Recurrent selection shapes the genomic landscape of differentiation between a pair of host-specialized haplodiploids that diverged with gene flow

Understanding the genetics of adaptation and speciation is critical for a
complete picture of how biodiversity is generated and maintained.
Heterogeneous genomic differentiation between diverging taxa is commonly
documented, with genomic regions of high differentiation interpreted as
resulting from differential gene flow, linked selection, and reduced
recombination rates. Disentangling the roles of each of these
non-exclusive processes in shaping genome-wide patterns of divergence is
challenging but will enhance our knowledge of the repeatability of genomic
landscapes across taxa. Here, we combine whole-genome resequencing and
genome feature data to investigate the processes shaping the genomic
landscape of differentiation for a sister-species pair of haplodiploid
pine sawflies, Neodiprion lecontei and Neodiprion pinetum. We find
genome-wide correlations between genome features and summary statistics
are consistent with pervasive linked selection, with patterns of diversity
and divergence more consistently predicted by exon density and
recombination rate than the neutral mutation rate (approximated by dS). We
also find that both global and local patterns of FST, dXY, and π provide
strong support for recurrent selection as the primary selective process
shaping variation across pine sawfly genomes, with some contribution from
balancing selection and lineage-specific linked selection. Because
inheritance patterns for haplodiploid genomes are analogous to those of
sex chromosomes, we hypothesize that haplodiploids may be especially prone
to recurrent selection, even if gene flow occurred throughout divergence.
Overall, our study helps fill an important taxonomic gap in the genomic
landscape literature and contributes to our understanding of the processes
that shape genome-wide patterns of genetic variation.