The genetic and the operative evidence relating to secondary sexual characters

by Thomas Hunt Morgan

D. Evidence from Crustaceans.

In the Crustacea the secondary sexual characters are not marked, except in a few cases. In the amphipods, Holmes has shown direct contact plays the chief rôle in mating, and in the crayfish it has been shown by Dearborn, Andrews, and Pearse that sex recognition is largely tactile. Chidester also has shown this in crayfish. Even in crabs, and especially those living on land which have well-developed eyes and good vision, secondary sexual differences are as a rule slight and the mating instincts simple. On the other hand, the enormous chela of the male of the fiddler is supposed to be a secondary sexual difference (mainly because no other use for it has been found). Pearse suggests that the waving of this claw by the male is used as a sex signal, although he is disinclined to accept Alcock’s view that it has become “conspicuous and beautiful in order to attract the female.”

The most remarkable case known of a change in the secondary sexual characters of one sex into those of the other was discovered by Giard in 1886. As a result of infection by parasitic crustacea (e. g., Sacculina), the male crab develops the secondary sexual characters of the female. It has been generally supposed, following Giard, that this result is due to the destruction of the testes of the male by the roots of the parasite that invades the spaces between the organs of the host, and, in the case of the testis, ultimately brings about its partial or complete destruction. Not unnaturally the results here were supposed to be parallel to those of castration in vertebrates, and received in fact the name of “parasitic castration.” More recently Geoffrey Smith has studied this phenomenon in the crab Inachus, infected by the parasite Sacculina, and has reached the conclusion that the change is not due to injury or to destruction of the testes, but to a change in the metabolism of the crab brought about by the parasite.

Taking Geoffrey Smith’s case of Inachus-Sacculina as typical, the changes brought about are as follows: The parasites attach themselves to the young crabs before the external secondary sexual differences have appeared. In the females, the effect is to cause them to develop prematurely the distinctively female characters. In the male, on the other hand, the narrow abdomen of the male changes after a molt into the broad abdomen of the female, which also develops ovigerous appendages on its ventral surface like those of the female in every detail. The larger claw of the male changes into that of the female, which is different in form as well as in size. Some years ago I ventured to raise the question as to whether these effects on the male might not be interpreted as retention of the juvenile characters rather than development of the female characters in the male. This might appear more especially the case in the somewhat more juvenile shape of the anterior abdominal appendages and possibly also in the shape of the broader abdomen; but Smith has later shown that the results can not be interpreted as juvenile, for when the changed organs are examined in detail they are found to differ from the same organs in the juvenile condition, and to be identical with those of the adult female. I think, therefore, that we must accept this interpretation of Giard and of Smith as correct. But Smith goes further and believes that the effects may be carried so far that eggs develop in the old testes; in other words, that the testis changes to an ovary. It seems to me that the evidence to support this last point should be much stronger than that advanced by Smith before we can accept this interpretation, for we lack the essential control for this evidence. In only a single case were eggs found—in the testis of a male that had been infected, but from which the parasite had fallen off, and which was presumably recovering from the effects of its presence. Now, it is known that in the testes of some male animals a few eggs may occasionally be found where there is no suspicion that the animal has changed its sex. In some crustacea, in scorpions, and in insects, isolated instances of this kind have been found. Abnormal division of a spermatogonial cell, of such a kind that both sex chromosomes (in the case of insects at least) got into the same cell might be expected to cause such a cell to become, even in the male, an egg-cell rather than a sperm-cell. The degenerative changes of the testes in the hermit crab caused by the parasite might be imagined to favor such abnormal division with its consequences. More significant, however, is the fact that the parasite causes the absorption of the ovary when it infects a young female, so that even all its eggs disappear. In other words, the parasite is as injurious to the peculiarly female organ as it is to the testis. Why then, one can not but ask, should an influence that causes such effects on the ovary first change a male into a female so long as it is present and then when the parasite has disappeared leave an influence behind of a kind that causes the ovary to develop—an organ which the parasite destroys when the parasite is present? Is it not more probable that only the secondary sexual organs were changed, without change in sex, the single case of eggs observed being caused in another way? This point can only be settled by direct experimentation either by removal of the testis, by injuring it, or by injection, grafting, or feeding experiments. The extent of the testis and its position make it impossible to remove it by an operation, as I have found after repeated attempts. It seemed easier to destroy it by radium. This I have tried to do, using very powerful tubes, treating the crab (fiddler crabs) for several hours. The crabs had had one claw removed—the enormously large one—and were kept until the next molt, that occurred from a week to six weeks later. In none of the cases was any change produced. The large claw of the male regenerated, of course, not full size after only one molt, but after several nearly full size and always with the peculiarities of the male crab. The abdomen and the appendages were not changed. Whether the significant cells of the testes, if there are such cells apart from the germ-cells, were destroyed, can not be told, for as yet the histological examination of the material has not been made. Until a successful operation has been done, I think we must hesitate to accept Smith’s argument, although based as it is on a series of interesting observations. His speculation is as follows:

