George K. Sage

Polar and brown bear genomes reveal ancient admixture and demographic footprints of past climate change

Polar bears (PBs) are superbly adapted to the extreme Arctic environment and have become emblematic of the threat to biodiversity from global climate change. Their divergence from the lower-latitude brown bear provides a textbook example of rapid evolution of distinct phenotypes. However, limited mitochondrial and nuclear DNA evidence conflicts in the timing of PB origin as well as placement of the species within versus sister to the brown bear lineage. We gathered extensive genomic sequence data from contemporary polar, brown, and American black bear samples, in addition to a 130,000- to 110,000-y old PB, to examine this problem from a genome-wide perspective. Nuclear DNA markers reflect a species tree consistent with expectation, showing polar and brown bears to be sister species. However, for the enigmatic brown bears native to Alaskas Alexander Archipelago, we estimate that not only their mitochondrial genome, but also 5–10% of their nuclear genome, is most closely related to PBs, indicating ancient admixture between the two species. Explicit admixture analyses are consistent with ancient splits among PBs, brown bears and black bears that were later followed by occasional admixture. We also provide paleodemographic estimates that suggest bear evolution has tracked key climate events, and that PB in particular experienced a prolonged and dramatic decline in its effective population size during the last ca. 500,000 years. We demonstrate that brown bears and PBs have had sufficiently independent evolutionary histories over the last 4–5 million years to leave imprints in the PB nuclear genome that likely are associated with ecological adaptation to the Arctic environment.

Founding events influence genetic population structure of sockeye salmon (Oncorhynchus nerka) in Lake Clark, Alaska.

Bottlenecks can have lasting effects on genetic population structure that obscure patterns of contemporary gene flow and drift. Sockeye salmon are vulnerable to bottleneck effects because they are a highly structured species with excellent colonizing abilities and often occupy geologically young habitats. We describe genetic divergence among and genetic variation within spawning populations of sockeye salmon throughout the Lake Clark area of Alaska. Fin tissue was collected from sockeye salmon representing 15 spawning populations of Lake Clark, Six‐mile Lake, and Lake Iliamna. Allele frequencies differed significantly at 11 microsatellite loci in 96 of 105 pairwise population comparisons. Pairwise estimates of FST ranged from zero to 0.089. Six‐mile Lake and Lake Clark populations have historically been grouped together for management purposes and are geographically proximate. However, Six‐mile Lake populations are genetically similar to Lake Iliamna populations and are divergent from Lake Clark populations. The reduced allelic diversity and strong divergence of Lake Clark populations relative to Six‐mile Lake and Lake Iliamna populations suggest a bottleneck associated with the colonization of Lake Clark by sockeye salmon. Geographic distance and spawning habitat differences apparently do not contribute to isolation and divergence among populations. However, temporal isolation based on spawning time and founder effects associated with ongoing glacial retreat and colonization of new spawning habitats contribute to the genetic population structure of Lake Clark sockeye salmon. Nonequilibrium conditions and the strong influence of genetic drift caution against using estimates of divergence to estimate gene flow among populations of Lake Clark sockeye salmon.

Population genetic structure of annual and perennial populations of Zostera marina L. along the Pacific coast of Baja California and the Gulf of California

The Baja California peninsula represents a biogeographical boundary contributing to regional differentiation among populations of marine animals. We investigated the genetic characteristics of perennial and annual populations of the marine angiosperm, Zostera marina, along the Pacific coast of Baja California and in the Gulf of California, respectively. Populations of Z. marina from five coastal lagoons along the Pacific coast and four sites in the Gulf of California were studied using nine microsatellite loci. Analyses of variance revealed significant interregional differentiation, but no subregional differentiation. Significant spatial differentiation, assessed using θST values, was observed among all populations within the two regions. Z. marina populations along the Pacific coast are separated by more than 220 km and had the greatest θST (0.13–0.28) values, suggesting restricted gene flow. In contrast, lower but still significant genetic differentiation was observed among populations within the Gulf of California (θST = 0.04–0.18), even though populations are separated by more than 250 km. This suggests higher levels of gene flow among Gulf of California populations relative to Pacific coast populations. Direction of gene flow was predominantly southward among Pacific coast populations, whereas no dominant polarity in the Gulf of California populations was observed. The test for isolation by distance (IBD) showed a significant correlation between genetic and geographical distances in Gulf of California populations, but not in Pacific coast populations, perhaps because of shifts in currents during El Niño Southern Oscillation (ENSO) events along the Pacific coast.

