Sexual interactions and local selection shape reproductive gene diversity and divergence

Genes involved in genotype x genotype coevolution display unique patterns of nucleotide diversity and population divergence. In Drosophila melanogaster, Sex Peptide is a key sperm competition gene that is an outlier for both pi within populations and Fst between populations. This pattern is not predicted by current theoretical expectations of selective sweeps highlighting the need to develop predictions to identify genes experiencing balancing selection. We compared pi and FST in D. melanogaster populations to identify other genes following a co-evolutionary model that generates divergence and diversity. Multiple male and female genes that interact with Sex Peptide exhibited elevated FST x pi values. Genome-wide analyses also revealed an enrichment of genes critical for neuronal development, pointing to courtship evolution. Specifically, fruitless, its interacting genes, and a female behavior gene were identified as outliers. These parallel findings indicate that both sperm competition and mating behaviors are subject to co-evolutionary selection.