Paper - On the phenomena of sex-differentiation (1892)

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Watase S. On the phenomena of sex-differentiation. (1891) J Morphol. 6: 481-493.

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This 1892 historic paper by Watase describes sex differentiation as understood at that time.


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On the Phenomena of Sex-Differentiation

S. Watase.


In the fifty-seventh Exercitation of his work On Animal Generation^ ^ Harvey states that he has frequently wondered how it happens that the offspring, mixed as it is in so many particulars of its structure and constitution, and with the stamp of both parents so obviously upon it in many parts, should still escape all mixture in the matter of sex, and that it should uniformly prove either Male or Female.


An obvious inference that suggests itself from this point of looking at the problem, as stated by Harvey, is that we may here be dealing with two questions which are independent of each other, viz. :

(a) The phenomena of heredity y or the mixture of the parental eliaracteristics in the offspring ; (b) The phenomena of sexual differentiation in the organism^ in which the parental c/iaracters have already been mixed.

Without therefore weakening even in the least degree the singularly suggestive form in which Harvey's reflection is put, we may for the sake of convenience separate the first half of the paradox from the second and consider them separately as two independent problems. We are, however, concerned at present with the second portion of the problem only, or the phenomena of sexual differentiation of the young developing organism in which the materials representing two parental characters already exist. It does not make any difference from our point of view whether this mixture of parental characters has taken place directly, in which case the embryo is the immediate outcome of tlie sexually fertilized ovum, or indirectly, in which case such mixture may have taken place some generations back, as must be considered to be the case in those eggs which are produced parthenogenetically.

Oh Animal CeneratioH, 1651, London. Tlie works of William Harvey, Willis' Cilition, 1S47, p. 429.


The present paper is the preliminary statement of my conclusions on this subject, as based principally on my studies in the line of work recently inaugurated by Auerbach,* who investigated the sexual substance of male and female organisms by means of differential staining. Auerbach's method has been applied with a certain modification, in two special lines of study, viz. the phenomena of spermatogenesis and of fecundation. This afforded me the opportunity of tracing the micro-chemical reaction of the male sexual cell through all stages of its transformations from the moment of its origin in the seminiferous gland of the paternal organism, until it ends in the formation of a mature male pronucleus ready to unite with the female pronucleus. The principal point which led to the writing of the present paper consists in the fact that the micr(xhemical reaction of the sperm-nucleus^ which is entirely different from that of the ovum-nucleus during the earlier stages of its existence^ becomes essentially like that of the female pronucleus at the moment 0of fecundation. Thus the distinction of sexes in the nuclei of the germ-cells, which Auerbach has so clearly demonstrated with specific stains in a number of cases, disappears completely at the close of fecundation, so far as such a point can be determined by the micro-chemical test.^ The full bearing of this fact upon the subject of our discussion, as well as the similar observation of Lukjanovv,^ I shall attempt to point out later.

As has been truly said, the distinction of sex is probably the most nearly universal single attribute or property of organized beings. According to one view, the difference of sex is the absolute difference of material which enters into the formation of the male and the female organism. There is also a view in which the maleness and the femaleness of the organism may be described as due to the differetice of state in which essentially the same organized matter appears as two different organisms according to the different conditions in which it may happen to be placed. The sexes, according to the latter view, may be considered as two different aspects of one and the same thing. The male and the female offspring of a given organism both inherit a similar share of materials from both parents, but simply take different courses in the mode of their ontogenetic development.


^ L. Auerbach, Zur Characieristik von Ei und Samen^ Berl. Klin. Wochenschr., 1891, xxviii, 908; ifber einen sexiitllen Gc^etisatz in der Chromatopkilie der Keimsubstanzen, nebst Bemerknngen ztim Ban der Eier und Ovarien nuderer IVirbeWiiere, Sitzungsbcr. der K. Preuss. Akad. d. Wiss. zu Berlin. XXXV, Heft VII, 1891.

^ Some facts bearing on this subject may be found in the two following abstracts of mine, Tha Oripn of the Sertoli's Ceil, American Naturalist, May, 1892 ; On the Sii^nifuance 0/ Spermatos^enesis^ American Naturalist, July, 1892.

• Lukjanow, Kinii^e Bemerktini^en iiber sexueiie Elemente beim Sptdwurme des J/undes, Arch. f. Mikr. Anat., Vol. 34, 1889.



