Evolution and Adaptation

by Thomas Hunt Morgan

The Determination of Sex

A large number of views have been advanced as to what determines whether an egg will give rise to a male or to a female individual. The central question is whether the fertilized egg has its sex already determined, or whether it is indifferent; and if the latter, what external factor or factors determine the sex of the embryo. Let us first examine the view that some external factor determines the sex of the individual, and then the evidence pointing in the opposite direction. Among the different causes suggested as determining the sex of the embryo, that of the condition of the egg itself at the time of fertilization has been imagined to be an important factor in the result. Another similar view holds that the condition of the spermatozoon plays the same rôle. For instance, it has been suggested that if the egg is fertilized soon after it leaves the ovary, it produces a female, but if the fertilization is delayed, a male is produced. It has also been suggested that the relative age of the male and the female parents produces an effect in determining the sex of the young. There is no satisfactory evidence, however, showing that this is really the case.

Another view suggested is that the sex is determined by the more vigorous parent; but again there is no proof that this is the case, and it would be a difficult point to establish, since as Geddes and Thompson point out, what is meant by greater vigor is capable of many interpretations. Somewhat similar is the idea that if the conditions are favorable, the embryo develops further, as it were, and becomes a male; but there are several facts indicating that this view is untenable.

Düsing maintains that several of these factors may play a part in determining the sex of the embryo, and if this be true, the problem becomes a very complex one. He also suggests that there are self-regulative influences of such a kind that, when one sex becomes less numerous, the conditions imposed in consequence on the other sex are such as to bring the number back to the normal condition; but this idea is far from being established. The fact that in some species there are generally more individuals of one sex than of the other shows that this balance is not equally adjusted in such forms.

Of far greater value than these speculations as to the origin of sex are the experiments that appear to show that nutrition is an important factor in determining sex. Some of the earlier experiments in this direction are those of Born and of Yung. By feeding one set of tadpoles with beef, Yung found the percentage of females that developed to be greatly increased, and a similar increase was observed when the tadpoles were fed on the flesh of fish. An even greater effect was produced by using the flesh of frogs, the percentage rising to 92 females in every hundred. These results have been given a different interpretation by Pflüger and by others, and, as will be pointed out later, there is a possible source of error that may invalidate them.

Somewhat similar results have been obtained by Nussbaum for one of the rotifers. He found that if the rotifer is abundantly fed in early life, it produces female eggs, that is, larger eggs that become females; while if sparingly fed, it produces only small eggs, from which males develop. It has been claimed also in mammals, and even in man, that sex is to some extent determined by the nourishment of the individual.

Some experiments made by Mrs. Treat with caterpillars seemed to show that if the caterpillars were well nourished more female moths were produced, and if starved before pupation more males emerged. But Riley has pointed out that since the larger female caterpillars require more food they will starve sooner than the males, and, in consequence, it may appear that proportionately more male butterflies are born when the caterpillars are subjected to a starvation diet. This point of view is important in putting us on our guard against hastily supposing that food may directly determine sex. Unless the entire number of individuals present at the beginning of the experiment is taken into account, the results may be misleading, because the conditions may be more fatal to one sex than to the other.

