Complex effects of sex reversal on reproductive success in wild frogs

Veronika Bókony , Emese Balogh, Nikolett Ujhegyi, Zsanett Mikó, Andrea Kásler, János Ujszegi, Attila Hettyey, Dávid Herczeg, Tibor Papp, Edina Nemesházi

Sex reversal, when the environment overrides genotypic sex determination, is theorized to exert wide-ranging effects on population dynamics and evolution in ectothermic animals. The expected outcomes critically depend on the reproductive ability of sex-reversed individuals and the viability of their offspring, but empirically next to nothing is known about these traits in natural populations. Here, we address this knowledge gap with the first comprehensive dataset using the agile frog, an amphibian in which larval heat stress causes female-to-male sex reversal. In a wild population where 20% of adult males are genotypic females, we compare sex-reversed and sex-concordant males for fertility, attractiveness to females, intrasexual competitiveness, and offspring survival under benign conditions, heat stress, and viral infection. We demonstrate that sex-reversed males exhibit uncompromised potential to mate and produce viable offspring, which are all genotypic females with female-biased phenotypic sex ratios. However, clutch sex ratios sampled across wild populations reveal reduced paternity by sex-reversed males, and our experiment indicates cryptic female choice as the mechanism. Furthermore, the offspring of sex-reversed sires have higher ranavirus loads after larval heat exposure, suggesting increased vulnerability to multiple stressors. These effects of sex reversal predict complex consequences of environmental change for the fate of biodiversity.