Genotype-by-environment interactive effects and conflict solving during gonadal sex differentiation of pejerrey Odontesthes bonariensis, a fish with dual genotypic/environmental sex determination

Abstract Background Genotypic (GSD) and environmental (ESD) sex determination coexist in many species of reptiles, fish, and amphibians. Inherited genotypic signals and environmental factors conceivably interact as pro-testis or pro-ovary signals during sex determination, but how such interactions affect gonadal sex differentiation in these species remains largely unexplained. This study uses a model gonochoristic fish with coexisting GSD and ESD, the pejerrey Odontesthes bonariensis , to examine how synergism and antagonism between sex genotype (XX/XY) and thermal (feminizing/masculinizing) regimes interactively affect environmental sensitiveness and the critical time of environmental sex determination as well as how genotype-by-environment conflicts are resolved. Methods We performed a series of controlled rearing experiments involving shift-once and shift-twice transfers of fish of known sex genotype (XX/XY) between feminizing and masculinizing temperatures at different stages of gonadal sex differentiation. Match/mismatch analysis of phenotypic (ovary/testis) and genotypic (absence/presence of the master sex determining gene amhy ) sex was performed in juveniles to estimate sex reversal rates and the critical period of sex determination for each combination of sex genotype and thermal conditions. Results The results show that convergence/divergence between genotypic and environmental signals advances/delays the critical time of sex determination and lowers/raises the degree of environmental sensitiveness, respectively, even when genotypic control is ultimately overridden. This study also provides evidence that ovarian formation is the default state regardless of genotypic sex but commitment to femaleness is a lengthy, passive process requiring absolute seclusion from environmental pro-male stimuli in the span of weeks. Testis formation, in turn, is the alternative state that can be imposed on this default, regardless of genotype, by an extremely short (range of hours) environmental stimulus of sufficient strength at any time before ovarian commitment. We argue that this combination of developmental features increases the likelihood of male development and at the same time may be crucial to avoid ambiguous differentiation under conflicting genotypic/environmental signals in GSD + ESD species. Conclusions Overall, the results reveal genotypic sex-dimorphic critical periods of sex determination, show that it is “easier” to make males in pejerrey, and provide clues to understand how GSD + ESD species may prevent discrepant sex determination/differentiation when genotype and environment diverge.