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REPRODUCTIVE

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ENDOCRINOLOGY OF FISHES: Gonadal Cycles and Gonadotropin in Teleosts R. E. Peter Department of Zoology, University of Alberta, Edmonton

T6G 2E9,

Canada

L. W. Crim Marine Sciences Research Laboratory, Memorial University of Newfoundland, St. John's AlC 5S7, Canada

INTRODUCTION

This brief review is restricted to certain aspects of the endocrinology of reproduction of teleost fishes: (a ) the timing of reproductive cycles and the environmental cues involved; and (b ) the chemistry and actions of gonado­ tropin (GtH), its secretory cycles, and the regulation of its secretion. REPRODUCTIVE CYCLES AND ENVIRONMENTAL CUES

Annual reproductive cycles for many species of teleosts have most fre­ quently been described in terms of seasonal changes in the gonadosomatic index (gonad weight as a percent of total body weight) and/or histological changes in the ovary or testis (31, 33, 35, 36, 42, 74). Many salmonids spawn in the autumn. Short photoperiods, and accelera­ tion of the cyclic change of increasing and decreasing photoperiods induce earlier gonadal maturity in brook trout, Salvelinus fontinalis (50). In rain­ bow trout, Salmo gairdneri, decreasing photoperiods and warm tempera­ ture (16°C) accelerate spermatogenesis more than decreasing photoperiod

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and cold temperature (8°C) (8). These results, among others, indicate that acceleration of the photoperiod cycle, specifically decreasing daylength, induces gonadal maturation in autumn-spawning trout. The threespine stickleback, Gasterosteus aculeatus. spawns in the late spring--early summer; and gonadal recrudescence is regulated by a combi­ nation of photoperiod and temperature cues (2). Gonadal recrudescence can be induced in the winter in this species by exposure to a long photoperiod (16 hr light, 8 hr dark) and warm temperatures (20°C), short photoperiods (8 hr light, 16 hr dark) and such temperatures being ineffective. The sensi­ tive period for inducing gonadal maturation in the stickleback is about 12-1 8 hr after onset of the daily photoperiod. During the spring, long photoperiod induces more rapid gonadal maturation than short photoperiod in both warm and cold. During the summer, after termination of the normal spawning season, long photoperiod and warm conditions do not induce another cycle of gonadal recrudescence. This suggests a refrac­ tory period following spawning that terminates reproductive activity and prevents another cycle of gonadal recrudescence in the summer. In another stickleback, Culea inconstans. long photoperiod and temperatures of about 1 4-18°C, but not greater than 1 9°C, induce reproductive activity (71). Generally all freshwater temperate zone fishes spawning in the spring or early summer have gonadal recrudescence in the winter or spring in re­ sponse to long photoperiods and warm temperatures, although there may be more dependence on one factor or the other in different species (31, 35, 4 2, 46, 49, 56, 74). In these fishes warmth is necessary for final oocyte maturation or spermiogenesis and spawning. However, excessively high temperatures can cause gonadal regression, and additional factors such as vegetation may be necessary for spawning. The catfish, Heteropneustes tossilis. has a daily rhythm in photoresponsiveness, with the sensitive phases occurring at between 16-17 hr and 20-21 hr after onset of the daily light period; the catfish, however, responds primarily to warmth for gonadal recrudescence (74). Although a period of postspawning refractoriness prob­ ably occurs in most species, it has been demonstrated in only the threespine stickleback (2), the cyprinid Notropis bifrenatus (49), the catfish (74), and the medaka, Oryzias latpes (4 2). In the catfish, post-spawning gonadal regression is accelerated by low temperatures (74). Perhaps exposure to low temperatures is necessary to overcome refractoriness for many species, but this has not been investigated. In the cyprinid Couesius plumbeus. low temperatures in the winter favor the early stages of spermatogenesis (l); in goldfish, warm temperatures in the autumn inhibit, whereas cold tempera­ tures favor, the early stages of oogenesis (46). Cold temperatures are also favorable to gametogenesis in the cyprinid Notemigonus crysoleucas (36). Since many spring-spawning teleosts initiate gametogenesis in the autumn

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GONADAL CYCLES AND GONADOTROPIN IN TELEOSTS

325

or winter, the role of low temperatures for this process may be more important than is presently realized. Only a few marine and estuarine temperate-zone teleosts have been inves­ tigated. In the viviparous seaperch, Cymatogaster

aggregata, ovarian re­

crudescence is enhanced by the warm temperatures and shortening photoperiods of late summer,and final oocyte maturation occurs under cold temperatures (77). Copulation occurs in the summer months,but fertiliza­ tion of mature oocytes takes place in mid-winter from sperm stored since

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the summerj parturition occurs in the summer period. In the males, sper­ matogonia formation occurs under cold conditions,but remaining stages of spermatogenesis are enhanced by warm temperatures and long photoperi­ ods.

