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 colonization 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 recognized 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 favorable 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.

Winker, K., J. Withrow, D. D. Gibson, and C. L. Pruett. 2023. Beringia as a high-latitude engine of avian speciation. Biological Reviews 98:1081-1099.
https://doi: 10.1111/brv.12945

Ducks show different modes of speciation and pose avian influenza risks

The processes leading to divergence and speciation can differ broadly among taxa with different life histories. We examined these processes in the Green-winged Teal (Anas crecca) complex, a Holarctic species with three subspecies (Anas crecca crecca, A. c. nimia, and A. c. carolinensis) with a close relative, the Yellow-billed Teal (Anas flavirostris) from South America. A. c. crecca and A. c. carolinensis are seasonal migrants, while the other taxa are sedentary. We examined divergence and speciation patterns in this group, determining their phylogenetic relationships and the presence and levels of gene flow among lineages using both mitochondrial and genome-wide nuclear DNA obtained from 1,393 ultraconserved element (UCE) loci. Phylogenetic relationships using nuclear DNA showed A. c. crecca, A. c. nimia, and A. c. carolinensis clustering together to form one polytomous clade, with A. flavirostris sister to this clade. This relationship can be summarized as (crecca, nimia, carolinensis)(flavirostris). However, whole mitogenomes revealed a different phylogeny: (crecca, nimia)(carolinensis, flavirostris). The best demographic model for key pairwise comparisons supported divergence with gene flow as the probable speciation mechanism in all three contrasts (crecca−nimia, crecca−carolinensis, and carolinensis−flavirostris). Given prior work, gene flow was expected among the Holarctic taxa, but gene flow between North American carolinensis and South American flavirostris (M ~0.1–0.4 individuals/generation), albeit low, was not expected. Three geographically oriented modes of divergence are likely involved in the diversification of this complex: heteropatric (crecca−nimia), parapatric (crecca−carolinensis), and (mostly) allopatric (carolinensis−flavirostris).

Avian influenza (AI) is a zoonotic disease that will likely be involved in future pandemics. Because waterbird movements are difficult to quantify, determining the host-specific risk of Eurasian-origin AI movements into North America is challenging. We estimated relative rates of movements, based on long-term evolutionary averages of gene flow, between Eurasian and North American waterbird populations to obtain bidirectional baseline rates of the intercontinental movements of these AI hosts. We used population genomics and coalescent-based demographic models to obtain these gene-flow–based movement estimates. Inferred rates of movement between these continental populations varies greatly among species. Within dabbling ducks, gene flow, relative to effective population size, varies from ~3 to 24 individuals/generation between Eurasian and American wigeons (Mareca penelope and M. americana) to ~100–300 individuals/generation between continental populations of Northern Pintails (Anas acuta). These are evolutionary long-term averages and provide a solid foundation for understanding the relative risks of each of these host species in potential intercontinental AI movements. We scale these values to census size for evaluation in that context. In addition to being AI hosts, many of these bird species are also important in the subsistence diets of Alaskans, increasing the risk of direct bird-to-human exposure to Eurasian-origin AI virus. We contrast species-specific rates of intercontinental movements with the importance of each species in Alaskan diets to understand the relative risk of these taxa to humans. Assuming roughly equivalent AI infection rates among ducks, Greater Scaup (Aythya marila), Mallard (Anas platyrhynchos), and Northern Pintail (Anas acuta) were the top three species presenting the highest risks for intercontinental AI movement both within the natural system and through exposure to subsistence hunters. Improved data on AI infection rates in this region could further refine these relative risk assessments. These directly comparable, species-based intercontinental movement rates and relative risk rankings should help in modeling, monitoring, and mitigating the impacts of intercontinental host and AI movements.

Spaulding, F. R., J. F. McLaughlin, K. G. McCracken, T. C. Glenn, and K. Winker. 2023. Population genomics indicate three different modes of divergence and speciation with gene flow in the green-winged teal duck complex. Molecular Phylogenetics and Evolution 182:107733.
https://doi.org/10.1016/j.ympev.2023.107733

Spaulding, F. R., J. F. McLaughlin, T. C. Glenn, and K. Winker. 2022. Estimating movement rates between Eurasian and North American birds that are vectors of avian influenza (AI). Avian Diseases 66:155-164. https://doi.org/10.1637/aviandiseases-D-21-00088

