Robert E. Wilson

Hybridization is a common process among bird species that can precipitate a mix of positive or negative species outcomes. Particularly for rare populations, detrimental effects of hybridization on demographic growth rates and genetic integrity are of serious concern. In Alaska and a small region of northwestern Canada, the endemic subspecies of Gray‐headed Chickadee ( Poecile cinctus lathami ) has declined in recent decades from being locally common to being extremely rare. The more widespread Boreal Chickadee ( P. hudsonicus ) has become increasingly abundant in areas of sympatry. These changes in abundance may have led to hybridization between Gray‐headed Chickadees and Boreal Chickadees. We used a series of analyses to test for signatures of introgression at mitochondrial DNA and nuclear DNA using historical museum samples of both species collected between 1875 and 1979 as well as contemporary Boreal Chickadee samples. In addition, we modeled Gray‐headed Chickadee and Boreal Chickadee demographic histories to better understand patterns of effective population size changes and gene flow over time. Introgression of Gray‐headed Chickadee nuclear DNA was detected in contemporary and historical Boreal Chickadee populations, and two first‐generation hybrid backcrosses were observed in the historical Boreal Chickadee samples. Lack of mitochondrial DNA introgression or backcrossing into the Gray‐headed Chickadee historical samples may be an artifact of mate scarcity during the period before local abundances of Boreal Chickadee exceeded Gray‐headed Chickadees. Demographic modeling with nuclear loci estimated a low level of symmetric gene flow between Gray‐headed Chickadees and Boreal Chickadees since the time of divergence. Our study suggests that hybridization may be linked to Gray‐headed Chickadee declines and represents a case study of how museum collections can be used to infer introgression in a population too scarce to directly investigate.

Greenland White‐fronted Geese Anser albifrons flavirostris exhibit prolonged parent–offspring and sibling–sibling associations, suggesting fitness advantages to such behaviour, so we used reduced representation genome sequence data to determine the degree to which marked flock members observed associating in apparent parent–offspring and sibling–sibling relationships in the field were genetically related. Among 50 bled, marked and released geese, we genetically identified members of 11 different family groups, confirming all observed male parent–offspring relationships as genetically predicted, but only 10 out of 12 (83%) possible female parent–offspring relationships (i.e. two offspring were not genetically related to the adult female in their family groups observed in the field); these two ‘adopted’ offspring were responsible for four (15%) of the cases where observed ‘siblings’ were not genetically related to other family‐member first‐winter birds with which they associated. One multigenerational family consisted of three genetically confirmed grandmother–mother–sibling offspring relationships, not previously reported in arctic‐nesting geese, as well as one of the two ‘adopted’ first‐winter geese.

Genetic variation in Arctic species is often influenced by vicariance during the Pleistocene, as ice sheets fragmented the landscape and displaced populations to low‐ and high‐latitude refugia. The formation of secondary contact or suture zones during periods of ice sheet retraction has important consequences on genetic diversity by facilitating genetic connectivity between formerly isolated populations. Brant geese (Branta bernicla) are a maritime migratory waterfowl (Anseriformes) species that almost exclusively uses coastal habitats. Within North America, brant geese are characterized by two phenotypically distinct subspecies that utilize disjunct breeding and wintering areas in the northern Pacific and Atlantic. In the Western High Arctic of Canada, brant geese consist of individuals with an intermediate phenotype that are rarely observed nesting outside this region. We examined the genetic structure of brant geese populations from each subspecies and areas consisting of intermediate phenotypes using mitochondrial DNA (mtDNA) control region sequence data and microsatellite loci. We found a strong east–west partition in both marker types consistent with refugial populations. Within subspecies, structure was also observed at mtDNA while microsatellite data suggested the presence of only two distinct genetic clusters. The Western High Arctic (WHA) appears to be a secondary contact zone for both Atlantic and Pacific lineages as mtDNA and nuclear genotypes were assigned to both subspecies, and admixed individuals were observed in this region. The mtDNA sequence data outside WHA suggests no or very restricted intermixing between Atlantic and Pacific wintering populations which is consistent with published banding and telemetry data. Our study indicates that, although brant geese in the WHA are not a genetically distinct lineage, this region may act as a reservoir of genetic diversity and may be an area of high conservation value given the potential of low reproductive output in this species.

