Genomic evidence of geographically widespread effect of gene flow from polar bears into brown bears

Polar bears are an arctic, marine adapted species that is closely related to brown bears. Genome analyses have shown that polar bears are distinct and genetically homogeneous in comparison to brown bears. However, these analyses have also revealed a remarkable episode of polar bear gene flow into the population of brown bears that colonized the Admiralty, Baranof and Chichagof islands (ABC islands) of Alaska. Here, we present an analysis of data from a large panel of polar bear and brown bear genomes that includes brown bears from the ABC islands, the Alaskan mainland and Europe. Our results provide clear evidence that gene flow between the two species had a geographically wide impact, with polar bear DNA found within the genomes of brown bears living both on the ABC islands and in the Alaskan mainland. Intriguingly, while brown bear genomes contain up to 8.8% polar bear ancestry, polar bear genomes appear to be devoid of brown bear ancestry, suggesting the presence of a barrier to gene flow in that direction.     

Gene flow between insular, coastal and interior populations of brown bears in Alaska

The brown bears of coastal Alaska have been recently regarded as comprising from one to three distinct genetic groups. We sampled brown bears from each of the regions for which hypotheses of genetic uniqueness have been made, including the bears of the Kodiak Archipelago and the bears of Admiralty, Baranof and Chichagof (ABC) Islands in southeast Alaska. These samples were analysed with a suite of nuclear microsatellite markers. The 'big brown bears' of coastal Alaska were found to be part of the continuous continental distribution of brown bears, and not genetically isolated from the physically smaller 'grizzly bears' of the interior. By contrast, Kodiak brown bears appear to have experienced little or no genetic exchange with continental populations in recent generations. The bears of the ABC Islands, which have previously been shown to undergo little or no female-mediated gene flow with mainland populations, were found not to be genetically isolated from mainland bears. The data from the four insular populations indicate that female and male dispersal can be reduced or eliminated by water barriers of 2–4 km and 7km in width, respectively.     

Genomic Evidence for Island Population Conversion Resolves Conflicting Theories of Polar Bear Evolution

Despite extensive genetic analysis, the evolutionary relationship between polar bears (Ursus maritimus) and brown bears (U. arctos) remains unclear. The two most recent comprehensive reports indicate a recent divergence with little subsequent admixture or a much more ancient divergence followed by extensive admixture. At the center of this controversy are the Alaskan ABC Islands brown bears that show evidence of shared ancestry with polar bears. We present an analysis of genome-wide sequence data for seven polar bears, one ABC Islands brown bear, one mainland Alaskan brown bear, and a black bear (U. americanus), plus recently published datasets from other bears. Surprisingly, we find clear evidence for gene flow from polar bears into ABC Islands brown bears but no evidence of gene flow from brown bears into polar bears. Importantly, while polar bears contributed <1% of the autosomal genome of the ABC Islands brown bear, they contributed 6.5% of the X chromosome. The magnitude of sex-biased polar bear ancestry and the clear direction of gene flow suggest a model wherein the enigmatic ABC Island brown bears are the descendants of a polar bear population that was gradually converted into brown bears via male-dominated brown bear admixture. We present a model that reconciles heretofore conflicting genetic observations. We posit that the enigmatic ABC Islands brown bears derive from a population of polar bears likely stranded by the receding ice at the end of the last glacial period. Since then, male brown bear migration onto the island has gradually converted these bears into an admixed population whose phenotype and genotype are principally brown bear, except at mtDNA and X-linked loci. This process of genome erosion and conversion may be a common outcome when climate change or other forces cause a population to become isolated and then overrun by species with which it can hybridize.     

