It is increasingly recognized that sex chromosomes are not only the battlegrounds between sexes but also the Great Walls fencing off introgression between diverging lineages

Neo-sex chromosome evolution shapes sex-dependent asymmetrical introgression barrier. Silu Wang et al. xxx, May 5, 2022 | 119 (19) e2119382119 | https://doi.org/10.1073/pnas.2119382119

Significance: It is increasingly recognized that sex chromosomes are not only the battlegrounds between sexes but also the Great Walls fencing off introgression between diverging lineages. Here we dissect the multifaceted roles of sex chromosomes using experimental evolution, whole-genome resequencing, and theoretical modeling, taking advantage of hybrid populations between a Drosophila sister species pair in the early stage of speciation that have different sex chromosome systems. Our work sheds light onto the complex roles of neo-sex chromosome evolution in creating a sex-dependent asymmetrical introgression barrier at a species boundary, and we show how diverse population genetic forces act in concert to explain observed patterns of introgression across the genome.

Abstract: Sex chromosomes play a special role in the evolution of reproductive barriers between species. Here we describe conflicting roles of nascent sex chromosomes on patterns of introgression in an experimental hybrid swarm. Drosophila nasuta and Drosophila albomicans are recently diverged, fully fertile sister species that have different sex chromosome systems. The fusion between an autosome (Muller CD) with the ancestral X and Y gave rise to neo-sex chromosomes in D. albomicans, while Muller CD remains unfused in D. nasuta. We found that a large block containing overlapping inversions on the neo-sex chromosome stood out as the strongest barrier to introgression. Intriguingly, the neo-sex chromosome introgression barrier is asymmetrical and sex-dependent. Female hybrids showed significant D. albomicans–biased introgression on Muller CD (neo-X excess), while males showed heterosis with excessive (neo-X, D. nasuta Muller CD) genotypes. We used a population genetic model to dissect the interplay of sex chromosome drive, heterospecific pairing incompatibility between the neo-sex chromosomes and unfused Muller CD, neo-Y disadvantage, and neo-X advantage in generating the observed sex chromosome genotypes in females and males. We show that moderate neo-Y disadvantage and D. albomicans specific meiotic drive are required to observe female-specific D. albomicans–biased introgression in this system, together with pairing incompatibility and neo-X advantage. In conclusion, this hybrid swarm between a young species pair sheds light onto the multifaceted roles of neo-sex chromosomes in a sex-dependent asymmetrical introgression barrier at a species boundary.