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ENDOCRINOLOGY OF REPTILES AND AMPHIBIANS: GONADOTROPINS Paul Licht Department of Zoology, University of California, Berkeley, California 94720

INTRODUCTION The components of the reproductive endocrine systems of the Reptilia and Amphibia are similar to those of other vertebrates. Evidence shows that the activities of the gonads are largely dependent upon hormones-gonadotro­ pins-secreted by the pars distalis; secretion of these gonadotropins is regulated by hypothalamic releasing factors; and a feedback relationship exists between gonadotropin secretion and sex steroids produced by the gonads (4,8, 31, 53,56). This review focuses on the roles of the gonadotro­ pins in the regulation of testicular and ovarian function. The superficial resemblances in reproductive endocrinology among all tetrapod vertebrates have often led to the assumptions that the nature and function of the nonmammalian hormones are essentially the same as, or reflect the evolu­ tionary stages leading to, the mammalian condition. Recent progress on the biochemistry and physiology of reptilian and amphibian pituitary hormones now permits evaluation of such suppositions. IDENTIFICATION OF PITUITARY GONADOTROPINS Two chemically distinct glycoprotein hormones, follicle-stimulating hor­ mone (FSH) and luteinizing hormone (LH), play separate roles in the regulation of gonadal function in eutherian mammals. Until recently, the presence of such a dual hormone system in lower vertebrates was in ques­ tion. Information on gonadotropin physiology in reptiles and amphibians 337


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was indirect (e.g. seasonal asynchrony between different gonadal activities suggested two hormones) or largely derived from the use of heterologous, mammalian hormones. However, there were anomalies (e.g. FSH and LH did not always have the action expected from mammalian studies) and complications in interpreting gonadal responses resulting from poikilo­ thermy (e.g. temperature can modify the hormonal sensitivity of gonads). Consequently, it was postulated that reptiles (31, 47) and amphibians (70) might possess only a single "complete" gonadotropin, but results of direct biochemical investigations on the amphibian and reptilian pituitary hor­ mones did not support this hypothesis. Fractionation of pituitary hormones from diverse nonmammalian spe­ cies, including anuran (14, 45) and urodele (49) amphibians and chelonian (44, 50) and crocodilian (50) reptiles, revealed two chemically distinct gonadotropins. The chemical characteristics of these hormones have re­ cently been reviewed in detail (53, 61). Biochemical, immunological, and biological data all indicate a marked structural homology between the two gonadotropins of reptiles and amphibians and the FSH and LH of mammals and birds. Thus these two gonadotropins are probably a primitive feature of the tetrapod vertebrates, but important exceptions to this general pattern may exist. No information on the hormones of caecilian amphibians is available. More importantly, limited data for squamates (snakes and liz­ ards) have failed to demonstrate two distinct gonadotropins (32, 53); this one reptilian order may lack the dual gonadotropin system. HORMONAL REGULATION OF TESTICULAR AND OV ARIAN FUNCTION The gonads of all vertebrates consist of several types of tissues and perform a number of functions: the production of gametes (spermatogenesis and oogenesis); the release of gametes (spermiation and ovulation); and the secretion of sex steroids (e.g., androgens, estrogens, and progestogens). The mammalian system is frequently used as a model for studying the roles of gonadotropins in comparative studies on reproductive endocrinology. Ac­ cordingly, FSH is classically associated with gametogenesis, while LH is clearly important for gamete release (at least ovulation) and many aspects of steroidogenesis (especially testicular androgens and ovarian progester­ one). In conjunction with these different functions, there are separate gona­ dal binding sites (receptors) for each gonadotropin. FSH and LH binding sites tend to be localized on different tissues corresponding to their physio­ logical targets (e.g. FSH receptors on Sertoli and granulosa cells and LH receptors on Leydig and luteal cells); each binding site tends to show a high degree of specificity for one type of gonadotropin.



The apparent antiquity of the FSH- and LH-like gonadotropins certainly suggests a common pattern of gonadotropin regulation of reproduction among tetrapods. However, purified mammalian gonadotropins often fail to have the expected actions when injected into reptiles and amphibians. These discrepancies reflect either an artifact of using heterologous hormones or the existence of phylogenetic variations in the functions of the FSH- and LH-type gonadotropins.