Ancestral Polymorphisms and Sex-Biased Migration Shaped the Demographic History of Brown Bears and Polar Bears

Recent studies have reported discordant gene trees in the evolution of brown bears and polar bears. Genealogical histories are different among independent nuclear loci and between biparentally inherited autosomal DNA (aDNA) and matrilineal mitochondrial DNA (mtDNA). Based on multi-locus genomic sequences from aDNA and mtDNA, we inferred the population demography of brown and polar bears and found that brown bears have 6 times (aDNA) or more than 14 times (mtDNA) larger population sizes than polar bears and that polar bear lineage is derived from within brown bear diversity. In brown bears, the effective population size ratio of mtDNA to aDNA was at least 0.62, which deviated from the expected value of 0.25, suggesting matriarchal population due to female philopatry and male-biased migration. These results emphasize that ancestral polymorphisms and sex-biased migration may have contributed to conflicting branching patterns in brown and polar bears across aDNA genes and mtDNA.     

Extensive sampling of polar bears (Ursus maritimus) in the Northwest Passage (Canadian Arctic Archipelago) reveals population differentiation across multiple spatial and temporal scales

As global warming accelerates the melting of Arctic sea ice, polar bears (Ursus maritimus) must adapt to a rapidly changing landscape. This process will necessarily alter the species distribution together with population dynamics and structure. Detailed knowledge of these changes is crucial to delineating conservation priorities. Here, we sampled 361 polar bears from across the center of the Canadian Arctic Archipelago spanning the Gulf of Boothia (GB) and M'Clintock Channel (MC). We use DNA microsatellites and mitochondrial control region sequences to quantify genetic differentiation, estimate gene flow, and infer population history. Two populations, roughly coincident with GB and MC, are significantly differentiated at both nuclear (F_ST = 0.01) and mitochondrial (Φ_ST = 0.47; F_ST = 0.29) loci, allowing Bayesian clustering analyses to assign individuals to either group. Our data imply that the causes of the mitochondrial and nuclear genetic patterns differ. Analysis of mtDNA reveals the matrilineal structure dates at least to the Holocene, and is common to individuals throughout the species’ range. These mtDNA differences probably reflect both genetic drift and historical colonization dynamics. In contrast, the differentiation inferred from microsatellites is only on the scale of hundreds of years, possibly reflecting contemporary impediments to gene flow. Taken together, our data suggest that gene flow is insufficient to homogenize the GB and MC populations and support the designation of GB and MC as separate polar bear conservation units. Our study also provide a striking example of how nuclear DNA and mtDNA capture different aspects of a species demographic history.     

Brown Bear Den Habitat and Winter Recreation in South-Central Alaska

ABSTRACT Increasing demand for backcountry recreation opportunities during winter (e.g., snowshoeing, helicopter-assisted skiing, snowmobiling) in steep, high-elevation terrain has elevated concern about disturbance to brown bears (Ursus arctos) denning on the Kenai Peninsula, Alaska, USA. To help identify areas where such conflicts might occur, we developed a spatially explicit model to predict potential den habitat. The model indicated brown bears selected locations for den sites with steep slopes, away from roads and trails. Den sites were associated with habitat high in elevation and away from potential human contact. We then compared areas with the highest probability of providing den habitat with patterns of snowmobile and nonmotorized recreation on a portion of the Kenai Peninsula. We found limited overlap between the 2 recreation activities and potential den habitat for brown bears. At the landscape scale, however, backcountry skiing overlapped more high-quality den habitat than did snowmobile riding. Our results may be used by land management agencies to identify potential conflict sites and to minimize the potential effects of recreation activities on brown bears in dens.     

