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

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
used resequenced whole genomes to investigate how demography and natural
selection interact to generate the genomic landscapes of Downy and Hairy
Woodpeckers, species co-distributed in previously glaciated North America.
First, we explored the spatial and temporal patterns of genomic diversity
produced by neutral evolution. Next, we tested (1) whether levels of
nucleotide diversity along the genome are correlated with intrinsic
genomic properties, such as recombination rate and gene density, and (2)
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.