Paper - Studies in the embryology of the ferret (1911)
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Yeates T. Studies in the embryology of the ferret. (1911) J Anat. 45(4): 319–335. PMID 17232892
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Studies in the Embryology of the Ferret
By Thomas Yeates, M.B., Senior Demonstrator in Anatomy, The University, Birmingham.
Part I.
Whilst a study of the general embryology of the Carnivora has been made by several observers, no clear view has, so far as I am aware, been presented of the various phases of the earliest stages of development of the group by means of models.
I have therefore commenced to make a series of reconstruction models of the ferret which will, it is hoped, show the more salient points of its embryological history.
I have been directed thereto through the kindness of Professor Arthur Robinson, who has placed his extensive collection of ferret embryos at my disposal.
The specimen with which I have embarked on the work is convenient in size and age, and I intend to’ follow this up with models of other specimens both older and younger.
Ture Embryo.
The embryo (fig. 1) is distinctly asymmetrical, lying outstretched on the wall of the yolk sac, towards the cavity of which its long axis is very slightly curved.
The tail fold has not yet appeared, but there is a well-marked cephalic flexure.
Extending from the cephalic to the caudal end of the embryo, the neural groove is seen; on the tail bud it suddenly becomes shallower, and disappears gradually as it curves round the extremity of the bud. Closure
1 The specimen was taken from a ferret fifteen days after coitus, and cut, in wtero, into 390 sections of 104 thick. Each section was drawn for the complete reconstruction, magnified 100 diameters ; whilst for the reconstruction of the organs the sections were magnified 300 diameters. Blotting paper was incorporated in the wax plates, in accordance with the suggestion of Professor A. Thomson of Oxford, to give strength to the model.
ach plate for the model of the entire embryo was made 1 mm. thick, and as there were 390 wax plates, the entire plates should have measured 39cm. They actually measured, however, 38°6 cm., giving an error of 1:03 per cent., which was disregarded.
The actual length of the embryo as calculated from the sections was 32 mm., and its age was under fifteen days, of the groove has occurred at a level corresponding to the interval between the second and third somite of the right side. Just in front of the tail the groove is broad and deep, forming the sinus rhomboidalis, whilst immediately behind its closed portion an elongated dilatation, extending over about one-sixth of the total length of the embryo, is evident. At the head end of the embryo the right lip of the groove considerably overlaps the left.
Fig. 1. — Dorsal view of embryo,
The head is well developed, and presents a distinct cephalic flexure ; in addition to this flexure the long axis of the head is curved, so that the snout and mouth are directed towards the right (fig. 2).
Extending from the cephalic end of the pericardium dorsally towards the head is a prominent first right branchial arch, immediately behind and parallel with which is a depression constituting the first right visceral cleft, intervening between the prominent first arch in front and the second right — arch behind. The latter is not so well developed as the former. Projecting ventrally from the dorsal end of the first right arch is the right maxillary process, whilst immediately ventral to its other extremity is the cephalic end of the pericardium.
Fig. 2, — Side view of head (block A). First M.A., first right maxillary arch ; 1st M.A’., first left maxillary arch ; 1st R.A., first visceral arch ; B.P., buccopharyngeal membrane; Sn.R., right half of snout; Sn.L., left half of snout; Ist R.C., first right visceral cleft; P.C., cephalic end of pericardium ; N.G., neural groove.
The two branchial arches on the left side with the pouch between them and the left maxillary process are disposed more caudally than those on the right. This fact, in conjunction with the curvature of the mouth and snout to the right, has caused the left maxillary process to project towards the right as the caudal boundary of the mouth, which is a depression opening towards the right; its floor is formed by a well-marked rounded projection, the bucco-pharyngeal membrane. Bounding it on its cephalic and on its caudal sides are the right and left maxillary arches respectively. On the right and dorsally it is limited by the first right branchial arch, whilst on its left and ventrally are both the right- and left-hand sides of the snout. A clear conception of the boundaries of the mouth can only be obtained by ' remembering that the snout is curved over towards the right side and so twisted that its right side is nearer to the cephalic end of the embryo, whilst its left is nearer the caudal.