Cymatogaster males and females thus apparently respond to different

environmental cues. The marsh killifish, Fundulus, spawns in the late spring and apparently resembles many spring-spawning freshwater fishes in that some early stages of gametogenesis are dependent on cold tempera­ tures, whereas rapid gonadal recrudescence and gamete maturation are induced by warm temperatures in the spring (31). For the estuarine gobiid fish, Gillichthys

mirabilis, the primary environmental cue is temperature (32-34). Gonadal recrudescence occurs under cool temperatures (l0-20°C) and is accelerated by short photoperiodsj spawning occurs in the winter. Regardless of photoperiod length, gonadal regression occurs only above

22°C in females,24°C in males. Thus,this species seems to lack an obliga­ tory refractory period following spawning. It is obvious from the above discussion that regulation of gonadal re­ crudescence in teleosts involves a complex interaction of temperature and photoperiods. The environmental cues involved in initiating the stages of final oocyte maturation and ovulation, or spermiation,are largely uninvesti­ gated. Social and physical environmental factors, such as courtship and photoperiod in the medaka (42), undoubtedly interact at this stage of the reproductive cycle. However, the cues involved in gonadal recrudescence cannot be viewed in isolation from those involved at other stages of the cycle,because the whole system is physiologically integrated.

GONADOTROPIN

Chemistry and Actions of Gonadotropins (GtH) Relatively pure GtH has been obtained from carp Cyprinus carpio (17), chinook salmon Oncorhyncus tshawytscha (14, 39,40, 70), chum salmon, O. keta, (53, 54, 77,78), rainbow trout (12),and Tilapia (43) pituitaries. GtH of these teleosts shares some structural properties with the GtHs of higher vertebrates; it is a glycoprotein (17, 43, 53, 70, 79), a feature used to retain salmon GtH on concanavalin A-Sepharose in some purification

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procedures (53,70). Although the amino acid composition of each fish GtH is unique, similarities to mammalian luteinizing hormone (LH) (43, 70, 79) and FSH (79) have been reported. The subunit nature of fish GtH (12, 17, 53, 70) and the ease of dissociation of the native hormone have also been examined (17, 70). The number of GtHs present in the fish pituitary gland has been debated and is currently unresolved. Biological studies of chinook salmon (SO­ Gl00) (39, 40) and carp (4) GtH preparations showed that complete gametogenesis can be produced in hypophysectomized test animals, favor­ ing the one-hormone hypothesis. However, extensive fractionation of chum (54) and chinook (14) salmon GtH produced preparations with some male or female specificity. The two forms of chinook salmon GtH are chemically very similar and immunologically identical (14), and are qualitatively simi­ lar in biological activity (75). Tilapia pituitaries were fractionated accord­ ing to purification procedures for mammalian GtH (43); an "LH-like" preparation with the ability to stimulate in vitro testosterone production in rat Leydig cells was obtained. An "FSH-like" fraction of unspecified activ­ ity was also extracted. A glycoprotein GtH obtained from pituitary glands of the American plaice induced oocyte maturation and ovulation (20). Within the fraction lacking affinity for concanavalin A-Sepharose, a non­ glycoprotein fraction produced yolk incorporation into the ovary of the winter flounder (19). Extraction of the salmon pituitary has also produced a nonglycoprotein vitellogenic factor that stimulates oocyte uptake of la­ belled vitellogenin in vitro (18). GtH apparently regulates some events of oocyte development directly and others indirectly via sex steroid hormones. Maintenance and mitotic division of oogonia, as well as initial oocyte growth through protoplasm synthesis, seem to be independent of GtH requirements. The evidence for GtH action begins with induction of endogenous yolk formation marked by the appearance of multivesicular bodies (75) or intravesicular yolk frag­ ments (59). A major part of oocyte growth is dependent upon uptake of exogenous yolk material (vitellogenin) synthesized in the liver. Synthesis and secretion of vitellogenin is indirectly regulated by the pituitary through the actions of estrogen. Treatment of adult female brown trout, Salrna trutta, with crude extracts of the sockeye salmon pituitary gland increased plasma estradiol levels and stimulated yolk accumulation into growing oocytes (24). Treatment of immature female rainbow trout with purified chinook salmon GtH initiated endogenous yolk formation but not incorpo­ ration of vitellogenin (75). In contrast, crude sockeye salmon pituitary extract induced both phases of vitellogenesis in the immature brown trout. The evidence for a nonglycoprotein pituitary factor that stimulates vitel­ logenin uptake by oocytes (18, 20) implies that this phase is directly regu-