It is interesting in this connection to recall the beautiful experiment of Maupas^ on the artificial determination of sexes in a Rotifer, Hydatina scnta. The Rotifer, as is known, produces three kinds of eggs, viz. two kinds of " summer eggs ** and one kind of

' winter egg." Of the two kinds of " summer eggs,'* it is known that the smaller egg always gives rise to the male, and the larger to the female. Under the ordinary circumstance, a certain female Hydatina produces exclusively the female eggs, while another female individual produces exclusively the brood of male offspring. Taking advantage of this fact, Maupas tried a series of experiments to determine under what circumstances this exclusive production of the male and the female offspring comes into play. Maupas holds, and his view seems to be amply justified by the results of his experiments, that the ova of the Rotifer up to a certain stage of their ovarian existence are devoid of sex or are neutral. Once this stage is passed, they are fated to develop either into the male or the female organism, as the case may be. Maupas considers that the determining influence which deflects the type of development of the organism, either to the male or to the female side, is due to temperature. If the ovarian ova which maintain the neutral stage as regards their sex are exposed to the influence of a higher temperature, they give rise to a far greater proportion of male organisms; while, on the contrary, if they are exposed to a lower temperature, a far greater proportion of the offspring are females.

In his first experiment, Maupas took five young females of Hydatifta, and kept them in his laboratory, whore the temperature was maintained between 26** C. and 28** C. The five females were kept till death, and in their lifetime they laid 104 eggs, of which 97 per cent, were males and only 3 per cent, were females. He took another set of five young females, and kept them in a refrigerator where the temperature was between 14** C. and 15° C. They laid 260 eggs during their lifetime, of which 95 per cent, were females and only 5 per cent, were males.


' Maupai, Sur la determiniime de la sexualiii chez rilyJntina scnhi, Coinpc. Rend. Acmd. Sci., rarit, T. cxiii, 189 1.



In his second experiment, he took five young females, and kept them in the temperature between 14** C. and 15° C. They laid no eggs, of which jS per cent, gave rise to females and 24 per cent, to males. He then transferred the same five females into the humid chamber, with the temperature 26°— 28° C. They produced, up to the time of their death, 1 18 eggs, of which 81 per cent, gave rise to males and 19 per cent, to females.

In his third experiment, Maupas took six young females, and these when kept in the lower temperature (14°-! 5° C.) laid 34 eggs, of which ^2^ per cent, were females and 12 per cent, were males. When the same female parents were placed under the influence of the higher temperature (26°-28° C), they laid 44 eggs, of which 95 per cent, were males and 5 per cent, were females. Maupas exposed the same females alternately to the higher and the lower temperature, and in one instance fully 100 per cent, of the eggs produced in the higher temperature turned out to be males. In the last four days of their existence they were placed in the cold chamber again, when they produced 50 eggs, of which 83 per cent, were females and 17 per cent, were males.

In short, when the young females of Hydatina were placed under the influence of the lower temperature, only 5-24 per cent, of eggs laid gave rise to males, while 76-95 per cent, of the eggs gave rise to females ; when, however, they were placed under the influence of the higher temperature, 81-100 per cent, of the eggs were males and 0-19 per cent, were females.

These observations of Maupas are most conclusive in showing that external influence does actually determine the sex of the offspring. The works of Mrs. Mary Treat,^ on Lcpidopteray of Bom * and of Yung * on Amphibians^ as to the influence of nutrition in the determination of sexes, are well known to all naturalists.

1 Mrs. Mary Treat, Controlling Sex in Butterflies^ American Naturalist, Vol. 7, 1S73.




The works of botanists in a similar line of observation are highly instructive, but I cannot dwell on these topics at present. The object of the present paper being only to bring out a certain illustration of general significance in connection with our subject, an extensive multiplication of analogous instances is not exactly to the point.

From what has been said, it is clear that the differentiation of sex in the developing embryo is purely an ontogenetic phenomenon. Observing farther that the conditions of the surroundings can effect such a determining influence as has been described, we may say from one standpoint that the sex-difFerentiation of the embryo is in the hands of external forces. On the other side, the maleness or the femaleness of the organism may be said to be the result of the responsive reaction on the part of the given protoplasm to the external stimuli. The sexdifFerentiation is, according to this view, due partly to a property of the protoplasm as determined by its inherent structure, and partly to the action of definite external influences which act upon the protoplasm from without. In this respect, to anticipate my conclusion, I may say that the plunovicnon of sex-differentiation is one with tliat of irritability ^ and is the most pronounced of all the phenomena of protoplasmic irritability^ because the stimulus acts at an early stage of ontogeny^ and thus at the outset profoundly deflects the course of behavior of the whole organism.

