Identification of hybrid male-sterility genes in sibling species of Drosophila

Hybrid male sterility (HMS) is a common postzygotic reproductive barrier caused by intrinsic incompatibilities between genes that have undergone functional divergence in isolated subpopulations. To understand how genomic incompatibilities relate to postzygotic isolation as well as the molecular nature and epistatic effects of genes driving HMS, we have studied two recently diverged fruitfly species, the cosmopolitan Drosophila simulans and the island-endemic D. mauritiana, for which interspecific matings conform to the Haldane’s rule in producing sterile F1 hybrid males. To complement introgression genetic mapping, we analyzed fertility in transgenic organisms to identify the genetic factors responsible for male sterility in a small 20-kb autosomal region in chromosome 3R denoted region HMS1. Whereas hybrid SimB fruitfly males homozygous for D. mauritiana at HMS1 are typically sterile, we find that, on average, 58% males in all agt-sim-transformed and 45% males in all TAF1-sim-transformed hybrid lines have fertility in the normal range. Our results emphasize the highly polygenic nature of postzygotic reproductive isolation. The findings also indicate that the evolutionary basis of HMS1 likely results from the passive accumulation of functional divergence in the agtmau and TAF1mau alleles leading to negative epistatic incompatibilities affecting male sterility in the hybrid background.