Genomic Evidence for Rare Hybridization and Large Demographic Changes in the Evolutionary Histories of Four North American Dove Species

SIMPLE SUMMARY: Range expansions of invasive species continue to increase due to the direct or indirect influences of humans on global habitats. Understanding how these introductions and invasions increase the potential for interaction and hybridization between colonists and closely related native species is therefore increasingly important. We examine the evolutionary histories and signatures of hybridization among introduced feral Rock Pigeon and Eurasian Collared-Dove and native White-winged and Mourning doves in southwestern North America. Analyzing thousands of genomic markers, we find little evidence that hybridization has been extensive in their evolutionary histories or today. Despite this, evidence from multiple population genetics analyses supports the presence of six putative contemporary late-stage hybrids among the 182 sampled individuals. These putative hybrids all involve the most populous species, the Mourning Dove. We discuss the importance of using multiple marker types when attempting to infer complex evolutionary histories and propose important considerations when analyzing populations that were recently established or of domestic origins. ABSTRACT: Introductions and invasions provide opportunities for interaction and hybridization between colonists and closely related native species. We investigate this phenomenon using the mitochondrial DNA COI and 81,416 base-pairs of overlapping nuclear variation to examine the evolutionary histories and signatures of hybridization among introduced feral Rock Pigeon and Eurasian Collared-Dove and native White-winged and Mourning doves in southwestern North America. First, we report all four species to be highly divergent across loci (overall pair-wise species Φ(ST) range = 0.17–0.70) and provide little evidence for gene flow at evolutionary timescales. Despite this, evidence from multiple population genetics analyses supports the presence of six putative contemporary late-stage hybrids among the 182 sampled individuals. These putative hybrids contain various ancestry combinations, but all involve the most populous species, the Mourning Dove. Next, we use a novel method to reconstruct demographic changes through time using partial genome sequence data. We identify recent, species-specific fluctuations in population size that are likely associated with changing environments since the Miocene and suggest that these fluctuations have influenced the genetic diversity of each dove species in ways that may impact their future persistence. Finally, we discuss the importance of using multiple marker types when attempting to infer complex evolutionary histories and propose important considerations when analyzing populations that were recently established or of domestic origins.