It seems rather superfluous to dwell, in this place, on the well-established conception of the relation between the stimulus and the protoplasmic reaction. If I touch briefly on this subject, as I venture to do in the following, it is not with the view of unnecessarily repeating what is already fully treated in standard works on the subject, but to illustrate more fully exactly what I . mean by identifying the phenomenon of sex differentiation with that of irritability, and to point out the close parallels which exist between the two.^


1 G. Born, ExperimentelU UntersMckuHgen Ubtr die Entstehung der CetcfUtcktiunUnchiidi, Breslauer &rztliche Zeitschrift» 1881.

£. Yung, De rinftuenct de la HtUure des aliments sur la sexualite^ Compt Rend. Acad. Scl, Parii, T. xciii, 1881.



" When by a touch on a trigger the explosion of a pistol is caused, we do not say that the pistol is irritable, but when in an organism a similar release of stored-up energy occurs, we apply the term irritability to the phenomenon, and we call the influence which produced the change a stimulus.*** Or, in the words of Sachs, the stimulus is the name which is given to any alteration in the environment of the irritable organs by means of which stimulation is caused, such as intensity of light, variation of temperature, alteration of electrical conditions, instantaneous shocks, sudden pressure, etc. Considered from another point of view, irritability is fundamentally nothing other than the reactions of the organs or organism towards the outside world, in the way determined by the conditions of their inherited structure. Among such specific phenomena of irritability as heliotropism, geotropism, etc., Sachs also includes such phenomena as gall-formation, which is the abnormal reaction of the vegetable protoplasm towards the abnormal stimulus caused by the insect. He also includes in this category the phenomena that follow the fecundation of the ovum, the ovum being an organism which, under the stimulus from without of the fertilizing substance reacts in so astonishing a manner that new processes of configuration and growth arise from it. The association of these two phenomena in the same category, viz. gall-formation, and the development of the embryo following fecundation of the ovum, is extremely suggestive. Darwin^ has already remarked that every species of gall formed by different insects possesses a specific anatomical structure and textural form "as if the gall were an organism sui generis, The comparison between the phenomena of gall-formation and development of the embryo after fecundation of the ovum, becomes still more suggestive when we remember that entirely different kinds of galls are produced on the same plant by different insects, just as different organisms are produced from the ova of the same animal when the ova are fertilized by sperms of different parentage, as is illustrated in the difference observable between a normal offspring of the same species and a hybrid.


I take the following accounts on irritability mostly from Sachs, Lectures on the Physiology of Plants ; and also from Vines, Physiology of Plants.

2 Francis Darvvin, On Growth-curvatures in Plants, Nature, Vol. 44, 189 1. ^Darwin, Animals and Plants under Domestication , Vol. II.



A conspicuous feature of the phenomena of irritability, to follow Professor Sachs again, is that they correspond with the stimulus neither qualitatively nor quantitatively, and it is in this very fact that the essential distinction between the phenomena of irritability and simple mechanical and physical and chemical action lies. The explanation of this remarkable circumstance lies in the irritable structure of the organ itself. The clearest expression of the internal condition of an irritable organ may be obtained by saying that its parts are in a condition of unstable equilibrium. Hence any sudden change in the surrounding conditions may serve to upset the equilibrium and precipitate a change, the final outcome of which is that the protoplasm is bound to follow either one direction or the other. As has been already stated, any deviation in the constitution of the protoplasm that takes place at the beginning of the life-history of the organism must extend through the whole series of its cell derivatives, and hence the effects of the changes in the surroundings, which may be difficult to detect in the early stages, become more and more discernible as the growth and development of the organism proceed. The organisms up to a certain stage of their existence are neutral as regards sex, as the result of experiments leads us to infer. At this stage of sexual neutrality, the organism appears to be potentially capable of assuming either the female or the male organization. WJuther it becomes the male or the female is entirely due to the play of external forces. It is objectionable to call this stage of neutral sexuality a stage of hermaphroditism, as it has been designated by some naturalists, for hermaphroditism implies the existence of two distinct sexual characters, while neutrality implies the existence of a third but distinct stage, in which any character approaching either male or female is presumed to be entirely absent.

The view that the development of two sexes implies the existence of two different conditions of the surroundings, holds true in the development of two sexual cells, even when they are developed in one and the same organism, as in some hermaphroditic mollusca, in which the two sexual cells may arise in one and the same alveolus of the germ-gland. The male cell leads a free and a more or less migratory existence from a very early stage of its development, while the female cell is sessile and non-migratory up to the last stage of its ovarian existence. The ovum lies close to the wall of the alveolus and is surrounded with the follicular cells, while the spermcell drops into the lumen of the alveolus and there completes its metamorphosis. This difference of conditions, in which the male and female sexual cells respectively develop in the same germ-gland, has been already pointed out by Platner^ in Arioftt and I have witnessed the same fact in a number of other organisms.