Evidence from a variety of organisms points to convergent evolution on the mitochondria associated with a physiological response to oxygen deprivation or temperature stress, including mechanisms for high-altitude adaptation. Here, we examine whether demography and/or selection explains standing mitogenome nucleotide diversity in high-altitude adapted populations of three Andean waterfowl species: yellow-billed pintail (Anas georgica), speckled teal (Anas flavirostris), and cinnamon teal (Spatula cyanoptera). We compared a total of 60 mitogenomes from each of these three duck species (n = 20 per species) across low and high altitudes and tested whether part(s) or all of the mitogenome exhibited expected signatures of purifying selection within the high-altitude populations of these species. Historical effective population sizes (N_e) were inferred to be similar between high- and low-altitude populations of each species, suggesting that selection rather than genetic drift best explains the reduced genetic variation found in mitochondrial genes of high-altitude populations compared to low-altitude populations of the same species. Specifically, we provide evidence that establishment of these three Andean waterfowl species in the high-altitude environment, coincided at least in part with a persistent pattern of negative purifying selection acting on oxidative phosphorylation (OXPHOS) function of the mitochondria. Our results further reveal that the extent of gene-specific purifying selection has been greatest in the speckled teal, the species with the longest history of high-altitude occupancy.

Integrating tracking technology and molecular approaches provides a comprehensive picture of contemporary and evolutionary mechanisms promoting connectivity. We used mitochondrial DNA and double digest restriction-site associated DNA (ddRAD) sequencing combined with satellite telemetry to investigate the connectivity of geographically disparate breeding populations of a declining boreal shorebird, the lesser yellowlegs (Tringa flavipes). We were able to track 33 individuals on their round-trip migrations to Central and South America and back to the boreal wetlands of North America. Nearly all (93%) adults captured on the breeding grounds returned to within 5 km of the original capture site, with a median dispersal distance of 629 m. While our telemetry data revealed limited breeding dispersal in adults, genetic data uncovered significant interconnectedness across the species’ range. Very little genetic structure was estimated at ddRAD autosomal (Φ_ST = 0.001), Z-linked (Φ_ST = 0.001), and mtDNA loci (Φ_ST = 0.020), and maximum likelihood-based clustering methods placed all individuals in a single cluster regardless of capture location, indicating the species is panmictic. Our data indicate that large-scale juvenile dispersal is the main mechanism maintaining connectivity in this species, resulting in the absence of genomic structure.

Migration schedules and the timing of other annual events (e.g., pair formation and molt) can affect the distribution of genetic diversity as much as where these events occur. The greater white-fronted goose (Anser albifrons) is a circumpolar goose species, exhibiting temporal and spatial variation of events among populations during the annual cycle. Previous range-wide genetic assessments of the nuclear genome based on eight microsatellite loci suggest a single, largely panmictic population despite up to five subspecies currently recognized based on phenotypic differences. We used double digest restriction-site associated DNA (ddRAD-seq) and mitochondrial DNA (mtDNA) sequence data to re-evaluate estimates of spatial genomic structure and to characterize how past and present processes have shaped the patterns of genetic diversity and connectivity across the Arctic and subarctic. We uncovered previously undetected inter-population differentiation with genetic clusters corresponding to sampling locales associated with current management groups. We further observed subtle genetic clustering within each management unit that can be at least partially explained by the timing and directionality of migration events along with other behaviors during the annual cycle. The Tule Goose (A. a. elgasi) and Greenland subspecies (A. a. flavirostris) showed the highest level of divergence among all sampling locales investigated. The recovery of previously undetected broad and fine-scale spatial structure suggests that the strong cultural transmission of migratory behavior restricts gene flow across portions of the species’ range. Our data further highlight the importance of re-evaluating previous assessments conducted based on a small number of highly variable genetic markers in phenotypically diverse species.

