns the evolution of man, part of whose early ancestral history is related to the habit of living in trees. It is common for arboreal animals to retain unspecialised limbs, and to rmrsrcnr. AND cnmnrrc FACTORS - 361 k \

acquire the capacity of opposing one or more digits to the others, and so be able to grasp branches ﬁrmly. At the same time the sense of smell becomes less important, while that of sight becomes dominant, leading to binocular and stereoscopic vision, and the capacity to estimate distance. This is of importance to an arboreal animal in estimating the strength of its leaps from branch to branch. The neurological changes which accompany these anatomical ones are the subordination of the olfactory cortex of the cerebral hemisphere (hippocampus) and the elevation of the non-olfactory cortex or neopallium to a dominant position. In other words, arboreal life favoured the development and evolution of the brain, which is the organ which most distinguishes the Primates, and especially man, from the remainder.

In previous paragraphs it was shown how the minimum limit of size of homothermous animals was determined, and it was found to ’ be aﬁ'ected by the climatic temperature. The minimum size of poikilothermous Tetrapods has no relation to temperature, but is determined by the capacity of the muscles to actuate the skeleton and move the animal about.

The maximum size of landwertebrates is limited by the ratio between the weight of the body and the supporting strength of the legs. The weight varies with the volume, which is proportional to the cube of the linear dimensions of the animal. But the strength of the legs is measured by the cross-sectionaharea, which is proportional to the square only of the linear dimensions. The larger the animal is, therefore, the relatively heavier will the load be which the legs have to carry. If the length of a rabbit is 10 times more than that of a mouse, the weight which the rabbits legs carry is 1000 times greater than that which the legs of the mouse support. Against this the cross-sectional area of the rabbit’s leg is 100 times that of the leg of the mouse. The result is that the weight per square millimetre on the legs of the rabbit is 10 times more than that on the legs of the mouse. As the strength of the skeletal material (bone) cannot be increased, a stage is reached at which the legs can no longer safely carry the weight of the body, or they must be so large as to be almost immovable. Already in the elephants they are like pillars, and these animals are near the maximum size for land-vertebrates. For aquatic forms, the conditions are of course different, since by Archimedes’ principle the buoyancy of the water reduces the relative weight of the animal, which is usually not borne on the limbs at all. So the whales and sharks can reach sizes which are impossible for land forms. For this reason, it is likely that the largest of the Dinosaurs

were more or less aquatic. 364 , EVOLUTIONARY MORPHOLOGY

Allied to Baianoglosm are the Pterobranchia, which show some chordate features, but no dorsal tubular nerve-cord. One of them, Cephalodiscus, has the three sets of ccplomic pouches, each with a coelomostome, and a pair of gill-slits. Itis sessile, reproducing actively by budding. Atubaria seems to have nephridia. Apother, Rhabdopleura, is not only sessile but colonial, for the buds formed remain in connexion with the parent stock. Rhabdopleura has the three sets of cmlomic pouches, and cmlomostomes, but no gill-slits. The fossil Graptolites were perhaps related to these forms.

The next form to consider is Phoronis, which is worm-like with the anterior end modiﬁed into a row of tentacles. The anterior region of the body corresponding to the proboscis is reduced to a ﬂap overhanging the mouth, so that the body contains only two sets of coelomic pouches. The larval form of Phoronis, which is called the Actinotrocha, has ciliated bands reminiscent of those of the Tornaria. Plzoranis has nephridia, and as these structures are also present in Amplzioxus, it is possible that they were present in the original common ancestor from which all these forms were descended.

Phoronis is related to the Ectoproctous Polyzoa, and to the Brachiopoda. All these forms, so far as is known, tend to have ccelomic pouches developed as enterocoels, and usually showing a tripartite arrangement. Many of them have open cmlomostomes. The larval forms usually have a ciliated band passing behind the mouth, and cleavage of the egg is indeterminate. These features distinguish the chordates and their allies from the other great group of invertebrates comprising the Annelida, Arthropoda, and Mollusca.

There is reason to believe that the concentration of nerve-cells to form a central nervous system out of the more primitive diffuse nerve-net took place in the region of greatest stimulation. This is the ventral side in Annelida, Arthropoda, and Mollusca, all of which typically crawl on the ventral surface. The fact that the central nervous system of chordates is dorsal seems to show that the ancestral chordates were not ventral crawlers, but pursued a freeliving pelagic existence, receiving the greatest stimulation on the dorsal side from the surface of the sea. There is some reason to suppose that these ancestral chordates resembled the larva: of Echinoderms and of Balanoglossus.

Returning now from these more or less distant allies to true chordates, the next group to consider is one which, like the Hemichordates, has left the main line of chordate evolution and become specialised in different directions: the Urochordata. These preserve the notochord in the tail in the larval stage only, and the dorsal tubular nerve-cord of the larva degenerates in the adult. They possess Tl-[B ORIGIN OF CHORDATES

Figure 175. A few examples illustrating the radiation of the lower chordates as aquatic animals. (Not drawn to scale.)

a, Balanoglosms: b. larva of an Eehinoderm for comparison with _c, Tornaria l:_u'va of Balanogbgsta; J, Ascidian (sessile degenerate type); e, restoration of Cephalaspis (Ostracoderm); L typlgal Teleost W311} homocercal tall; 3', eel; I1, (deep~sea type, with dwarf male attached to female); 1', Rain (SelachIa_n bottom-living type); j_, sole (Teleost bottom-living 15: type: “ﬂat—ﬁsh"); k, Exoca-ms (so-called “ﬂying ﬁsh"). (2 after Goodnch, I: after Regan, simplified.) in 366 svonurronxnv MORPHOLOGY

gill-slits, and a typical well-developed endostyle, used in connexion with the method of feeding. Their development is also typical of chordates.,;;One group of these animals, the Larvacea, retainsthe larval structure throughout life, with the tail and notochord. The others pass through a free-swimming larval stage, and then undergo

»a retrograde metamorphosis into sessile animals, losing the tail,

notochord, and larval eyes and organs of balance. These are the Ascidiacea or sea-squirts. Some of these are solitary, but most are colonial, reproducing extensively by asexual reproduction or

" budding, as is commonly the case with sessile forms. Others, forming

the group of Thaliacea or salps, have returned to a free-swimming existence, but retaining many traces of former sessile habits; in particular the habit of budding, which is very prevalent. Some of them have a true alternation of sexually produced (from fertilised eggs) and asexually produced (from buds) generations; and one form is further interesting in that the sexually produced generation is nourished during its development by the mother by means of a placenta (SaIpa).

None of these forms, however, exhibit the typical chordate segmentation of the body, which enables them to swim in deﬁnite directions instead of being carried aimlessly about at the mercy of currents. The immediate ancestors of Amphioxus and of the higher chordates were elongated, compressed from side to side and deep from dorsal to ventral edge. As a consequence, they were able to bend the body from side to side, and perform undulatory movements. The body was made up of several segments. Each segment was separated from the ones in front and behind by septa or partitions, and stretching from septum to septum were the myotomic muscleﬁbres. When the myotome on one side of a segment contracts, the septa bounding that segment come closer together, and the body becomes concave on that side. The advantage of having several segments made it possible for the body to bend in several places. By bending alternately right and left in successive regions of the body, and making the bends pass down the length of the body by throwing the myotomes into contraction in succession, the undulatory movements are produced which enable the organism to swim. These movements were made still more eﬁicacious by lengthening the body, which was accomplished by the development of an extension behind the anus forming the tail. After bending in any place, the body became straight (before bending in the opposite direction), and this was elfected not only by the relaxation of the myotome on that side, and the contraction of the myotome on the opposite side, but by the possession of a still‘ yet elastic rod running along the whole length of the animal: the notochord. This is the typical primitive ma ORIGIN or cnonnsrss 357

method of chordate locomotion which persists not only in the ﬁsh, but also in the lowest land-vertebrates.‘

The fact that the animal moved in aideﬁnite direction had um

consequence that the front end was‘ further specialised by a con-‘

centration of sense-organs, which ultimately was to bring about the formation of a head and of a skull which is characteristic of the Craniata. '

It has been held, with some degree of probability, that the habit of swimming in a deﬁnite direction was evolved in response to the constant direction of flow of water in rivers or large estuaries, and that the evolution of the early true chordates took place in such surroundings. The formation of the glomerular type of kidney also suggests that the early vertebrates evolved in fresh water.

The ciliary method of feeding which these animals possessed limited the size of the particles of food which they could ingest, and the size to which they could grow.

The earliest recognisable chordates of which fossil remains are known include Jamoytius from the Silurian. With its v-shaped myotomes like those of Amphioxus, continuous median and lateral ﬁn-folds, and its unarmoured skin, it probably represents the most primitive chordate yet known, belonging to a group from earlier members of which the Craniata might have evolved.

At about the same period there appear the Ostracodcrms (from the upper Silurian and Devonian), which recent work has shown to be related to the Cyclostomes, especially as regards the brain. auditory organs, and blood-vessels. This raises some interesting problems, because the Ostracoderms possessed denticles, bone, and paired ﬁns, all of which structures are lacking in Cyclostomes. The mode of life of Petromyzon, Bdellostoma, and M yxine is undoubtedly degenerate with their sucking mouth, but they would be more degenerate than otherwise expected if they had lost the structures possessed by the Ostracoderms. The curious fossil Palceospondylus (from the Devonian) may be related to these forms, in all of which evolution had proceeded far enough for the formation of a deﬁnite head.

The ﬁrst Gnathostomes, i.e., Craniata provided with biting jaws, to appear are the Acanthodians (upper Silurian), which had skeletons of cartilage and bone and in which the hyoid arch and slit were similar to the branchial arches and slits behind them (the Aphetohyoidea). All these forms had two pairs of paired ﬁns, and heterocercal tails.

The ﬁrst true ﬁsh or Pisces (in which the hyoid arch,support_s the jaws) to appear are the bony ﬁsh or Osteichthyes In the middle Devonian, and the lungs which they possess were pT0i_’3blY_lﬂ connexion with the poor oxygen-content of the fresh water in which 368 EVOLUTIONARY MORPHOLOGY

they lived. The Dipnoi were represented by Dipterus (Devonian), and the non-Dipnoan bony ﬁsh, or Teleostomi, were represented by Ostealepis (also Devonian). These two forms were closely related, and they had the following characters in common: blunt lobate ﬁns, a pair of external and a pair of internal nostrils, the general arrangement of the bones of the roof of the skull, heterocercal tails, and, most important of all, cosmoid scales. There is no doubt that they had a common ancestor, perhaps in the Silurian, and from a close relative of this ancestor the Tetrapods arose. One of the Osteolepidoti, Sauripterus, had ﬁns from which the structure of the pentadaetyl limb of the Tetrapod might be derived. In the Ctelacanths, which are Teleostomes related to the Osteolepidoti, there is deﬁnite evidence of the presence of a lung, for it was calciﬁed and fossilised. The Coelacanths are represented today by Latimeria. The Dipnoi evolved into the forms living at the present day, and became more and more adapted to life in rivers which are liable to dry up. The wide and discontinuous distribution of Ceratodus (Australia), Lepidosiren (South America) and Prozopterus (Africa) today is evidence of the antiquity of the group. The evolution of these forms went on parallel to that of the early Tetrapods, and independently from them.

On the Teleostome side, another group arose in the Devonian from some relatives of the Osteolepidoti: the Palaeoniscoidea. These ﬁsh are characterised by the possession of scales of the type called palzeoniscoid. Cheirolepis resembled Osteolepis in the structure of its skull, but its eyes were larger and the heterocercal tail was more accentuated. This provision for more active swimming was probably connected with the improvement of the eyes as sense-organs. Polypterus, alive today, may be regarded as a descendant of the Pala:oniscoids. It has palzeoniscoid scales, and preserves the open spiracle. It inhabits certain rivers in Africa. On the other hand, the Palaaoniscoids also gave rise to the sturgeons. Chondrosteus (Jurassic) is already like the sturgeon Acipenser. These animals preserve the open spiracle, but the palaaoniscoid structure of the scales is lost. Sturgeons are both ﬂuviatile and marine.

