Use of Physiological Indices to Define Critical Periods for Puberty Onset in Male Pacific Salmon and Steelhead

Age of maturity (puberty) is a key component of the species-specific life history strategy in fish, which has evolved to achieve maximal reproductive fitness. In some fishes the age of puberty is highly plastic, but the underlying mechanisms involved are not understood. Development of reproductive competence relies on the integration of a wide variety of internal and external cues. These signals provide critical information on when an animal should reproduce: whether it is of sufficient size or energy status to reproduce (metabolic cues), whether conditions are optimal for reproductive success (environmental cues), and whether an appropriate mate is present (social cues). Although the mechanisms involved in integrating this information are not known, ultimately the onset and completion of puberty involves increases in brain gonadotropin-releasing hormone (GnRH) and subsequent effects on pituitary gonadotropins and gonadal physiology. In fishes, metabolic cues play an important role in puberty onset because of the large commitment of body energy reserves to the gonad. For capital breeders with long spawning migrations such as Pacific salmon, the physiological commitment to mature in a given year must be made well in advance of spawning and is influenced by body energy stores. In this talk, information on the timing of male puberty onset relative to the life history of three Oncorhynchus species will be presented. In males, puberty onset (defined by the initiation of spermatogenesis) involves the rapid proliferation of spermatogonia and expansion of seminiferous tubules in the testis. This was associated with an activation of pituitary follicle stimulating hormone (FSH) and luteinizing hormone (LH) subunit mRNAs and down regulation of testicular anti-mullerian hormone (AMH) mRNA. Fish showing high rates of spermatogonial proliferation and some meiotic germ cells (spermatocytes), had elevated plasma levels of 11-ketotestosterone (11-KT).  The seasonal timing of puberty onset varied with species. In hatchery-reared spring Chinook salmon, for example, initiation of spermatogenesis occurred over several months, from late September through March. During this period metabolic status influenced the proportion of pubertal males. These data suggest that “maturation decisions” were being made in some fish a year in advance of spawning and if spermatogenesis was not initiated by the spring, it was delayed until subsequent years.  Furthermore, because puberty onset was not synchronous, yet spermiation occurred only in the fall, our data suggest that the rate at which spermatogenesis is completed is not constant, and probably influenced by a variety of factors including genetics and environment.