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Abstract New study systems and tools are needed to understand how divergence and speciation occur between lineages with gene flow. Migratory birds often exhibit divergence despite seasonal migration, which brings populations into contact with one another. We studied divergence between 2 subspecies of Northern Saw-whet Owl (Aegolius acadicus), in which a sedentary population on the islands of Haida Gwaii, British Columbia (A. a. brooksi), exists in the presence of the other form (A. a. acadicus) during migration but not during the breeding season. Prior research showed fixed mtDNA divergence but left open the question of nuclear gene flow. We used 2,517 ultraconserved element loci to examine the demographic history of this young taxon pair. Although we did not observe fixed single nucleotide polymorphism differences between populations among our genotyped individuals, 100% of the birds were diagnosable and δaδI analyses suggested the demographic model best fitting the data was one of split-bidirectional-migration (i.e. speciation with gene flow). We dated the split between brooksi and acadicus to ~278 Kya, and our analyses suggested gene flow between groups was skewed, with ~0.7 individuals per generation coming from acadicus into brooksi and ~4.4 going the opposite direction. Coupled with an absence of evidence of phenotypic hybrids and the birds’ natural history, these data suggest brooksi may be a young biological species arising despite historic gene flow. 

Abstract Understanding how gene flow affects population divergence and speciation remains challenging. Differentiating one evolutionary process from another can be difficult because multiple processes can produce similar patterns, and more than one process can occur simultaneously. Although simple population models produce predictable results, how these processes balance in taxa with patchy distributions and complicated natural histories is less certain. These types of populations might be highly connected through migration (gene flow), but can experience stronger effects of genetic drift and inbreeding, or localized selection. Although different signals can be difficult to separate, the application of high-throughput sequence data can provide the resolution necessary to distinguish many of these processes. We present whole-genome sequence data for an avian species group with an alpine and arctic tundra distribution to examine the role that different population genetic processes have played in their evolutionary history. Rosy-finches inhabit high elevation mountaintop sky islands and high-latitude island and continental tundra. They exhibit extensive plumage variation coupled with low levels of genetic variation. Additionally, the number of species within the complex is debated, making them excellent for studying the forces involved in the process of diversification, as well as an important species group in which to investigate species boundaries. Total genomic variation suggests a broadly continuous pattern of allele frequency changes across the mainland taxa of this group in North America. However, phylogenomic analyses recover multiple distinct, well supported, groups that coincide with previously described morphological variation and current species-level taxonomy. Tests of introgression using D-statistics and approximate Bayesian computation reveal significant levels of introgression between multiple North American taxa. These results provide insight into the balance between divergent and homogenizing population genetic processes and highlight remaining challenges in interpreting conflict between different types of analytical approaches with whole-genome sequence data. [ABBA-BABA; approximate Bayesian computation; gene flow; phylogenomics; speciation; whole-genome sequencing.]