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Reproduction in the Male SPERMATOGENESIS

Although it was commonly assumed that spermatogenesis in anurans was controlled primarily by FSH (56), newer data indicate rela­ tively little gonadotropin specificity for this process. Attempts to accelerate the onset of spermatogenesis in larval or subadult anurans have met with varying success, depending on the developmental pattern of the species. Administration of either mammalian FSH or LH to tadpoles frequently caused a rapid dilation and partial evacuation of the seminiferous tubules without appreciable spermatogenic stimulation (12, 65). When spermato­ genesis was initiated in juvenile anurans, mammalian LH was often more potent than FSH (19). In contrast, the few studies on larval urodeles suggest that spermatogenesis is primarily responsive to FSH. In the newt, Pleuro· deles waltii, ovine FSH, but not LH, promoted complete spermatid produc­ tion in hypophysectomized animals (3); and ovine FSH was more potent than either ovine LH or the LH-like human chorionic gonadotropin (hCG) in stimulating initiation of spermatogenesis in intact and hypophysec­ tomized larval salamanders, Ambystoma tigrinum (57). Results for adult amphibians are also contradictory. While various stud­ ies on adult anurans indicated that mammalian FSH acted primarily on the seminiferous tubules and LH on the steroidogenic interstitial tissues (54, 56), hCG promoted complete spermatogenesis in several species (16, 20, 24). Similarly, ovine FSH and LH had the expected effects on seminiferous tubules and interstitial cells in adult newts, P. waltii- (2); but in another newt, Triturus cristatus, combinations of LH and FSH were most potent in promoting early stages of spermatogenesis, and thereafter, either hor­ mone alone stimulated further maturation of primary spermatocytes (72). The apparent FSH specificity for spermatogenesis in some amphibians may be an artifact of heterologous hormones, since, in the only study of homologous hormones in a frog, Rona catesbeiana, no difference was evi­ dent between FSH and LH. Muller (58) found that increases in the number of germ-cell cysts were stimulated either by FSH or LH treatment in adult hypophysectomized bullfrogs. Furthermore, when incubated with 3H_




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thymidine in vitro, testes from these FSH- and LH-treated frogs showed approximately the same incorporation of counts into acid-precipitable ma­ terial in spermatogonial cells. Reptilia In vivo studies on the actions of mammalian gonadotropins in lizards (e.g. 21, 37, 47, 63), snakes (28, 68), and turtles (6, 29) indicated that testis growth and spermatogenesis were highly specific for FSH. In fact, the marked discrepancy in relative potencies of the two gonadotropins sug­ gested that the activity of mammalian LH preparations might be due largely to their contamination with FSH; the testis growth response in lizards was adopted as a relatively specific FSH bioassay. However, subsequent im­ munoadsorption tests confirmed that both mammalian gonadotropins had intrinsic spermatogenic stimulating activity in lizards (42, 48), and further comparative studies using hormones from a variety of nonmammalian sources confirmed this nonspecificity (reviewed in 53). Potency ratios for different species of FSH and LH varied widely, but both hormones were always active; there was no clear phylogenetic pattern in relative potencies. The rate of hormonally induced testicular recrudescence in reptiles is highly temperature-dependent; this thermal effect is a property of the testis rather than the gonadotropin, since it is evident with both mammalian and reptilian hormones (22, 33, 47, 68). While temperature may alter the nature of the testis response (e.g. spermatogenesis and steroidogenesis do not show the same thermal sensitivities) there is no indication that activities of the two gonadotropins are differentially affected by temperature. Also, the sensitivity of the testis to gonadotropins may vary with the stage of sper­ matogenesis [e.g. more hormone is required to initiate than to maintain spermatogenesis (47, 63)], but no differential actions of FSH and LH on certain stages of spermatogenesis have been detected. It is likely that variations in FSH/LH potency ratios are related in large part to the half-lives of the two gonadotropins, rather than to specificity of gonadal receptors. The potency of gonadotropins in lizards depends on the presence of sialic acid (41, 43), which presumably affects clearance rates; LH preparations with relatively high potencies (e.g. from sea turtle) tend to be the most enriched in this carbohydrate moeity (50). Furthermore, our direct estimates of clearance rates of bullfrog and sea turtle hormones in a lizard (E. Daniels, A. Bona Gallo, P. Licht, unpublished data) correlate well with relative potencies. Unfortunately, there is no information on the effects of nonmammalian hormones on spermatogenesis in reptiles other than lizards. Since the re­ sponses of turtles to mammalian hormones are generally not comparable to those obtained with homologous hormones (see discussions of steroidogene­ sis), the apparent FSH specificity of spermatogenesis shown with ovine hormones in turtles cannot be generalized.



The release of sperm from the testis has been treated as a separate component of testicular activity in anuran amphibians. Interest in the endocrinology of this "reflex" grew out of its application as a bioassay for detection of human pregnancy-the Galli Mainini reaction. Although once considered to be primarily an LH-dependent response, it is now clear that spermiation is essentially nonspecific for the two gonadotropins. Tests in a variety of genera and families (e.g. Xenopus, Hyla, Rana, Eleuthrodac­ tylus, and Bufo) showed that spermiation could be induced readily with either purified mammalian FSH or LH, even in hypophysectomized ani­ mals, and that FSH was usually equal to or more potent than LH (30). Spermiation in a Rana and a Hyla has also been shown to be nonspecific for FSH and LH derived from several nonmammalian species (44, 45). Moreover, bullfrog FSH and LH were essentially equipotent in stimulating �permiation in the bullfrog (58). Information on the spermiation response in nonanurans is sparse. Injec­ tions of hCG have been used to induce spermatophore deposition in intact salamanders, A. mexicanum (66), but no complete comparisons ofFSH and LH have been reported. In reptiles, spermiation has not been studied as an independent process, but sperm release into the epididymis has been ob­ served regularly in conjunction with the studies on testis growth and sper­ matogenesis already discussed, and there is no evidence for a gonadotropin specificity.