In some of the hymenopterous insects, the bees for example, it has been discovered that the sex of the embryo is determined by the entrance, or lack of entrance, of the spermatozoon. In the honey-bee all the fertilized eggs produce females and the unfertilized eggs males. The same relation is probably true also in the case of ants and of wasps. In the saw-flies, the conditions are very remarkable. Sharp gives the following account of some of these forms:[^[35]]—“It is a rule in this family that males are very much less numerous than females, and there are some species in which no males have been discovered. This would not be of itself evidence of the occurrence of parthenogenesis, but this has been placed beyond doubt by taking females bred in confinement, obtaining unfertilized eggs from them, and rearing the larvæ produced from the eggs. This has been done by numerous observers with curious results. In many cases the parthenogenetic progeny, or a portion of it, dies without attaining full maturity. This may or may not be due to constitutional weakness, arising from the parthenogenetic state. Cameron, who has made extensive observations on this subject, thinks that the parthenogenesis does involve constitutional weakness, fewer of the parthenogenetic young reaching maturity. This, he suggests, may be compensated for—when the parthenogenetic progeny is all of the female sex—by the fact that all those that grow up are producers of eggs. In many cases the parthenogenetic young of Tenthredinidæ are of the male sex, and sometimes the abnormal progeny is of both sexes. In the case of one species—the common currant-fly, Nematus ribesii—the parthenogenetic progeny is nearly, but not quite always, entirely of the male sex; this has been ascertained again and again, and it is impossible to suggest in these cases any advantage to the species to compensate for constitutional parthenogenetic weakness. On the whole, it appears most probable that the parthenogenesis, and the special sex produced by it, whether male or female, are due to physiological conditions of which we know little, and that the species continues in spite of the parthenogenesis rather than profits by it. It is worthy of remark that one of the species in which parthenogenesis with the production of males occurs—Nematus ribesii—is perhaps the most abundant of saw-flies.”

[35]. “The Cambridge Natural History,” Vol. V, “Insects,” by David Sharp.

It has been pointed out that in a number of species of animals and plants only parthenogenetic females are present at certain times. In a sense this means a preponderance of one sex, but since the eggs are adapted only to this kind of development, it may be claimed that the conditions in such cases are somewhat different from those in which eggs that would be normally fertilized may develop in the absence of fertilization. Nevertheless, it is generally supposed that the actual state of affairs is about the same. It is usually assumed, and no doubt with much probability, that these parthenogenetic forms have evolved from a group which originally had both male and female forms. One of the most striking facts in this connection is that in the groups to which these parthenogenetic species belong there are, as a rule, other species with occasional parthenogenesis, and in some of these the males are also fewer in number than the females.

In the aphids, the parthenogenetic eggs give rise during the summer to parthenogenetic females, but in the autumn the parthenogenetic eggs give rise without fertilization both to males and to females. It appears, therefore, that we can form no general rule as to a relation between fertilization and the determination of sex. While in certain cases, as in the bees, there appears to be a direct connection between these two, in other cases, as in that of the aphids just mentioned, there is no such relation apparent.

Geddes and Thompson have advocated a view in regard to sex which at best can only serve as a sort of analogy under which the two forms of sex may be considered, rather than as a legitimate explanation of the phenomenon of sex. They rest their view on the idea that living material is continually breaking down and building up. An animal in which there is an excess of the breaking-down process is a male, and one that is more constructive is a female. Furthermore, whichever process is in the excess during development determines the sex of the individual. Thus, if conditions are very favorable, there will be more females produced; but if, on the other hand, there is an excess of the breaking-down process, males are produced. So far, the process is conceived as a purely physiological one, but to this the authors then apply the selection hypothesis, which, they suppose, acts as a sort of break or regulation of the physiological processes, or in other words as a directive agent. They state: “Yet the sexual dimorphism, in the main, and in detail, has an adaptive significance, also securing the advantages of cross-fertilization and the like, and is, therefore, to some extent the result of the continual action of natural selection, though this may, of course, check variation in one form as well as favor it in another.” Disregarding this last addition, with which Geddes and Thompson think it necessary to burden their theory, let us return to the physiological side of the hypothesis. Their idea appears to me a sort of symbolism rather than a scientific attempt to explain sex. If their view had a real value, it ought to be possible to determine the sex of the developing organism with precision by regulating the conditions of its growth, and yet we cannot do this, nor do the authors make any claim of being able to do so. The hypothesis lacks the only support that can give it scientific standing, the proof of experiment.