Another line of evolution from the Palaeoniscoids leads to the higher bony ﬁsh or I-lolostei. These ﬁsh lose the open spiracle and their tails assume the homocercal pattern. At the same time the radials of the paired ﬁns become reduced, and the web of the ﬁn is supported mostly by the dermal ﬁn-rays or lepidotrichia. In the median dorsal and ventral ﬁns the lepidotrichia correspond in pairs to the radials, so that the ﬁns can be lowered and raised. Of the Holostei, two groups are primitive. One of these contains Amia, an inhabitant of the rivers of North America. Its lung is still highly ms oiucm or cnonmxras 359

vascular and supplied by pulmonary arteries, and in the region of the tail its vertebral column consists of separate hypo- and pleuracentra. The other group contains Lepidosreus, likewise an inhabitant of North American rivers. Its scales are of the peculiar pattern known as lepidosteoid, with a covering of ganoin. The lung is vascular, but supplied by arteries from the dorsal aorta. It is worth noticing that the primitive Osteichthyes are ‘almost exclusively inhabitants of fresh water. '

In the remaining highest bony ﬁsh or Teleostei (a term not to be confused with Teleostorni), the scales lose the layer of ganoin and become thin and transparent. The lung becomes modiﬁed into a swim-bladder, and loses the vascular spongy walls characteristic of a lung. It functions as a hydrostatic organ of adaptation to different depths, and this illustrates the fact that the Teleostei are a group which has reinvaded the sea from fresh water. Rivers do not possess sufficient depth to necessitate a swim-bladder. A number of Teleosts, however, are inhabitants of fresh water, to which they have presumably returned from the sea. The Teleosts have radiated into a great many different lines, and are the most successful of the ﬁsh. They have become specialised to various modes of life, but they must be regarded as a sterile side branch on the tree of vertebrate evolution, for their specialisations have prevented them from evolving into anything further. Although some of them, such as Periophthalmus, are capable of coming out on dry land and hobbling about, they cannot compete with the true land-vertebrates, which are less specialised but more progressive descendants of their ancestors, the pre-Osteolepids. Of the adaptations which Teleostei have undergone, one of the most interesting is the modiﬁcation in connexion with the habit of living on the sea-bottom, and which has resulted in the “flat ﬁsh”. When hatched, these ﬁsh, of which Select (the sole) is an example, are normal and symmetrical in form but they undergo a metamorphosis as a result of which they lie on one side on the bottom. The head becomes twisted so that the eye of the “underside” (right or left, according to the species) moves on to the “upper side”. It is interesting to compare this ﬂattened condition of the body with that of the rays. The modiﬁcations in the two groups are totally different, but both are adaptations to one and the same mode of life, and this accounts for what similarity there is between them.

The so-called ﬂying ﬁshes, of which Exocartus is an example, have enlarged pectoral ﬁns, and are capable of prolonged leaps through the air rather than of true ﬂight. Lastly, attention may be called'to certain deep-sea ﬁsh Edriolyclinus, which are not only of a peculiar shape, but are remarkable in that the males are dwarfed and

l3—v.z. 370 EVOLUTIONARY MORPHOLOGY

degenerate, and live attached to the females on which they are parasitic. .

Returning now to the upper Devonian, the cartilaginous ﬁshes or Chondrichthyes make their appearance with Cladoselache. Their possession“of cartilage but lack of bone raises the question whether the Chondrichthyes may not have lost the bone perhaps possessed by their ancestors, and which was present in the Ostracoderms and Osteichthyes, which appear before the Chondricthyes. But although the Chondrichthyes appear later than the Osteichthyes, they seem to present a lower grade of structure and organization.

True Selachii related to Heterodontus (the Port Jackson Shark) appeared in the Carboniferous. Pléuracanthus appears in the Permian. At the present day, the Selachii are represented by the true sharks (and dogﬂsh), and by the rays (Raia, Torpedo), which have become adapted to living on the sea bottom and have become ﬂattened in consequence. Their pectoral ﬁns have expanded and fused with the sides of the body. The gill-slits are on the under surface, the spiracle is above. One member of the rays, Pristis the saw-ﬁsh, has returned to an active mode of life. The angel-ﬁsh Rhino is intermediate in form between the sharks and the rays.

Another group of cartilaginous ﬁshes diverged in the Devonian and gave rise to the Holocephali, represented at the present day by Chimera.

LITERATURE

BULMAN, O. M. The Caradoc Graptolites. Memoirs of the Paleontographical Society. London, 1944-7.

DELAGE, Y., et HEROUARD, E. Zoologie Concrete, 8, les Procordés. Schleichcr Frércs, Paris, 1898.

KOMAI, T. Internal structure of the Pretobranch Atubaria. Proceedings of the Japan Academy, Vol. 25, 1949.

MOY-THOMAS, J. A. Palteozoic Fishes. Mcthuen, London, 1939.

REGAN, C. T. Dwarfcd Males parasitic on the Females in Oceanic AnglerFishcs. Proceedings of the Royal Society, B, vol. 97, 1925.

WATSON, D. M. S. The Acanthodian Fishes.PhilosophicalTransactions of the Royal Soct'et_r. B, vol. 228. I937.

Wtu't‘E, E. I. Jamoytius kerwoodi. Geological Magazine, vol. 83, 1946. CHAPTER XXXVI“

THE EVOLUTION on THE AMPHIBIA: THE FIRST LAND CHORDATES

THAT the amphibia arose from ﬁsh there is no doubt, and their ancestor must have been one of the primitive Osteichthyes, related to the stock which also gave rise to Ostealepis and Dipterus. For

purposes of comparison Osteolepis may be taken as approaching the structure of this ancestor.

The resemblances between Osteolepis, on the one hand, and one of the earliest Stegocephalian amphibia such as Loxomma on the other, extend to the following features. In both, the skull is a complete bony box, the dermal bones of which can in most cases be identiﬁed with certainty because the amphibia also had lateral-line canals which occupied grooves in the bones. The bones of the palate are similar, and both had nostrils which lead through into the cavity of the mouth. The amphibian Eogyrinus had a shoulder girdle the dermal bones of which were attached to the post-temporal bone of the skull by the supra-cleithrum, as in the ﬁsh. Also, these early amphibia had no sacrum, for the ilium was not attached to the ribs. The walls of the teeth were folded, in the Labyrinthodont pattern. The amphibia are autostylic, as are the Dipnoi including Diptivmr. The amphibian Ichthyostega is the most primitive yet known, and, like 0.rteoIepz°s, it has nostrils on the ventral side of the snout, and the lateral-line canals run in tubes in the bones.

The ancestor of the Tetrapods must, however, have had pectoral and pelvic ﬁns equally developed and similar in structure, and this condition has not yet been found in any Osteolepid (or other) ﬁsh. The really distinctive feature of all the Tetrapods is the possession of limbs ending in ﬁve digits, and it has already (see p. 272) been shown that the skeleton of the pectoral fin of the Osteolepid ﬁsh Saurrpterus is such as to render it easy to suppose that the pentadactyl limb arose from a ﬁn like that of the Osteolepids. 0SI€01£’pl.$‘ is Devonian, and the earliest known amphibia are from thc_lowcr Carboniferous. It is fairly certain, therefore, that at some llm8‘lll the Devonian ﬁsh living in the estuaries and fresli-water basins became subjected to the desiccation which characterised this period. They were able to breathe atmospheric oxygen by means of their

nostrils and lungs, and as they flilaundered about in the mud, the 37 372 EVOLUTIONARY MORPHOLOGY

number of rows of radials in their ﬁns became reduced to ﬁve, separate from one another instead of being united by the web of a fin. The persistence of the lateral-line canals shows that these animals still spent much of their time in the water, and their excursions on land probably took the form of wandering from pond to pond. In fact, the amphibia never succeeded in making themselves completely independent of water, and for three reasons. In the ﬁrst place the eggs had to be laid in water, and the larval stages which breathed by gills required then, as they do now, a watery medium. Next, fertilisation was external, and for the sperms to be able to ﬁnd the eggs,

Figure 176. A few examples of differelnt types of Amphibia. (Not drawn to sea e.)

a, restoration of Stegocephalian; [2, male newt in breeding season (Urodele); c, Amblysroma (larval form or Axolotl showing the external gills); d, frog (Anuran); c, lchtltyophis (Gymnophiona). (c after Sarasin).

there must be a liquid medium for them to swim in. Lastly, amphibia breathe largely through their skins, and these must be moist to enable the gaseous exchange to take place.

The transition from water to air necessitated a development of the olfactory organs to greater sensitiveness, for the concentration of substances in water is very much greater than that which can be obtained in air. The result was an increase in development of the olfactory organs and of the corresponding centres in the forebrain. The latter development accompanied and perhaps assisted the formation of the cerebral hemispheres, which are regarded as TI-IE EVOLUTION or rm: AMPHIBIA _, 373

connected with an adaptation to the poor oxygen-content of the water in which the amphibia and their ancestors evolved.

It appears, therefore, that the transition from aquatic to terrestrial life was accomplished without any very striking changes or modiﬁcation of organs, but it must be remembered that the function of these organs is controlled by the pattern of nerve-ﬁbres in the central nervous system, and it becomes necessary to inquire whether the transition necessitated any great neurological rearrangement. Two aspects of the transition will be considered, regarding breathing and locomotion. In connexion with respiration, it will be remembered that the amphibia breathe by means of respiratory movements performed by the visceral muscles in the ﬂoor of the mouth, in a manner very similar to that of the fish. The only real difference is that whereas the ﬁsh take in water and pass it back and out through the gill-slits, the amphibia take in air and pass it back and into the lungs. The mechanism is the same, and it is obvious that the transition from water to air involved no functional rearrangement of importance as regards respiration.

The same holds true with regard to locomotion. The amphibia were clumsy sluggish beasts with bodies disproportionately large in comparison with their limbs. As a consequence, the body was not supported by the limbs but its ventral surface dragged along the ground. The limbs stuck out at right angles to the body. and as the body performed the same undulatory movements by means of the myotomes as does a ﬁsh when swimming, the limbs were moved forwards and backwards. In other words, the limbs were used as oars to row the animal along on land, and the same muscles and nervous coiinexions came into play as in the aquatic ancestor. In the very earliest Amphibia, the sacrum was absent (e.g., Eogyrinus). In the others it was present, and by anchoring the pelvic girdle on to the vertebral column, it strengthened the hind limbs.

One consequence must be mentioned of the possession of an autostylic method of suspension of the jaws, and of the abolition of branchial respiration and the closure of the visceral clefts, in particular the spiracle. The hyomandibula being no longer required to suspend the quadrate from the auditory capsule, its function became converted into that of conveying vibrations from the skin covering the spiracular cleft to the auditory capsule. In this way the hyomandibula became the columella auris; the covering of the spiracular cleft became the tympanic membrane, and the cavity of the spiracular cleft became the middle-ear and Eustachian tube; all quite simply and without involving any great rearrangement. So the ear became an organ for the delicate appreciation of sound as well as balance.

The early amphibia had a covering of dermal bones more or less 374 EVOLUTIONARY MORPHOLOGY

all over the body. The vertebral column of the earliest forms, or Embolomeri, is remarkable in that each vertebra possessed two centra. There was an anterior hypocentrum and a posterior pleuracentrum. The later amphibia preserved the hypocentrum at the expense of the pleurocentrum, which disappeared. It will be seen that in the reptiles the opposite occurred.

Collectively, the early amphibia are known as the Stegocephalia or Labyrinthodonts, the former term referring to the complete bony covering of the skull. They ﬂourished in the Carboniferous, and persisted until the Triassic period, when they were extinguished by the competition of their more successful descendants the reptiles. The Carboniferous Embolomeran Miobatraclzus may well have been ancestral to the Triassic Anuran Protobatrachus. Besides the Anura there are alive today only the Urodela and Gymnophiona as very specialised relicts of the amphibia. An important feature in the structure of the amphibia is the outgrowth from the gut to form a bladder. It is homologous with the allantois of the Amniotes.

With regard to the living amphibia, it is most important to realise that they have departed far from the primitive type of their Stagecephalian ancestors. This is shown by the great reduction in the bones of the skull and other parts of the skeleton. The Gymnophiona have evolved a worm-like burrowing habit; the frogs have become modified in connexion with the habit of leaping with the hind legs, and the newts have become secondarily readapted to living in water. Many of them (Cryptobranchus, Siren, Necturus) are neotenous, i.e., they do not undergo metamorphosis and they resemble larvae. In some points, the newts of today resemble living Dipnoi. It is of the utmost importance, however, to realise that these resemblances are due to parallel evolution and convergence, and not to genetic aﬂinity. It is only necessary to look at the list of specialised characters of Ceratodus to see that forms like it could not have given rise to the Tetrapods: they are cousins and not ancestors. Similarly, an examination of the specialised characters of Triturus and a comparison between it and the Stegocephalia show that all the points in which Triturus resembles Ceratodus have been evolved within the amphibia, and a long time after the amphibia came on land.

LITERATURE WATSON, D. M. S. The Structure, Evolution and Origin of the Amphibia. Philosophical Transactions of the Royal Society, Ser. B, Vol. 209, 1919. —-—. The Evolution and Origin of the Amphibia. Philosophical Transactions of the Royal Society, Ser. B, Vol. 214, 1926.

—. The Origin of Frogs. Transactions of the Royal Society of Edinburgh, Vol. 60, 1940.

WESTOLL, T. S. The origin of the Tetrapods. Biological Reviews, Vol. 18, CHAPTER XXXIX t THE EVOLUTION OF THE REPTILES

THAT the Reptiles were evolved from the amphibia there is no doubt whatever, and indeed, in some cases it is difiicult to decide whether a fossil is an amphibian or a reptile. The most important distinctive reptilian features are that the centre of the vertebral column are formed from the pleurocentral elements while the hypocentral elements are very much reduced, and the absence of grooves for lateral-line canals on the skull. This latter point shows that the reptiles had become deﬁnitely terrestrial. They emancipated themselves from the water by overcoming the three obstacles which checked the amphibia; viz. the necessity of water for breathing, for copulating, and for the embryo to develop in.

The ﬁrst of these was countered by a better development of the lungs and the adoption of the method of expanding the thoracic cavity by means of the ribs, for replenishing their content of air. The skin was thus enabled to become dry and horny, and to be of greater eﬂiciency in protection.

The next diﬂiculty was surmounted by the development of copulatory organs with which the sperm can be inserted straight into the oviducts of the female, and fertilisation is internal. The sperm swims to the egg in the mucous ﬂuid of the oviduct instead of in the pond water.