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Indirect estimates of andro­ gen secretion, such as histological changes in androgen-dependent target organs or in the interstitial cells thought to be the major site of androgen production, formed the bases of much early research. More !,ecently, addi­ tional information has come from direct measurements of in vitro steroid biosynthesis and androgen secretion in vivo. The response of the testes may vary with the source of the gonadotropin in reptiles and amphibians, but there is also good evidence for important interspecific differences in the gonadotropin dependence of testicular steroid secretion.


Amphibians, like mammals, appear to show a relatively high specificity for LH in the regulation of interstitial cell activity and androgen production, although the use of heterologous hormones complicates the picture. Ovine LH has generally been found to be more effective than FSH in stimulating the activity of the interstitial tissue in frogs and salamanders as judged by histological and histochemical criteria (56). However, Wiebe's (74) studies on 3,B-dehyroxysteroid dehydrogenase activity in Xenopus Zae­ vis suggested that ovineFSH was, if anything, more potent than either ovine LH or hCG; a wide range of doses was not examined. Lofts (54) also found Amphibia

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that FSH stimulated histochemical changes indicative of steroidogenic ac­ tivity in the Sertoli cells of frogs, but the nature and importance of the steroids produced by the seminiferous tubules remain undefined. Direct measures of androgen production by amphibian testes also suggest LH specificity. Ovine LH stimulated an elevation in plasma androgen in the salamander Necturus, whereas FSH was inactive; but FSH was more potent than LH in stimulating a slight rise in estrogen (8). In the bullfrog, R. catesbeiana, the homologous LH, but not FSH, stimulated a rise in plasma androgen (60). The LH specificity of the bullfrog testis was further con­ firmed by in vitro studies on minced testicular tissues (59); bullfrog LH was 300-1000 times as potent as FSH. Likewise, the testis of a salamander, A. tigrinum, was at least 50 times as sensitive to LH as FSH when studied with homologous hormones (58). In vitro studies with Xenopus and Bufo dem­ onstrated a similar dependency of steroidogenesis on LH, but less distinctly than in assays with homologous hormones. For example, in Xenopus, the bullfrog LH was only about 6 times as potent as FSH, and ovine FSH was almost equipotent to LH (58). Testicular androgen production in both the anurans and urodeles proba­ bly follows the classical mammalian pattern in being primarily regulated by LH. However, the gonadotropin specificity of the amphibian testis may be reduced when challenged with heterologous hormones. Among the most unexpected results of comparative studies on gonadotropin actions in tetrapods are those relating to the regulation of androgen production by the reptilian testis. A variety of approaches have led to the conclusion that reptiles lack the LH specificity characteristic of this component of mammalian and amphibian steroidogenesis (reviewed in 8, 34, 53). Androgen production in the reptilian testis initially appeared, unlike that of amphibians and mammals, to be regulated by FSH. This conclusion probably resulted from the use of heterologous hormones or inappropriate experimental protocols. In fact, the "peculiarity" of reptiles seems to be their general nonspecificity for FSH or LH. For example, in vivo and in vitro studies with several turtles demonstrated that Leydig cell morphology and androgen production were sensitive only to mamm alian FSH (5, 6, 26, 29, 69); but it is now known from tests with other species of hormone, including the homologous ones, that steroidogenesis in turtles can be stimu­ lated with either FSH or LH (26, 69). Other reptiles, including squamates and crocodilians, tend to respond to both FSH and LH from all tetrapods (67, 69). Moreover, the apparent inactivity of some LH preparations in lizards when tested by chronic in vivo injections may have been due to their relatively short half-lives, as discussed above. When tested by acute injecReptilia

