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 (creccanimia, creccacarolinensis, and carolinensisflavirostris). 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