Instability of natural selection at candidate barrier loci underlying speciation in wood ants

Abstract

Speciation underlies the generation of novel biodiversity. Yet, there is much to learn about how natural selection shapes genomes during speciation. Selection is assumed to act against gene flow at barrier loci, promoting reproductive isolation. However, evidence for gene flow and selection is often indirect and we know very little about the temporal stability of barrier loci. Here we utilize haplodiploidy to identify candidate male barrier loci in hybrids between two wood ant species. As ant males are haploid, they are expected to reveal recessive barrier loci, which can be masked in diploid females if heterozygous. We then test for barrier stability in a sample collected 10 years later and use survival analysis to provide a direct measure of natural selection acting on candidate male barrier loci. We find multiple candidate male barrier loci scattered throughout the genome. Surprisingly, a proportion of them are not stable after 10 years, natural selection apparently switching from acting against to favouring introgression in the later sample. Instability of the barrier effect and natural selection for introgressed alleles could be due to environment‐dependent selection, emphasizing the need to consider temporal variation in the strength of natural selection and the stability of the barrier effect at putative barrier loci in future speciation work.

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