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tion or in vitro, LH preparations are equipotent to, or even more potent than, FSH (53, 67, 69). Finally, immunoadsorption techniques have con­ firmed that both FSH and LH from several mammalian and nonmam­ malian species possess intrinsic steroid-stimulating activities in lizards and turtles (69). The exact source ofandrogen production in the reptilian testis, and hence the target site for gonadotropin stimulation, is still controversial. Studies of in vitro steroid biosynthesis from labeled precursor (pregnelone) in the cobra led to the postulate that mammalian FSH stimulates the Sertoli cells, whereas LH acts on Leydig cells (55). A similar suggestion came from seasonal in vivo tests with mammalian gonadotropins in a turtle (6); how­ ever, such data are difficult to interpret because of the general insensitivity of turtles to mammalian LH. In vitro measurements of androgen produc­ tion in isolated Leydig cells from a lizard demonstrated that ovineFSH and LH were equipotent; furthermore, androgen production by the Leydig cells was considerably greater than from the seminiferous tubules (67). Thus it is unlikely that the difference between reptiles and mammals in the respon­ siveness of steroidogenesis to FSH is due only to differences in the primary site of androgen production. Further evidence for the sensitivity of Leydig cells to FSH in reptiles comes from data on gonadotropin binding sites. Autoradiographic studies with 125I-Iabeled human FSH demonstrated that, in contrast to the case in mammals, FSH-binding sites are present on both the seminiferous tubules and interstitial cells in lizards, snakes, and turtles (40). Moreover, competi­ tive-inhibition tests showed that these FSH-binding sites were not as hor­ mone specific as they are in mammals (38, 39, 51). Results were in good agreement with physiological studies; turtle testis receptors had specificity for mammalian FSH (38, 51), but not for other species of gonadotropins (39, 51), whereas binding sites on snake and lizard testes displayed non­ specificity for all species of gonadotropins (38, 39, 51). Reproduction in the Female

The classical view of hormone function in mammals would lead one to predict distinctive roles for FSH and LH in ovarian function: regulation of oocyte development (vitellogensis in the case of the lower tetrapods) for FSH; control of ovulation and the subsequent secretion of progesterone from the post-ovulatory follicles (corpora lutea) for LH. However, data for both amphibians and reptiles do not support these predictions. The development of ova in reptiles and amphibians is characterized by the large accumulation of yolk in the follicles. The process of vitellogenesis is mediated by steroids (estrogens) that are secreted




by the ovaries and act on the liver to induce the synthesis of vitellogenin; this protein is then transported via the circulation to the ovary, where it is taken up by the follicles (15). Gonadotropins probably affect at least two steps of this process: They stimulate the secretion of ovarian steroids and then act directly on the follicle wall to enhance uptake of vitellogenin. Mammalian FSH may be more potent than LH in stimulating ovarian growth in anurans (56), but heG is usually the most effective hormone (62, 73). The inactivity of ovine LH compared to hCG has been attributed to the relatively short half-life of the pituitary gonadotropin (62), but the possibility of species specificity was not fully considered. The few studies dealing with the mediation of vitellogenin uptake at the level of the follicle also suggest nonspecificity in gonadotropin dependence. For exam­ ple, ovine FSH enhanced vitellogenin uptake in estrogen primed X. laevis (15), but hCG had the same effect in this and other species (13, 17, 73). Tests of amphibians with nonmammalian hormones, especially homologous ones, remain to be done.

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Reptilia Full ovarian growth and ovulation can be stimulated in hypo­ physectomized lizards by treatment with purified mammalian or reptilian FSH (23, 27, 35, 37), even after removal of all LH contamination by immunoadsorption (35, 48). Although analyses have not yet been per­ formed to determine whether LH has the same intrinsic activities as FSH on the ovary, this might well be expected in light of the overlap in activities observed in spermatogenesis. OVULATION

Although ovulation represents the functional counterpart of spermiation, these two processes of gamete release do not appear to share a common hormonal dependence in amphibians. Studies on the ovarian tissues of diverse anurans under defined in vitro conditions have established that ovulation and the preceding stages of oocyte maturation-germinal vesicle breakdown-are highly specific for LH; hormones from a wide array of species, including the homologous one, have been tested (14, 44, 45, 49, 50, 64). The sensitivity to LH may vary depending on the recipient species, and there is little phylogenetic predictability in hormone potency (46); FSH preparations, however, are consistently inactive. Although few studies have examined the effects of purified hormones on urodele amphibians, members of this order appear to exhibit the same LH specificity for ovulation as do the anurans. Vellano et al (71) found that only purified ovine LH, and not FSH, would induce ovulation in intact newts. Amphibia



In attempts to develop practical methods for harvesting eggs (18, 25), large doses of crude preparations of both mammalian FSH and LH have been used to induce spawning in intact axolotls, A. mexicanum. However, in vitro studies with the related A. tigrinum, using purified hormones derived from mammalian, reptilian, and amphibian sources (including the homolo­ gous hormone), clearly demonstrated that ovulation was LH-specific (49). Gonadotropin specificity of ovulation in some reptiles may be the opposite to that in amphibians. Mammalian (27, 37, 48) and reptilian (35) FSH were both considerably more potent than the corresponding LH for inducing ovulation in intact and hypophysectomized lizards. Furthermore immunoadsorption of FSH preparations to remove any residual LH con­ tamination had no effect on their ovulating activity (35, 48). Similar tests have not yet been performed to ascertain whether LH possesses intrinsic ovulating activity. Unfortunately, data for ovulation in other reptiles are sparse. A rise in circulating LH during the ovulatory season was observed in a turtle (4), but data for concomitant changes in FSH titers are not available. The non­ specificity for FSH or LH in other aspects of ovarian function, such as steroid secretion in turtles and other reptiles (see below), suggests either FSH specificity or, more likely, a general lack of gonadotropin specificity.

