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REPRODUCTIVE ENDOCRINOLOGY OF FISHES - Gonadal Cycles and Gonadotropin in Teleosts
REPRODUCTIVE ENDOCRINOLOGY OF FISHES - Gonadal Cycles and Gonadotropin in Teleosts
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REPRODUCTIVE .1222
ENDOCRINOLOGY OF FISHES:
Gonadal Cycles and Gonadotropin
Annu. Rev. Physiol. 1979.41:323-335. Downloaded from www.annualreviews.org
in Teleosts
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R. E. Peter
L. W. Crim
INTRODUCTION
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
323
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324 PETER & CRIM
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
Annu. Rev. Physiol. 1979.41:323-335. Downloaded from www.annualreviews.org
12-1 8 hr after onset of the daily photoperiod. During the spring, long
photoperiod induces more rapid gonadal maturation than short
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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
the summerj parturition occurs in the summer period. In the males, sper
matogonia formation occurs under cold conditions,but remaining stages of
Annu. Rev. Physiol. 1979.41:323-335. Downloaded from www.annualreviews.org
GONADOTROPIN
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
Annu. Rev. Physiol. 1979.41:323-335. Downloaded from www.annualreviews.org
(54) and chinook (14) salmon GtH produced preparations with some male
or female specificity. The two forms of chinook salmon GtH are chemically
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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
testes (61). Full sexual maturation of immature male rainbow trout was
produced with the GtH isolated from pituitary glands of either male or
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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
328 PETER & CRIM
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
did accelerate gonadal recrudescence (8).
Between February and July, 17, 24, and 30°C temperatures induced
Annu. Rev. Physiol. 1979.41:323-335. Downloaded from www.annualreviews.org
higher plasma GtH levels in male goldfish than did lOoe or natural pond
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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
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
Annu. Rev. Physiol. 1979.41:323-335. Downloaded from www.annualreviews.org
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),
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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
GONADAL CYCLES AND GONADOTROPIN IN TELEOSTS 331
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),
Annu. Rev. Physiol. 1979.41:323-335. Downloaded from www.annualreviews.org
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.
332 PETER & CRIM
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