Sex and breeding stage differences in neurogenomic profiles reflect hormone signaling in a socially polyandrous shorebird

Abstract

In sex-role reversed species, females are socially polyandrous and compete for multiple mates, whereas males conduct the majority of parental care. To understand the extent to which physiological differences between females and males are shaped by sex roles, we examined sex differences in gene expression in sex-role reversed northern jacanas (Jacana spinosa). Given that females compete for mating opportunities, and males cycle between courtship and parental care, we predicted that transcriptomic profiles would be more similar between females and courting males, in contrast to female and parenting males. Leveraging a high quality de novo genome assembly, we conducted RNA-seq on two brain regions associated with the regulation of social behavior: the preoptic area of the hypothalamus and the nucleus taeniae. The majority of genes differentially expressed between the sexes were male-biased. Of these male-biased genes, the majority were located on the Z-chromosome. Contrary to our prediction, the greatest difference in autosomal gene expression was between females and courting males, in the preoptic area of the hypothalamus. Several differentially expressed genes related to elements of hormone signaling that are likely to be behaviorally salient, including higher expression of androgen receptor in females relative to parenting males, and higher expression of prolactin receptor in males, regardless of breeding stage. Some sex-associated gene networks were also associated with competitive traits, whereas others were associated with aggressive behaviors, regardless of sex. Few genes were differentially expressed between courting and parenting males, yet some nonetheless had connections to behavioral endocrinology, including prolactin, thyroid and insulin-like growth factor pathways. Our investigation of sex differences in gene expression can help to reveal the molecular mechanisms underlying female competition and male parental care in socially polyandrous species. We conclude that social polyandry is not a simple reversal in the direction of sex-biased gene expression in the brain, but rather a result of complex genetic and hormonal interactions that warrants further study.