There is still another important feature in which the phenomena of sex-differentiation approximate to those of irritability. The most vital peculiarity of irritable organs, as Sachs says, lies less in the fact that their parts can be set in motion in virtue of the unstable equilibrium than in the fact that they subsequently again resume their irritable condition — their unstable equilibrium.

Exactly the same phenomenon takes place in connection with sexual differentiation. It is important to bear in mind at the outset certain superficial distinctions that exist between the phenomena of irritability as exhibited in the growing irritable organism and in the mature irritable organ of the adult organism. While the same irritable state of protoplasm returns again and again in an organ after proper restitution of its material, the case is somewhat different in an irritable organism during its growing period, for the simple reason that a greater part of the material which constitutes such an organism has been made irreversible by its growth. As a consequence, the whole mass of the growing organism does not reassume the irritable state in the way that an irritable organ does. But the return of the whole organism to a highly irritable state is attained in quite another way ; namely, by the formation of a unicellular embryo, such as the fertilized ovum in the sexual, and the parthenogenetic ovum in the non-sexual organism.

To return to the consideration of irritability in the matured organ and in the developing organism, we may observe that all of the material which the organism inherits from the par


1 Platner, Zur Bildung der Geschlechtsprodukte bei den Pulmonaten^ Arch. /. Mikr. Anat., Bd. xxvi, i8S6.


exits is not entirely consumed for the building up of the individual animal. A small portion of it goes to the formation of the germ-cell, which later develops into the sperm-cell or the eggcell, as the case may be. Thus the parts of an individual organism become divided into two fundamentally different structures which have been called by Weismann the soma and the

'germ Galton ^ designated these two parts of the organism as the ** faUnt ** a.nd the latent^' part respectively; Jager,^ as the ontogenetic part and the " phylogenetic part" ; and Rauber,® as the " personal part** and the " germinal part,"

There are several other eminent naturalists who have given expression to a similar view on this subject, but it is entirely unnecessary to enter into any historical review of the question at present. The point which is most important to us is the bearing of such a view of animal organization upon the question we have been considering. If the phenomena of sex-differentiation of the organism were to be identified with that of the irritability of an organ which regains its original irritable state after a short interval of restitution, it is evident that the period covered by the life-history of the individual organism of both sexes must be considered as one long continuous series of the reactions of the protbplasm to the surroundings. The return of the whole organism to its original irritable stage, as has already been stated, is accomplished by the formation of the unicellular embryo or by the union of two sexual cells which were reserved in the " germinal part *' of the male and female organism. The period, then, covered by the manifestation of irritable phenomena in a matured organ is comparable to the whole life-history of the growing organism ; and the recurrence of the irritable condition in the organ corresponds to the production of the unicellular embryo, which is ready to repeat in turn a series of developmental phenomena similar to those which its parents had already undergone before it. There is really no fundamental difference between the irritability of the growing organism and that of the organ.

1 Gallon, On Blood Relationship, Proc. Roy. See., XX, 1872.

Jfiger, Physiologischt Briefe Uher Vererbungt reprinted in hit Lehrbuch der allgem. Zoologie, II, 1878.

Rauber, Penonaliktil und Germinalthtil dts Individuums^ Zool. Anx. IX. In tbb paper Raaber gives references to hit earlier writings on the subject.



The point which requires our special consideration is that condition of the surroundings which determines the direction along which the non-sexual embryo develops. Maupas' experiments have shown conclusively that the variation of temperature exercises a controlling influence upon the type of the development of the non-sexual organism ; while the researches of Born and Yung tend to show that the condition of nutrition has a similar controlling influence. It is probable that several other

> agencies may be able to bring about the same results in the

differentiation of sex as that produced by variation in nutrition and temperature. For it seems probable, from what has been

, said, that the influence of these two factors cannot be considered

in any other light than that of a stimulus, and the forces which

, act as such a stimulus may not be restricted to the two already

mentioned. It is not easy to ascertain, however, the exact potentiality of constitution whereby one and the same organism which develops into a female under certain circumstances, is at the same time capable of developing into a male organism when placed in different surroundings. This is, nevertheless,

! a fact, and it does not seem unreasonable, therefore, to con sider that that structure or quality which appears in the male organism as distinctly masculine, becomes in the organism of opposite sex the very attribute of what we consider as distinctively feminine. According to this view, then, the two different qualities which characterize the two organisms of opposite sexes may be considered simply as two different phases of one and the same substance, which are brought about under the influence of different surroundings.