The last obstacle was overcome by a group of adaptations. The egg is laid on land, and the albumen surrounding it is itself surrounded by a shell composed of lime salts secreted by the oviducts. In this way the egg is protected from drying up, and from becoming ﬂattened and collapsed like a “poached egg”, which it would otherwise be. The embryo becomes surrounded by upgrowths of the blastoderm forming the amnion and enclosing the amniotic cavity. The embryo develops in the ﬂuid contents of this cavity. which may thus be regarded as an artiﬁcial enclosed pond. The food requirements of the developing embryo are met as in lower forms by a store of yolk in the yolk-sac. This entailed no new modii_'ications by itself, but as embryonic development takes a longer time, the quantity of yolk in the egg is relatively greater and this necessitated the modiﬁcation of the process of gastrulationi and the f0Tm3“°"

of a primitive streak. There remained the diliiculty of breathing, for 375 376 avowrronxnv MORPHOLOGY

although the gill-slits were developed they opened into the amniotic cavity, the oxygen-content of which could not be renewed. The problem was solved by the development of the allantois, representing the bladder of the amphibia. The allantois becomes applied to the inner surface of the porous shell, and as it is highly vascularised, the respiratory exchange takes place in it. At the same time, the allantois serves as a receptacle for the non-volatile excretory products of the embryo during development. Because of these structural adaptations, the reptile does not pass through a metamorphosis, but hatches from the egg as a more or less perfect miniature replica of the adult.

In the reptiles, the head is capable of extensive independent movement, and a deﬁnite neck is formed. In this connexion, the two ﬁrst vertebrae become modiﬁed into the atlas and the axis.

One of the most interesting forms is Seymouria (Penman), and it is remarkable for the fact that its characteristics are not intermediate between those of amphibia and of reptiles, but some of its characters are frankly amphibian and others reptilian. Seymouria is therefore a mosaic transitional form. It is probable that the transition from amphibia to reptiles took place in the Carboniferous.

Pareiasaurus belongs to the group of Reptiles known as Cotylosaurs, and they preserve the complete covering of dermal bones over the skull which they inherited from their Stegocephalian amphibian ancestors. The nature of the skull is of importance in tracing out the lines of evolution of the reptiles, and those forms in which the roof is complete and imperforate are often grouped together as the Anapsida.

The Chelonia are often classiﬁed among the Anapsida because their skull-roof is not fenestrated, although it may be reduced by emargination; i.e., bones may be lost round the edge but there is no separation of bones by a perforation forming a fossa. The Permian fossil Eunotosaurus which had osteoscutes and expanded ribs appears to be intermediate between Cotylosauria and Chelonia. The Chelonia preserve the osteoscutes (which covered the body of the Stegocephalia) and they contribute to the formation of the carapace which is so distinctive a feature of the Chelonia. The Triassic Triassochelys still had teeth and a cleithrum; these structures are absent from existing forms. The clavicular pectoral girdle of existing Chelonia. consisting of clavieles and interclavicle, is associated with the ventral covering of osteoscutes that form the plastron. The scapular pectoral girdle consists of a coracoid and a scapula bearing a large process as big as itself, directed forwards and inwards. This girdle and the pelvic girdle are remarkable in that they are situated within the ribs instead of outside them as in normal forms. It is interesting to note Figure 177. A few examples illustrating the radiation of the reptiles. (Not drawn to scale.) (Partly after Osborn and Lull, simpliﬁed.)

a. restoration of Pareiasaurus (cotylosaur); b, Sphenodan; c, restoration of Plesiosaur (aquatic adaptation); d, restoration of lchthyosaur (aquatic adaptation): a, tortoise (C itelonian); 1; snake (Ophidian); g, restoration of Tyrannosaurus (Dinosaur): Ir, restoration of St:-gamurus (Dinosaur); z’, restoration of Triceratops (Dinosaur); j, restoration of D1'pIad'ocu.r tbtnosaur); A-, restoration of Pterosaur (aeriai adaptation); I, crocodile; m. restoration of Cvnagnatlua ('I'herornorph).

rm: EVOLUTION or run REPTILES 377 378 EVOLUTIONARY MORPHOLOGY

that some Chelonia have become secondarily adapted to life in water, and their. limbs have been modiﬁed into paddles or ﬂippers, as in the turtles.

The osteoscutes of the carapace are covered by corneoscutes (“tortoise-shell") except in Sphargis, the “leathery turtle”, which form is further interesting in that the carapace attached to the expanded ribs as in other Chelonia is not present. Instead there is a bony shell formed of a great many little polygonal osteoscutes bearing no relation to the ribs.

The 5th metatarsal is hook-shaped in the Chelonia, but normal in the other Anapsida (Cotylosauria).

The next group of reptiles to consider is the Synapsida. They are characterised by the fact that the skull-roof is perforated by one inferior temporal vacuity or fossa, on each side, and the 5th metatarsal is normal. Here belong the Plesiosaurs and Theromorphs.

The Theromorphs are a very important group. They appear in the Permian, and preserve many primitive characters. They may have a precoracoid as well as a coracoid in the shoulder girdle, and some even retain the cleithrum. The most highly developed forms are the Theriodonts, which are the ancestors of the mammals, and they foreshadow the characters of the latter in many respects. The skull had two occipital condyles, a false palate was present, and the teeth were modiﬁed into incisors, canines, premolars and molars. The dentary was large and beginning to take on the articulation with the squamosal, while the quadrate became small and loose. In the pelvic girdle the ilium showed the mammalian character of pointing forwards, and the limbs were long and supported the body clean off the ground. A typical Theriodont is Cynognathus, but it is probable that several of its characters were evolved parallel with the mammals, having been derived from a more primitive ancestor common to it and to the mammals.

Among Synaptosauria, the Sauropterygia or Plesiosaurs have become secondarily adapted to an aquatic mode of life. They preserve primitive features such as the gastralia, which are remnants of the ventral dermal bones or osteoscutes of the Stegocephalian amphibia, but their limbs become modiﬁed into paddles. This modiﬁcation has not proceeded as far in the Triassic Nothosaurus as in the Jurassic Piesiosaurus. The Plesiosaurs reached lengths of 50 feet.

In the next group or Parapsida, the roof of the skull was perforated by a single superior temporal vacuity, above the post-orbital and squamosal bones. The hind border of the vacuity is formed by a bone concerning the homology of which doubt remains (see p. 86), but which may be the supratemporal. Here belong the Ichthyosaurs and the Squamata (Lacertilia and Ophidia). run EVOLUTION or ran REPTILES 379

The Ichthyosaurs are primitive in retaining the gastralia, and a foramen for the pineal eye between the parietals, but otherwise they are specialised in adaptation to an aquatic mode of life. Median dorsal and tail-ﬁns are developed, and the limbs become modiﬁed into paddles, so much so that it is impossible to determine the nature of the 5th metatarsal. A series of progressive modiﬁcation can be traced from the Triassic Mixosaunis, through the Jurassic Ichthyosaurus to the Cretaceous Oplithalmasaurus. They reached lengths of 30 feet.

All the Squamata which possess limbs have a hook-shaped 5th metatarsal. The ﬁrst group of these are the Lacertilia, ﬁrst appearing in the Jurassic, and represented now by the lizards, geckos, and chamaeleons. In the Cretaceous, a group of Lacertilia became adapted to an aquatic life——the Mosasauria. They_ reached a length of as much as 40 feet, and their limbs became modiﬁed into paddles. The second group of the Squamata are the Ophidia or snakes. It is characteristic of the Squamata that the quadrate is loose,_and in the Ophidia the two halves of the lower jaw are separate, which enables relatively enormous mouthfuls to be swallowed. . _

The remaining reptiles form the group Diapsida, for their slcull roof is perforated by two temporal fossie or vacuities on each side. So far as is known, all of them have a hook-shaped Sth metatarsal. Here belong the Rhynchocephalia, the Crocodilia, the Dinosaurs and the Pterosaurs, and the Diapsida also contained the ancestors of the birds. _ _ _

The Rhynchocephalia appear in the Triassic with Rhyn_chqs_t1uru_S. and are represented today by Sphenadorh The)! 31:6 P1‘1m't'V° “‘ retaining the gastralia. The Triassic Thalattosaurs, which had paddlelike limbs, were probably related to the Rhynchocephalia. _

The Crocodilia form a large group of generalised reptilcs. P05531131’ dating back to the Permian. The Triassic Pseudosuchia, of w ic Euparkeria is an example, are regarded as related to the ancestors of the Rhynchocephalia, the Dinosaurs and Pterosaurs, the existing crocodiles and the birds. The living crocodiles and a11lSf“°L-9 '3 zfdc the gastralia, and other deriiial ossiﬁcations. Mention may] 6 V13} ich of the Jurassic Thalattosuchia, yet another QFPUP Of 3’P:!]:’5 mum became secondarily adapted to aquatic life with Pad f" fiic an‘

The Dinosaurs were the dominant animal_s_in the C and Cretaceous. The skull had two temporal vacuities on ego ‘dal. and in addition a prelachrymal vacuity. Sor_ne Werc flUﬁuT1‘t’:P‘i*mmemc herbivorous, such as Diplodocus (JU_F3S51°)» 1'°;‘;‘l’1h‘f“5§midab1c tccth length of fe-ct. Others were camnf,'Omul§m“l,>ls soo that they were and the hmd hmbs larger than the me If H "s T vrminosauritg. probably bipedal. An example of 5°C“ 3 °”" ‘ ’ ’ 380 EVOLUTIONARY MORPHOLOGY

Cretaceous, reaching almost 50 feet in length. The foregoing types of

Dinosaurs had a pelvis of normal shape, and are grouped together under the term “Saurischia". The remainder, Predentata (or

Ornithischia), have an additional post-pubis which stretches back beneath the ischium, and a predentary bone in the lower jaw. The Predentata include the herbivorous bipedal Iguanodon from the Cretaceous, over 30 feet long; the absurd-looking Stegosaurus with its armour of large bony plates (Jurassic, 20 feet long); and the horned Triceratops (Cretaceous, 25 feet long).

The Pterosaurs were closely allied to the Dinosaurs, and like them had a pair of temporal vacuities and a prelachrymal vacuity on each side. They also preserved gastralia, and while some had teeth others were toothless. The fore limbs were modiﬁed for ﬂying, by means of a web of skin stretched from the greatly elongated fourth ﬁnger. The Cretaceous Pteranodon had an expanse of wings measuring 25 feet.

Of all this enormous wealth of reptilian life which dominated the land, water, and air, in the Jurassic and Cretaceous periods, only the Squamata, the Chelonia, the Crocodilia, and the Rhynchocephalia have survived, and in very reduced numbers. The rest went extinct before the Eocene. It may be that a reduction of temperature put an ‘end to them, or that the food supply became deﬁcient. Certain it is that their brains were ridiculously small, and they can have been no match for the small and agile mammals in intelligence.

Two main points for consideration arise out of a study of the reptiles. The ﬁrst concerns the structure of the 5th metatarsal bone. In the Cotylosaurs it was of a normal shape, as also in the Synapsida. Now, the Synapsida are to be regarded as having been derived from the Cotylosaurs, and one group of them, the Theromorphs, gave rise to the mammals. The line of mammalian descent is therefore characterised by the possession of a normal-shaped straight 5th metatarsal. On the other hand, the other reptiles such as the Chelonia, together with the Squamata, and all the Diapsida have a hookshapcd 5th metatarsal. The birds were derived from a Diapsid stock, and so it may be said, therefore, that the line of avine descent is characterised by the possession of a hook-shaped 5th metatarsal. Actually what this modiﬁcation means or what function it serves is unknown, but it is to be noticed that among the animals possessing it are forms which live on land, in the water, and in the air, so that it would seem not to have an adaptive signiﬁcance, nor to be capable of modiﬁcation by different modes of life. It looks, therefore, as if it could be used as a diagnostic feature inherited from a common ancestor by all the forms possessing it. This common ancestor was probably a late Anapsidan, and the importance of this matter is that from this point onwards the reptiles were divided into two main THE EVOLUTION or THE, REPTILES 331

and divergent branches. One branch which may be called the Sauropsidan includes the Chelonia, the Parapsida, the Diapsida. and the birds. The other or Theropsidan branch includes the Synapsida perhaps (the Synaptosauria), and the mammals. As a result of these considerations, it appears that the term “Reptilia" is applied not so much to a uniﬁed group of related animals as to two divergent stocks. It therefore refers to a grade of structure and degree of evolution; and when the knowledge of fossil forms is more complete, it will be possible to abolish the class “Reptilia”, or to restrict it to the primitive Anapsida, and to substitute the classes “Sauropsida“ and “Theropsida”, containing the birds and mammals respectively.

That these conclusions are sound is shown by a consideration of the aortic arches. It is to be noticed that all the living reptiles belong to the Sauropsidan branch, and in all of them the systemic aorta is split into two right down to the ventricle of the heart. The result is that there are right and left systemic arches springing respectively from the left and right sides of the ventricle. The condition of the bird ﬁts into this scheme, for it differs from the arrangement in the crocodile only by the loss of the left arch. Now, in the mammal, the systemic aorta is single and undivided. The point is that it is impossible to derive the Sauropsidan type of aorta from the mammalian, or vice versa, and it is necessary to go back to a primitive type like that of the amphibia where the aorta is not only undivided but the pulmonary arch has not yet become separated oil". The primitive Cotylosaurs may have been of this type. It is certain that the Synapsida must have resembled the mammal (for the latter was derived from the former), and therefore differed from the Sauropsida as regards the structure of the aortic arches. This is the same divergence which appeared from a consideration of the hook-shaped 5th

metatarsal.

