Hybrid Breakdown in Male Reproduction Between Recently-DivergedDrosophila melanogasterPopulations Has a Complex and Variable Genetic Architecture

Abstract

Populations no longer experiencing a sufficient rate of gene flow will accumulate genetic differences over time. One potential consequence of divergence between natural populations is hybrid breakdown, which can occur during secondary contact when untested allelic combinations in hybrids beyond the F1 generation are maladaptive and restrict gene flow. Hybrid breakdown is an important process in the development and maintenance of species boundaries, and has largely been studied between populations that are completely or nearly completely isolated. Here, we leverage the recent worldwide expansion of Drosophila melanogaster to investigate signatures of hybrid breakdown between populations that diverged within approximately the last 13,000 years. We did not find clear evidence for hybrid breakdown in viability or female reproductive performance. In contrast, we found that many but not all between-population crosses yielded an elevated fraction of second generation male offspring that were unable to reproduce. The frequency of non-reproducing F2 males varied among different crosses involving the same southern African and European populations, as did the qualitative effect of cross direction, implying a genetically variable basis of hybrid breakdown and a role for uniparentally inherited factors. The levels of male reproductive failure observed in F2 hybrids were not recapitulated in backcrossed individuals, suggesting the existence of incompatibilities with at least three partners. These results suggest that some of the very first steps toward reproductive isolation may involve incompatibilities with complex and variable genetic architectures, and they support the prediction that hybrid breakdown affects the heterogametic sex first. Collectively, our findings on polymorphic incompatibilities within D. melanogaster emphasize this system's potential for future studies on the genetic and organismal basis of early-stage reproductive isolation.