GONADAL CYCLES AND GONADOTROPIN IN TELEOSTS

327

lated by the pituitary gland. GtH is responsible for oocyte maturation by stimulation of release of a maturational steroid produced by cells of either the interrenal gland (48) or the ovarian follicular layer (55). Corticosteroid hormone may play a role by sensitization of oocytes to GtH (55). Dissocia­ tion of oocyte maturation and ovulation is experimentally possible,and in vitro oocyte studies suggest that a prostaglandin mediates the ovulation process (55). Fish GtH stimulates complete development of the male gonad (4,34,61,

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75). Whether GtH acts directly, or indirectly via androgens, or in both ways,is unclear,although high doses of testosterone alone can maintain the testes (61). Full sexual maturation of immature male rainbow trout was produced with the GtH isolated from pituitary glands of either male or female chinook salmon (75). GtH caused hypertrophy of Leydig cells and also stimulated the Sertoli cells surrounding the germinal cysts.

Secretion of Gonadotropin Spermiating and ovulated pink salmon,

Oncorhynchus gorbuscha, on

spawning grounds had consistently elevated plasma GtH levels (females having the highest levels) compared to fish undergoing gonadal develop­ ment (25); during gonadal development the plasma GtH levels were fre­ quently undetectable with the radioimmunoassay used. Data for brook trout and sockeye salmon,O.

nerka, indicate that a small increase in plasma

GtH levels generally occurs as the fish progress through gonadal develop­ ment; during spermiation in males there is usually an increase, and in ovulated females a marked increase,over the levels found during gonadal development (28). However,in female brown trout (24) and male (7) and female

(44)

rainbow trout plasma GtH levels did not change until the fish

had nearly completed gonadal recrudescence, when levels rose slightly. Male parr Atlantic salmon,

Salrno salar, frequently become precociously

sexually mature; in the precocious males the plasma GtH levels increase somewhat during recrudescence and are elevated even more at spermiation (23). Increased levels of plasma GtH were also found in other species at spermiation and ovulation (9,11). These data generally support the hypoth­ esis of gradual incremental secretion of GtH to stimulate progressive gona­ dal recrudescence,with a sharp rise in secretion occurring at ovulation and spermiation. Because teleosts time reproductive cycles by response to environmental cues,it is necessary to know the effects of environmental factors on GtH secretion. Exposure of immature rainbow trout to a decreasing photoperiod (16 hr light to 8 hr light) and to 16°C or 8°C between February and June induced testicular recrudescence through to complete development of sper­ matozoa (8). In the trout exposed to 16°C plasma GtH levels increased

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about the middle of the experimental period; at goC, however, only a slight rise,if any,occurred. Trout at 16°C had higher plasma GtH levels than at 8°C over the whole experimental period, regardless of the photoperiod imposed. For autumn-spawning rainbow trout, gonadal recrudescence un­ der a decreasing photoperiod is obviously a functional response. However, it is difficult to evaluate the functionality of increased GtH levels at higher temperatures because temperatures normally decrease prior to spawning in the autumn. Experiments on the rainbow trout at the higher temperature

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did accelerate gonadal recrudescence

(8).