LITERATURE

Goonrucn, E. S. On the Classiﬁcation of the Reptilia. Proceedingr of the Royal Society, Ser. B, Vol. 89, l9l6.

NOPCSA, F. Die Familien der Reptilten. Fortsclzrirte tier Gettlogie and Palteontologie, 2, 1923.

WATSON, D. M. S. On Seymouria, the Most Primitive ltnown Reptile. Proceedings of the Zoological Society, London. 1913WILLISTON, S. W. Water Reptiles of the Past and Present. University Press, Chicago, 1915.

—-—. Osteology of the Reptiles. Harvard University Press, 1925. CHAPTER XL

THE EVOLUTION OF THE BIRDS

THE birds present so many similarities to the reptiles that they have .

been classiﬁed together with them in the group Sauropsida. The resemblances extend to the following features. The heart and arteries of the bird are the same as those of the crocodile with the exception of the left systemic arch, which in birds is abolished. The perivisceral coelomic cavity of birds is divided up into pulmo-hepatic recesses and pleural cavities, by means of the pulmo-hepatic ligaments and oblique septa; this arrangement is also present in the crocodile. The lung of birds gives rise to a number of diverticula or air-sacs which ramify about inside the body; small air-sacs are formed by the lung of the chamteleon. With regard to the nervous system, the brain of birds is an elaboration of the grade of structure shown by the brain of crocodiles, and its distinctive feature is that the corpus striatum has been especially developed while the cerebral cortex remains small and thin. The cerebellum of birds presents many resemblances to that of the Pterosaurs, which can be explained as due to the action of similar modes of life working on related materials. The early stages of development, amnion and allantois, are very similar. Coming to the skeleton, the single occipital condyle, the interorbital septum, the limb girdles, the hollow nature of several of the bones and the mesotarsal articulation of the feet, are all characters which appear in some or most of the reptiles of the Sauropsidan branch. In addition, the Jurassic fossil Archceapteryx had gastralia, a prelachrymal and remnants of two temporal vacuities, a long tail with several separate caudal vertebrae, and a lower jaw perforated by a foramen as in crocodiles. It is possible that Archaopteryx had cartilaginous uncinate processes on its ribs.

Nothing can be regarded as more certain than that the birds were evolved from reptiles of the Sauropsidan branch, and the only point left to consider in this connexion is, which.

Birds share with:

K Crocodiles: the structure of the heart and arteries, the arrangement of the ccnlom, the large corpus striatum, the foramen in the mandible (of Archaopteryx); and according to the precipitation blood-tests a high degree of blood-relationship; 332 “’ CHAPTEILXLI

THE EVOLUTION OF THE MAMMALIA

IN considering the evolution of the mammals it is necessary to revert to the Theromorph reptiles, in the more highly developed members of which, such as Cynagnathus or Tritylodan, it was found that the following characters were present. The skull had two occipital condyles, a false palate, heterodont teeth in sockets with the mammalian method of replacement. The dentary was large, the remaining membrane-bones of the lower jaw were small, and the jaw articulation was beginning to be taken on by means of the squamosal; the quadrate was loose and small. The limb girdles were of the mammalian type, and the limbs were long and supported the body clean oil‘ the ground. These characters point unmistakably to the fact that the mammals were derived from ancestors which were Theromorph reptiles.

The dominant factor in mammalian evolution appears to have been the development of the brain along the lines of increase in size of the roof of the cerebral hemispheres, and the formation of a special area of cerebral cortex called neopallium, which was no longer under the dominance of the ﬁbres coming from the olfactory centres. The neopallium became an organ for the retention of past sensations and for the delicate co-ordination of the activities of the body of the animal, which thus became capable of more eﬁlcient response to external sets of circumstances, and capable of proﬁting b_yexper1ence. It enabled the animal to improve the speed and precision of its method of locomotion with the‘ help of the long and delicately formed limbs; and the fact that the skin lost its hard horny scales and became supple and covered with hairs enabled it to Increase its sensrtiveness. The hair covering, furthermore, was a non-conductor of heat, and this fact together with the greater activity of the ammal and more intense metabolism enabled the mammals to become warm-blooded. Later on, with the development of the sweat-glands in the skin, the mammals were able to regulate their loss of heat, and so become constant-temperatured or homothermous. The mod}ﬁcation of some of the skin-glands into mammary glands made It possible for the young mammals to pass through a protected P¢“°d of infancy during which the ﬁnishing touches to their development were put on, and they became apprenticed under the care of the

family to the conditions of their3r;c7lult life. 388 EVOLUTIONARY MORPHOLOGY

The transition from Theromorph reptiles to mammals probably took place in the Permian period, for in the Triassic, fossils are found which show an advance in grade of structure. Of these, the Multituberculata are a group which persisted until the Eocene. They advanced in general evolution and grade of structure as far as the Marsupials. The pelvis was narrow as in the reptiles, and the lower jaw, which contained a single bone, had inﬂected angles. The single bone (dentary) in the lower jaw is a characteristic mammalian feature. The Multituberculata were, however, specialised, and possessed molar teeth with a large number of cusps. They are probably a divergent line which evolved parallel with but independently from the remaining mammals.

At this stage it must be imagined that the primitive mammals had seven cervical vertebrae as a constant number, and that they had evolved the characters enumerated above, together with the diaphragm and the non-nucleated red blood-corpuscles. The epipterygoid had been converted into the alisphenoid, and the quadrate (incus) and articular (malleus) into auditory ossicles. They retained, however, the reptilian characters of the presence of the coracoid, precoracoid, and interclavicle, the cloaca and the habit of laying eggs. They had not yet evolved the viviparous habit or the formation of a placenta, epiphyses were not yet well ebgal cglrhin the bones, the mammary glands were unprovided with ts many resem»,wo halves of the neopallium were not connected byd as due to the afnsverse commissure: the corpus callosum. mate,.ia1s_ T}, T The Monotremes must have diverged fro- ....,. ......u stem at this point, and they are represented today by Ornithorhynchus and Echidna, to which the description just given ﬁts well. They are inhabitants of the Australasian region.

The remaining mammals were the ancestors of the Marsupials and of the Placentals. These two groups are fairly closely allied, and have the following characters in common: the mammary glands have teats, they are viviparous, a placenta of some kind is present, the car has an external pinna, the bones mostly have epiphyses; the coracoids, interclavicle, and cloaca have been lost.

It is clear from the reduction of the milk—dentition and of the allantoic placenta (which is only preserved in Perameles) in Marsupials, that they are derived from a stock with two sets of teeth and with a well-fonned allantoic placenta. On the other hand, some primitive Placentals show evidence of descent from forms with marsupioid characters, such as alleged traces of a marsupial pouch, of coracoids, and other features. The conclusion to be drawn is that Marsupials and Placentals had a common ancestor perhaps in the

Jurassic. Now, in the Jurassic the fossil Trituberculata are found, Fngure 179. A few examples showing the radiation of the mammals. (Not drawn to scale.)

a, ()rnz'tizarh_vnchu.s- (Monotreme); b, kangaroo (Marsupial); c, armadillo (Edcntatc); d, restoration of primitive Condylarth; e. camel (Aniodactyl Ungulat.-:): f, hippopotamus (Artiodacty! Ungulatc); g, rhinocerps (Pensaodauqtyl Ungulate): I1. restoration of Titanotherium; i, restoration of Uintatherfum (Amblypoda); j, bat (Chen-optera); k, 110:: (Camivora); l, dolphin (Cetaoca); m, sea! (Camix-or-a pinnipedia); n, Sirenian; 0, Tania: (Primate).

me EVOLUTION or nus MAMMALIA 389 390 EVOLUTIONARY MORPHOLOGY

and they are regarded as related to the Marsupials by some, and to the Insectivores (Placentals) by others. The number of teeth was large. The Trituberculata which derive their name from the pattern of the cusps on the molars were probably related to the common ancestors of Marsupials and Placentals. It is a signiﬁcant fact that the arrangement of the cusps on the molar teeth in several primitive groups of mammals is of this type, regardless of the diet for which the teeth of the higher members of these groups are modiﬁed. Molars with separate cusps like this are called bunodont.

In the Eocene period, the Marsupials had a wide distribution over the earth, but at the present day they are restricted to the Australian and southern and central American regions. These regions are characterised by their isolation and the comparative absence of mammals of the Placental type. If it had not been for the latter fact, there is little doubt that the Marsupials would have become extinct, for they cannot compete with the Placentals. Instead, in the security of their isolation, they radiated out into a number of types which are especially interesting in that they have evolved parallel with several groups of Placentals, and by becoming adapted to equivalent biological environments have developed a convergent resemblance to these Placentals. Nearly all Marsupials have a marsupial pouch in the female and epipubic bones in both sexes.

The opossum (Didelphys) and Ccenolestes are American; all the remainder are restricted to Australasia, though fossils related to these are also found_ in South America. Dasyurus is the Marsupial equivalent of the cats, while the dogs are represented by Thylacinus; Perameles (the bandicoot) is an attempt at a rabbit, Petaurus (the phalanger) resembles the ﬂying squirrels, while Notoryctes is a remarkable imitation of the mole. Phascolarctos (the koala) is the “marsupial bear”, Phascolomys (the wombat) is the “marsupial rodent", the extinct Thylacaleo was the “marsupial lion”, while Macropus (the kangaroo) represents the swift-moving Ungulates.

The Cretaceous strata of Mongolia have revealed fossils of apparently Placental mammals, of which Deltatlzeridium is an example, and which can be regarded as intermediate between the Jurassic Trituberculata and the true Placentals of the Eocene.

The Placentals are characterised by the possession of an allantoic placenta, a corpus callosum joining the two halves of the neopallium, and a typical dental formula of i-3-, c*}, p%, m:?;. This number of teeth is, however, often modiﬁed and reduced.

At the beginning of the Eocene period there appeared a group of true Placentals which were primitive in that they were of small size, with tritubercular short-crowned molars, ﬁve ﬁngers and toes, and walking on the ﬂat of the hand and foot. Among them can be ma BVOLUT#l0N or ran MAMMALIA 391

recognised some with a tendency to modiﬁcation of the teeth for a carmvorous d1et—-the Creodonta; others for a herbivorous diet...

the Condylarthra. Others again were generalised Insectivora. Very

early, a branch diverged from the Condylarthran stock and gave

1'i5° t0 the Amb1)’P0da. large. clumsy, premature rhinoceros-like forms such as Uintatherium, and which soon went extinct

In the later Eocene divergent evolution has progressed, and it is very interesting to notice that a number of the Orders of Mammals have become diﬁbrentiated, and that these are not yet split up into the various families. The Creodonta had given rise to the Carnivore which branched out into the Pinnipedia or seals, and Fissipedia or dogs, cats, bears, civets, and badgers. The Rodentia came oil‘ from near the primitive Insectivora, as did also the Primates (Lemuroids and Tarsioids) and the Edentates. The Perissodactyla or odd-toed Ungulates emerged from a stock intermediate between Condylarthra and Insectivora, and blossomed out into the huge Titanotheres which soon went extinct, the horses, tapirs, and rhinoceroses. The even-toed Ungulates or Artiodactyla emerged from some form between the Creodonta and the Insectivora, and, apart from a number of short-lived groups, radiated out into the pigs and hippopotamuses on the one hand, and the camels, antelopes, deer, cattle, and giralfes on the other. Related to the Ungulates are the conies (Hyracoidea) and the elephants (Proboscidea). The whales (Cetacea) may perhaps have arisen from a stock related to the Artiodactyla, and the Sirenia may have a common descent with the Proboscidea. South America became inhabited by a peculiar collection of archaic forms which were all doomed to extinction, but of which some such as the Thoatheria had evolved into a very remarkable imitation of the horses. The Edentata include armadilloes, sloths, and ant-eaters. The Cheiroptera or bats are related to the lnsectivora, while the Dermoptera have afﬁnities with the Insectivora and Primates.

In some cases suﬂicient fossil forms are known from successive strata to enable lines of descent to be traced with considerable precision. This applies especially to the horses, the camels, and the elephants. The evolution of the horses from Eohippus (Eocene) through Mesohippus (Oligocene), Miohippus (Miocene), Pliohippus (Pliocene) to Equus, was accompanied by a progressive increase in size, lengthening of the teeth which become “rootless”, development of ridges on the molars, fusion of ulna with radius and tibia with fibula, specialisation of the wrist and ankle joints into articulations allowing movement in only one plane, enlargement of the 3rd digit ‘in hands and feet, and reduction of all the other digits until their disappear3.1108. 392 EVOLUTIONARY MORJPHOLOGY

The evolution of the camels from the Eocene Protylopus through Poébrotherium (Oligocene), Procamelus (Miocene) to the present day is likewise a history of gradual increase in size, increase in length of the teeth and development of selenodont ridges on the molars, reduction of the upper incisors, enlargement of the 3rd and 4th digits in hands and feet with suppression of‘ the remainder, and fusion of the 3rd and 4th metacarpals and metatarsals.

