Ontogenetic complexity of sexual dimorphism and sex-specific selection

Abstract

Sex-biased gene expression is becoming an increasingly important way to study sexual selection at the molecular genetic level. However, little is known about the timing, persistence, and continuity of gene expression required in the creation of distinct male and female phenotypes, and even less about how sex-specific selection pressures shift over the life cycle. Here, we present a time-series global transcription profile for autosomal genes in male and female chicken, beginning with embryonic development and spanning to reproductive maturity, for the gonad. Overall, the amount and magnitude of sex-biased expression increased as a function of age, though sex-biased gene expression was surprisingly ephemeral, with very few genes exhibiting continuous sex bias in both embryonic and adult tissues. Despite a large predicted role of the sex chromosomes in sexual dimorphism, our study indicates that the autosomes house the majority of genes with sex-biased expression. Most interestingly, sex-specific evolutionary pressures shifted over the course of the life cycle, acting equally strongly on female-biased genes and male-biased genes but at different ages. Female-biased genes exhibited high rates of divergence late in embryonic development, shortly before arrested meiosis halts oogenesis. The level of divergence on female-biased late embryonic genes is similar to that seen in male-biased genes expressed in adult gonads, which correlates with the onset of spermatogenesis. These analyses reveal that sex-specific selection pressure varies over the life cycle as a function of male and female biology.