Recombination rate and recurrent linked selection shape correlated genomic landscapes across a continuum of divergence in swallows

Abstract

Disentangling the drivers of genomic divergence during speciation is essential to our broader understanding of the generation of biological diversity. Genetic changes accumulate at variable rates across the genome as populations diverge, leading to heterogenous landscapes of genetic differentiation. The 'islands of differentiation' that characterise these landscapes harbour genetic signatures of the evolutionary processes that led to their formation, providing insight into the roles of these processes in adaptation and speciation. Here, we study swallows in the genus Hirundo to investigate genomic landscapes of differentiation between species spanning a continuum of evolutionary divergence. Genomic differentiation spans a wide range of values (FST = 0.01-0.8) between species, with substantial heterogeneity in genome-wide patterns. Genomic landscapes are strongly correlated among species (ρ = 0.46-0.99), both at shallow and deep evolutionary timescales, with broad evidence for the role of linked selection together with recombination rate in shaping genomic differentiation. Further dissection of genomic islands reveals patterns consistent with a model of 'recurrent selection', wherein differentiation increases due to selection in the same genomic regions in ancestral and descendant populations. Finally, we use measures of the site frequency spectrum to differentiate between alternative forms of selection, providing evidence that genetic hitchhiking due to positive selection has contributed substantially to genomic divergence. Our results demonstrate the pervasive role of recurrent linked selection in shaping genomic divergence despite a history of gene flow and underscore the importance of non-neutral evolutionary processes in predictive frameworks for genomic divergence in speciation genomics studies.