Demography and linked selection interact to shape the genomic landscape of codistributed woodpeckers during the Ice Age.

Abstract

The influence of genetic drift on population dynamics during Pleistocene glacial cycles is well understood, but the role of selection in shaping patterns of genomic variation during these events is less explored. We resequenced whole genomes to investigate how demography and natural selection interact to generate the genomic landscapes of Downy and Hairy Woodpecker, species codistributed in previously glaciated North America. First, we explored the spatial and temporal patterns of genomic diversity produced by neutral evolution. Next, we tested (i) whether levels of nucleotide diversity along the genome are correlated with intrinsic genomic properties, such as recombination rate and gene density, and (ii) whether different demographic trajectories impacted the efficacy of selection. Our results revealed cycles of bottleneck and expansion, and genetic structure associated with glacial refugia. Nucleotide diversity varied widely along the genome, but this variation was highly correlated between the species, suggesting the presence of conserved genomic features. In both taxa, nucleotide diversity was positively correlated with recombination rate and negatively correlated with gene density, suggesting that linked selection played a role in reducing diversity. Despite strong fluctuations in effective population size, the maintenance of relatively large populations during glaciations may have facilitated selection. Under these conditions, we found evidence that the individual demographic trajectory of populations modulated linked selection, with purifying selection being more efficient in removing deleterious alleles in large populations. These results highlight that while genome-wide variation reflects the expected signature of demographic change during climatic perturbations, the interaction of multiple processes produces a predictable and highly heterogeneous genomic landscape.