So far as is known the history of the elephants starts with the Eocene Moerltherium, of about the size of a pig, and with the primitive dental formula of ii-, cﬁ, pi-, m%. Its ridged (lophodont) molars had only two ridges. In the upper Eocene, Palteomastodon was larger, and had a not inconsiderable trunk. The canines and all the incisors except one pair in each jaw had disappeared, and the molars had three ridges. Tetrabelodon from the Pliocene was still larger and its incisors were elongated into tusks with persistent pulps. The molars had as many as six ridges and were so large that there was not room in the jaws for more than two teeth in each jaw on each side. Furthermore, instead of being replaced from beneath as in ordinary mammals, they were replaced from behind, the new tooth pushing the old one out forwards in front of it. It is worth noticing that although these animals grew large and tall their necks were very short, and it was only by means of the long trunk that they were able to reach down to the ground for eating and drinking. The next step, shown by the Pliocene Mastodon, was accomplished by a shortening of the lower jaw and the loss of the lower incisortusks. Lastly in Elcﬁhas the grooves between the ridges on the molars become ﬁlled with cement. The ridges may be a dozen in number, and the maximum number of molars on each side in each jaw in use at one time is one and a half.

LITERATURE

BROOM, R. On the Origin of Mammals. Philosophical Transactions of the Royal Society, Ser. B, Vol. 206, 1914. ‘ BROOM, R. T he Origin of the Human Skeleton. Witherby, London, 1930.

Gnmonv, W. K., and SIMPSON, G. C. Cretaceous Mammal Skulls from Mongolia. Nature, Vol. 118, 1926.

MATTHEW, W. D. The Evolution of the Mammals in the Eocene. Proceedings of the Zoological Society of London, 1927.

OSBORN, H. F. The Age of Mammals. Macmillan, New York, 1910.

SIMPSON, G. G. The principles of classiﬁcation and a classiﬁcation of Mammals. Bulletin of the American Museum of Natural History, Vol. 85, 1945.

WEBER, M. Die Saiigetierc. Fischer, Jena, 1927. CHAPTER XLII

THE EVOLUTION OF THE PRIMATES AND‘ MAN

THE Primates originated from a stock related to the Insectivora probably in Cretaceous times. Plesiadapis, from the Early Eocene, had characters in common with the lnsectivora and the Lemurs, which are the lowest Primates. The characteristic of the higher Primates is that the bony bar separating the orbit from the temporal fossa is complete; or in other words. the eye-socket is round and protected all round by bone. At the same time, both eyes look more or less forwards so that their fields of vision overlap and may coincide (stereoscopic vision). There are live ﬁngers and toes, and the ﬁrst digits are opposable to the others, except in the case of the ﬁrst toe of man. This opposability makes the limbs efficient grasping organs, and is evidence for the fact that the early Primates lived on the branches of trees. It will be seen in the sequel that this arboreal habit had consequences of the highest importance in the evolution of the Primates. Lastly, the most important character of all in the Primates is the great development of the neopallium in the cerebral hemispheres.

In the Eocene the fossil Notlzarctus is found, representing the earliest member of the group of the Lemuroidea. It was very generalised, for whereas the primitive dental formula in mammals is i%, 0}‘, p%, me}, that of Notharcrus was ii-, e}, p-‘,3, mg. From forms of this type the Lemurs must have descended. The Lemurs alive today are nearly restricted to Madagascar, though a few occur in Africa, Ceylon and Malaya. They are fairly primitive animals, but show certain specialisations which rule them out from the main line of Primate evolution. Among these may be mentioned the peculiar procumbency of the incisors of the lower jaw, with which they comb their fur.

The tail of a Lemur is long but not prehensile, and its skull may be recognised by the fact that the cavity of the orbit can still communicate with that of the temporal fossa beneath the post-orbital bar.

Another Eocene fossil allied to Notharctus is Temmhs, the earliest representative of the group Tarsioidea. Tetanius had an enlarged rounded brain-case and a small face. Its brain must have been relatively larger than in any other known Eocene animal. It also

was not on the direct line of descent owing to specialisations such 393 394 EVOLUTIONARY MORPHOLOGY

as the loss of the lower incisors, but a close relative of it must have been the ancestor of Tarsius, which lives at the present day. In Tarsius the post-orbital bar is splayed out and almost but not quite prevents communication between the orbit and the temporal fossa. It shows important advances in the structure of the brain, and of the external car. In the fact that it has a diseoidal placenta with a thickened

Figure 179a.

B, Ausrralapithecus, for comparison with A, chimpanzee. (From Le Gros C ark.)

trophoblast hollowed out into lacuna: ﬁlled with maternal blood, and in the fact that the mesoderm ap ars very early in the development of the embryo, Tarsius resembleﬁhe higher Primates and Man, and differs from the Lemuroidea.

In the true monkeys, apes and man, or Anthropoidea, the orbit is completely shut off from the temporal fossa. From some Tarsioid ancestor with aflinities to Notharctus there diverged a branch which gave rise to the New World monkeys. These forms which are EVOLUTION or THE PRIMATES AND mm 395

included in the group Platyrrhi h '

with the nostrils wide apart, anlcliwa tﬁilevihﬁrlfziisi tigtiziiitairilatiigg-5': They show a considerable advance in the structure of the brain and in the fact that their dental formula is reduced to if, cf pg m5; at

Figure 179b. A, Pithecamhropus ; B, Neanderthal man (From A. S. Romer.)

the same time they are deﬁnitely oil‘ the main line of Primate evolu-» tion because of the structure of the tympanic bone which forms a ring. The Old World monkeys and apes form the group Catarrhinze, in which the internasal septum is narrow, the tympanic bone forms a tubular external ear, the tail when present is never prehensile, and the dental formula is reduced to i%, tr}, pit, m}. The Catarrhina: must have emerged in the Eocene period from 396 EVOLUTIONARY MORPHOLOGY

Tarsioid ancestors related to those which gave rise to the Platyrrhinae. In the Oligocene, Parapithecus is found, and from forms related to it the ordinary monkeys or Cercopithecidze must have been derived. These forms are again ruled out from the main line of Primate evolution by specialisations such as the development of two transverse ridges on the molars. At the same time, the Cercopithecidae, which include the baboons and mandrills, show a great development

Figure 180. Skull of Skhul man (Mount Carmel). (From T. D. McCown and Sir Arthur Keith.)

of the brain, which must have undergone an evolution parallel to that which went on in the stock leading to the apes and man. The main stem of the Primates leading to the anthropoid apes and perhaps to man was represented in the Oligocene by the little Propliopithecus. The fact that it was small is important, for so many divergent branches became specialised in the direction of large size, and in the search for the ancestors of the apes and man, choice is avoumou or THE pnrmvras AND MAN 397

limited to forms considerably smaller th th t ‘

nlrlight have given rise. The anthropoid apeasnhavgsliastoththtﬁill

..;::..:,;:"::':.:z.::...i:*:“ 3.2:“; .l‘“‘’

and developed. P C e , and the brain 18 greatly enlarged

A generalised form of ape, th M‘ - .

been ancestral to the modern antliropgdeggeflzaggiggghcngzngglﬁ of Propliapithecus was the Pliocene form Pliopithecus which itself was 3“ ancesmr °f the Sibbml (Hylobates), the smallest of the apes.

Figure 181. Skull of Rhodesian man, drawn by T. L. Poulton. (From Elliot Smith.)

Other lines of descent from forms like Propliopithecus led to the Orang, and to the Gorilla, while the Miocene I’ro(.'rm.s'uI may have been on the line of descent of the Chimpanzee. The apes, while having highly developed brains and retaining the power to oppose the ﬁrst toe to the others, have not got brains large enough to enable them to do otherwise than remain brutes, relying on their strength and their long canines instead of on memory, skill, and the neopallium. There are some characters possessed by adult modern man which are present in the young but lost in the adult apes. An example of these is the absence of large brow-ridges in young apes and man. In general, however, the degree of specialisation shown by the apes 398 EVOLUTIONARY MORPHOLOGY

makes it probable that the Hominoidea were derived from some pre-anthropoid stock of Primates.

The fossil record of the Hominoidea is not yet by any means as complete as could be desired, but there is already suﬁicient evidence to enable an outline to be given of the more important changes and modiﬁcations which accompanied the evolution of modern man: Homo sapiens.

The Hominoidea include all the members of the human family and it must be noted that they differ from other Primates not so much in matters of kind as in matters of degree. Essentially, the evolution of the Hominoidea is a story of enlargement of the brain, reduction of the nose, face, teeth and jaws, perfection of the erect position, and loss of opposability of the large toe.

The nearest approach to the human condition without achieving it is the early Pleistocene Australopithecus, from South Africa. Australopithecines show some similarity to certain gross features of the Gorilla and Chimpanzee, but its brain is slightly larger and its face smaller, its teeth and jaws show unmistakably human characteristics, and, most surprising of all, its pelvis and femur prove that it stood erect. Australopithecus is known from the specimen of a young individual which lacked brow-ridges. Related adult forms of Australopithecina: are Paramhropus and Plesianthropus.

The earliest known member of the Hominidte is Pithecanthropus from Java and Peking. This form had a. much enlarged brain with a cubic capacity ranging from 850 to 1,300 c.c., while the maximum volume of an ape’s brain is 650 c.c. Pillrecanthropus was acquainted with the use of ﬁre and made rough quartz implements. From the structure of its femur, it walked quite erect. In some respects it preserves primitive features such as the continuity between the occipital and temporal crests on the skull, and many features in the conformation of the brain, but in others it is specialised, as in the development of the large brow-ridges.

Pithecanthropus was Lower Pleistocene, and in Europe this type was represented by the Heidelberg jaw, and in North Africa by the slightly later jaws from Terniﬁne. They are massive and show complete lack of any chin eminence although the teeth are fundamentally human in character.

The next human fossils to appear, in the Middle Pleistocene, are the Swanscombe and Steinheim skulls, which show an interesting mixture of characters. Some of these characters are reminiscent of Pithecantlzropus. Others, such as the brow-ridges, resemble the Neanderthal type to be described below. Others again, such as the occipital region, herald the appearance of Homo sapiens.

In the Upper Pleistocene, the Skuhl skull from Mount Carmel EVOLUTION or THE PRIMATES AND MAN 399

shows a similar mosaic of characters. The Piihecanrhropus traits have become reduced, while those of Homo sapiens have increased. The forehead approaches a more vertical condition although the browridges are still present; and in the lower jaw there is the rudiment of a chin eminence although the jaws are still prognathous.

During the Upper Pleistocene, there appears to have been an increasing divergence between the types which have led to Homo sapiens and Homo neanderthalensis. In the sapiens type, represented by Cro-magnon man, the brain, with an average volume of 1,350 c.c., often exceeded, has achieved maximum development, so much so that its front wall has been pushed forwards to form a more or less vertical forehead. This vertical wall of bone provides the necessary resistance for the reduced lower jaw to bite against. In the ‘apes, Pithecanthropus, and Neanderthal man, where the lower jaw is large and there is no forehead, the strain of the bite is taken up in the large brow-ridges which are developed in the adult. These brow-ridges are not a primitive feature at all, but were independently acquired as an adaptation in certain groups. Their presence rules their possessors out from modern man’s ancestry.

The face in Homo sapiens is relatively smaller than in any mammal. the lower jaw is slender and provided with a prominent chin, and the canine teeth are small. The hip-girdle is short and wide, and the vertebral column and legs enable modern man to stand bolt upright.

Specimens of Homo neanderthalensis have been found from a number of localities in Europe, from Gibraltar to Palestine. In addition to the bones themselves, there is considerable evidence concerning these men from the weapons and tools which they fashioned from ﬂint, and which consequently have been preserved. An indication of the degree of mental development of these people is obtained from the fact that some of the individuals which have been discovered appear to have been intentionally buried. The brain is big, about 1,350 c.c. on an average. At the same time, the browridges were large, as were also the face, palate, and jaws. There was no chin, and the lower jaw preserves the large attachments for the digastric muscles. The vertebrae and the legs show that the Neanderthal man did not stand straight up, but stooped considerably. The hip-girdle was long, and the foot rested mostly on its outer border, as in young children and certain savage races today. While lacking the capacity to be opposed to the other toes, the large toe was considerably separate from the remainder. The Neanderthal race has gone extinct, doubtless because of its specialisations, and the insuﬁcient development of the brain which handicapped it In the competition with Homo sapiens. 400 EVOLUTIONARY MORPHOLOGY

Compared with Homo sapiens, Neanderthal man is in many respects retrogressive, and there is reason to believe that later types of Neanderthal man show these specialised features even more markedly than earlier types. An extreme example of this evolution, which resulted in certain types of men presenting a spurious resemblance to the larger apes, is found in the skull from Broken Hill in

Figure 182. The skeletons of Neanderthal man and of modern man compared. (From Boule.)