The heart and pericardium form a bulging on the ventral aspect of the ~ embryo caudal to and on the right of the head. It is covered by the wall of the yolk sac, but is still outside the amnion.
The Yolk Sac and Extra-embryonic Coelom
Fig. 3. — Uterine wall from within.
The yolk sac is large, and forms a lining to that portion of the uterus not occupied by the embryo and amnion (figs. 1 and 3). It is separated from the uterine wall by the chorion. In the neighbourhood of the embryo it is reflected from the uterus and closely applied chorion to reach the margin of the embryo. It is sufficiently stretched, as it passes from the one to the other, to aid in suspending the embryo from the uterine wall, Along a line corresponding to the root of the amnion it finds attachment to the embryo, but in the cephalic and pericardial regions it can be traced centripetally from the uterine wall in contact with the outer surface of the proamnion to reach the pericardium. The yolk sac and proamnion, on reaching the pericardium, part company: the former covers the ventral and caudal aspects of the pericardium, covered by the mesoderm of the septum transversum, and gains attachment to the embryo along the ventral margin of the entrance to the fore gut; the latter is, however, reflected dorsally on to the cephalic aspect of the pericardium, to become continuous with its ectodermal surface. Ventral to the tail the allantoic diverticulum exists as an outgrowth from the cavity of the yolk sac, whilst between the body wall and the pericardium a second diverticulum, extending cephalad, constitutes the fore gut.
The outer mesodermal surface of that portion of the wall of the yolk sac which extends from the uterine wall to the embryo forms the ventral wall of the extra-embryonic ccelom (fig. 1), which on the other hand is bounded dorsally and laterally by the uterine wall lined by the chorion (fig. 3). Traversing the extra-embryonic ccelom at the cephalic half of the embryo is a tube, more widely open at its uterine extremity, where it is attached along the margin of the chorion, than at its embryonic extremity, which is attached to the periphery of the embryo in front and at the sides, whilst caudally the wall of the tube is continuous with the closed portion of the amnion. This ‘tube suspends the middle and heavy cephalic part of the embryo to the uterus, and thus forms the second means by which the embryo is fixed to the uterus.
The Amnion
The amnion is attached to the embryo along the line where it becomes continuous with the somatopleure, which corresponds to the line of communication of the intra- with the extra-embryonic coelom. In front it is attached to the lateral aspect of the pericardium. At the cephalic end of the pericardium it intervenes between it dorsally and the yolk sac ventrally, on both sides, as cecal diverticula (fig. 4, A, A) of its cavity open towards the cephalic end of the embryo. The left diverticulum is more caudad than the right. Mesially, the amnion covers the cephalic end of the pericardium, and meets the yolk sac ventrally, with which it passes as the proamnion to the uterine wall; it does not intervene as a diverticulum between the yolk sac and the pericardium. To sum up the relations of the amnion to the pericardium briefly: The heart and pericardium are being encroached on by the amnion, more rapidly at the sides than mesially, and still more rapidly on the left than on the right—the latter being, apparently, due to the asymmetry of the embryo. Closure of the amnion has occurred over the posterior half of the embryo, but it remains open over the anterior half, being attached to the tube already described as traversing the extraembryonic ccelom. The amnion and yolk sac have already been stated to be the means by which the embryo is attached and suspended to the uterine wall; at the cephalic end of the embryo they are more tense, and present fewer folds than at the tail end, due probably to the excess of weight of the former end.
Fig. 4. — Cephalic end of block B. A., amniotic cavity; P.C., pericardial cavity; T.A., truncus arteriosus ; 1st R.Aor., first right aortic arch ; 1st L.Aor., first left aortic arch; V.F., ventral wall of fore gut; Y, 8., cut edge of combined yolk sac and proamnion.
The Allantois
The anlage (fig. 1) is a mass of mesoderm projecting into the extra-embryonic coelom from the extreme caudal end of the embryo, and is separated dorsally from the tail bud by the attachment of the amnion. Two spaces exist within the substance of this mass of mesoderm: one—the allantoic diverticulum of the yolk sac—is a wide space lined by the continuation of the entoderm of the yolk sac, and projecting caudally more towards the right of the enveloping mesoderm ; the other — a cleft in the mesoderm — is irregular, small, devoid of a lining, and situated on the right of the allantoic diverticulum.