There have been made, from time to time, a number of attempts to show that the sex of the embryo is predetermined in the egg, and is not determined later by external circumstances. In recent years this view has come more to the front, despite the apparent experimental evidence which seemed in one or two cases to point to the opposite view. One of the most complete analyses of the question is that of Cuénot, who has attempted to show that the sex of the embryo is determined in the egg, before or at the time of fertilization. He has also examined critically the evidence that appeared to show that external conditions, acting on the embryo, may determine the sex, and has pointed out some possible sources of error that had been overlooked. The best-known case is that of the tadpole of the frog, but Cuénot shows not only that there are chances of error in this experiment as carried out, but also, by his own experiments and observations, that the facts themselves are not above suspicion. He points out that at the age at which some of the tadpoles were when the examination was made, it was not always possible to tell definitely the sex of the individual, and least of all by means of the size alone of the reproductive organs, as was supposed, in one case at least, to be sufficient. In his own experiments he did not find an excess of one sex over the other as a result of feeding.

Cuénot points out that Brocadello found that the larger eggs laid by the silkworm give rise to from 88 to 95 per cent of females, and the small eggs to from 88 to 92 per cent of males. Joseph has confirmed this for Ocneria dispar, and Cuénot himself also reached this conclusion. Korschelt found that the large eggs of Dinophilus produced females and the small ones males. Cuénot experimented with three species of flies, and found that when the maggots were well nourished the number of the individuals of the two sexes was about equal, and when poorly nourished there were a few more females in two cases, and in another about the same number of males and females.

It has been claimed that the condition of nourishment of the mother may determine the number of eggs of a particular sex, but Cuénot found, in three species of flies which he raised, that there was a slight response in the opposite direction. He concludes that the condition of the mother is not a factor in the determination of sex.

The first egg of the two laid in each set by the pigeon is said, as a rule, to produce a male, and the second a female. Both Flourens and Cuénot found this to be the case in the few instances that they examined, but Cuénot has shown that this does not always happen. Even when this occurs, it has not been determined whether the result depends on something in the egg itself, that causes a male egg to be set free first, or on some external condition that determines that the first egg shall become a male. It has been claimed that the age of the spermatozoon might in this and in other cases determine the result; but Gerbe has shown that if the domestic hen is isolated for fifteen days after union with the male, she will continue to produce fertile eggs from which both sexes are produced, without showing any relation between the time the eggs are laid and the particular sex that develops.

Cuénot does not discuss whether sex is determined by the nucleus or by the protoplasm, but if, as he thinks probable, the size of the egg is a determining factor, it would appear that the protoplasm must be the chief agent. Even if this were the case it would still be possible that the size of the egg itself might be connected with some action on the part of the nucleus. If, as seems probable, identical twins come from halves of the same egg, then, since they are of the same sex, the absolute amount of protoplasm cannot be a factor in sex determination.

Fig. 6.—Diagram showing the maturation of the egg.

As a basis for the discussion that follows, certain processes that take place during the maturation divisions of the egg and of the spermatozoon must be briefly noticed. After the egg leaves the ovary it extrudes a minute body called the first polar body (Fig. [6 B, C, D]). This process of extrusion is really a cell division accompanied by the regular mitotic division of the nucleus; but since one of the products of the division, the polar body, is extremely small, the meaning of the process was not at first understood. The half of the nucleus, that remains in the egg, divides again, and one of its halves is thrown out into a second polar body (Fig. [6 E, F, G])). Meanwhile, the first polar body has divided into two equal parts, so that we find now three polar bodies and the egg (Fig. [6 G])). A strictly analogous process takes place in the formation of the spermatozoa (Fig. [7 B-F]). The mother-cell of the spermatozoon divides into two parts, which are equal in this case (Fig. [7 B-D]). Each of these then divides again (Fig. [7 E, F]), producing four cells that are comparable to the three polar bodies and the mature egg. Each of the four becomes a functional spermatozoon (Fig. [7 G, H]). Thus while in the maturation of the egg only the egg itself is capable of development, in the case of the male cells all four products of the two maturation divisions are functional.

Fig. 7.—Diagram showing the maturation of the spermatozoon.