“The reason why Sacculina causes the assumption of the adult female state in Inachus is found in the facts: (1) that the roots of Sacculina elaborate a yolk-substance from the blood of Inachus of a similar nature to that which is elaborated in the ovaries of an adult Inachus; (2) that in order to elaborate this yolk-substance the roots take up from the blood of Inachus the female sexual formation substance, which is the necessary material for forming the yolk; (3) that the female sexual formative substance being absorbed by the Sacculina roots is regenerated in excess; (4) that the presence of the female formative substance continually circulating in large quantities in the body-fluids of the infected crabs causes the production of adult female secondary sexual characters, and, when the parasite dies, of yolk-containing eggs.”

In brief, the evidence consists in showing that in the parasite a yolk-substance appears, which Smith says comes from the blood of the crab that produces it under the influence of the parasite. Incidentally, as it were, this is said to be the same yolk-substance (but no sufficient evidence that it is the same is given) that the egg stores up inside itself, and it is assumed that it is a formative substance that causes the cell that gets it (or contains it or secretes it—details are wanting) to become an egg-cell. It is the excess of this substance produced by the male crab, while still a male, under the influence of the parasite, that affects the abdomen and its appendages in such a way that they assume the female condition. There are too many assumptions in the argument, some of which are scarcely of a kind that our knowledge of development, incomplete as it is, can allow us to accept without more direct evidence in their support, to make this view very plausible. Until better evidence is forthcoming, I fail to be convinced by Smith’s interpretation of his facts.

Into Smith’s and Robson’s interesting observations on the blood of crabs, described in Smith’s later paper (part 7, 1911), it is not necessary to enter here, since the evidence taken as a whole offers little further in support of his view than had been already assumed. The argument on page 263 should not, however, pass unchallenged. Smith says:

“It is clear that the old and familiar idea of an internal secretion produced by the gonad being the stimulus for the development of the secondary sexual character could not be applied here, since at the time that the alterations in the secondary sexual characters take place no ovary is present to give rise to the required stimulus. It is suggested, therefore, that in some way the stimulus must reside in the roots of the Sacculina,” etc.

The argument seems to imply that, since the secondary sexual characters of the female can not be produced by an ovary in the infected male, therefore the Sacculina must take the place of the ovary. But why make such a supposition, for if the testes simply keep down the development of the female characters, as Giard supposes, there is no need either for an ovary or for a Sacculina to develop them. One might as well argue that since the cock does not develop the secondary sexual characters of the hen that an ovary is essential for their development—which is true, but not in the sense implied.

Stamati (1888) states that he attempted to remove the testes of adult crayfish and apparently succeeded, but since no effects are expected until after a molt occurs (that may not take place for two years or more), no results were obtained. Injections of the gonads with an acid failed, since the animals died.