Between February and July, 17, 24, and 30°C temperatures induced higher plasma GtH levels in male goldfish than did lOoe or natural pond temperatures for a period of about 3 months; but then GtH levels in the fish in warm temperatures decreased, apparently in association with testicular regression,to levels similar to the other groups (45). Testicular development in the male goldfish at 30°C did not advance beyond the spermatocyte stage, in spite of the high plasma GtH levels. This suggests some sort of tempera­ ture block of GtH action on the testes. High temperatures also caused increased plasma GtH levels in male and female goldfish during autumn and winter, but no photoperiodic effects were found (46). In the spring (March to June) exposure to warm temperatures for long periods were associated with ovarian regression,and plasma GtH levels were generally not elevated at higher temperatures. These data suggest that in goldfish warm temperatures stimulate GtH secretion, and regression of the gonad under warm conditions is associated with decreased plasma GtH levels. Significant daily fluctuation occurs in plasma GtH levels in female goldfish under summer pond conditions (9). Recently (52) significant daily fluctuations in serum GtH levels have been found in female goldfish under­ going ovarian recrudescence (maturing females) and in females with oocytes that have completed vitellogenesis (mature females). However, in goldfish with regressed or relatively inactive gonads, significant daily fluctuations in serum GtH levels are either absent or the fluctuations are smaller than in the maturing and mature females under the same environmental conditions. Under comparable conditions,the lower levels of serum GtH in the matur­ ing and mature fish are similar to those found in the fish with regressed or inactive gonads. In fish at a similar stage of gonadal development, warm temperatures (21°C) caused some elevation in the lower serum GtH levels over that in fish at cold temperatures (12°C). Also,exposure of maturing females to the stimulatory conditions of long photoperiod and warmth caused a large daily fluctuation. The presence of daily cycles of secretion, presumably the presence of peaks in blood GtH,appear to be important in stimulating gonadal activity in female goldfish. Injection of GtH may be effective in N.

crysoleucas at one time of day and not at another in inducing

GONADAL CYCLES AND GONADOTROPIN IN TELEOSTS

329

gonadal development (38). Perhaps the responsiveness of the gonad to GtH varies daily; presumably the daily fluctuations in blood levels of GtH would be related to these changes in gonadal responsiveness to GtH.

Regulation of Gonadotropin Secretion Pituitary transplantation experiments in various teleosts generally result in regression of the gonads and inactivity of the gonadotroph cells (63). Thus GtH secretion seems to be regulated primarily by a releasing factor (GRP).

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Lesioning a part of the nucleus lateralis tuberis (NTL) in goldfish blocks gonadal recrudescence and induces regression (62, 65). Interestingly, no significant differences in serum GtH levels were found between NLT­ lesioned and control animals (65). However,the effects of NLT lesions may be due to abolition or alteration of the daily cycle of secretion of GtH (R. E. Peter, unpublished). This supports the hypothesis (52) that daily fluctua­ tions in blood GtH levels, specifically the presence of daily peaks in levels, have significance for stimulation of gonadal activity. With the possible exception of the nucleus preopticus (NPO) region,[ (65),but cf (62) and R. E. Peter and L. W. Crim, unpublished] lesions in brain regions other than the NL T do not affect gonadal activity. Thus, the results indicate involve­ ment of the NLT in secretion of GRF for regulation of GtH secretion to induce gonadal recrudescence. Lesions in the NLT of sexually mature female goldfish held in running cold water,conditions under which ovulation would normally never occur, produced ovulation within 2-4 days (66). In addition, serum GtH levels were very markedly increased after 2 days,and after 12 days they were still significantly higher, but reduced to near levels in control fish. There is apparently tonic inhibition of GtH secretion in the sexually mature female goldfish. This inhibition must be abated or abolished to allow the ovulatory surge in GtH secretion. Whether this inhibition involves a GtH release­ inhibitory factor (GIF) or some other mechanism is not known. Prostaglan­ dins (pG) F2a and E2 injected into the third ventricle in sexually mature goldfish suppress serum GtH levels (64), which suggests that PG may be a part of the GIF mechanism. Simultaneous intraventricular injection of PG F2o. and synthetic luteinizing hormone-releasing hormone (LHRH) in female goldfish results in an increase in serum GtH levels (R. E. Peter, unpublished),which indicates that the action of PG in blocking GRF action is not at the level of the pituitary. Since lesions in the NLT in goldfish block gonadal recrudescence and cause gonadal regression, whereas similar le­ sions in mature females cause ovulation,the NLT may be the source of both GRF and GIF. The ovulatory surge in GtH secretion may also in part be due to spontaneous activity of the gonadotrophs after release from inhibi­ tion. The brain areas other than the NLT that might be involved in this