The two spaces are almost in contact in places, and the appearance suggests that ultimately the tissue between them will disappear and cause their cavities to be continuous.
Caudally the extremity of the anlage presents three small primary bulgings placed side by side. The mesial of these is the largest, and shows no indication that it is bifurcating; the lateral bulgings, however, present two small secondary prominences at their extremities, indicating that subdivision is taking place. Of the two lateral bulgings the right is more prominent, and extends further back than the left. -It is difficult to explain the significance of these prominences.
Strahl, in describing the development of the allantois in the typical mammal, affirms that it begins as a bud at the caudal end of the embryo, projecting into the extra-embryonic ccelom. The bud is invaded by an entodermal diverticulum from the yolk sac during the formation of the tail fold, which when completed causes the diverticulum and enveloping. mesoderm to be placed ventral to the hind gut.
The origin of the allantois in Lacerta viridis, Lacerta agilis, and Lacerta vivipara has been described by Strahl, Peters, and Schauinsland as arising in a somewhat unusual manner. The anlage is a solid mass of mesoderm, which is present previous to the splitting of the middle layer to form the somatopleure and splanchnopleure. It is situated at the extreme posterior end of the embryo, in the region of the anterior part of the primitive streak, immediately behind the neurenteric canal.
This portion of the primitive streak divides transversely into two, the anterior of which becomes the tail anlage, the posterior the allantoic anlage ; the latter projects into the extra-embryonic ccelom after the splitting of the mesoderm has taken place. In the allantoic anlage a space now appears: it at first is devoid of a lining and has no communication with the cavity of the gut; later it bursts into the cavity of the gut, the lining of which grows into and lines the original mesodermal space. The last stage in the process is the development of the tail fold.
Two distinct modes of development of the allantois have thus been described, one of the typical mammal and the other of the Lizards. In the writer's specimen (ferret), the condition of the allantois does not agree with any stage of the development of this structure in either the typical mammal or the lizard. In this specimen the allantoic anlage exhibits two spaces which appear to be growing towards each other, to unite to form one. If this is so then the allantoic cavity has a double origin, and is developing in a manner intermediate between that of the typical mammal and that of the lizard.
The Nervous System
Except opposite the second and third somites, the nervous system is an open tube, subdivided into brain and spinal cord, although there is no sharp line of demarcation between one and the other. 326 Mr Thomas*Yeates
The brain consists of three asymmetrical vesicles, and presents a wellmarked cephalic flexure (fig. 5). Its long axis, in addition to presenting the typically cephalic flexure, exhibits a lateral curve, so that it presents a concavity towards the right, in which an excess of mesoderm surrounding the anterior end of the fore gut is lodged.
The fore brain presents on its exterior three prominences which correspond with dilatations of the tube, and represent from the cephalic end in a caudal direction—the first or olfactory prosomere, the second or optic prosomere, and the third prosomere, which shows both internally and externally evidence of subdivision into two parts—an anterior thalamic part, a posterior geniculate part. Limiting the fore brain caudally is a sudden constriction of the neural tube, which sharply demarcates the expanded fore brain vesicle from the more constricted mid brain.
Fig. 5. — Right-hand view of model of brain,
Pl, P2, P3, 1st, 2nd, and 8rd prosomeres ; R!-R7, 1st-7th rhombomeres ; M1, M2, position of ~ lat and 2nd mesomere ; N.G., neural groove ; I.R., isthmus rhombencephali.
The mid brain is situated at the most anterior (cephalad) part of the cephalic flexure. Its dorsal wall is much longer than its ventral wall. It ig the smallest part of the brain, and is sharply demarcated from the hind brain by a groove—the isthmus rhombencephali. It presents two mesomeres, which are subdivided on the inner surface of the tube by a ridge running parallel with its long axis into a basal and alar lamina (fig. 6). The ridge probably represents the position of the future sulcus of Monro. It fades away towards the fore and hind brain.
The hind brain, as has already been stated, is demarcated off from the mid brain by the isthmus rhombencephali; caudally it merges gradually into the spinal cord. Seven rhombomeres are recognisable.