A Signal for Independent Coastal and Continental histories among North American wolves

Relatively little genetic variation has been uncovered in surveys across North American wolf populations. Pacific Northwest coastal wolves, in particular, have never been analysed. With an emphasis on coastal Alaska wolf populations, variation at 11 microsatellite loci was assessed. Coastal wolf populations were distinctive from continental wolves and high levels of diversity were found within this isolated and relatively small geographical region. Significant genetic structure within southeast Alaska relative to other populations in the Pacific Northwest, and lack of significant correlation between genetic and geographical distances suggest that differentiation of southeast Alaska wolves may be caused by barriers to gene flow, rather than isolation by distance. Morphological research also suggests that coastal wolves differ from continental populations. A series of studies of other mammals in the region also has uncovered distinctive evolutionary histories and high levels of endemism along the Pacific coast. Divergence of these coastal wolves is consistent with the unique phylogeographical history of the biota of this region and re‐emphasizes the need for continued exploration of this biota to lay a framework for thoughtful management of southeast Alaska.

Implications of the Circumpolar Genetic Structure of Polar Bears for Their Conservation in a Rapidly Warming Arctic

We provide an expansive analysis of polar bear (Ursus maritimus) circumpolar genetic variation during the last two decades of decline in their sea-ice habitat. We sought to evaluate whether their genetic diversity and structure have changed over this period of habitat decline, how their current genetic patterns compare with past patterns, and how genetic demography changed with ancient fluctuations in climate. Characterizing their circumpolar genetic structure using microsatellite data, we defined four clusters that largely correspond to current ecological and oceanographic factors: Eastern Polar Basin, Western Polar Basin, Canadian Archipelago and Southern Canada. We document evidence for recent (ca. last 1–3 generations) directional gene flow from Southern Canada and the Eastern Polar Basin towards the Canadian Archipelago, an area hypothesized to be a future refugium for polar bears as climate-induced habitat decline continues. Our data provide empirical evidence in support of this hypothesis. The direction of current gene flow differs from earlier patterns of gene flow in the Holocene. From analyses of mitochondrial DNA, the Canadian Archipelago cluster and the Barents Sea subpopulation within the Eastern Polar Basin cluster did not show signals of population expansion, suggesting these areas may have served also as past interglacial refugia. Mismatch analyses of mitochondrial DNA data from polar and the paraphyletic brown bear (U. arctos) uncovered offset signals in timing of population expansion between the two species, that are attributed to differential demographic responses to past climate cycling. Mitogenomic structure of polar bears was shallow and developed recently, in contrast to the multiple clades of brown bears. We found no genetic signatures of recent hybridization between the species in our large, circumpolar sample, suggesting that recently observed hybrids represent localized events. Documenting changes in subpopulation connectivity will allow polar nations to proactively adjust conservation actions to continuing decline in sea-ice habitat.

Population Genetic Structure in Lahontan Cutthroat Trout

Abstract We used 10 microsatellite loci to examine the genetic population structure of cutthroat trout Oncorhynchus clarki within the Lahontan Basin complex. Genetic diversity was analyzed for trout from Nevada, California, and Utah representing three putative subspecies: Lahontan O. c. henshawi, Paiute O. c. seleniris, and Humboldt (an unnamed subspecies) cutthroat trout. We found significant differences in microsatellite diversity among the three putative subspecies found in this area. Analysis of molecular variance partitioned microsatellite variation as 9.8% among subspecies, 27.7% among populations, and 62.5% within populations of Lahontan Basin cutthroat trout. Genetic distance analyses (Cavalli-Sforza-Edwards and F st) supported unique population structure in cutthroat trout from the Humboldt and Pilot Peak drainages. Pairwise F st values for Lahontan cutthroat trout were not significantly correlated with geographic distance between population pairs (r 2 = 0.008; P < 0.0001), suggesting that they a...

Genetic Variation, Relatedness, and Effective Population Size of Polar Bears (Ursus maritimus) in the southern Beaufort Sea, Alaska

Polar bears (Ursus maritimus) are unique among bears in that they are adapted to the Arctic sea ice environment. Genetic data are useful for understanding their evolution and can contribute to management. We assessed parentage and relatedness of polar bears in the southern Beaufort Sea, Alaska, with genetic data and field observations of age, sex, and mother-offspring and sibling relationships. Genotypes at 14 microsatellite DNA loci for 226 bears indicate that genetic variation is comparable to other populations of polar bears with mean number of alleles per locus of 7.9 and observed and expected heterozygosity of 0.71. The genetic data verified 60 field-identified mother-offspring pairs and identified 10 additional mother-cub pairs and 48 father-offspring pairs. The entire sample of related and unrelated bears had a mean pairwise relatedness index (r(xy)) of approximately zero, parent-offspring and siblings had r(xy) of approximately 0.5, and 5.2% of the samples had r(xy) values within the range expected for parent-offspring. Effective population size (N(e) = 277) and the ratio of N(e) to total population size (N(e)/N = 0.182) were estimated from the numbers of reproducing males and females. N(e) estimates with genetic methods gave variable results. Our results verify and expand field data on reproduction by females and provide new data on reproduction by males and estimates of relatedness and N(e) in a polar bear population.