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Since follicular growth is probably mediated by ovarian estro­ gen, nonspecificity for FSH or LH in the regulation of this steroid can be extrapolated from data on ovarian growth. In contrast, the dependence of oocyte maturation and ovulation on progesterone (64) suggests that its secretion is regulated primarily by LH in anurans and urodeles. Such speci­ ficity has been confirmed by direct radioimmunological measurements of in vitro progesterone secretion in ovaries of the bullfrog and tiger salamander, using mammalian and homologous hormones in each case (36).


Sensitivity of ovarian estrogen secretion to FSH is suggested by the hypertrophy of estrogen-dependent target organs in gonadotropin­ treated lizards (23, 27, 35, 48). This action of FSH, at least with hormones derived from turtles (35) and mammals (48), was intrinsic to the molecule and independent of LH. Direct measurements in intact turtles demon­ strated a rise of plasma estrogen in response to ovineFSH, whereas LH was relatively inactive; seasonal changes in ovarian sensitivity to gonadotropin were also revealed (4, 8). In vitro results on steroid biosynthesis in turtles conflict, depending on whether production was studied with reference to endogenous or exogenous precursors [cf. (7, 9) vs (10, 36)]. Reptilia

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Determination of in vivo progesterone secretion in reptiles is limited to tests with mammalian hormones in turtles: In the season when the ovary is responsive, both ovine FSH and LH were effective (4). Similar results were obtained in several in vitro studies. Progesterone production from endogenous precursors in minced tissues (10, 36) and suspended cells (4) from ovaries of several species of turtle were shown to respond to both mammalian and reptilian FSH, including the hormone from homologous species (36); LH preparations, especially from mammals, were relatively inactive. Furthermore, FSH was able to stimulate progesterone secretion from both pre-ovulatory and post-ovulatory (luteal) tissues in the turtle (10, 36). In parallel in vitro tests with crocodilian ovary (pre-ovulatory), proges­ terone secretion was found to respond almost equally to FSH and LH of either mammalian or crocodilian origin (36). Results of studies of progesterone biosynthesis from labeled exogenous precursors (cholesterol and pregnenolone) are not entirely consistent with those described above. In particular, progesterone conversion from labeled precursors appeared to be stimulated predominantly by LH (mammalian or avian); FSH had only minor effects (7, 9). Perhaps the stimulatory effect of FSH on a large pool of endogenous precursors obscures its effect on incor­ poration of labeled steroid; in contrast, LH may act on only the precursor step (8). Discrepancies between the various types of measurements imply a difference in the actions of the two gonadotropins on the steps of the steroid metabolic pathways. However, in the absence of information on dose-response characteristics, kinetics, and homologous hormones, inter­ pretation of the conversion studies is difficult. Preliminary information on the localization and characteristics of FSH­ binding sites in the reptilian ovary is consistent with physiological studies and supports the conclusion that FSH may have broad effects on steroido­ genesis. Autoradiographic studies with 125I-Iabeled human FSH revealed binding sites on the granulosa cells of the pre-ovulatory follicles in lizards and turtle ovaries, as well as on the post-ovulatory luteal tissues in turtles (40). Moreover, the hormonal specificity of these binding sites determined by competitive inhibition analyses was like that of the reptilian testis. Thus, FSH-binding sites on turtle ovaries were specific for mammalian FSH (l , 38, 51) but not for various nonmammalian gonadotropins (39, 51); squa­ mate ovaries showed little specificity for any species of gonadotropin (38, 39, 51). CONCLUSIONS Perhaps the most impressive aspect of the information on hormone function in reptiles and amphibians is the conspicuous variability in results obtained for each type of gonadal function. Thus, even though a pair of pituitary

