Variability of GnRH secretion in two goby species with socially controlled alternative male mating tactics.

Male reproductive phenotypic plasticity related to environmental-social conditions is common among teleost fish. In several species, males adopt different mating tactics depending on their size, monopolizing mates when larger, while parasitizing dominant male spawns when smaller. Males performing alternative mating tactics are often characterized by a strong dimorphism in both primary and secondary reproductive traits. According to studies on sex-changing species and on species where only one male morph is reproductively active, male alternative phenotypes are expected to vary also in gonadotropin-releasing hormone (GnRH) neurons in forebrain preoptic area (POA). Here, we compared the intra- and inter-sexual variations in number and size of GnRH neurons, along with gonads and male accessory structure investment, in two goby species, the grass goby, Zosterisessor ophiocephalus, and the black goby, Gobius niger, characterized by male alternative mating phenotypes. In both species, older and larger males defend nests, court and perform parental care, while younger and smaller ones try to sneak territorial male spawning. We found that grass goby and black goby have different patterns of GnRH expression. Grass goby presents a clear intra-sexual dimorphism in GnRH expression, related to the occurrence of alternative mating tactics, while in the black goby, only inter-sexual differences are observed. The inter- and intra-specific variability in the GnRH neurons in these two goby species is discussed in light of the differences in migratory behavior, nest type, and mating system.

Changes along the male reproductive axis in response to social context in a gonochoristic gobiid, Zosterisessor ophiocephalus (Teleostei, Gobiidae), with alternative mating tactics.

Sexual selection has given rise, in several taxa, to intrasexual variation in male phenotype. While evolutionary studies have provided explanations of the adaptive function of this dramatic male phenotypic diversity, the proximate control of its expression has still to be completely understood. Several observations, primarily from sex-changing species, indicated a major role of social interactions in reproductive axis regulation and consequently in the expression of alternative male phenotypes. Here we documented changes along the male reproductive axis in response to social context in a gonochoristic species, the grass goby Zosterisessor ophiocephalus, where fully functional alternative male mating tactics appear to be expressed as an ontogenetic gradient. In the grass goby, larger and older males dig a nest and perform parental care, while smaller males sneak fertilization during territorial male spawning. Territorial males are characterized by a higher number of gonadotropin-releasing hormone (GnRH) neurons in forebrain preoptic area, smaller testes, larger seminal vesicles, and viscous ejaculates that last longer and contain fewer sperm than those of sneakers. To experimentally investigate the role of social factors in inducing changes along the male reproductive axis, sneakers were tested in two different situations: nesting alone or with ripe females. Sneakers that mated and performed parental care showed dramatic changes in brain, reproductive apparatus morphology, and ejaculate traits. GnRH-immunoreactive cells in forebrain preoptic area increased in number, reaching values typical of wild-caught parental males. Testes size decreased while seminal vesicle size increased and ejaculates showed lower sperm densities. These results were discussed within the framework of the social transduction hypothesis, which predicts that social experience should mediate, through a cascade of internal processes, shifts between morphs throughout life.

Individual adjustment of sperm expenditure accords with sperm competition theory.

Sperm competition theory predicts that males should strategically allocate their sperm reserves according to the level of sperm competition, defined as the probability that the sperm of two males compete for fertilizing a given set of ova. Substantial evidence from numerous animal taxa suggests that, at the individual level, sperm expenditure increases when the risk of sperm competition is greater. In contrast, according to the "intensity model" of sperm competition [Parker, G. A., Ball, M. A., Stockley, P. & Gage, M. J. G. (1996) Proc. R. Soc. London Ser. B 263, 1291-1297], when more than two ejaculates compete during a given mating event, sperm expenditure should decrease as the number of competing males increases. Empirical evidence supporting this prediction, however, is still lacking. Here we measured sperm expenditure in two gobiid fishes, the grass (Zosterisessor ophiocephalus) and black goby (Gobius niger), in which up to six sneakers can congregate around the nest of territorial males and release their sperm when females spawn. We show that, in accordance with theory, sneaker males of both species release fewer sperm as the number of competitors increases.