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.

Heteropatric speciation in a duck, Anas crecca.

Heteropatric differentiation is a mode of speciation with gene flow in which divergence occurs between lineages that are in sympatry and allopatry at different times during cyclic spatial movements. Empirical evidence suggests that heteropatric differentiation may prove to be common among seasonally migratory organisms. We examined genetic differentiation between the sedentary Aleutian Islands population of green-winged teal (Anas crecca-nimia) and its close migratory relative, the Eurasian, or Old World (OW), Anas c. crecca population, a portion of which passes through the range of nimia during its seasonal migrations. We also examined its relationship with the parapatric North American, New World (NW), A. c. carolinensis population. Sequence data from eight nuclear introns and the mtDNA control region showed that the nimia-crecca divergence occurred much more recently than the deeper crecca-carolinensis split (~83 000 years vs. ~1.1 Myr). Despite considerable spatial overlap between crecca and nimia during seasonal migration, three key predictions of heteropatric differentiation are supported: significant genetic divergence (overall mean Φst  = 0.07), low gene flow (2Ne m ~ 1.8), and an effective population size in nimia that is not especially low (Ne  ~ 80 000 individuals). Similar levels of gene flow have come into nimia from carolinensis, but no detectable nuclear gene flow has gone out of nimia into either OW (crecca) or NW (carolinensis) populations. We infer that adaptations of these populations to local optima in different places (e.g. each matching their reproductive effort to different resource blooms) promote genetic isolation and divergence despite periods of sympatry between them, as the heteropatric model predicts.

A parapatric propensity for breeding precludes the completion of speciation in common teal (Anas crecca, sensu lato).

Speciation is a process in which genetic drift and selection cause divergence over time. However, there is no rule dictating the time required for speciation, and even low levels of gene flow hinder divergence, so that taxa may be poised at the threshold of speciation for long periods of evolutionary time. We sequenced mitochondrial DNA (mtDNA) and eight nuclear introns (nuDNA) to estimate genomic levels of differentiation and gene flow between the Eurasian common teal (Anas crecca crecca) and the North American green-winged teal (Anas crecca carolinensis). These ducks come into contact in Beringia (north-eastern Asia and north-western North America) and have probably done so, perhaps cyclically, since the Pliocene-Pleistocene transition, ~2.6 Ma, when they apparently began diverging. They have diagnosable differences in male plumage and are 6.9% divergent in the mtDNA control region, with only 1 of 58 crecca and 2 of 86 carolinensis having haplotypes grouping with the other. Two nuclear loci were likewise strongly structured between these teal (Φ(st) ≥ 0.35), but six loci were undifferentiated or only weakly structured (Φ(st) = 0.0-0.06). Gene flow between crecca and carolinensis was ~1 individual per generation in both directions in mtDNA, but was asymmetrical in nuDNA, with ~1 and ~20 individuals per generation immigrating into crecca and carolinensis, respectively. This study illustrates that species delimitation using a single marker oversimplifies the complexity of the speciation process, and it suggests that even with divergent selection, moderate levels of gene flow may stall the speciation process short of completion.

The Asia-to-America influx of avian influenza wild bird hosts is large.

Recent literature has underestimated the number and taxonomic diversity of wild birds moving between Asia and North America. Our analyses of the major avian influenza (AI) host groups show that fully 33 species of waterfowl (Anatidae), 46 species of shorebirds (Charadriidae and Scolopacidae), and 15 species of gulls and terns (Laridae) are involved in movements from Asia to Alaska across northern oceans (Table 1). Our data suggest that about 1.5-2.9 million individuals in these important host groups move from Asia to Alaska annually. Among all of the host groups we consider most relevant for AI virus movement models in this region (waterfowl, shorebirds, and gulls and terns), it seems likely that thousands of AI-infectious birds may be involved in annual Asia-to-America migrations. Importantly, host availability in Alaska once these vectors arrive is also very high, representing at least 5-10 times more birds and infectious birds than the host populations moving from Asia to North America. Incorporating our data into a recent model of the global spread of the highly pathogenic H5N1 suggests that wild birds are a more likely source of this strain being brought into the United States than trade in domestic birds, although the latter remain a numerically more probable source of introduction into the New World. Our results should help in defining the key taxonomic, geographic, and seasonal factors involved in this complex intercontinental association of wild bird AI hosts. The next steps are to determine infection rates of low pathogenicity and highly pathogenic viruses among these hosts and to incorporate these into dynamic models.

Movements of birds and avian influenza from Asia into Alaska.

Asian-origin avian influenza (AI) viruses are spread in part by migratory birds. In Alaska, diverse avian hosts from Asia and the Americas overlap in a region of intercontinental avifaunal mixing. This region is hypothesized to be a zone of Asia-to-America virus transfer because birds there can mingle in waters contaminated by wild-bird-origin AI viruses. Our 7 years of AI virus surveillance among waterfowl and shorebirds in this region (1998-2004; 8,254 samples) showed remarkably low infection rates (0.06%). Our findings suggest an Arctic effect on viral ecology, caused perhaps by low ecosystem productivity and low host densities relative to available water. Combined with a synthesis of avian diversity and abundance, intercontinental host movements, and genetic analyses, our results suggest that the risk and probably the frequency of intercontinental virus transfer in this region are relatively low.