Most observers agree as to the number of segments in the fore and mid brain, but many different opinions exist with regard to the number in the hind brain. Bradley states that there are seven in the pig. Prenant mentions six as the number, whilst Lewis affirms that he can only make out five. The lack of agreement between different workers may possibly be explained by assuming that the number of rhombomeres differs at different stages of the development of the hind brain. The same idea is expressed by Professor P. Thompson. In describing the brain of a 2°5 mm. human embryo he states: “The ganglia of the ninth and tenth cranial nerves are not yet visible, and this may possibly explain the imperfect differentiation of the sixth and seventh neuromeres opposite which the ganglia of these nerves normally develop.”
AL Miller del. MY, M”, Fic. 6.—Model of right half of brain.
Pl, P2, PS, lst, 2nd, and 8rd prosomeres; M1, M1’, M2, M2, 1st and 2nd mesomeres ; 5.M., ridge corresponding to the position of the suicus of Monro. Subdividing the mesomeres into a basal and alar portion. R1-R7, 1st to 7th rhombomeres.
In the spinal cord three pairs of posterior root ganglia exist: one pair, just in front of the first mesoblastic somite, and pairs opposite the first and second somite.
The Alimentary System
This is represented by the yolk sac and the allantoic and fore gut
diverticula. The yolk sac and allantois have already been discussed. The fore gut exhibits to a marked degree the asymmetry of the embryo.
The long axis of its lumen is in the main directed transversely, but at its cephalic end the gut is bent ventrally and curved towards the right so as to terminate in the mesoderm on the right-hand side of the mid brain (fig. 7).
The first right visceral pouch is well developed, and corresponds to the first visceral cleft externally. The mesoderm along the line of contact of the pouch and cleft is absent, the ectoderm and entoderm being in contact. The second visceral pouch is present, but is not so well developed, and is situated on a level with the first mesoblastic somite. Separating the first and second pouch is the first arch, which is represented as a broad groove on the solid reconstruction of the pharynx (fig. 4). The left pouches and cleft agree generally with those on the right, but are disposed nearer the caudal end of the embryo.
Fig. 7. — Special section through block A to show extreme cephalic end of fore gut.
Sn., snout; L.M.A., left maxillary arch; F., fore gut; Be.E., blind end of fore gut; Cav., cavity from which brain has been removed; ist L.Aor., first left aortic arch ; 1st R.Aor., first right aorticarch ; 1st L.P., first left pouch ; lst R.P., first right pouch ; I.C., internal carotid artery.
On a level with the ventral ends of the first arches, and in front of (cephalad) the first mesoblastic somite, the median thyroid projects as a conical proeess from the ventral wall of the fore gut.
Radiating from it are five ridges: one passes to each first pouch, one to both sides of extreme end of fore gut. The fifth ridge extends caudally Studies in the Embryology of the Ferret 329
to the liver anlage, which is seen projecting from the ventral aspect of the gut into the septum transversum, opposite the interval between the first and second left somite. The above description is taken from the solid reconstruction of the pharynx (fig. 8).
1st right pouch. ~-~-—-- :
Cephalic end of fore gut.
Grooves for Ist..........-.---arch,
2nd right pouch. -----.---... -- 1st left pouch.
Median thyroid.
- 2nd le t pouch.
Osenng Pays. oe
Liver bud, Fie. 8.—Solid reconstruction of pharynx.
The Notochord
The notochord is forming, and presents different appearances according to the level at which it is examined.
On a level with the junction of the posterior fourth with anterior threefourths of the embryo it exists as a notochordal plate for a distance of about 60 4. Cephalad to this it is present as a groove in the entoderm, with thick walls gradually merging into a fully formed rod, at first connected to the entoderm, but finally separated from it. As it is traced towards the cephalic end of the embryo it tapers very gradually, but beneath the brain it again expands somewhat, and follows the cephalic curve, to terminate at the junction of the middle and posterior thirds of the mid brain by apparently becoming continuous with the surrounding mesoderm.
