A complex genomic architecture underlies reproductive isolation in a North American oriole hybrid zone

Abstract

Natural hybrid zones provide powerful opportunities for identifying the mechanisms that facilitate and inhibit speciation. Documenting the extent of genomic admixture allows us to discern the architecture of reproductive isolation through the identification of isolating barriers. This approach is particularly powerful for characterizing the accumulation of isolating barriers in systems exhibiting varying levels of genomic divergence. Here, we use a hybrid zone between two species—the Baltimore (Icterus galbula) and Bullock’s (I. bullockii) orioles—to investigate this architecture of reproductive isolation. We combine whole genome re-sequencing with data from an additional 313 individuals amplityped at ancestry-informative markers to characterize fine-scale patterns of admixture, and to quantify links between genes and the plumage traits. On a genome-wide scale, we document several putative barriers to reproduction, including elevated peaks of divergence above a generally high genomic baseline, a large putative inversion on the Z chromosome, and complex interactions between melanogenesis-pathway candidate genes. Concordant and coincident clines for these different genomic regions further suggest the coupling of pre- and post-mating barriers. Our findings of complex and coupled interactions between pre- and post-mating barriers suggest a relatively rapid accumulation of barriers between these species, and they demonstrate the complexities of the speciation process.