Evidence for ancient selective sweeps followed by differentiation among three species of Sphyrapicus sapsuckers.

Genomic differentiation usually accompanies speciation, but that differentiation is often highly heterogeneous across the genome. Understanding what parts of the genome are more prone to differentiation can inform us about genomic regions and evolutionary processes that may be central to the speciation process. Here, we study genomic variation among three hybridizing species of North American woodpecker: red-breasted, red-naped, and yellow-bellied sapsuckers (Sphyrapicus ruber, S. nuchalis, and S. varius). We use whole genome resequencing to measure genetic variation among these species and to quantify how the level of differentiation varies across the genome. We find that regions of high relative differentiation between species (FST) tend to have low absolute differentiation between species (πB), indicating that regions of high relative differentiation often have more recent between-population coalescence times than regions of low relative differentiation do. Most of the high-FST genomic windows are found on the Z chromosome, pointing to this sex chromosome as being particularly important in sapsucker differentiation and potentially speciation. These results are consistent with a model of speciation in which selective sweeps of globally advantageous variants spread among partly differentiated populations, followed by differential local adaptation of those same genomic regions. We propose that sapsucker speciation may have occurred primarily via this process occurring on the Z chromosomes, resulting in genetic incompatibilities involving divergent Z chromosomes.