Towards the tail end of the embryo the notochordal plate rather abruptly becomes a well-marked rod; this gradually expands and, being closely pressed against the ventral aspect of the nervous system, terminates by imperceptibly fusing with the mesoderm anterior to (cephalad) the tail bud.
The Excretory System
The nephrotome is situated in the somatopleure, just external to the dorsal part of the paraxial mesoderm. It is a column of cells which extends cephalad from a point some distance behind the notochordal plate to the junction of the middle and anterior thirds of the embryo.
The Mesoblastic Somites
There are three pairs of asymmetrically disposed mesoblastic somites which are not as yet visible on the surface of the embryo. In front of the first pair of somites the mesoderm is continuous, whilst behind the third pair it does not exhibit segmentation, but is differentiated into paraxial and lateral mesoderm as far caudally as the extremity of the nephrotome, behind which (caudad) the paraxial mesoderm and lateral plates are continuous.
The Septum Transversum and Pericardium
The septum transversum (figs. 9 and 13), a crescentic mass of mesoderm stretching transversely across the embryo on a level with the first somite, is so disposed that its surfaces are directed towards the cephalic and caudal ends of the embryo, and its right extremity extends more cephalad than its left. Dorsally it surrounds the junction of the fore gut and yolk sac (fig. 9, E. to F.), whilst ventrally it extends towards the head in close apposition with the pericardium, to end along the line of reflection of the proamnion from the pericardium.
Its caudal surface is covered by the wall of the yolk sac, whilst its cephalic surface is in contact with the pericardium ; and from it prominences, covered by pericardium, project towards the pericardial cavity to constitute the right, left, and dorsal mesocardia.
The right lateral mesocardium is a transversely disposed prominence on a level with the first right somite, containing within its substance the right horn of the sinus venosus, whilst the left mesocardium is disposed obliquely, being directed towards the cephalic end and to the right. Within its substance is the left horn of the sinus venosus (fig. 10). The dorsal mesocardium consists of caudal and cephalic portions separated by an interval behind the middle free portion of the heart tube; the former (caudal) portion (fig. 10) connects the corresponding portion of the heart tube to the dorsal pericardial wall and the surface of the Template:Septum transversum, whilst the latter (cephalic) portion (fig. 11) connects the truncus arteriosus with the dorsal and left lateral walls of the pericardium. Extending between these two portions of the dorsal mesocardium is a ridge on the dorsal wall of the pericardium which forms a prominence as it joins the cephalic portion of the mesocardium behind the truncus arteriosus, corresponding with the median thyroid pouch of the pharynx.
Fig. 9. — Caudal end of block C, viewed slightly from front.
Ht., heart; L.H.V., left horn of sinus venosus; 8.Tr., septum transversum; V.V., V.V’., vitelline vein; E. to F., entrance to fore gut; N., notochord ; D.A., dorsal aorta; I.C., intra-embryonic coelom.
Fig. 10. — Block C, seen from the front.
N., notochord ; D.A., dorsal aorta ; P.P., pleural péricardial passage; V.V., V.V’., vitelline vein; R.H.V., right horn of sinus venosus ; L.H.V., left horn of sinus venosus ; T.A., truncus arteriosus; Ht., heart ; C.P.M., caudal portion of posterior mesocardium. 832 Mr Thomas Yeates
Behind the lateral mesocardia and on either side of the caudal part of the dorsal mesocardium are the pleuroperitoneal passages, which connect the pericardial cavity with the intra-embryonic ccelom, which latter communicates by clefts between the somatopleure and splanchnopleure with the extra-embryonic ccelom already described (figs. 9 and 10).
Ose Dey Tacyee S,
C.F, Fie. 11.—Caudal end of block B.
P.C., pericardium ; Tr.A., truncus arteriosus ; R.P., recess of pericardium ; C.F., cavity of fore gut; C.P.M’., cephalic portion of posterior mesocardium.
The Vascular System
Coursing in the wall of the yolk sac are many vessels which join and terminate in two vitelline veins on both sides of the embryo (figs. 7, 9, 10). These are situated along the line of contact of the splanchnopleure and somatopleure.
