Hormonal and pheromonal control of spawning behavior in the goldfish

Species that employ sexual reproduction must synchronize gamete maturity with behavior within and between genders. Teleost fishes solve this challenge by using reproductive hormones both as endogenous signals to synchronize sexual behavior with gamete maturation, and as exogenous signals (pheromones) to synchronize spawning interactions between fish. This dual role of hormonal products is best understood in the goldfish, an external fertilizer with a promiscuous mating system. Female gonadal growth and vitellogenesis is stimulated by 17β-estradiol (E2) which also evokes release of a recrudescent pheromone. At the completion of vitellogenesis, ovarian E2 production drops and plasma testosterone increases, sensitizing the female gonadotropin II (luteinizing hormone; LH) system to environmental cues (temperature, spawning substrate, pheromones). These cues eventually trigger a LH surge that alters steroidogenesic pathways to favor the production of progestins including 17,20β-dihydroxy-4-pregnen-3-one (17,20β-P). Plasma 17,20β-P stimulates oocyte maturation but is also released to the water along with sulfated 17,20β-P and androstenedione to serve as a preovulatory pheromone. This pheromone stimulates male behavior, LH release, and sperm production. At the time of ovulation, females become sexually active in response to prostaglandin F2α (PGF2α) synthesized in the oviduct. PGF2α and its metabolites are released as a postovulatory pheromone that induces male spawning behavior which further increases male LH and sperm production. Androgenic hormones are required for male behavior and LH release. Although goldfish are gonochorists, hormone treatments can induce heterotypical functions in adults. Similar findings in other fish demonstrate that a sexually bipotential brain is not restricted to hermaphroditic fishes.