Evidence for a chromosomal inversion maintaining divergent plumage phenotypes between extensively hybridizing yellowhammers (Emberiza citrinella) and pine buntings (E. leucocephalos)

Abstract

In an allopatric speciation model, populations of a species become isolated by a geographic barrier and develop reproductive isolation through genetic differentiation. When populations meet in secondary contact, the strength of evolved reproductive barriers determines the extent of hybridization and whether the populations will continue to diverge or merge back together. The yellowhammer (Emberiza citrinella) and pine bunting (E. leucocephalos) are avian sister species that diverged in allopatry during the Pleistocene glaciations. Though they differ greatly in plumage and form distinct genetic clusters in allopatry, these taxa show negligible mitochondrial DNA differentiation and hybridize extensively in sympatry lending uncertainty to the state of reproductive isolation in the system. To assess the strength of reproductive barriers between taxa, we examined genomic differentiation across the yellowhammer and pine bunting system. We found that extensive admixture has occurred in sympatry, indicating that reproductive barriers between taxa are weak. We also identified a putative Z chromosome inversion that underlies plumage variation in the system, with the "pine bunting" inversion form showing dominance over the "yellowhammer" form. Our results suggest that yellowhammers and pine buntings are currently at a crossroads and that evolutionary forces may push this system towards either continued differentiation or population merging. However, even if these taxa merge, recombination suppression between chromosome Z inversion forms may maintain divergent plumage phenotypes within the system. In this way, our findings highlight the important role hybridization plays in increasing the genetic and phenotypic variation as well as the evolvability of a system.