CHARA CTERS* nearly sterile. As in other similar combinations the sex glands are reduced ZOOLOGY: E. WITSCHI
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1 ZOOLOGY: E. WITSCHI VOL. 23, STIMULATIVE AND INHIBITIVE INDUCTION IN THE DEVELOPMENT OF PRIMARY AND SECONDARY SEX CHARA CTERS* By EMIL WITSCHI DEPARTMENT OF ZOOLOGY, STATE UNIVERSITY OF IOWA Read before the Academy November 16, 1936 It is a well established fact that in the development of the vertebrate gonad the cortex functions as an inductor of ovarian differentiation and the medulla as an inductor of testicular differentiation. Embryologically, sex is determined on the basis of a competition between these two inductors, each of which stimulates differentiation of one sex and tends to prevent the development of the other. A closer analysis of the inductor activity indicates, furthermore, that the visible morphological differentiations are evoked by special chemical substances which are produced and released by the inductors. This assumption was probably first suggested and supported by F. R. Lillie' in his classical studies on the cattle free-martins. The now equally well established fact that in primates a similar exchange of blood between male and female embryos does not interfere with normal sex development cannot reduce the importance of the free-martin case; though it proves that the mechanism of induction deserves a more detailed investigation. Evidently cortex and medulla produce different inductive substances; it has been proposed to designate them as cortexin and medullarin. In the experiments to be described now, we have investigated the question of whether the stimulative and the inhibitive inductions are due to one or to two (or more) substances. The evidence points to the separate existence of a stimulative and of an inhibitive medullarin. Using the technique of Born2 we made parabiotic pairs of salamanders, and observed the effects of inductive substances which are transmitted from one twin into the other. In the case represented in figure 1 an Ambystoma maculatum female is loosely attached to an A. tigrinum male by a strand of tissue between the right gill arches. The maculatum female proves to be nearly sterile. As in other similar combinations the sex glands are reduced to small vestiges, without ovarial differentiation (compare Fig. 2C). This proves that the blood passing through the narrow connection has carried enough medullarin into the female to suppress cortical development. On the other hand no sign of testicular differentiation is visible in the medulla. Stimulation of testicular differentiation is restricted to the gonad of the tigrinum male while inhibition of ovarial differentiation spreads also into the maculatum female. In another series of twins it was observed that males with hermaphrodite
2 36 ZOOLOGY: E. WITSCHI PROC. N. A. S. FIGURE 1 Pair of parabiotic twins. The large A. tigrinum member is a male, the small A. maculatum co-twin is a female freemartin. They are connected by a narrow strand of tissue between the gill arches. Age 5 months. X1/2. tendencies do not emit the inhibitive medullarin in appreciable amounts (Witschi3), indicating a wider quantitative variability in the inhibitive than in the stimulative medullarin. In a third series two males which differ in developmental speed were united. The fact that the pace of the later and more slowly differentiating twin is not speeded up, proves most directly that stimulative medullarin is not transmitted from one twin into the other (Witschi4). Experimental evidence leads, therefore, to the conclusion that in salamanders the medulla produces two inductive substances. The first one which stimulates testicular differentiation, produces reactions only within the gonad. Like many other substances which induce embryonic differentiations, it seems to diffuse very slowly and only by direct contact through the tissues. The second one, which A B C D FIGURE 2 Sex glands of a female pair (A, B) and a heterosexual pair (C, D) of salamanders (171/2 and 131/2 months old). A, B, normal ovaries; C, vestigial sex glands of the female (free-martin) in parabiosis with a male; D, normal testes. X5.
3 VOL. 23, 1937 ZOOLOGY: E. WITSCHI 37 FIGURE 3 FIGURE 4 FIGURE 5 Urogenital organs of the lumbar and cloacal region of three specimens of A. jeffersonianum, dwarf race of Cedar Falls, Iowa. Age, over one year. X10. C, cloaca; D, collecting ducts; K, lumbar kidney (metanephros); 0, oviduct; R, rectum; U, ureter (metanephric duct); V, vesica; W, wolffian (mesonephric) duct; 1, 2, 3, pelvic, abdominal and labial glands. Figure 3. Sterile female (free-martin, in parabiosis with mature male of A. tigrinum). Figure 4. Male, near maturity. Figure 6. Female type at maturity.
4 38 inhibits ovarial differentiation of the cortex, spreads more easily and is carried by the blood stream, like a typical hormone. The next question which had to be investigated is that of the possible identity of one or both of the medullarins with the sex hormone which in the adult stimulates the development of secondary sex characters. In salamanders the sex hormones appear in distinctly detectable quantities only toward the approach of sexual ma- 7 6 turity. By the method of parabiosis, one can beautifully demonstrate the transmis- Sion of the male sex hormone from one ~~~ ~~twin into the other. In combinations of a x! t %large atg Ambystoma tigrinum male with a,5 1 idwarf Ambystoma jeffersonianum female the latter becomes completely sterilized during the period of larval development, /> _ S S as we have described above. At the age 8 of seven to ten months the tigrinum male w w ;-- ZOOLOGY.-'E. WITSCHI PROC. N. A. S. reaches full sexual maturity. Due to the release of testicular hormone its secondary sex characters acquire the characteristics of the adult male. However, the same course of development is also taken by the sterile female parabiont. Figure 3 shows how, by a strong development of the vas deferens, by the formation of a separate ureter and through exuberant growth of Figures 6-8. Cross-sections cloacal glands (1-3), the urogenital organs through urogenital ducts of sala- of these free-martin salamanders assume manders at the level of the gonads. X55. 0, oviduct; the male (Fig. 4) rather than the female W, wolffian duct. type (Fig. 5). Cross-sections through the Figure 6. Same free-martin ducts at the level of the mesonephric as in figure 3. kidneys prove also that development in Figure 7. A. tigrinum male, the free-martin (Fig. 6) follows the same co-twin to the free-martin (Fig. 6). Figure 8. Same female type as pattern as i the male twn (Fig. 7) rather in figure 5. than the female type (Fig. 8). The wolffian duct enlarges. The cells of its epithelium become high and glandular, and the surrounding connective tissue swells and assumes the spongy type characteristic for the mature male. At the same time the oviduct remains rudimentary. It is included in the distal part of the peritoneal fold surrounding the wolffian duct and is not separately visible in gross dissections (Fig. 3). Evidently the male sex hormone passes from one twin into the other in the same way as the inhibitive medullarin does. Nevertheless they are
5 VOL. 23, 1937 ZOOLOGY: E. WITSCHI 39 different substances as is indicated by the fact that the latter inhibits ovarial development but is without direct influence on secondary sex characters, while the former does not interfere with ovarial development (Witschi6) but stimulates functional growth of male secondary sex characters. The medullarin is in control of a phase of the embryonic differentiation of the sex gland while the testicular hormone stimulates merely the last functional development of male secondary sex characters. The comparison of these two hormones and their reactions in parabiotic twins is of particular interest since they represent so clearly the opposed types of inhibitive and stimulative induction. * This investigation was supported by grants from the NATIONAL RESEARCH COUNCIL Committee for Research in Problems of Sex. 1 Lillie, F. R., Jour. Exp. Zool., 23, (1917); and Biol. Bull., 44, (1923). 2 Born, G., Arch. Entw. Mech., 4, (1897). 3 Witschi, E., Anat. Rec., 66, (1936). 4 Witschi, E., Jour. Exp. Zool., (in press) (1937). ' Witschi, E., Bull. Soc. Biol. Lettonie, 5, (1936).
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