Selection on a pleiotropic color gene block underpins early differentiation between two warbler species

Abstract

When one species gradually splits into two, divergent selection on specific traits can cause peaks of differentiation in the genomic regions encoding those traits. Whether speciation is initiated by strong selection on a few genomic regions with large effects or by more diffused selection on many regions with small effects remains controversial. Differentiated phenotypes between differentiating lineages are commonly involved in reproductive isolation, thus their genetic underpinnings are key to the genomics architecture of speciation. When two species hybridize, recombination over multiple generations can help reveal the genetic regions responsible for the differentiated phenotypes against a genomic background that has been homogenized via backcrossing and introgression. We used admixture mapping to investigate genomic differentiation and the genetic basis of differentiated plumage features (relative melanin and carotenoid pigment) between hybridizing sister species in the early stage of speciation: Townsends (Setophaga townsendi) and Hermit warblers (S. occidentalis). We found a few narrow and dispersed divergent regions between allopatric parental populations, consistent with the divergence with gene flow model of speciation. One of the divergent peaks involves three genes known to affect pigmentation: ASIP, EIF2S2, and RALY (the ASIP-RALY gene block). After controlling for population substructure, we found that a single nucleotide polymorphism (SNP) inside the intron of RALY displays a strong pleiotropic association with cheek, crown, and breast coloration. In addition, we detect selection on the ASIP-RALY gene block, as the geographic cline of the RALY marker of this gene block has remained narrower than the plumage cline, which remained narrower than expected under neutral diffusion over two decades. Despite extensive gene flow between these species across much of the genome, the selection on ASIP-RALY gene block maintains stable genotypic and plumage difference between species allowing further differentiation to accumulate via linkage to its flanking genetic region or linkage-disequilibrium genome-wide.