Rhodesia. Here the brow-ridges were enormous and there was no forehead at all, although the brain-volume was about 1,250 c.c. An interesting feature about the early Hominoidea is that the young skulls of Australopithecus, Pithecanthropus, and Homo neanderthalensis are free from many of the specialisations which disqualify the adults of these types from occupying places on the direct line of ancestry of Homo sapiens. In this respect, therefore, the evolution of sapiens may be said to have been characterised by a retention of many juvenile features in the adult, by retardation of development, particularly of the teeth, jaws, and sutures of the skull. EVOLUTION on THE pamnas AND mm 401

Attention may now be turned to some ' presented by_ the series of types of the Homitigiodeaatiologcal features

In connexion with the expansion of the brain and the assumption of an erect attitude, it IS consistently found, on ascending the scale of Primate evolution to man, that the foramen magnum through which the spinal cord joins the brain is moved relatively farther and farther forward. This fact is obvious when it is considered that the head of an ordinary lower mammal projects forwards horizontally from its neck, whereas man’s head is carried vertically above his neck. At the same time, the eyes of lower mammals and of man look horizontally from about the middle of the front of the face. There has therefore been a progressive expansion of the binder and upper part of the skull accompanying the development of the brain, and which moves the face-region farther and farther forwards. The ordinary superposition of median vertical sections through skulls suffers from the fact that it is then difficult to distinguish between diﬂerences of actual size and differences of development. This difficulty vanishes when the sections are superposed on a common centre, and then rotated so that certain standard radius-lines coincide. Other lines can then be read-oﬁ‘ by angular measurement regardless of the actual size of the skull. The centre of gravity is chosen as the common centre since it is the morphological centre of form. It may be called Sollas’ centre. The sections are then rotated so that the radius-lines from the centre to the middle of the foramen magnum coincide. The sections are then “set", and reference—lines are made by continuing the radius of coincidence up to the top of the skull, and drawing a line at right angles to it through Sollas‘ centre.

One of the most instructive readings is the measurement of the angle made between the line of the foramen magnum, and the line from the centre to the point of junction between the nasal and frontal bones (the nasion). It is essential for this comparison that the sections be taken from specimens of equivalent age, for during development the angle changes. Nevertheless, taking adult material it is possible

to make out the following: _ Angle between foramen magnum and nasion in adult:

Gibbon . . . . . . . . . . . . 238° Chimpanzee . . . . . . . . . . 239° Pithecanthropus . . . . . 251° (conjcctural) Homo neanderthalensis . . . . . . . . 25 3° Rhodesian man . . . . . . . . . . 262° Homo sapiens . . . . . . . . circ. 270’°

These measurements show that the periphery of the brain-case in 14-—v.z. 402 EVOLUTIONARY MORPHOLOGY

modern man amounts to three right angles, and it is interesting to note in comparison with lower forms that the accommodation for the increased size of man’s brain is obtained by the angular increase in the periphery of the brain-case as well as absolute increase in size.

It is noticeable that the increase in the value of the angle is progressive all the way from the apes, through Pithecanthropus and Neanderthal Man to Homo sapiens.

As regards Australapithecus, the following table shows the comparison between it and juvenile specimens of other forms.

Angle between foramen magnum and nasion in young:

Orang .. .. .. .. .. .. .. 243° Chimpanzee . . . . . . . . . . . . 252° Australopithecus . . . . . . . . . . . . 258° Homo sapiens child . . . . . . . . . . 282°

It is clear, therefore, that the Taungs skull approaches the human condition in this respect.

Having now reviewed the material on which all study of the evolution of man must be based, it remains to consider what causes were probably operative during the history of human descent. It may be said at once that just as the rise of the mammals was due to the development of the brain and formation of a neopallium, so a continuation and perfection of that process led to the rise of the Primates and man, and that this development was largely associated with the sense of sight.

It has been seen that the history of the Primates can be traced from lnsectivore-like ancestors, through Tarsioid, monkey, and ape stages, and that their evolution was accomplished under arboreal conditions of life. Now, the lnsectivora, Tarsioidea, monkeys and apes have living representatives at the present day, some of which have changed but little from their Eocene ancestors. Without in the least suggesting that these living forms are on the main line of descent (which indeed it has been shown carefully that they are not), they may be taken and studied for their brains and organs of sight, as showing grades of structure approximately representative of the stages through which it is known that the Primates passed.

Of the Insectivora, Macroscelides (the jumping shrew) may be taken as a primitive mammal, in which the neopallium is developed, but the archipallium related to the sense of smell is still very large. In particular it is important to notice that the region of the neopallium (parietal region) related to the sense of sight is small.

Tupaia (the tree shrew) is related to Macroscelides, and the difference which it shows in its brain is related to the habit of living in trees. Life in trees is conducive to the better development of the sense of sight, for jumping from one branch to another, and 239 \' 210° A N \ \ 5 /251°

3.‘

Figure 183. Diagrams of longitudinal sections of skulls, superimposed on their centres. (After Sollas)

Showing the difference in angular measurement between the nasion-line (from the centre to the top of the nasal bone) and the line through the {nramen magnum (from the centre): in Gibbon 238"; in Chimpanzee 239°; in HI/wcranthropus 251": in Neanderthal man 253'’; in Rhodesian man 262°; and in modern man 264“

to 270°. 404 EVOLUTIONARY MORPHOLOGY

ineﬁicient perception of spatial relations would lead to disaster, Accordingly, it is not surprising to ﬁnd that the visual area of the neopallium of Tupaia is better developed than in Macrascelides, and that in the nature of its retina and other features connected with the eyes Tupaia approaches the Lemurs.

The stage represented by Tarsius, which is also arboreal, is of great importance,_ for here for the ﬁrst time the sense of smell is reduced below the level of the sense of sight, which becomes the dominant sense in the body. The eyes of Tarsius look forwards, and the fact that they have rotated on to the front of the face necessitates the reduction of the nose and snout. At the same time, the senses of hearing and touch are better developed, together with their respective temporal and tactile areas in the neopallium. The development of the tactile area is important because it is associated with that area of the cerebral cortex which is concerned with the performance of delicately adjusted and skilful muscular movements. Such movements are essential for an active arboreal animal, but there is another reason for referring to this part of the neopallium. and that is that a portion of it (the prefrontal region) is concerned with the coordination of the movements of the two eyes.

In the prefrontal area of Marsupials there are centres which control the eye-muscles and therefore the movements of the eyeball of the opposite side. The movements of the two eyes are linked together in higher forms, and this is especially signiﬁcant in the Primates, where the visual axes of the eyes become parallel. Further, whereas in lower vertebrates the ﬁbres from each eye all go to the other side of the brain (the crossing at the optic chiasma is complete), in the mammals a certain number of ﬁbres remain uncrossed, and go to the same side of the brain. Now, in the Platyrrhine stage of evolution, represented by the Marmoset, the co-ordination between the movements of the two eyes is perfected, and both eyes are able to follow one and the same object. A consequence of this is that “corresponding points” are developed in the retina: of each eye, on which the images of one object are formed, and the most important of these points is the macula lutea or spot of optimum sensitiveness.

Consequent on the power of making conjugate eye-movements, the Anthropoidea and Hominoidea have evolved a macula lutea, and this still further increases the importance of the parietal (visual) and prefrontal (skilled movement) areas, which features already distinguish the brain of the Platyrrhine from that of Tarsius. A continuation of the process of enlargement and perfection of the parietal, prefrontal and temporal areas can be gradually traced through the grades of structure shown by the Catarrhine, the ape (Gorilla), Ausrralopithecus, Pithecanthropus, Neanderthal to Homo avownon or run pmmxras AND MAN 405

,g.‘. 1-g"!

Brain of the Tree (T upaia)

. - - - ' - .1 - th cortex associated with vIs:o_n an_ rd- t vemems J:-¢g1:n;Baa%{1 thi: decrease in the olfactory T631013, In co-o mac mo _ v 406 EVOLUTIONARY MORPHOLOGY

sapiens. There is further the very interesting fact that in human development the regions of the neopallium which are the last to be formed are precisely these parietal, prefrontal and temporal areas.

There is therefore good reason to believe that the perfection of these areas of the cerebral cortex and of the functions with which they are associated played the major part in the evolution of man. The brain developed ﬁrst, and other features such as the reduction of the face and assumption of the erect attitude followed. It is to be noted that the perfection of the parietal and prefrontal areas is directly or indirectly concerned with the function of vision, so that it may be said that sight was of capital importance in the evolution of man. In this connexion, mention may be made of some other aspects of the bearing of sight on evolution.

In the ﬁrst place, it will be remembered that the eyes are “distancereceptors”, and that the responses which they evoke on the part of the animal are anticipatory rather than consummatory movements. Next, there is the fact that in man the number of nerve-ﬁbres entering the brain from one eye vastly exceeds the number of all the other afferent nerve-ﬁbres of one side put together. From the physiological side, it is found that in the higher Primates including the monkeys, apes, and man, the eyes assume great importance in regulating the posture of the organism, a regulation which in lower forms is principally dependent on the semicircular canals of the ear. Lastly, from the psychological point of view, experiments on the behaviour of chimpanzees when confronted with problems show that the eyes play a very important part in solving the problem. Cases of great interest are those in which there lies close at hand some instrument, such as a stick, and by using which the ape would be able to solve its problem easily. Unless the instrument to be used is seen by the ape in the same ﬁeld of vision as the object or goal for which it is to be used, it pays no attention to it. Without this optic co-presence, the ape does not “see” the solution to the problem.

Perhaps the most important of all the consequences of the perfection of the sense of sight in the Primates is the fact that it is the neopallium which undergoes commensurate development in the brain, and the neopallium is the physical companion of memory, of the ability to proﬁt by experience, and of the arbitrator of possible responses, known as the will. There is also to be noticed here the importance of remaining unspecialised. For if the great development of the sense of sight had taken place earlier in evolution, in an ancestor of the mammals, it would have been not the neopallium, but the optic lobes which would have undergone specialisation, and for a number of reasons these are unsuited for the development of the higher mental faculties. The success of man is therefore also due EVOLUTION OF THE PRIMATES AND MAN 40']

to the fact that his ancestors did not shoot their bolt of specialisation prematurely.

A consequence of binocular vision and conjugate movement is the power to converge the eyes on an object. In the first place, this enables an estimate of distance to be made, which is important in leaping from branch to branch. Feeling of the degree of convergence is conveyed by stimuli from proprioceptive sense-organs in the eyemuscles by afferent ﬁbres in the eye-muscle nerves. When, however, the eyes are converged on an object, that object occupies the attention of the animal, and the stereoscopic vision which it now enjoys enables it to become aware of the true geometrical and spatial relations of the objects in the world around it.

To return to the face, it is obvious that when the nose and snout are reduced as a result of the eyes coming on to the front of the face, the mouth itself can no longer so easily be used as a food-obtaining organ, as it is in lower forms. Here, the hands come to the rescue, and being ﬁve-ﬁngered and with opposable thumbs, capable of pronation and supination, they undertake the function of carrying food to the mouth. At the same time, the development of the prefrontal area of the neopallium enables delicate movements to be made, in the course of which the animal acquires skill. It is an interesting fact that in the higher Primates the focal length of the eyes for most acute vision should be just within the reach of the hands. The assumption of the erect posture which is made possible by the increased power of co-ordination of _the brain relieves the hands from the service of locomotion, which is performed solely by the feet. The latter therefore lose the opposability of the big toe.

Lastly, in connexion with the greater development of the temporal region of the neopallium, the power of hearing bc_carne_more acute. and with it came the development of speech. There isclinical evidence that in man one of the lobes of the temporal region is concerned with the faculty of stringing words together into sentences with a logical meaning, and it has been shown above that this is one of the regions of the neopallium which has undergone progressive development in the evolution of man. It is not claimed that man isnothing more than a mammal which sees, hears, and co-:ordinates_ his movements better than other mammals. All that is intended is to show that the development and perfection of these functions of sight, auditory discrimination with which must be coupled 'specc‘h and language, and muscular skill. bring about changes which 3}‘: PW" requisite for the development of that peculiarly human attribute-—

the higher mental faculties. 408 EVOLUTIONARY MORPHOLOGY LITERATURE

BOULE, M. Les Hammesfossiles. Masson, Paris, 1921. (English translation, Oliver & Boyd, Edinburgh, 1923.)

BROOM, R. and SCI-IEPERS, G. W. H. The South African Fossil Ape-Men. The Australopithecinae. Transvaal Museum Memoir, 2, Pretoria, 1946.

ELLIOT SMITH, G. Essays on the Evolution of Man. Oxford University Press, 1927.

GREGORY, W. K. The Origin and Evolution of the Human Dentition. Williams and Wilkins, Baltimore, 1922.

LE Guos CLARK, W. E. History of the Primates, British Museum (Natural History), London, 1949.

SOLLAS, W. J. Ancient Hunters. Macmillan, London, 1924.

SONNTAG, C. F. The Morphology and Evolution of the Apes and Man. John Bale, Sons and Danielsson, London, 1924.

THOMSON, A. A Consideration of the more Important Factors concerned in the Production of Man's Cranial Form. Journal of the Anthropological Institute. Vol. 33. 1903. PART V

CHAPTER XLlll

CONCLUSIONS

NOT the least of the interests aroused by the study of Vertebrates is due to the fact that they form a group which lends itself perhaps better than any to a consideration of general principles and matters of wide importance. This is largely because, although imperfect, present knowledge covers a considerable amount of the results of vertebrate evolution, and still more because between the most widely separated members of the group, between Aiiip/zio.rus and man, there is suﬂicient similarity in plan of structure to enable comparisons to be made with advantage. Comparative Anatomy as an intellectual weapon is the more satisfactory when the number of correspondences of kind which can be established is great, regardless of course of matters of detail. So it is not astonishing that the Anatomy of, for example, Nematodes and Echinoderms when compared should be less fertile in conclusions of general interest than a comparison between Vertebrates as distant from one another as are ﬁsh and mammals. From the fact of the general homogeneity of the group as a whole, the variations to be observed in dillerent vertebrates become all the more interesting.

