Cryptic and extensive hybridization between ancient lineages of American crows

Abstract

Most species and therefore most hybrid zones have historically been described using phenotypic characters. However, both speciation and hybridization can occur with negligible morphological differentiation. The Northwestern Crow (Corvus caurinus) and American Crow (Corvus brachyrhynchos) are sister taxonomic species with a continuous distribution that lack reliable traditional characters for identification. In this first population genomic study of Northwestern and American crows, we use genomic SNPs (nuDNA) and mtDNA to investigate whether these crows are genetically differentiated and the extent to which they may hybridize. We found that American and Northwestern crows have distinct evolutionary histories, supported by two nuDNA ancestry clusters and two 1.1%-divergent mtDNA clades dating to the late Pleistocene, when glacial advances may have isolated crow populations in separate refugia. We document extensive hybridization, with geographic overlap of mtDNA clades and admixture of nuDNA across >1,400 km of western Washington and western British Columbia. This broad hybrid zone consists of late-generation hybrids and backcrosses, not recent (e.g., F1) hybrids. Nuclear DNA and mtDNA clines were both centered in southwestern British Columbia, farther north than previously postulated. The mtDNA cline was narrower than the nuDNA cline, consistent with Haldanes rule but not sex-biased dispersal. Overall, our results suggest a history of reticulate evolution in American and Northwestern crows, consistent with potentially recurring neutral expansion(s) from Pleistocene glacial refugia followed by lineage fusion(s). However, we do not rule out a contributing role for more recent potential drivers of hybridization, such as expansion into human-modified habitats.