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gonadotropins similar to mammalianFSH and LH can be identified within most orders of these two classes, it may be erroneous to assume commonal­ ity among all vertebrates in the physiological roles of these hormones. Moreover, it is possible that some reptiles, notably the Squamata, are highly divergent, having lost one gonadotropin. Because absolutely no data cur­ rently exist on the gonadotropin biochemistry or physiology of the orders Gymnophiona (Amphibia) and Rbyncocephalia (Reptilia), any generaliza­ tion about the two classes must be regarded as tentative. At least two major sources of variability may be identified in comparative studies: the species of hormone employed and the species tested. Because the effects of a particular type of gonadotropin, i.e. FSH or LH, may depend on the species from which it was derived, data based on heterologous hormones are often difficult to interpret. A notable example is the marked insensitivity of steroid production by the turtle testis and ovary to mam­ malian LH; this lack of LH response is not evidenced in other reptilian orders, nor is it seen when turtles are tested with nonmammalian hormones. The relative potencies of heterologous preparations of FSH and LH in squamates may have little relevance to the endocrinology of these reptiles if indeed they have only a single gonadotropin. Since there is little phylogen­ etic predictability in the actions of heterologous hormones, they should not be relied upon to define hormone function within a species. Notwithstanding the problems associated with heterologous hormones, it is clear that the sensitivity of several gonadal functions to FSH vis-a-vis LH is not the same in all species. This variability is most striking when species are tested with homologous hormones, but it occurs to some extent even with heterologous hormones. Comparative data are insufficient to evaluate differences among members of the same order; however, significant divergence in hormone function between Reptilia and Amphibia is evident in several aspects of gonadal physiology, especially ovulation and steroid secretion. Several components of gonadal physiology, including testicular and ovarian growth, spermiation, and estrogen secretion, seem to exhibit little FSH/LH specificity in either Amphibia or Reptilia. In contrast, ovulation, testicular androgen secretion, and ovarian progesterone secretion tend to be highly LH-dependent in Amphibia, whereas they are either predominantly FSH-sensitive or nonspecific in Reptilia. Comparative studies employing different species of gonadotropins together with information on gonadotro­ pin binding sites indicate that this divergence in hormone action between reptiles and amphibians is probably related more to evolution in gonadal receptors (i.e. their localization and specificity) than to changes in gonado­ tropin structure. The broader phylogenetic implications of these species differences in gonadotropin physiology have been discussed in detail else­ where (53). Suffice it to say that neither the Amphibia nor Reptilia show a

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consistent correspondence to the mammalian model, nor do they represent a simple evolutionary progression to the mammalian condition. Before the significance of this apparent evolutionary divergence can be appreciated fully it must be recognized that virtually all available informa­ tion on gonadotropin function deals with the responses to exogenously administered hormones. These data provide insight into the potential ac­ tions of each gonadotropin, but they do not rule out the possibility that activities of endogenously secreted hormones may differ. The recent devel­ opment of sensitive radioimmunoassays that can be used to measure circula­ tory levels of gonadotropin in reptiles (4, 52) and amphibians (11) will facilitate future explorations into the roles of gonadotropins in reproductive endocrinology. ACKNOWLEDGMENT

Preparation of this review and unpublished observations were supported by grant BM-75-16138 from the National Science Foundation. Literature Cited


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(Rana pipiens). Gen. Compo Endocrinol

32:158-62 15. Follett, B. K., Redshaw, M. R. 1974. The physiology of vittelogenesis. In PhYSiology of the Amphibia, ed. B. Lofts. pp. 219-309. London: Academic 16. Guha, K. K., Jorgensen, C. B. 1978. Effects of hypophysectomy on structure and function of testes in adult toads, Bufo bufo bufo (L.). Gen. Compo Endo­ crinol. 34:201-10 17. Holland, C. A., Dumont, J. N. 1975. Oogenesis in Xenopus laevis (Daudin). IV. Effects of gonadotropin, estrogen and starvation on endocytosis in devel­ oping oocytes. Cell Tiss. Res. 162: 177-84 18. Humphrey, R. R. 1977. Factors in­ fluencing ovulation in the Mexican ax­ olotl as revealed by inducing spawnings. J. Exp. Zool 199:209-14 19. Iwasawa, H. 1978. Spermatogonial re­ sponsiveness to mammalian gonadotro­ pins in subadult Rana nigromaculata. Gen. Comp. Endocrinol. 34:1-5 20. Iwasawa, H., Michibata, H., Satoh, N. 1973. Effects of exogenous gonadotro­ pins on spermatogenetic activity in summer and autumn frogs. Sci. Rep. Niigata Univ., Ser. D. 10:71-78 21. Jalali, S., Arslan, M., Qazi, M. H. 1975. Effect of mammalian gonadotropins (FSH, LH and PMSG) on the testes of the spiny-tailed lizard, Uromastix hard­ wickl: Islamabad J. Sci 2:10-14 22. Jalali, S., Arslan, M., Qureshi, S., Qazi, M. H. 1976. Effect of temperature and pregnant mare's serum gonadotropin on testicular function in the spiny-tailed lizard, Uromastix hardwicki. Gel!. Compo Endocrinol. 30:162-70 23. Jones, R. E. 1969. Effect of mammalian gonadotropins on the ovaries and ovi­ ducts of the lizard, Lygosoma laterale. J. Exp. Zool 171;217-22 24. Kasinathan, S., Basu, S. L. 1973. Effect of hormones on spermatogenesis in hypophysectomized Rona hexadactyla (Lesson). Acta Morphol. Acad. Sci. Hung. 21:249-59 25. Ketterer, D., Forbes, W. R. 1972. In­ duction of spawning in the Mexican ax-