As marine ecosystems respond to climate change and other stressors, it is necessary to evaluate current and past hybridization events to gain insight on the outcomes and drivers of such events. Ancestral introgression within the gadids has been suggested to allow cod to inhabit a variety of habitats. Little attention has been given to contemporary hybridization, especially within cold-water-adapted cod ( Boreogadus saida Lepechin, 1774 and Arctogadus glacialis Peters, 1872). We used whole-genome, restriction-site associated, and mitochondrial sequence data to explore the degree and direction of hybridization between these species where previous hybridization had not been reported. Although nearly identical morphologically at certain life stages, we detected very distinct nuclear and mitochondrial lineages. We detected one potential hybrid with a Arctogadus mitochondrial haplotype and Boreogadus nuclear genotype, but no early generational hybrids. The presence of a late generation hybrid suggests that at least some hybrids survive to maturity and reproduce. However, a historical introgression event could not be excluded. Contemporary gene flow appears asymmetrical from Arctogadus into Boreogadus, which may be due to overlap in timing of spawning, environmental heterogeneity, or differences in population size. This study provides important baseline information for the degree of potential hybridization between these species within Alaska marine environments.

Aim: Connectivity is vital to the resiliency of populations to environmental change and stochastic events, especially for cold‐adapted species as Arctic and alpine tundra habitats retract as the climate warms. We examined the influence of past and current landscapes on genomic connectivity in cold‐adapted galliformes as a critical first step to assess the vulnerability of Alaska ptarmigan and grouse to environmental change. We hypothesize that the mosaic of physical features and habitat within Alaska promoted the formation of genetic structure across species.Location: Alaska, United States of America.Taxa: Ptarmigan and Grouse (Galliformes: Tetraoninae).Methods: We collected double digest restriction‐site‐associated DNA sequence data from six ptarmigan and grouse species (N = 13–145/species) sampled across multiple ecosystems up to ~10 degrees of latitude. Spatial genomic structure was analysed using methods that reflect different temporal scales: (1) principal components analysis to identify major trends in the distribution of genomic variation; (2) maximum likelihood clustering analyses to test for the presence of multiple genomic groupings; (3) shared co‐ancestry analyses to assess contemporary relationships and (4) effective migration surfaces to identify regions that deviate from a null model of isolation by distance.Results: Levels of genomic structure varied across species (Φ_ST =0.009–0.042). Three general patterns of structure emerged: (1) east‐west partition located near the Yukon‐Tanana uplands; (2) north‐south split coinciding with the Alaska Range and (3) northern group near the Brooks Range. Species‐specific patterns were observed; not all landscape features were barriers to gene flow for all ptarmigan and grouse and temporal contrasts were detected at the Brooks Range.Main conclusions: Within Alaska galliformes, patterns of genomic structure coincide with physiographic features and highlight the importance of physical and ecological barriers in shaping how genomic diversity is arrayed across the landscape. Lack of concordance in spatial patterns indicates that species behaviour and habitat affinities play key roles in driving the contrasting patterns of genomic structure.

Introgression of beneficial alleles has emerged as an important avenue for genetic adaptation in both plant and animal populations. In vertebrates, adaptation to hypoxic high-altitude environments involves the coordination of multiple molecular and cellular mechanisms, including selection on the hypoxia-inducible factor (HIF) pathway and the blood-O₂ transport protein hemoglobin (Hb). In two Andean duck species, a striking DNA sequence similarity reflecting identity by descent is present across the ~20 kb β-globin cluster including both embryonic (HBE) and adult (HBB) paralogs, though it was yet untested whether this is due to independent parallel evolution or adaptive introgression. In this study, we find that identical amino acid substitutions in the β-globin cluster that increase Hb-O₂ affinity have likely resulted from historical interbreeding between high-altitude populations of two different distantly-related species. We examined the direction of introgression and discovered that the species with a deeper mtDNA divergence that colonized high altitude earlier in history (Anas flavirostris) transferred adaptive genetic variation to the species with a shallower divergence (A. georgica) that likely colonized high altitude more recently possibly following a range shift into a novel environment. As a consequence, the species that received these β-globin variants through hybridization might have adapted to hypoxic conditions in the high-altitude environment more quickly through acquiring beneficial alleles from the standing, hybrid-origin variation, leading to faster evolution.