One of these veins on both sides extends cephalad towards the septum transversum, and is joined by a short vein from the somatopleure, which is an early umbilical vein. Studies in the Embryology of the Ferret 333
The other passes caudad towards the septum transversum to unite © with the first-mentioned vitelline vein on a level with the second somite. The united vitelline veins pierce the septum transversum and course through the lateral mesocardia as the right and left horns of the sinus venosus.
Fig. 12. — Ventral view of cephalic half of model, showing division into three parts, viz. blocks A, B, and C.
1st R.A., first visceral arch, right side; Rt.M.A., right maxillary arch; N.G., neural groove; B.P., buccopharyngeal membrane; T.A., truncus arteriosus; Ht., heart; P.C., pericardial cavity; F.H., fretum Halleri ; S.Tr., septum transversum ; D.W., dorsal wall of yolk sac ; V.V., V.V’., vitelline veins.
As has already been pointed out, the lateral mesocardia, and consequently the two horns of the sinus venosus, are disposed differently on the two sides of the body. The right is disposed transversely, whilst the left courses obliquely cephalad and towards the right in line with the auricular portion of the heart tube. In fact, the left: horn of the sinus venosus and the heart appears to form one continuous tube into which, on its dorsal aspect, the right horn of the sinus opens. The auricle extends from the junction of the two horns of the sinus venosus upwards and towards the right, to end by bending caudally into the ventricular loop, which is completed by curving cephalad and towards the left to end by passing into the truncus arteriosus, the point of junction’ between the two being evident on the surface as a transverse groove (fretum Halleri). There is no evidence of a bulbus cordis (fig. 12). The truncus arteriosus extends over to the left across the bend joining the auricle and _ ventricle, and is connected dorsally and on the left to the pericardial wall by the cephalic portion of the dorsal mesocardium. Within the pericardium the truncus subdivides into two vessels (fig. 11), the first left and right aortic arches, which pierce the pericardium. dorsally and on the left. On emerging from the pericardium they bend cephalad in the corresponding branchial arches and curve over the first left and right visceral pouches respectively, to become the dorsal aortee (figs. 4 and 13).
Fig. 18. — Caudal end of block A. 1st L.Aor., yfiret left aortic arch ; 1st R.Aor., first right aortic arch; 1st L.P., first left pharyngeal pouch; F., fore gut; N., Notochord; Sn. R. » Tight side of snout; 8n.L., Left side of ‘snout; 1st M.A., first left ‘maxillary arch ; B c., pericardial cavity (cephalic end) ; Cav, cavity from which the brain has been removed.
From the crown of these arches the internal carotid artery springs, and extends for a short distance into the mesoderm at the sides of the mid brain (fig. 7).
The dorsal aorte course caudally, remain separate throughout, and very gradually pass on to the wall of the yolk sac, where they terminate in many branches.
It can be fairly assumed that the causes which have produced the Studies in the Embryology of the Ferret ‘Rah
asymmetry of this embryo have acted on the heart, and consequently its right-hand side is nearer the cephalic end and more dorsal than its left. One of the effects of this is that the curves of the heart tube’ are less pronounced than they would be under strictly normal influences.
In conclusion, I should like to thank Professor A. Robinson for his kindness in lending me this specimen, and Professor Peter Thompson for his kindly advice and the stimulating interest he has taken in the work.
I should further like to thank Messrs A. L. Miller and Oscar Parkes for their kindness in drawing the illustrations.
Bibliography
(1) Brapuey, ‘‘Neuromeres of the Rhombencephalon of the Pig,” Review of Neurology and Psychiatry, Sept. 1904.
(2) MeeK, Anatomischer Anzeiger, “The Cranial Segments and Nerves of the Rabbit, with some remarks on the Phylogeny of the Nervous System,” 9th June 1910.
(3) THompson, Jour. of Anat. and Phys., “Description of a Human Embryo of Twenty-three Paired Somites,” vol. xli. .
(4) ScuaurnsLanp, Hertwig’s Handbuch, “ Die Entwickelung der Reptilien und der Vogel.”
(5) Keiset, Normentafeln zur Entwicklungsgeschichte der Wirbelthiere.
(6) Strant, Hertwig’s Handbuch, “Die Embryonalhiillen der Sauger und die Placenta.”
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