An Overview of Speciation and Species Limits in Birds

Accurately determining avian species limits has been a challenge and a work in progress for most of a century. It is a fascinating but difficult problem. Under the biological species concept, only lineages that remain essentially independent when they are in sympatry are clearly species. Otherwise, there is no clear line yet found that marks when a pair of diverging lineages, e.g., in allopatry, become different enough to warrant full biological species status. Also, with more data, species limits often require re-evaluation. The process of divergence and speciation is itself very complex and is the focus of intense research. Translating what we understand of that process into taxonomic names can be challenging. A series of issues are important. Single-locus criteria are unlikely to be convincing. Genetic independence is not a species limits requirement, but the degree of independence (gene flow) needs to be considered when there is opportunity for gene flow and independence is not complete. Time-based species (limits determined by time of separation) are unsatisfactory, though integrating time more effectively into our datasets is warranted. We need to disentangle data signal due to neutral processes versus selection and prioritize the latter as the main driver of speciation. Assortative mating is also not likely to be an adequate criterion for determining species limits. Hybridization and gene flow are more important than ever, and there is a condition not being treated evenly in taxonomy: evolutionary trysts of two or more lineages stuck together through gene flow just short of speciation over long periods. Comparative methods that use what occurs between good species in contact to infer species limits among allopatric forms remain the gold standard, but they can be inaccurate and controversial. Species-level taxonomy in birds is likely to remain unsettled for some time. While the study of avian speciation has never been more exciting and dynamic, there is no silver bullet for species delimitation, nor is it likely that there will ever be one. Careful work using integrative taxonomy in a comparative framework is the most promising way forward.

Winker, K. 2021. An overview of speciation and species limits in birds. Ornithology 138: ukab006 1-27.

Demographic Consequences of Foraging Ecology Explain Genetic Diversification in Neotropical Birds

Comparisons of divergence among 58 lineages of Middle American birds reveal that diet is the most important driver, with insectivore and mixed-diet populations diverging more than plant-dependent species (mostly fugivores and nectivores). We propose and test a model for why this occurs and find support for dispersal and demographic expansion periodically reuniting plant-dependent species across this geographic space. Thus, local ecological and demographic factors here scale up to macroevolutionary phenomena.

Miller, M. J., E. Bermingham, B. L. Turner, S. E. Lipshutz, J. C. Touchon, A. B. Johnson, and K. Winker. 2021. Demographic consequences of foraging ecology explain genetic diversification in Neotropical bird species. Ecology Letters In press. https://doi.org/10.1111/ele.13674


Population Genomics of Trans-Beringian Birds

Contrasts of UCE-based genomic estimates of divergence and demographic processes in co-distributed high-latitude taxa having divergence levels from populations to full species show that gene flow is a predominant factor in avian speciation in this region. In addition, these taxa are discontinuously distributed on the speciation continuum, showing two clusters in a divergence space defined by FST and gene flow.

McLaughlin, J. F., B. C. Faircloth, T. C. Glenn, and K. Winker. 2020. Divergence, gene flow, and speciation in eight lineages of trans-Beringian birds. Molecular Ecology 29: 3526-3542. https://doi.org/10.1111/mec.15574 .


Sample Size Effects on Population Demographic Estimates in Birds using Ultraconserved Elements (UCEs)

Sample size is a critical aspect of study design in population genomics research, yet few empirical studies have examined the impacts of small sample sizes. We used datasets from eight diverging bird lineages to make pairwise comparisons at different levels of taxonomic divergence (populations, subspecies, and species). Our data are from loci linked to ultraconserved elements and our analyses used one single nucleotide polymorphism per locus. All individuals were genotyped at all loci, effectively doubling sample size for coalescent analyses. We estimated population demographic parameters (effective population size, migration rate, and time since divergence) in a coalescent framework using Diffusion Approximation for Demographic Inference, an allele frequency spectrum method. Using divergencewith-gene-flow models optimized with full datasets, we subsampled at sequentially
smaller sample sizes from full datasets of 6–8 diploid individuals per population (with both alleles called) down to 1:1, and then we compared estimates and their changes in accuracy. Accuracy was strongly affected by sample size, with considerable differences among estimated parameters and among lineages. Effective population size parameters (ν) tended to be underestimated at low sample sizes (fewer than three diploid individuals per population, or 6:6 haplotypes in coalescent terms). Migration (m) was fairly consistently estimated until <2 individuals per population, and no consistent trend of over-or underestimation was found in either time since divergence (T) or theta (Θ = 4Nrefm). Lineages that were taxonomically recognized above the population level (subspecies and species pairs; that is, deeper divergences) tended to have lower variation in scaled root mean square error of parameter estimation at smaller sample sizes than population-level divergences, and many parameters were estimated accurately down to three diploid individuals per population. Shallower divergence levels (i.e., populations) often required at least five individuals per population for reliable demographic inferences using this approach. Although divergence levels might be unknown at the outset of study design, our results provide a framework for planning appropriate sampling and for interpreting results if smaller sample sizes must be used.

McLaughlin, J. F., and K. Winker. 2020. An empirical examination of sample size effects on population demographic estimates in birds using single nucleotide polymorphism (SNP) data. PeerJ 8:e9939 DOI 10.7717/peerj.9939

Ooooh, shiny!

It’s finally time to update my web site. It was looking pretty dated (but it loaded fast and delivered information effectively to people with low bandwidth). I’ll keep up the details on the “Old School” page. Just use your browser’s search function there to find what you want. I’ll peck away at bringing other attributes to bear over time.