Now, in certain cases of parthenogenesis, it has been found that one of the polar bodies may not be given off, but, remaining in the egg, its nucleus reunites with the egg nucleus, and thus takes the place of the spermatozoon, which does exactly the same thing when it fertilizes the egg, i.e. the nucleus of the spermatozoon unites with the nucleus of the egg. This fact in regard to the action of the polar body in fertilization is not as surprising as appears at first sight, for if each of the polar bodies is equivalent to a spermatozoon, the fertilization of the egg by one of its own polar bodies conforms to theory.

There is a considerable body of evidence showing that in many eggs at one of the two maturation divisions the chromatin rods derived from the nucleus are divided crosswise (Fig. [6 B, C]). The same thing occurs at one of the two divisions in the formation of the spermatozoon (Fig. [7 B, C]). At the other division to form the other polar body (or the other sperm-cell) the chromatin rods appear to be split lengthwise, as in ordinary cell division (Fig. [6 E, F, G]). In recent years the cross-division of the chromatin rods has attracted a great deal of notice, and Weismann in particular drew attention to the possible importance of this kind of division.

There is another fact that gives this division especial significance. It has been discovered that the number of chromosomes that appears in each dividing cell of the organism is a constant number, but it has also been discovered that the egg, before extruding its polar bodies, and the mother-cell of the spermatozoon (Figs. [6], [7 B]), contain exactly half of the number of chromosomes that are characteristic of the body-cells of the same animal (Figs. [6], [7 A]). Now there is good evidence to show that the reduction in number is due to the chromosomes uniting sometimes end to end in pairs, as shown in Figures A and B. Furthermore, it has been suggested that at one of the maturation divisions, when the chromosomes divide crosswise, the united chromosomes are separated (Figs. [6], [7 B, C]), so that one remains in the egg and the other goes out into the polar body. The same thing is supposed to occur at one of the maturation divisions of the sperm mother-cell. A further consideration of capital importance in this connection has been advocated by Montgomery and by Sutton, namely, that, when the chromosomes unite in pairs, a chromosome from one parent unites with one from the other parent. Consequently at one of the two reduction divisions maternal and paternal chromosomes may separate again, some to go to one cell, some to the other.

When the spermatozoon enters the egg it brings into the egg as many new chromosomes as the egg itself possesses at this time, and the two nuclei, uniting into a single one, furnish the total number of chromosomes characteristic of the animal that develops from the egg. At first the chromosomes that are brought in by the spermatozoon lie at one side of the fused nucleus, and those from the egg itself at the other side. This arrangement appears, however, in some cases at least, to be lost later. At every division of the nucleus, each chromosome divides and sends a half to each of the daughter-nuclei. Thus every cell in the body contains as many paternal as maternal chromosomes. This statement also applies to the first cells that go into the reproductive organs, some of which become the mother-cells of the germ-cells. Later, however, in the history of the germ-cells,—just before the maturation divisions,—these chromosomes are supposed to unite in pairs, end to end, as explained above, to give the reduced number. Later there follows the separation of these paired chromosomes at one of the two maturation divisions. If at this time all the paternal chromosomes should pass to one pole, and all the maternal to the other, the germ-cell ceases to be mixed, and becomes purely paternal or maternal. If this ever occurs, the problem of heredity may become simplified, and even the question of sex may be indirectly involved; but it has not been established that, when the reduced number of chromosomes is formed, there is a strict union between the paternal and maternal chromosomes, and if not, the subsequent separation is probably not along these lines. If, however, the chromosomes contain different qualities, as Boveri believes, there may be two kinds of eggs, and two kinds of spermatozoa in regard to each particular character. It is this last assumption only that is made in Mendel’s theory of the purity of the germ-cells.

