Endocrine Changes During Onset of Puberty in Male Spring Chinook Salmon, Oncorhynchus tshawytscha1

Abstract

In male salmonids, the age of maturation varies from 1 to 6 years and is influenced by growth during critical periods of the life cycle. The endocrine mechanisms controlling spermatogenesis and how growth affects this process are poorly understood. Recent research has indicated that gonadotropins, 11-ketotestosterone, and insulin-like growth factor I play roles in spermatogenesis in fish. To expand our understanding of the roles of these endocrine factors in onset of puberty, male spring chinook salmon (Oncorhynchus tshawytscha) were sampled at monthly intervals 14 mo prior to spermiation. This sampling regime encompassed two hypothesized critical periods when growth influences the initiation and completion of puberty for this species. Approximately 80% of the males matured during the experimental period, at age 2 in September 1999. An initial decline in the ratio of primary A to transitional spermatogonia was observed from July to December 1998, and during this period plasma levels of 11-ketotestosterone and pituitary levels of FSH increased. From January 1999 onward, males with low plasma 11-ketotestosterone levels (<1 ng/ml) had low pituitary and plasma FSH levels and no advanced development of germ cells. Conversely, from January through September 1999, males with high plasma 11-ketotestosterone levels (>1 ng/ml) had testes with progressively more advanced germ cell stages along with elevated pituitary and plasma FSH. Plasma levels of insulin-like growth factor I increased during maturation. These data provide the first physiological evidence for activation of the pituitary-testis axis during the fall critical period when maturation is initiated for the following year.

Oestrogen-induced androgen insufficiency results in a reduction of proliferation and differentiation of spermatogonia in the zebrafish testis

“…To our knowledge, this is the first study localizing specific, androgen-dependent germ cell stages during adult spermatogenesis in teleost fish. This observation correlates well with both the high level of ar mRNA expression in Sertoli cells contacting type A spermatogonia in zebrafish testis (De Waal et al 2008) and the elevation of circulating androgen levels in Chinook salmon at the time when seasonal spermatogonial proliferation starts (Campbell et al 2003).…”

“…In immature Japanese eel testis containing type A and a few type B spermatogonia only, androgens can induce rapid proliferation of spermatogonia and their terminal differentiation into spermatozoa under tissue culture conditions (Miura et al 1991). Androgen treatment of juvenile male African catfish (Clarias gariepinus) induced precocious testis growth, spermatogonial proliferation and entry into meiosis (Cavaco et al 1998), and the rise of androgen plasma levels in pubertal Chinook salmon (Oncorhynchus tshawytscha) coincided with the start of rapid spermatogonial proliferation (Campbell et al 2003). However, scarce information is available on the role of androgens in adult spermatogenesis in fish.…”

Gh is produced by the testis of Japanese eel and stimulates proliferation of spermatogonia

“…In addition to these roles, Gh has been implicated, directly and indirectly, in the regulation of reproductive processes in several vertebrate taxa. In salmonid fishes, several studies have shown that growth rate at critical periods determines whether animals will undergo gonadal maturation and initiation of spermatogenesis or secondary ovarian follicle growth, an effect that may be mediated through plasma levels of Igf (Campbell et al 2003(Campbell et al , 2006. Gh and Igf1 have also been shown to act on the gonad to stimulate steroid production (Lubzens et al 2010, Schulz et al 2010 and Igf1 is involved in the regulation of final oocyte maturation (Lubzens et al 2010).…”

Changes in the plasma levels of insulin-like growth factor-I from the onset of spawning migration through upstream migration in chum salmon

“…They estimated growth history from annuli of scales in hatchery-arrived chum salmon, and showed that the recent growth rate is the most important factor for oceanic fish to determine whether mature or not mature in the subsequent spawning period. Since the plasma levels of IGF-I correlated well with the growth rates and body sizes in immature and early maturing salmonids (Beckman et al, 1998;Shimizu et al, 2000;Campbell et al, 2003;Campbell et al, 2006), the plasma IGF-I levels may be an important somatotropic signal that interrelated with the onset of spawning migration.…”

“…The previous studies in salmonid reproduction established that the plasma levels of insulin-like growth factor I (IGF-I), a liver polypeptide that acts as a mediator of growth-promoting action of growth hormone (GH) in teleost fishes (Duan and Hirano, 1992), are increased with body growth during winter and spring, and the seasonal increase in circulating IGF-I was linked to initiation of gametogenesis in male chinook salmon (Campbell et al, 2003) and female coho salmon (Campbell et al, 2006). We thus hypothesized that IGF-I might be involved in reproductive maturation of oceanic chum salmon.…”