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olotl (Ambystoma mexicanum) by lutei­ nizing hormone. J. EndocrinoL 55: 457-58 Lance, V., Scanes, C., Callard, I. P. 1977. Plasma testosterone levels in male turtles, Chrysemys picta, following sin­ gle injections of mammalian, avian and teleostean gonadotropins. Gen. Compo Endocrinol. 31:435-41 Licht, P. 1970. Effects of mammalian gonadotropins (ovine FSH and LH) in female lizards. Gen. Compo Endocrinol. 14:98-106 Licht, P. 1972. Action of mammalian pituitary gonadotropins (FSH and LH) in reptiles. I. Male snakes. Gen. Camp. Endocrinol. 19:273-81 Licht, P. 1972. Action of mammalian pituitary gonadotropins (FSH and LH) in reptiles. II. Turtles. Gen. Compo En­ docrinol. 19:282-89 Licht, P. 1973. Induction of spermia­ tion in anurans by mammalian gonado­ tropins and their subunits. Gen. Compo Endocrinol. 20:522-29 Licht, P. 1974. Endocrinology of Rep­ tilia-the pituitary system. Chem. Zool. 9:399-448 Licht, P. 1974. Luteinizing hormone (LH) in the reptilian ituitary gland. Gen. Comp. Endocrino . 22:463-69 Licht, P. 1975. Temperature depen­ dence of the actions of mammalian and reptilian gonadotropins in a lizard. Comp. Biochem Physiol. 50A:221-22 Licht, P. 1977. Evolution in the roles of gonadotropins in the regulation of the tetrapod testes. See Ref. 4, pp. 101-10 Licht, P., Crews, D. 1975. Stimulation of ovarian and oviducal growth and ovulation in female lizards by reptilian (turtle) gonadotropins. Gen. Comp. En­ docrinol 25:467-71 Licht, P., Crews, D. 1976. Gonado­ tropic stimulation of in vitro progester­ one production in reptilian and am­ phibian ovaries. Gel!. Compo Endo­ crinoL 29:141-51 Licht, P., Hartree, S. 1971. Actions of mammalian, avian and piscine gonado­ tropins in the lizard. J. Endocrinol. 53 :329-49 Licht, P., Midgley, A. R. Jr. 1976. In vitro binding of radioiodinated human follicle-stimulating hormone to reptil­ ian and avian gonads: radioligand stud­ ies with mammalian hormones. BioL Reprod. 15:195-205 Licht, P., Midgley, A. R. Jr. 1976. Competition for the in vitro binding of radioiodinated human follicle-stimulat­ ing hormone in reptilian, avian and



LICHT mammalian gonads by nonmammalian gonadtropins. Gen. Comp. EndocrinoL

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40. Licht, P., Midgley, A. R. Jr. 1977. Au­ toradiographic localization of binding sites for human follicle-stimulating hor­ mone in reptilian testes and ovaries. Bioi. Reprod. 16:117-21 41. Licht, P., Papkoff, H. 1972. Relation­ ship of sialic acid to the biological activ­ ity of vertebrate gonadotropins. Gen. Comp. EndocrinoL 19:102-14 42. Licht, P., Papkoff, H. 1973. Evidence for an intrinsic gonadotropic activity of ovine LH in the lizard. Gen. Comp. En­ docrinol 20:172-76 43. Licht, P., Papkoff, H. 1974. Phylogen­ etic survey of the neuraminidase sen­ sitivity of reptilian gonadotropin. Gen. Camp. Endocrinol 23:415-20 44. Licht, P., Papkoff, H. 1974. Separation of two distinct gonadotropins from the pituitary gland of the snapping turtle (Chelydra serpentina). Gen. Compo En­

ciocrinol 22:218-37

45. Licht, P., Papkoff, H. 1974. Separation of two distinct gonadotropins from the pituitary gland of the bullfrog Rona catesbeiana. Endocrinology 94:1587-94 46. Licht, P., Papkoff, H. 1976. Species specificity in the response of an in vitro amphibian (Xenopus laevis) ovulation assay to mammalian luteinizing hor­ mone. Gen. Comp. Endocrinol 29: 552-55 47. Licht, P., Pearson, A. K. 1969. Effects of mammalian gonadotropins (FSH and LH) on the testis of the lizard Anolis carolinensis. Gen. Compo Endocrinol.

52. Licht, P., MacKenzie, O. S., Papkoff, H., Farmer, S. W. 1977. Immunological studies with the gonadotropins and their subunits from the green sea turtle Chelonia mycias. Gen. Co mpo Encio­ crinol 33:231-41 53. Licht, P., Papkoff, H., Farmer, S. W., Muller, C. H., Tsui, H. W., Crews, D. 1977. Evolution of gonadotropin struc­ ture and function. Rec. Frog. Horm. Res. 33:169-248 54. Lofts, B. 1961. The effects of follicle­ stimulating hortnone and luteinizing hormone on the testis of hypophysecto­ mized frogs (Rana temporaria). Gen. Compo Endocrinol. 1:179-89 55. Lofts, B. 1972. The Sertoli cell. Gen. Compo Endocrinol., Suppl. 3, 636-48 56. Lofts, B. 1974. Reproduction. See Ref. 15, pp. 107-218 57. Moore, F. L. 1975. Spermatogenesis in larval Ambystoma tigrinum: positive and negative interactions of FSH and testosterone. Gen. Compo Endocrinol. 26:525 -33 58. Muller, C. H. 1976. Steroidogenesis and spermatogenesis in the male bullfrog, Rana catesbeiana: Regulation by puri­ fied bullfrog gonadotropins. Ph.D. the­ sis, Univ. California, Berkeley. 156 pp. 59. Muller, C. H. 1977. In vitro stimulation of 5a-dihydrotestosterone and testost­ erone secretion from bullfrog testis by nonmammalian and mammalian gonadotropins. Gen. Comp. Endocrinol.

