Recurrent selection and reduction in recombination shape the genomic landscape of divergence across multiple population pairs of Green-backed Tit

Abstract

AbstractSpeciation is fundamental for building and maintaining biodiversity. The formation of the highly differentiated genomic regions between diverging taxa has been interpreted as a result of divergence with gene flow, linked selection, and reduction in recombination. It is challenging to unravel these nonexclusive processes in shaping genomic divergence. Here, we investigate the relative roles of these processes in shaping genomic differentiation in a montane bird, the Green-backed Tit (Parus monticolus). Our genetic structure and demographic analyses identify that four genetic lineages diverge between 838 and 113 thousand years ago and there is evidence of secondary gene flow. The highly divergent genomic regions do not increase with the divergence time, as we found that the old lineages show relatively fewer numbers and smaller sizes of highly differentiated regions than the young divergent lineages (numbers, 118–138 vs. 156–289; sizes, 5.9–6.9 vs. 7.8–14.5 megabase). Across the genome, the outlier windows show a reduction in nucleotide diversity, absolute genetic divergence, and recombination rate, suggesting recurrent selection in regions with low recombination being the major driver of genomic divergence. Finally, we show that secondary gene flow tends to affect the highly differentiated genomic regions if these regions are less likely to be the targets of selection. Altogether, our study shows how common ancestry, recurrent selection, low recombination rate, and gene flow have contributed to the emergence of genomic islands at different stages of speciation.