Maternal deposition of hormones and contaminants shape the gonadal transcriptome in American alligators

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.