33:109-21 60. Muller, C. H. 1977. Plasma Sa-dihy­


48. Licht, P., Tsui, H. W. 1975. Evidence for the intrinsic activity of ovine FSH on spermatogenesis, ovarian growth, steroidogenesis and ovulation in lizards. BioL Reprod. 12:346-50 49. Licht, P., Farmer, S. W., Papkoff, H. 1975. The nature of the pituitary gonadotropins and their role in ovula­ tion in a urodele amphibian (Amby­ stoma tigrinum). Life Sci. 17:1049-54 50. Licht, P., Farmer, S. W., Papkoff, H. 1976. Further studies on the chemical nature of reptilian pituitary gonado­ tropins: FSH and LH in the American alligator and green sea turtle. BioI. Re­ prod. 14:222-32




51. Licht, P., Bona Gallo, A., Daniels, E. L. 1977. In vitro binding of radioiodinated

sea turtle (Chelonia mytlas) follicle­ stimulating hortnone to reptilian gona­ dal tissues. Gen. Compo Endocrinol. 33:226-30


drotestosterone and testosterone in the bullfrog, Rona catesbeio1lo: stimulation by bullfrog LH. Gen. Compo Endo­ crinoL 33:122-32 Papkojf, H., Farmer, S. W., Licht, P. 1977. Biochemical aspects of the evolu­ tion of the pituitary gonadotropins. Ex­ cerpta Med. Found. Int. Congr. Ser. 403:77-8 1 Roos. J., Jorgensen, C. B. 1974. Rates of disappearance from blood and biolOgi­ cal potencies of mammalian gonadotro­ pins (bCG and ovine LH) in the toad Bufo bufo bufo (L.). Ge1/. Camp. Enda­ crinoL 23:432-37 Reddy, P. R. K., Prasad, M. R. N. 1970. Effect of gonadotropins and tes­ tosterone on the initiation of spermato­ genesis in hypophysectomized Indian house lizard, Hemiciactylus f/aviviriciis RuppeU. J. Exp. Zool 174:205-14 Schuetz, A. W. 1974. Role of hormones in oocyte maturation. BioL Reprod. 10:150-78

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REPTILIAN & AMPHIBIAN GONADOTROPIN PHYSIOLOGY 65. Simon, N., Reinboth, R. 1966. Juvenile Anuren als Testobjekte fUr gonado­ tropische Hormone. Verh. Dtch. Zool. Ges. (Suppl.) 30:254-64 66. Trottier, T. M., Armstrong, J. B. 1975. Hormonal stimulation as an aid to arti­ ficial inse mination in Ambystoma ti­ grinum Can. J. Bioi. 53:171-73 67. Tsui, H. W. 1976. Stimulation of andro­ gen production by the lizard testes: site of action of ovine FSH and LH. Gen. Camp. Endocrinol. 28:386-94 68. Ts ui, H. W., Licht, P. 1974. Pituitary independence of sperm storage in male snakes. Gen. Camp. EndocrinoL 22: 277-79 69. Tsui, H. W., Licht, P. 1977. Gonadotro­ pin regulation of in vitro androgen pro­ duction by reptilian testes. Gen. Camp. EndocrinoL 31 :422-34 70. Van Oordt, P. G. W. J. 1974. Cytology of the adenohypophyses. See Ref. 15, pp. 53-106


71. Vellano, C., Lodi, G., Bona, A., Mazzi, V. 1974. Endocrine determinism of ovu­ lation in the crested newt: effects of mammalian gonadotropins (LH and FSH) . and ACTH. Manit. Zool. Ital. 8:221-26 72. Vellano, C., Sacerdote, M., Mazzi, V. 1974. Effects of mammalian gonadotro­ pins (FSH and LH) on spermatogenesis m the crested newt under different tem­ perature conditions. Monit Zool Ital 8:177-88 73. Wallace, R. A., Jared, D. W., Nelson, B. L. 1970. Protein incorporation by isolated amphibian oocytes. 1. Prelimi­ nary studies. J. Exp. Zool. 175:259':'70 74. Wiebe, J. P. 1970. The mechanism of action of gonadotropic hormones in am­ phibians: The stimulation of il5 3/J ­ hydroxysteroid dehydrogenase activity in testes of Xenopus laevis Dandin. J. Endocrinol 47:439-50 -

Reproductive endocrinology of reptiles and amphibians: gonadotropins.

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