It is very striking to ﬁnd organs such as notochord, nerve-tube, dorsal and ventral nerve-roots essentially the same in Anipliioxus and man, but the most striking case of homologous organs is that of the thyroid. From the endostyle oi‘ Aiiipliioxus, through Petromyzon with its tell-tale Ammococte larva, to all the Craniatcs, the chain is complete, and not the least remarkable feature of it is the great change in function which has taken place from an organ connected with the ciliary method of feeding to a ductlessglaiid regulating the metabolism of the body. This case is a good 'lllUSIl'£‘lllOl1 of the fact that function is no criterion whatever in questions of homology, and that the sole condition which organs must fulﬁl to be homologous is to show similarity in their fundamental structure and morphological relations. _ _

A fact which the vertebrates illustrate well is that the numerical correspondence of segments which give rise to particular structures

is not a necessary criterion for homology. This is well shown by a 14"‘ 409 410 coucwsrons

consideration of the pectoral and pelvic limbs. The fore limb is formed from trunk-segments 2, 3, 4, and Sin the newt (Salamandra), whereas in the lizard it arises from segments 6, 7, 8, and 9. Similarly the hind limb arises from segments 16, 17, and 18 in the newt, but segments 26 to 31 in the lizard. Countless similar examples are afforded by other vertebrates, and it is to be noticed that the limbs not only vary in their position, but also in the number of segments which have contributed to their formation. Yet wherever they may be and however many or few segments they may contain, fore limbs are homologous throughout the vertebrates, and so are hind limbs. During evolution transposition has occurred; new adjacent segments have taken to contributing to the formation of the limb, and at the opposite end segments which hitherto contributed may cease to do so. In this way the limbs may become transposed over the trunk of the animal much as a tune can be transposed over the keys. But it is the same tune and the same limb.

Another case is that of the position of the occipital arch at the back of the skull. The neurocranium of Scyllium occupies 7 segments while that of a form as closely related to it as Squalus occupies 9. Although they are situated in different segments, there can be no doubt that the occipital arches of these two animals are similar structures descended from the occipital arch of a common ancestor, and are therefore homologous.

A very interesting example of the same kind is furnished by the number of gill-slits in various Selachii. Heptanchus has 7, Hexanchus and Pliotrema have 6, and the remaining Selachii have 5 gill-slits and branchial arches on each side.

The 7th or facial nerve contains ﬁbres of the special visceral efferent component system, which innervate the striated visceral muscles of the hyoid arch (see p. 319). The centre of origin of these ﬁbres is called the motor VII nucleus, and is situated in the medulla oblongata, but its precise position varies in diﬁ'erent classes of vertebrates. In the dogiish, this nucleus has a dorsal position, but in the rabbit it lies ventrally. On looking for a reason for this displacement, it is found that the motor VII nucleus of the dogﬁsh receives its stimulating impulses from the visceral afferent sensory centre. This centre lies dorsally, and it receives impulses from the senseorgans of taste and mucous surfaces of the gill-slits. The reﬂex response to these impulses passes from the visceral afferent centre to the motor VII nucleus and out to the muscles of the hyoid arch.

In the rabbit, the motor VII nucleus receives impulses from a number of sensory centres, such as: the general somatic sensory centre, which receives impulses from the skin of the face and ears; an auditory centre; an optic centre; and a centre which receives CONCLUSIONS 411

impulses from the sense-organs of pain in the body. Now, all these centres have a ventral position, and the reﬂex responses to the various impulses pass from the sensory centres to the motor nucleus, and so out to the muscles. In the rabbit these muscles are not restricted to the hyoid arch, but they form the muscles of expression which move the face, lips, and external ears, and close the eyes. This is why ii grimace is made when the face is tickled or the body is hurt, why the ears are pricked to a sound, and why the eyes are closed to a dazzling light. But the point of importance to note for the present purpose is that the ventral position of the motor VII nucleus in the rabbit is due to the ventral position of the sensory centres which stimulate it, just as the dorsal position of the nucleus in the dogﬁsh is related to the dorsal position of the sensory centre in question in that animal. In other words, the cell-bodies of neurons appear to have been displaced towards the source of the impulses which they most habitually receive. This apparent process of migration is known as neurobiotaxis, and it has been of great importance in the evolution of the nervous system. The apparent migration of the centres during the course of evolution is probably due to the _formation of the centres in changed position during successive individual developments. A matter like this is worth some attention, for it man example of how principles of general and wide interest can be derived from comparative anatomical studies.

In sharp contrast to homologous structures are_the resemblances between different and unrelated groups of animals as regards characters which can be proved to have been separately and independently evolved. These resemblances are analogies. and. they give rise to the phenomenon of convergence in evolution which I; well illustrated by vertebrates. The instances of convergence whicd might be given are so numerous that only very few need be mentioneb here. A good example is the modiﬁcation of the pentadactyl lirn ’ into a paddle, thereby losing its typical appearance and prescnlttﬂls a superﬁcial resemblance to the ﬁns of ﬁsh. But the interesting t ing is that this process has occurred not once but several llillgrh IE: dependently, in diﬁerent gf0UP5 0f T¢ll'aP°d53 Ch°1°“_‘a'hf Pym saurs, Plesiosaurs, Mosasaurs,_ Thalattos_aurs_. Th3l3“°5j“°d‘;sf: cm guins, Cetacea (whales), Carnivora Pmmpcdla (Seals)-3“ e" H; The Ichthyosaurs and some of_ the Cetacea are further lnlcféﬁﬁlgiﬁu that they have developed median dorsal ﬁns which nrejsuptﬁm. bub; very similar to those of ﬁsh. The Urodela also have mle: ldnqtruaurcs in all these cases a little study sufﬁces to show that ,t isle; sthat they not only diﬁ‘er very much from the ﬁns of ﬁsh, but a.

differ between themselves. _ d d Convergence is also to be found in the case of the elongate an 412 CONCLUSIONS

limbless condition of Gymnophiona, certain lizards such as Anguis, Amphisbwna, Scincus, and the snakes. Or again, the fore limb has been modiﬁed into a wing independently in Pterosaurs, birds, and bats. The marsupial “mole” Notoryctes is very similar to the true placental moles (Talpa).

Now it is noteworthy that these cases of convergence are each of them related to a particular mode of life. So the paddle-like modiﬁcation of the limbs is an adaptation to life in the water, just as wings are adapted to life in the air; the limbless condition is a form of adaptation to a burrowing habit, while another form of this habit characterises the “moles”. It is because of their adaptations to their environment that these animals come to resemble one another, and these adaptations have of course no value in determining aﬂinities or descent.

Another phenomenon may now be considered, which is in some ways intermediate between homology and convergence. It is often the case that in two groups of related animals which have recently diverged the same evolutionary changes take place. This may be called parallelism, and it is illustrated in certain groups of Ungulates such as the Titanotheres and the rhinoceroses. In several distinct stocks of Titanotheres peculiar bony knobs appear on the skull. These structures were not visibly present in the common ancestor of the forms which have evolved them; the structures cannot therefore strictly be called homologous, yet they are so similar that it is impossible to avoid the impression that they have some common cause. The independent development of such similar structures in related groups of animals is often ascribed to a so-called process of “orthogenesis”, or variation along “straight” and constant lines. The working of this process in two or more related groups is supposed to result in parallel evolution.

Now it is worthy of note that when tracing lines of descent through fossil forms, it is rarely possible to identify one form as the direct ancestor of another. Instead, it is more usual to ﬁnd that one fossil form is related to the ancestor of another, because it possesses characters which that ancestor must have possessed, while at the same time showing other characters which proclaim that it had diverged from that ancestor. The characters of the ancestor in question are, of course, to a certain extent deducible from those of the form descended from it.

The incompleteness of knowledge of the fossil record makes it diﬂicult to ﬁnd “fathers“, but it supplies a number of “uncles”. The question now is this: why do the “fathers” and “uncles” resemble one another? Cynognatlms itself is not the ancestor of the mammals, for in several respects it is too specialised, but it must have evolved CONCLUSIONS 413

parallel with the ancestor of the mammals or it would not possess so many similarities. In the same way it can be shown that the later Stegocephaltans, which were not on the line of descent of the reptiles, nevertheless show a number of changes in evolution which took place parallel to those which were going on in their “cousins" the reptiles.

The answer must be that the “fathers” and the “uncles” inherited something from the “grandfather” which determines the course of their evolution. This something need not, however, have been visible in the “grandfather”, so that the “fathers” and the “uncles" in which the something does become visible appear to have evolved it independently. In these cases there appears what may be called a latent homology between the structures in question, and which accounts for the so-called “orthogenesis". In any case, it is most important to avoid the impression that “orthogenesis“ implies a purposeful or directive force, or that evolution takes place in straight lines. Such impression is quickly dispelled by a consideration of the record of success and failure of the different groups of animals during evolution. If a directive force were responsible for evolution, it would seem to be peculiarly malicious, for most groups of animals have been “directed” to their doom by extinction.

An insight into what “orthogenesis" may mean is given by a study of the relative sizes of parts of animals to the whole animals. at different absolute sizes. It is found, for example, that the size of the antlers in Red deer is relatively larger in large animals than it is in small ones. That is to say, that the larger a Red deer grows, the relatively larger do its antlers become, on the average. These cases are susceptible of mathematical treatment, and it is found that the antlers not only grow faster than the body, but they grow faster at a constant rate, for the ratio of the growth-rates of antlers and body remains constant. Organs to which this principle applies are called allometric, and allometry is of wide occurrence in the horns and bony knobs of various groups of Ungulatc mammals. Now just as the allometric organ is relatively smaller in small animals. it is found as a rule that in two species of one genus both of which possess this organ, the larger species will have the relatively larger allometric organ. So the antlers of the little Muntjack are relatively smaller than those of the larger Red deer. There are of course exceptions and complications, but from the present point of view the mam thing to notice is that for an organ which shows allometnclgrowth to appear at all, the animal’s body must have reached a,certam absolute size. Now as the different races of Titanotheres evolved. their size increased, in common with nearly all. the groups of mammals. Independently, each of these races of Titanotheres developed bony 414 concwsrons

knobs on the skull, and as the size-increase of the animals continued, the bony knobs became relatively larger still. The bony knobs are allometric organs, and their independent appearance in dilferent races is not due to any directive force, but automatically to the increase in size of the body of the animal. This increase of body-size was probably due to random variation selected by natural selection in the direction of greater size because it is (up to a point) advantageous, and has survival value. From the common ancestor of the diﬂ"erent races it is only necessary to assume that the capacity was inherited to produce bony knobs if and when a certain body-size is reached. On this view, therefore, “orthogenesis” does not mean directed evolution, but merely directional. It also enables an explanation to be given for the cases of extinction of animals in which the size of the allometric organ (consequent on the large size of the body) had become so great as to reduce the animal’s chances of survival. This applies to the Irish elk, which was a very large deer with relatively immense antlers.

Attention must now be paid to the terms “primitive” and “specialised”, which were deﬁned early in this book, and which have been consistently used throughout. In the ﬁrst place, it is necessary to notice that their meaning is relative, so that it is possible to ﬁnd an animal which is primitive when compared with one and specialised when compared with another animal. A specialised animal is one which is committed to a particular line and so has a restricted potency of evolution. As a rule, specialised animals are adapted to a particular mode of life, and this adaptation has entailed either the development or loss of certain structures which render the animals unﬁt to live in any other environment but their own. Once committed, they are committed for always, for in its broad lines evolution is irreversible.

Primitive animals, on the other hand, are not committed to any particularly restricted mode of life; they do not have any delicate adaptations with the structural modiﬁcations which they involve, and they are, in a word, generalised.

It is from generalised ancestors that the main groups of animals have evolved, and as these groups radiated out they became specialised in their various ways. Specialisation and evolutionary capacity are roughly inversely proportional.

The signiﬁcance of primitiveness and specialisation is thus related to evolution. Amphioxus is primitive because it possesses many characters which the early ancestral Chordates must have bad. But its specialised characters show that it was not itself that ancestor. Amphioxus is with regard to the higher Chordates not a “father" but an “uncle".

It is worth noticing that the primitive arrangement of several CONCLUSIONS 415

structures was segmental, and that as evolution proceeded this simple scheme was departed from. So the gonads of Amphiaxus, myotomes of Amphioxus, kidney tubules of Myxine, ribs of Cotylosaurs, and respiratory centres of Rafa show that “a pair of each in each segment” was the primitive outﬁt, on which evolution has worked. When man is considered in relation to his ancestors, a signiﬁcant fact emerges. Man is not adapted to any restricted mode of life at

, . - ‘_v d- C‘ chick' 1), rabbit;

Figure 185. Views of embryos of dpgﬁshi 3.1%?‘ _» ~_ __ ' b - .

and E, man; showing the similarity at early stages between em ryonic forms of related animals.

all; instead he is ﬁtted for almost all sorts of hl'.:b:ts_ .a3:c¢1(:;;"$c stances; he is generalised not specialised. and i 3 '5‘ have been secrets of his evolutionary success. l_lis ancestors‘ musals. they did among the most primitive and generalised of the mattnmandi Spend it not live on the capital of their evolutionary cap?!“ '35

_ . - hjch while perhaps allowing exchan e for delicate adaptations. W_ _» _ . loI;“‘easierg1iving”, would have resulted in side-tracking the face "N0

a rut or backwater of life. 416 CONCLUSIONS

Lastly, mention may be made of the material which the vertebrates supply for a consideration of what was called the law of recapitulation. It is not astonishing that a group as broad and as well known as the vertebrates should provide several examples of embryos which seem to reﬂect something in the ancestral stages of the forms to which the embryos in question belong. As an example, the gill-slits (or rather gill-pouches) of the mammals may be taken. It is rightly held that these structures in the embryo mammal represent the gillpouches and slits of the ﬁsh-stage ancestor of the mammals. But the most important thing to notice is that it is the gill-pouches of embryo ﬁsh and not those of adult ﬁsh which the gill-pouches of mammalian embryos resemble; indeed, not much observation is needed to see that between the gill-pouches of the mammalian embryo and the gill-slits of an adult ﬁsh there is but little resemblance, whereas the gill-pouches of embryonic stages are very similar in all groups of vertebrates. This explanation covers all cases of so-called recapitulation. It follows that it is inaccurate and misleading to say that Ontogeny (the development of the individual) recapitulates Phylogeny (the evolution of the race). What may be true is that Ontogeny repeats the Ontogeny of the ancestor, and even then, it is not necessarily true of all embryonic forms. While the gill-pouches are repeated in this sense, other organs such as the primitive streak or the extra-embryonic ccelom are not. It is also to be noted that the order of appearance of structures in Ontogeny is not necessarily the same as in Phylogeny. Denticles appeared early in evolution, but they arise late in the development of the dogﬁsh. The embryo is phylogenetically older than the amnion, but in the development of the mouse, the amnion arises first and the embryo afterwards.

