Beringia as a high-latitude engine of avian speciation.

Beringia is a biogeographically dynamic region that extends from northeastern Asia into northwestern North America. This region has affected avian divergence and speciation in three important ways: (i) by serving as a route for intercontinental colonisation between Asia and the Americas; (ii) by cyclically splitting (and often reuniting) populations, subspecies, and species between these continents; and (iii) by providing isolated refugia through glacial cycles. The effects of these processes can be seen in taxonomic splits of shallow to increasing depths and in the presence of regional endemics. We review the taxa involved in the latter two processes (splitting-reuniting and isolation), with a focus on three research topics: avian diversity, time estimates of the generation of that diversity, and the regions within Beringia that might have been especially important. We find that these processes have generated substantial amounts of avian diversity, including 49 pairs of avian subspecies or species whose breeding distributions largely replace one another across the divide between the Old World and the New World in Beringia, and 103 avian species and subspecies endemic to this region. Among endemics, about one in three is recognised as a full biological species. Endemic taxa in the orders Charadriiformes (shorebirds, alcids, gulls, and terns) and Passeriformes (perching birds) are particularly well represented, although they show very different levels of diversity through evolutionary time. Endemic Beringian Charadriiformes have a 1.31:1 ratio of species to subspecies. In Passeriformes, endemic taxa have a 0.09:1 species-to-subspecies ratio, suggesting that passerine (and thus terrestrial) endemism might be more prone to long-term extinction in this region, although such 'losses' could occur through their being reconnected with wider continental populations during favourable climatic cycles (e.g. subspecies reintegration with other populations). Genetic evidence suggests that most Beringian avian taxa originated over the past 3 million years, confirming the importance of Quaternary processes. There seems to be no obvious clustering in their formation through time, although there might be temporal gaps with lower rates of diversity generation. For at least 62 species, taxonomically undifferentiated populations occupy this region, providing ample potential for future evolutionary diversification.

The genetic basis of plumage coloration and elevation adaptation in a clade of recently diverged alpine and arctic songbirds.

Trait genetic architecture plays an important role in the probability that variation in that trait leads to divergence and speciation. In some cases, speciation may be driven by the generation of novel phenotypes through the recombination of genes associated with traits that are important for local adaptation or sexual selection. Here, we investigate the genetic basis of three plumage color traits, and one ecological trait, breeding elevation, in a recent avian radiation, the North American rosy-finches (Leucosticte spp.). We identify unique genomic regions associated with each trait and highlight 11 candidate genes. Among these are well-characterized melanogenesis genes, including Mitf and Tyrp1, and previously reported hypoxia-related genes including Egln1. Additionally, we use mitochondrial data to date the divergence of rosy-finch clades which appear to have diverged within the past 250 ky. Given the low levels of genome-wide differentiation among rosy-finch taxa, and evidence for extensive introgression in North America, plumage coloration and adaptation to high elevations have likely played large roles in generating the observed patterns of lineage divergence. The relative independence of these candidate regions across the genome suggests that recombination might have led to multiple phenotypes, and subsequent rosy-finch speciation, over short periods of time.

Phylogenomic Data Reveal Widespread Introgression Across the Range of an Alpine and Arctic Specialist.

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.].