Maternal social environment shapes yolk testosterone allocation and embryonic neural gene expression in tree swallows

Abstract

Offspring from females breeding in competitive social environments are often exposed to more testosterone (T) during embryonic development, which can affect traits from growth to behavior in potentially adaptive ways. Despite the important role of maternally derived steroids in shaping offspring development, the molecular mechanisms driving these processes are currently unclear. Here, we use tree swallows (Tachycineta bicolor) to explore the effects of the maternal social environment on yolk T concentrations and genome-wide patterns of neural gene expression in embryos. We measured aggressive interactions among females breeding at variable densities and collected their eggs at two timepoints, including the day laid to measure yolk T concentrations and on embryonic day 11 to measure gene expression in whole brain samples. We found that females breeding in high-density sites experienced elevated rates of physical aggression and their eggs had higher yolk T concentrations. A differential gene expression and weighted gene co-expression network analysis indicated that embryos from high-density sites experienced an upregulation of genes involved in hormone, circulatory, and immune processes, and these gene expression patterns were correlated with yolk T levels and aggression. Genes implicated in neural development were additionally downregulated in embryos from high-density sites. These data highlight how early neurogenomic processes may be affected by the maternal social environment, giving rise to phenotypic plasticity in offspring.