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inhibitory action on GtH secretion have not yet been explored, and there is no information as to whether the inhibitory mechanism is of importance in males. GRF activity has been claimed in crude hypothalamic extracts from carp (10,15,16,76),rainbow trout (16),goldfish (27) and N. crysoleucas (37). Unfortunately, a control brain extract was not used in many of these studies and the conditions of the donor and test animals were not always clear. The GRF activity in carp hypothalamic extract has been shown to be associated with a substance having a molecular weight of less than 5000 (13). Neurohypophysial hormones, epinephrine, norepinephrine, serotonin and dopamine do not have GRF activity on carp pituitaries in vitro (13). How­ ever, large doses of LHRH have GtH releasing activity in carp (16, 79), brown trout (22) and goldfish (27), the most responsive period of the reproductive cycle of carp and brown trout being when the fish have mature gonads. Large doses of LHRH also induce ovulation in goldfish (60) and ayu, Plecoglossus altivelis (51), and induce gonadal recrudescence in medaka (21). The argument justifying the use of large doses of LHRH is that the native molecule is different from LHRH and that consequently the

GRF receptors are not highly responsive to LHRH. LHRH immunohisto­ chemical-reactive material has been demonstrated in the neurohypophysial tissue invading the proximal pars distalis in the pituitary (41) and in the area dorsalis pars medialis (Om) of the telencephalon (47) of rainbow trout. However, destruction of the Om telencephalon blocks neither ovulation induced by NLT lesions in goldfish (66) nor reproductive activity in other species (30, 73). Neurosecretory axons directly invade the pars distalis of the pituitary of teleosts. This phenomenon is unique among the vertebrates (67). In the goby (81),goldfish (57), and the black molly, Poecilia latipinna, (69) gonado­ trophs are directly innervated by neurosecretory endings containing dense­ cored granulated vesicles of appearance and size similar to those found in some NLT neurons in these species (68,69, 80). In the goby one group of NLT neurons shows retrograde degeneration after hypophysectomy (81) and activation following castration (82); the effects of castration are re­ versed by androgen treatment. In other teleosts investigated either the gonadotrophs are directly innervated by neurosecretory endings supposedly originating from the NLT or the endings are separated from the gonado­ trophs by a basement membrane (67). The gonadotrophs of goldfish (57), the black molly (69),and a number of other species (67) are also directly innervated by neurosecretory endings originating from NPO neurons, al­ though in many species the NPO endings are separated from the gonado- . trophs by a basement membrane (67). While these observations implicate

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GONADAL CYCLES AND GONADOTROPIN IN TELEOSTS

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the NLT and NPO regulation of gonadotroph activity, the specific functions are not revealed. Another means of control of GtH secretion is by the feedback actions of gonadal steroids. Plasma GtH levels increase after castration of rainbow trout at any stage of the testicular cycle, including when the testes are inactive (6, 7); the most pronounced increase occurs after castration of spermiating trout, which indicates that a negative feedback effect by testicu­ lar steroids occurs at all gonadal stages in rainbow trout. Sex steroids are taken up in the pituitary, NLT, NPO, nucleus recessus lateralis, and other locations in male paradise fish, Macropodus opercularis (29), goldfish (58), and platyfish, Xiphophorus maculatus (58), which suggests that a wide variety of sites could serve for feedback actions by sex steroids. Markedly increased serum GtH levels occurred in sexually mature female goldfish following implantation of anti-estrogens in the pituitary; only a small rise occurred due to implantation in the NLT, and no effects occurred as a result of implantation elsewhere (5). These results indicate that the pituitary and the NLT are sites for negative feedback action of estrogens in female goldfish. In vitro studies indicate that the pituitary is a site of negative feedback in the platyfish (72), and in rainbow trout the post-castration rise in plasma GtH levels can be partially blocked by pituitary implantation of l l-ketotestosterone (3). In male and female Atlantic salmon parr, implanta­ tion of testosterone in the pituitary and brain, particularly in the NLT region, caused greater levels of pituitary GtH and tended to cause onset of testicular recrudescence (26). These results indicate a positive feedback action by testosterone on the pituitary and brain in the immature parr, and lead to the speculation that positive feedback action by testosterone may be a part of the mechanism of onset of precocious sexual maturity in the males. CONCLUSION

The information reviewed above is based on very few species in each in­ stance, and information between species is not always consistent. Many previously held assumptions have not been supported by recent investiga­ tions. New hypotheses are being presented currently, and exciting develop­ ments in this field are anticipated for the near future.

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