Genetic Structure of Columbia River Redband Trout Populations in the Kootenai River Drainage, Montana, Revealed by Microsatellite and Allozyme Loci

Abstract We describe the genetic divergence among 10 populations of redband trout Oncorhynchus mykiss gairdneri from the upper Columbia River drainage. Resident redband trout from two watersheds in the Kootenai River drainage and hatchery stocks of migratory Kamloops redband trout from Kootenay Lake, British Columbia, were analyzed using allele frequency data from microsatellite and allozyme loci. The Kamloops populations have significantly different allele frequencies from those of the Kootenai River drainage. Of the total genetic variation detected in the resident redband trout, 40.7% (microsatellites) and 15.5% (allozymes) were due to differences between populations from the two Kootenai River watersheds. The divergence among populations within each watershed, however, was less than 3.5% with both techniques. Our data indicate that watershed-specific broodstocks of redband trout are needed by fisheries managers for reintroduction or the supplementation of populations at risk of extinction.

The Use of Genetics for the Management of a Recovering Population: Temporal Assessment of Migratory Peregrine Falcons in North America

Background Our ability to monitor populations or species that were once threatened or endangered and in the process of recovery is enhanced by using genetic methods to assess overall population stability and size over time. This can be accomplished most directly by obtaining genetic measures from temporally-spaced samples that reflect the overall stability of the population as given by changes in genetic diversity levels (allelic richness and heterozygosity), degree of population differentiation (F ST and D EST), and effective population size (N e). The primary goal of any recovery effort is to produce a long-term self-sustaining population, and these genetic measures provide a metric by which we can gauge our progress and help make important management decisions. Methodology/Principal Findings The peregrine falcon in North America (Falco peregrinus tundrius and anatum) was delisted in 1994 and 1999, respectively, and its abundance will be monitored by the species Recovery Team every three years until 2015. Although the United States Fish and Wildlife Service makes a distinction between tundrius and anatum subspecies, our genetic results based on eleven microsatellite loci suggest limited differentiation that can be attributed to an isolation by distance relationship and warrant no delineation of these two subspecies in its northern latitudinal distribution from Alaska through Canada into Greenland. Using temporal samples collected at Padre Island, Texas during migration (seven temporal time periods between 1985–2007), no significant differences in genetic diversity or significant population differentiation in allele frequencies between time periods were observed and were indistinguishable from those obtained from tundrius/anatum breeding locations throughout their northern distribution. Estimates of harmonic mean N e were variable and imprecise, but always greater than 500 when employing multiple temporal genetic methods. Conclusions/Significance These results, including those from simulations to assess the power of each method to estimate N e, suggest a stable or growing population, which is consistent with ongoing field-based monitoring surveys. Therefore, historic and continuing efforts to prevent the extinction of the peregrine falcon in North America appear successful with no indication of recent decline, at least from the northern latitude range-wide perspective. The results also further highlight the importance of archiving samples and their use for continual assessment of population recovery and long-term viability.

Range overlap and individual movements during breeding season influence genetic relationships of caribou herds in south-central Alaska

Abstract North American caribou (Rangifer tarandus) herds commonly exhibit little nuclear genetic differentiation among adjacent herds, although available evidence supports strong demographic separation, even for herds with seasonal range overlap. During 1997–2003, we studied the Mentasta and Nelchina caribou herds in south-central Alaska using radiotelemetry to determine individual movements and range overlap during the breeding season, and nuclear and mitochondrial DNA (mtDNA) markers to assess levels of genetic differentiation. Although the herds were considered discrete because females calved in separate regions, individual movements and breeding-range overlap in some years provided opportunity for male-mediated gene flow, even without demographic interchange. Telemetry results revealed strong female philopatry, and little evidence of female emigration despite overlapping seasonal distributions. Analyses of 13 microsatellites indicated the Mentasta and Nelchina herds were not significantly differentiated using both traditional population-based analyses and individual-based Bayesian clustering analyses. However, we observed mtDNA differentiation between the 2 herds (FST = 0.041, P < 0.001). Although the Mentasta and Nelchina herds exhibit distinct population dynamics and physical characteristics, they demonstrate evidence of gene flow and thus function as a genetic metapopulation.