Before concluding this paper there are a few points which call for special remark : —

(i) It is obvious, according to the present view, that because two masses of the same kind of protoplasm react in two different ways towards two different stimuli, each develops respectively into a male and a female organism, and because they develop into two different organisms, each assumes the particular characteristics peculiar to each sex. This constitutional peculiarity of two sexes extends down to the sexual cells. The sexual differentiation of the organism does not exist, prop i erly speaking, for the purpose of bringing together the two germ-cells, as is frequently assumed by some naturalists, but the union of two sexual cells is itself the inevitable consequence of the sexual differentiation of the organism at the outset. Thus, instead of the necessity of the union of the germ-cells being the cause of the sexual differentiation of the organism, the sexual differentiation of the organism is the cause of the union of the germ-cells.

(2) The present view differs, moreover, from that in which the differences of sex are considered due to those differences existing between the anastate and katastate of the protoplasm. Instead of recognizing predominant katabolism as the male characteristic and predominant anabolism as the female characteristic, maleness and femaleness are considered to be due to two different kinds of katabolism or irritability of the protoplasm. For irritability of protoplasm is nothing more than the internal explosion of its higher complex substance into simpler and more stable substances, and this process of explosive change is what we understand as destructive metabolism or katabolism. According to the present view, it is the nature of the direction along which the katabolic changes of the protoplasm take place, and not the difference exemplified in the alternating phases of the protoplasmic changes, as anabolism and katabolism, that lies at the bottom of the phenomena of sex-differentiation.

(3) The remarkable phenomenon of the "action at a distance" between the two sexual cells observed by several naturalists, which HaeckeP has recently ascribed to the existence of what he calls " erotischer Chcmotropismus** must be considered as the repetition of the same phenomenon of irritability. In this case, it may be considered that each sexual cell acts as a stimulus to the other, owing to the difference of constitution which they temporarily assume. By the time the close approximation of their essential sexual substance is accomplished, the difference between the sperm-nucleus and the egg-nucleus completely disappears, and one morphological element — the .segmentation nucleus — which cannot be called cither male or female is the result. Maupas' conclusion^ that La f^condation, en dcmi^re analyse, est un pMnombne distinct et indipcndent de la sexualit^t* is highly instructive in this connection, if we define fecundation as a more or less complete approximation of two pronuclei^ just so soon as they can be considered a single morphological element in the ovum.

^ Hseckel, Anthropo^enie^ 4th edition, 1891, I^eipzig.

' Maupai, // rejeunissemetU karyogamiqui chez Us Ci/ies, Arch, de zuol. exp. et gen. T. VII, 1889, p. 479.


The facts which seemed to support this view I have already presented elsewhere.^ I have since determined, in the newt {Diemyctylus viridescens, Raf.), through the kindness of my friend, Dr. Edwin O. Jordan, that the two sexual cells which react differently in an unmistakable manner, to the microchemical test during the whole stage of their maturation, and during the early stages of fecundation, become more and more alike toward the completion of the latter process, and at the time when the two pronuclei come closely into contact, the micro-chemical reactions of the "male" and the "female" pronuclei become identical. Similar results were obtained by Lukjanow, as has already been mentioned, in the Ascaris of the dog. Lukjanow killed the ovum with corrosive sublimate, and applied the differential method of staining to the pronuclei. Lukjanow's staining substance consisted of haematoxylin, safranin, and aurantia. The micro-chemical reactions of the two pronuclei, according to this method, are "almost completely alike," although there exist some slight differences as in the number of vacuoles in the nucleolus and in other minor points. My study on the same subject leads essentially to the same result as that of Lukjanow, although pursued with different methods and on a different animal. The difference which exists between the two pronuclei is simply the difference which distinguishes one individual from another of the same species, as was pointed out by Weismann.

(4) I have already mentioned elsewhere that the sperm-cell undergoes a much more varied series of changes of form and of color-reaction during the period of its maturation than does the ovum in the corresponding period. Thus the law of the greater complexity of the male type of development as compared with that of the female type in " secondary sexual characters," as recognized by Hunter and Darwin, extends even to the essential parts of the "primary sexual character." In short, the phenomena of sex-diflFerentiation extend through the whole organization, including both the "germinal " and the " personal " parts of the organism. The organism is either a male or a female, not by the difference of "primary sexual characters" alone, but by the difference which saturates the whole of its entire structure. Such a difference is, however, neither absolute nor permanent. It is a temporary differentiation of protoplasm into one of two different directions, and sooner or later comes back to the original neutral or non-sexual state from which it started, thus manifesting the phenomenon characteristic of all protoplasmic irritability.

Clark Uniyersffy, Worcester, Mass., May, 1892.


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