Several attempts have been made at different times to connect the facts in regard to the extrusion of the polar bodies with those involved in the determination of sex. Minot suggested, in 1877, that the egg ejects by means of the polar bodies its male elements, which are again received in the fertilization of the egg by the spermatozoon. The same idea has also been expressed by others. It has been objected to this view that one polar body ought to suffice, and that no similar throwing out of part of its substance is found in the process of formation of the spermatozoon, which should, on the hypothesis, throw out its female elements. It would seem, on first thought, that this view might find support in the idea expressed above, namely, that in one of the polar bodies half of the chromosomes pass out, so that there is conceivably a separation of the maternal from the paternal. If this were the case also in the spermatozoa, then two of each four would be paternal and two maternal. This is, however, a very different thing from supposing them to be male and female, for it by no means follows, because the chromosomes correspond to those of the father or of the mother in the sum of their characters, that they are, therefore, also male or female in regard to sex.

It has been pointed out already, that in most parthenogenetic eggs only one polar body is extruded. There are, it is true, a few apparent exceptions to this rule, but in most cases it is certain that only one is extruded. In several cases the beginning of the formation of the second maturation division of the nucleus takes place, but after the chromosomes have divided they come together again in the nucleus. If each polar body be interpreted as equivalent to a spermatozoon, then this result is rather a process of self-fertilization than true parthenogenesis. It is, nevertheless, true that in some cases development seems to go on after both polar bodies have been extruded. Moreover, it has been found possible to cause the eggs of the sea-urchin to begin their development by artificial solutions after they have extruded both polar bodies. A single spermatozoon may also produce an embryo if it enters a piece of egg-protoplasm without a nucleus. The last instance is a case of male parthenogenesis, and if the theory of the equivalency of spermatozoon and egg be correct, this is what should occur.

Quite recently, Cuénot, Beard, Castle, and Lenhossek have contended that the differentiation of sex is the outcome of internal factors. They think that the view that sex is determined by external agents is fundamentally erroneous. The fallacies that have given rise to this conception, Castle points out, are, first, that in animals that reproduce sometimes by parthenogenesis and sometimes by fertilized eggs, the former process is favored by good nutrition and the latter by poor nutrition. This only means, in reality, Castle thinks, that parthenogenetic reproduction is favored by external conditions, and this kind of reproduction, he thinks, is a thing sui generis, and not to be compared to the formation of more females in the sexual forms of reproduction. There is no proof, however, that this is anything more than a superficial distinction, and it ignores the fact that in ordinary cases the females sometimes lay parthenogenetic eggs which differ, as far as we can see, from eggs that are destined to be fertilized in no important respect. More significant, it seems to me, is the fact that only parthenogenetic females develop the following spring from the fertilized eggs of the last generation of the autumn series, whose origin is described to be due to lack of food. We find, in the case of aphids, that unfertilized parthenogenetic eggs and also fertilized eggs give rise to females only, while a change in the amount of food causes the parthenogenetic eggs to give rise both to males and to females. This point is not, I think, fully met by Castle, for even if the change in food does not, as he claims, cause only one sex to appear, yet lack of food does seem to account for the appearance of the males at least.

The other fallacy, mentioned by Cuénot, is that the excess of males that has been observed when the food supply is limited is due to the early death of a larger percentage of females, which require more food, but this still fails to account for the excess of females when more food is given, provided Yung’s experiments on tadpoles are correct. It may be, however, in the light of Pflüger’s results, that there has been some mistake in the experiments themselves.

We may now proceed to examine Castle’s argument, attempting to show in what way sex is predetermined in the embryo. His hypothesis rests on the three following premises: “(1) the idea of Darwin, that in animals and plants of either sex the characters of the opposite sex are latent; (2) the idea of Mendel, that in the formation of the gametes [germ-cells] of hybrids a segregation of the parental characters takes place, and when in fertilization different segregated characters meet, one will dominate, the other become latent or recessive; (3) the idea of Weismann, that in the maturation of egg and spermatozoon a segregation is attended by a visible reduction in the number of chromosomes in the germinal nuclei.”

