A complex evolutionary history of genetic barriers to gene flow in hybridizing warblers

The Setophaga warbler sister species in western North America, Setophaga occidentalis and S. townsendi provide a rare opportunity to explore how the accumulation of genetic barriers to gene flow contributes to speciation. These sister species are at the very early stages of speciation, as their genome-wide divergence is limited, and they hybridize extensively upon secondary contact. However, there are several well-characterized loci involved in speciation. There is a plumage difference between the species controlled by mutations close to the agouti signaling protein (ASIP), which generates underdominance due to compromised hybrid territorial signaling. A second large region (~2Mb) on chromosome 5 encodes many mitochondrial-interacting genes and coevolves with the mitochondrial genome. Here we reconstructed the ancestral recombination graphs of these genomic regions relative to the genome-wide background to learn about the evolutionary history of these barriers. We find signatures of long-lasting barrier effects that lasted for ~190 K generations, and recent selective sweeps in chr5 mitonuclear genetic block in both species within the past 60 K generations ago. We further observed heterogeneity within the long-lasting mitonuclear barrier with localized signals of much more recent selective sweeps unique one of the species. The divergence of ASIP is elevated by a species-specific selective sweep within S. occidentalis that occurred 21 K generations ago. However, the signature of long-lasting barrier effect is much weaker at ASIP suggesting that it may have arisen later than the mitonuclear system. Associating the evolutionary history of these genetic barriers with Pleistocene climate change history sheds light on the intrinsic and extrinsic reciprocity underlying the origin of species.