Introgression and divergence in a young species group

Abstract

The process of speciation concerns often not only pairs of species but rather groups of diverging and interacting taxa, as highlighted by recent research. Hence, to understand the evolution of species diversity and their persistence, it is crucial to understand how gene flow and evolution of reproductive isolation shape groups of closely related species. Using resequencing data, we disentangle here genomic patterns of divergence and introgression in five Formica rufa group wood ant species that are at the early stage of speciation. We first revise earlier mitochondrial phylogenies with a nuclear genomic tree, and demonstrate then introgression that is in line with observations of their current day natural hybridisation. Investigating the genome-wide differentiation and divergence we find correlations between population genetic parameters of divergence, differentiation, and diversity, that are in line with theoretical expectations for young species. Despite previously found evidence for polygenic species barriers, our data lacks the genome-wide correlation between differentiation and divergence that would be expected under a model of polygenic barriers. The likely explanation for this lack is the dominating effect of ancestral diversity at these early stages of speciation. As hybridisation has led to both deleterious and adaptive consequences within the group, we examined the signatures of introgression. We find no strong positive correlation between introgression and recombination, suggesting introgression does not have a predominantly deleterious effect. We also infer low diversity in the genomic regions with high proportions of introgression, consistent with the idea that selection has locally favoured introgression. This could be due to sharing of adaptive alleles or reduction of genetic load in the receiving species. Interestingly, gene flow in this group could potentially cross multiple species boundaries even in the absence of direct interbreeding between all the species. We discuss the long-term benefits and costs of introgression in young species, including the effect of environmental fluctuations and multi-species introgression.