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Environmental conditions influence the maternal deposition of hormones into eggs, which is hypothesized to adaptively modify developmental outcomes in offspring. However, most ecosystems harbour environmental contaminants capable of disrupting endocrine signaling, and maternal exposure to these compounds has the potential to further alter offspring traits. Studies rarely examine maternally derived hormones and contaminants along with offspring phenotypes, and we know little about their interrelationships and potential interactions. Here, we measure yolk concentrations of 24 endocrine-disrupting compounds (EDCs) and 28 steroid hormones along with gonadal transcriptomes from two populations of the American alligator ( Alligator mississippiensis ) that differ in reproductive development and exposure to EDCs. Using a network-based approach, we identify gene expression modules associated with hormones and contaminants independently, in combination, or by potential indirect influences of EDCs on maternal hormone deposition. We find that yolk concentrations of both 17β-oestradiol and etiocholanolone differ across populations and explain substantial variation in gene expression. We further provide evidence for the indirect effect of the pesticide, methoxychlor, on gonadal gene expression through its relationship with 17β-oestradiol. Our results reveal novel pathways by which maternal exposure to environmental contaminants interacts with hormone provisioning to affect offspring sexual development.

Maternal provisioning and the developmental environment are fundamental determinants of offspring traits, particularly in oviparous species. However, the extent to which embryonic responses to these factors differ across populations to drive phenotypic variation is not well understood. Here, we examine the contributions of maternal provisioning and incubation temperature to hatchling morphological and metabolic traits across four populations of the American alligator ( Alligator mississippiensis ), encompassing a large portion of the species' latitudinal range. Our results show that whereas the influence of egg mass is generally consistent across populations, responses to incubation temperature show population-level variation in several traits, including mass, head length, head width, and residual yolk mass. Additionally, the influence of incubation temperature on developmental rate is greater at northern populations, while the allocation of maternal resources toward fat body mass is greater at southern populations. Overall, our results suggest that responses to incubation temperature, relative to maternal provisioning, are a larger source of interpopulation phenotypic variation and may contribute to the local adaptation of populations., Competing Interests: Authors declare no competing interests., (© 2024 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.)