Expressed in a somewhat more general way, Castle suggests that each egg and each spermatozoon is either a male or a female germ-cell (and not a mixture of the two), and when a female egg is fertilized by a male spermatozoon, or vice versa, the individual is a sexual hybrid with one sex dominating and the other latent. The assumption that there are two kinds of eggs, male and female, and two kinds of spermatozoa, male and female, is not supported by any direct or experimental evidence. Moreover, in order to carry out the hypothesis, it is necessary to make the further assumption that a female egg can only be fertilized by a male spermatozoon, and a male egg by a female spermatozoon. While such a view is contrary to all our previous ideas, yet it must be admitted that there are no facts which disprove directly that such a selection on the part of the germ-cells takes place. If these two suppositions be granted, then Castle’s hypothesis is as follows:—

In order that half of the individuals shall become males and half females it is necessary to assume that in some individuals the male element dominates and in others the female, and since each fertilized egg contains both male and female elements, it is necessary to assume that either the egg or the spermatozoon contains the dominating element.

Castle supposes that in hermaphroditic organisms the two characters “exist in the balanced relationship in which they were received from the parents,” but, as has just been stated, in unisexual forms one or the other sex dominates, except of course in those rare cases, as in the bees and ants, where half of the body may bear the characters of one sex, and the other half that of the other sex.

In parthenogenetic species the female character is supposed to be uniformly stronger, so that it dominates in every contest, “for the fertilized egg in such species develops invariably into a female.” Under certain circumstances, as Castle points out, the parthenogenetic female produces both males and females, and this is also true in the occasional development of the unfertilized egg of the silkworm moth, and of the gypsy moth, in which both male and female individuals are produced by parthenogenesis. These facts show that even in unfertilized eggs both sexes are potentially present; but this might be interpreted to mean that some eggs are male and some female, rather than that each egg has the possibility of both kinds of development. If, however, one polar body is retained in these parthenogenetic eggs, then ex hypothese each egg would contain the potentialities of both sexes (if the polar body were of the opposite sex character). It seems necessary to make this assumption because in some parthenogenetic forms males and females may be produced later by each individual, as in the aphids, and this could not occur if we assume that some parthenogenetic eggs are purely male and some female.

Castle assumes, in fact, that in animals like daphnids and rotifers one polar body only is extruded, and the other (the second) is retained in the egg, and hence the potentiality of producing males is present. In the honey-bee, on the contrary, Castle assumes that both polar bodies are extruded in the unfertilized egg (and there are some observations that support this idea), and since only males are produced from these, he believes it is the female element that has been sent out into the second polar body. This hypothesis is necessary, because Castle assumes that when both elements are present in the bee’s eggs, the female element dominates. “Hence, if the egg which has formed two polar cells develops without fertilization, it must develop into a male. But if such an egg is fertilized, it invariably forms a parthenogenetic female ♀ (♂), that is, an individual in which the male character is recessive. Accordingly the functional spermatozoon must in such cases invariably bear the female character, and this is invariably dominant over the male character when the two meet in fertilization.”

If it should prove generally true that the size of the egg is one of the factors determining the sex, we have still the further question to consider as to whether some eggs are bigger because they are already female, or whether all eggs that go beyond a certain size are females, and all those that fail to reach this are males. If this is the case, an animal might produce more females if the external conditions were favorable to the growth of the eggs, and if in some cases these large eggs were capable of developing, parthenogenetic races might become established. Should, however, the conditions for nutrition become less favorable, some of the eggs might fall below the former size and produce males. It is not apparent, however, why all the fertilized autumn eggs of the aphids should give rise to females, for although these eggs are known to be larger than the summer eggs, yet they are produced under unfavorable conditions.

The preceding discussion will show how far we still are from knowing what factors determine sex. Castle’s argument well illustrates how many assumptions must be made in order to make possible the view that sex is a predetermined quality of each germ-cell. Even if these assumptions were admissible, we still return to the old idea that the fertilized egg has both possibilities, and something determines which shall dominate. Until we have ascertained definitely by experimental work whether the sex in some forms can be determined by external conditions, it is almost worthless to speculate further. Whatever decision is reached, the conclusion will have an immediate bearing on the question to be next discussed. Meanwhile, we can at least examine some of the theories that have been advanced as to what advantage, if any, has been gained by having the individuals of many classes divided into two kinds, male and female.