Predictable ecological dynamics over incredibly small spatial scales influence early-life phenotypes in a species with temperature-dependent sex determination

Phenotype-environment associations in neonatal animals may arise in wild environments by virtue of ecological dynamics within the nest. Such dynamics may be of special importance to the evolution of temperature-dependent sex determination (TSD), an enigmatic trait that can be adaptive when the incubation temperatures that affect sexual differentiation also have differential effects on the fitness of the sexes. To infer the causal effects of the nest environment on fitness-relevant phenotypes, we apply structural equation modelling (SEM) to a 14-year dataset of 3085 individual embryos whose position in 179 wild snapping turtle nests could be estimated. We find that temperature has a positive effect on hatchling size, and that the same temperatures that predict hatchling size also predict the sex of hatchlings. Further, the probability that embryos develop as males is correlated with hatchling size in the wild, where across all environments, males are slightly and significantly larger than females at hatching. Our SEM reveals that the covariance between size and sex arises because of temperature effects on size, and because of a predictable covariance between egg placement within the nest coupled with maternal effects on egg size. Finally, embryos deep in the nest have a high probability of becoming male even in the hottest years. Our study suggests ecological dynamics occurring within the nest are an interesting and underappreciated source of phenotypic variation. Our study also supports the view that TSD is an adaptive trait, rather than a neutral trait, by showing consistent associations between phenotype and temperature in wild nests of a TSD reptile.