The real value of embryology from the point of view of evolution lies in the fact that embryonic forms are like the embryonic forms of related animals. As a rule, the younger the embryos are, and the closer akin the species to which they belong, the more closely do the embryos resemble one another. The more closely allied the species are, the longer does the resemblance between the embryos persist. Embryology furnishes valuable evidence therefore as to afﬁnities,

but it cannot profess to give deﬁnite information concerning the adult forms of ancestors.

LITERATURE

BATESON, W. Problems of Genetics. Yale University Press, 1913.

DE BEER, G. R. Embryos and Ancestors. Clarendon Press, Oxford, 1951.

GARSTANG, W. The Theory of Recapitulation: a Critical Restatement of

the Biogenetic Law. Journal Limzean Soc'iet_v, London, Zoology, Vol. 35, 1922. concwsxous 417

Goomucn, E. S. Metameric Segmentation and Homology. Quarterly Journal of Microscopical Science, Vol. 59, 1913.

HUXLEY, J. S. Constant Diiferential Growth-ratios and their Signiﬁcance. Nature, Vol. 114, December 20th, 1924.

KAPPERS, C. U. A. Three Lectures on Neurabiotaxis and other subjerts. Levin & Munksgaard. Copenhagen. 1928.

14.1 CLASSIFICATION OF THE ANIMALS AND GROUPS OF ANIMALS MENTIONED IN THIS BOOK

Phylum. Subphylum. Class.

Class. Subphyl um. Class. Order. Order. Order. Class. Class. Subphylum. Division. Branch. Class. Class. Subclass. Subclass.

Branch. Grade. Grade. Class. Order.

Order.

Order. Class. Subclass. Order.

Order.

(An asterisk denotes a totally extinct group)

CHORDATA. HEMICHORDATA. PTEROBRANCHIA, e.g. Cephalodiscus, Atubaria, Rhabdopleura. ENTEROPNEUSTA, e.g. Balanaglossus. PROTOCHORDATA (ACRANIA). UROCHORDATA. ASCIDIACEA, e.g. Ascidt'a. THALIACEA, e.g. Salpa. LARVACEA, e.g. Fritillaria. (‘I-ZPHALOCHORDATA, e.g. Amphiaxus. EUPHANERIDA"', e.g. Jamoytius. CRANIATA. ANAMNIA. CYCLOSTOMATA.

OSTRACODERMA,‘ e.g. Ceplzalaspis. CYCLOSTOMATA. PE1 DOMYZONTIA, e.g. Petramyzon. MYXMOIDEA, e.g. Myxine, BdelIoSlwmi.

GNATHOSTOMATA.

APHETOHYOIDEA,"' e.g. Acanthodes.

PISCES.

('HONDRI(‘HTHYES.

(‘.LADOSELACHIl,"' e.g. CIad0.s'eIaclte.

Pl.EURACANTHODIl,"' e.g.Pleuracuntlms.

SELACHII, e.g. Scyllium, Squalus, Hi-ptanc/ms, Hexanc/ms, Heterodontus, Pristis, Rlzimt, Pliotrema. Rain, Torpedo.

HULUCEPHALI, e.g. C/tirtrwra.

OSTEICHTHYES. TELEOSTOMI. OSTEOLI-2PlDOTl,"' e.g. Osteolepis, Saut-iptertts. CCELACANTHINI, e.g. Undina, Latittteria. 418 Order. Order.

Order.

Order. Order.

Order.

Subclass.

Class. Order.

Suborder. Suborder.

Suborder.

Order.

Division. Class.

Subdivision. Subdivision.

Order.

G roup. Superordcr. Order.

Order.

CLASSIFICATION or ANIMALS 419

—.———~

'r"'l'hi: C-I-0-’!-‘YLOSAURIA a

ANAPSIDA.

Ponvrn-znrm. e.g. Polyprerus.

PAL£oNrscoroai,"‘e.g. Cherralepis.

ACIPBNSEROIDEI. c.g. (Timudrosteus, Acipenrer.

AMIOIDEA, e.g. .-min.

LEPIDOSTEOIDFI, c.g. L¢'_nidusreus. «

TELEOST ax. e.g. Gadus, Arm'urus, 1i{ornr_rru.s*, I/maps, I’¢*n'~ oplulmlrnrts, F:'c'rasﬁ'r, Gabi?csax, Anrbly¢2p.w'.r, I..uc£fu,::cr, Snltra. E.\'0c‘a-ms, Edrialyc/inu.v. Eur_vpImr,vn.x:.

DI PNOI . e.g. C“¢'rmadu.s'. Lc*p.idu.w're'rz, [‘nm:pm'us. Dipterus.

A MP H I B! A .

LABYRlNTHOI)ONTlA"'

CEPHALIA ).

lC‘llTH\'0S'l‘l~.UM IA. It'hIhm.src*ga.

1=.MBm.oMi=.m. e.g. !i'u_q_vr:'nu.v. L4)xammu, Miolmrrm /ms.

SF.YM()URlAMORP!lA. c.g. .S'¢{r-— mom-m.

U R()DEl A, e.g. Trilurux, Sulmrmmlm. Prot¢~*u.s', Siren, Clrypmlnunclms, Nccturus.

ANU RA, c.g. Prnmbatrtlrimx, I~.’.mu, Pipa, Rlzinnclerma. A I yr:-3, I1; lumbales.

GYMN()PHl(>NA, e.g. lc-lnliynpluas, H_vp0,:,r('r2pIz_i'.s'.

A M N 101‘ A .

R E P T! L I A .

Tc 0 ‘T Y 1. 05 A U R 1 A,‘ c . g. Parc':'u.s'auru.s‘. sAuI<« JPSIDA.

Tcn m.oNi.\, c.g. 7’c.s‘tudo. Clwlmm, S];/zcir-g.'.s, l.ft¢rz()(u.s'az:rus. TI'i£l.S'S()C/wlys.

P A R A P S! 1: A .

SQUAMATA. L A r E 1: 11 MA, e.g. Laccrm, Immnus, Uromastix, (:'e¢'ko. Anguis, C'lm/ad:-.1‘, .‘>'z'irzm.s*, Amp/ri.s'bn-nu, Chumwiva, .'\1o.sa.s'auru.s~. ‘

OPHIDIA, e.g. Vipera.

(S‘l‘I-(.iOnd cHTsL'oN1A"arc often groubcd together as 420

Superorder and Order.

Group. Order.

Order. Su border.

Suborder. Suborder. Order.

Suborder.

Order.

Subdivision.

Group. Order.

Class. Grade.

Grade. Subclass.

Subclass.

Class. Grade.

Grade and Subclass.

Grade. Subclass. Subclass.

CLASSIFICATION OF ANIMALS

IC'I-ITHYOSAURIA, e.g. Mixesaurus, Ichthyosaurus, Ophthalmosaurus.

DIAPSIDA.

RHYNCHOCEPHALIA, e.g. Sphenodon (? Thalattosaurus).

cnoconuu. PSEUDOSUCI-lIA,"' e.g. Euparkeria. THALATTOSUCI-HA," e.g. Geasaurus.

EUSUCHIA, e.g. Crocodilus. mNosAun1A.*

VSAURISCHIA, e.g. Diplodocus,

Tyrannosaurus. PREDENTATA (or 0RNITHISCHIA), e.g. Iguanodon, Stegosaurus, Triceratops. PTEROSAURlA,"' e.g. Ptercmodon. TI-IEROPSIDA. SYNAPSIDA. TI-lEROMORPHA,"' e.g. Cynognathus. SYNAPTOSAURIA. SAUROPTBRYGIA,’ e.g. Nathasaurus, Plesiosaurus. AVES. ARCHIEORNITHES,‘ e.g. Archaeopteryx. NEORNITHES.

CARINATES, e.g. Columba, Gallus, Megapode, Grebe, Petrel, Diver, Gull, Flamingo, Duck, Phalarope, Dodo, Solitaire, Humming-bird, Penguin, Tinamu.

RATITES, e.g. Struthio, Emu, Rhea, C assowary, Apteryx (Kiwi), Moa.

MAMMALIA. MULTlTUBERCULATA."' MONOTREMATA, e.g. 0rm'thorhynchus, Echidna. DITREMATA. 1‘RITUBERCULATA."' MARSUPIALIA, e.g. Didelphys, C avnolestes, Dasyurus, Thyla-» cinus, Perameles, Phascolarctas, Phascalomys, Phalanger, Notoryctes, Thylacoleo, Macrapus. Subclass. Order.

Order. Order. Suborder.

Suborder. Order. Order.

Order. Suborder. Family.

Family. Family.

Family. Suborder. Tribe. Family. Family. Tribe. Family.

Tribe. Family. Family.

Family

Order. Order. Order. Order.

Order.

CLASSIFICATION or ANIMALS 421

PLACENTAI IA.

DEL'I‘ATHERlDlID.E,"' e.g. D91. ratheridium.

cIu2oI)oNrA.*

CARNIVORA.

FISSIPEDIA, e.g. Canis, Fells, Ursus, Civct, Badger.

PINNIPEDIA, e.g. Seal.

CONDYLARTHRA.

AMIII.YI>oI)A,"' e.g. Uimathermm.

UNGULATA. PERISSODACTYLA.

TITANOTHERID/l‘3.," e.g. TI'mnotherI'mn.

TAPIRIDIE, e.g. Tapir.

RHINO(‘l£ROTlD.l"'.. Lag. Rhinoreros.

EQUIIM-1, e.g. Er)hippu.s', Mesohippus, MioIu'ppu.s', Pliou hippus, Equus.

ARTIODACTYLA.

SUINA.

sum 5%, c.g. Sus.

l-lll’POl’OI‘AMll)A‘. e.g. Hippoputanms.

TYLOPODA.

CAMFHDIE, e.g. Pr'0!_lIn;mS. Poé'bI'othcrI'urn, l’rcu'mm'Iu.I', (‘amelu.s'.

PECORA.

CIIRAI I—'IIM=, e.g. Gimlfc.

( I=.RvImI=, c.g. (‘or-I-u.s-, Reindeer, Muntjzlck, Irish lilk.

B()Vll)/ls. e.g. Ox, Zebu. Sheep, (_in:.It, Antelope‘. AnIIlnczIprid'.I:, c.g. AMI’Iompra.

HYRACOIDEA, e.g. h'.I'rax lconey).

I>RonoscII>I~:A, c.g. McrrI'tharium, Pala'onm.s'mdun, Tetrabelodon, Elvp/mr.

SIRENIA, c.g. Manafus.

CETACEA, c.g. Whale, Dolphin, Porpoisc.

I.IToI~TIznr~IA," e.g. Thoatherium. 422 Order.

Order. Order.

Order. Order. Order. Suborder.

Suborder.

Suborder. Series.

Series. Family.

Family. Family.

Suborder. Family.

CLASSIFICATION OF ANIMALS

EDENTATA, e.g. Bradypus, Cholaepus, Armadillo, Pangolin.

nonanru, e.g. lzpus, Mus, Squirrel, Porcupine.

rnsacrrvoru, e.g. Mole, Hedgehog, Shrew, Plesiadapis,

Macroscelides, T upaia, Scalapus. Cl-IEIROPTERA, e.g. Bat. DERMOPTERA. PRIMATES. LEMUROIDEA, e.g. Notharctus, Lemur. TARSIOIDEA, e.g. Tetonius, T arsius. ANTI-IROPOIDEA. . PLATYRRHINIE, e.g. Marmoset. CATARRHINE.

PARAPITHECIDE, *e.g. Parapithecus.

cancoprrnecrwa, e.g. Cercopilhecus, Mandrill, Baboon.

smnna, e.g. Propliopitlrecus, Pllopithecus, Proconsul, H ylobares, Simia (Oran8). Chimpanzee, Gorilla.

HOMINOIDEA.

AUS'l'RALOPIT'HECIN.£, c.g. Australopithecus, Paranthropus, Plesiantlzropus.

HOMINIDIE, e.g. Pirhecanrhropus, Homo neanderlhalensis, Homo sapiens.

Book - Vertebrate Zoology 14 1922

XIV The development of Lepus (the Rabbit)

Fertilisation

PART III