Introgressive hybridization: brown bears as vectors for polar bear alleles

The dynamics and consequences of introgression can inform about numerous evolutionary processes. Biologists have therefore long been interested in hybridization. One challenge, however, lies in the identification of nonadmixed genotypes that can serve as a baseline for accurate quantification of admixture. In this issue of Molecular Ecology, Cahill et al. (2015) analyse a genomic data set of 28 polar bears, eight brown bears and one American black bear. Polar bear alleles are found to be introgressed into brown bears not only near a previously identified admixture zone on the Alaskan Admiralty, Baranof and Chichagof (ABC) Islands, but also far into the North American mainland. Elegantly contrasting admixture levels at autosomal and X chromosomal markers, Cahill and colleagues infer that male‐biased dispersal has spread these introgressed alleles away from the Late Pleistocene contact zone. Compared to a previous study on the ABC Island population in which an Alaskan brown bear served as a putatively admixture‐free reference, Cahill et al. (2015) utilize a newly sequenced Swedish brown bear as admixture baseline. This approach reveals that brown bears have been impacted by introgression from polar bears to a larger extent (up to 8.8% of their genome), than previously known, including the bear that had previously served as admixture baseline. No evidence for introgression of brown bear into polar bear is found, which the authors argue could be a consequence of selection. Besides adding new exciting pieces to the puzzle of polar/brown bear evolutionary history, the study by Cahill and colleagues highlights that wildlife genomics is moving from analysing single genomes towards a landscape genomics approach.     

Observations of mortality associated with extended open-water swimming by polar bears in the Alaskan Beaufort Sea

During aerial surveys in September 1987–2003, a total of 315 live polar bears were observed with 12 (3.8%) animals in open water, defined for purposes of this analysis as marine waters >2 km north of the Alaska Beaufort Sea coastline or associated barrier islands. No polar bear carcasses were observed. During aerial surveys in early September, 2004, 55 polar bears (Ursus maritimus) were seen, 51 were alive and of those 10 (19.9%) were in open water. In addition, four polar bear carcasses were seen floating in open water and had, presumably, drowned. Average distance from land and pack ice edge for live polar bears swimming in open water in 2004 (n=10) were 8.3±3.0 and 177.4±5.1 km, respectively. We speculate that mortalities due to offshore swimming during late-ice (or mild ice) years may be an important and unaccounted source of natural mortality given energetic demands placed on individual bears engaged in long-distance swimming. We further suggest that drowning-related deaths of polar bears may increase in the future if the observed trend of regression of pack ice and/or longer open water periods continues.     

Ancient DNA analyses reveal high mitochondrial DNA sequence diversity and parallel morphological evolution of late pleistocene cave bears

Cave bears (Ursus spelaeus) existed in Europe and western Asiauntil the end of the last glaciation some 10,000 years ago.To investigate the genetic diversity, population history, andrelationship among different cave bear populations, we havedetermined mitochondrial DNA sequences from 12 cave bears thatrange in age from about 26,500 to at least 49,000 years andoriginate from nine caves. The samples include one individualfrom the type specimen population, as well as two small-sizedhigh-Alpine bears. The results show that about 49,000 yearsago, the mtDNA diversity among cave bears was about 1.8-foldlower than the current species-wide diversity of brown bears(Ursus arctos). However, the current brown bear mtDNA gene poolconsists of three clades, and cave bear mtDNA diversity is similarto the diversity observed within each of these clades. The resultsalso show that geographically separated populations of the high-Alpinecave bear form were polyphyletic with respect to their mtDNA.This suggests that small size may have been an ancestral traitin cave bears and that large size evolved at least twice independently.     

Population-level resource selection by sympatric brown and American black bears in Alaska

Distribution theory predicts that for two species living in sympatry, the subordinate species would be constrained from using the most suitable resources (e.g., habitat), resulting in its use of less suitable habitat and spatial segregation between species. We used negative binomial generalized linear mixed models with fixed effects to estimate seasonal population-level resource selection at two spatial resolutions for female brown bears (Ursus arctos) and female American black bears (U. americanus) in southcentral Alaska during May–September 2000. Black bears selected areas occupied by brown bears during spring which may be related to spatially restricted (i.e., restricted to low elevations) but dispersed or patchy availability of food. In contrast, black bears avoided areas occupied by brown bears during summer. Brown bears selected areas near salmon streams during summer, presumably to access spawning salmon. Use of areas with high berry production by black bears during summer appeared in response to avoidance of areas containing brown bears. Berries likely provided black bears a less nutritious, but adequate food source. We suggest that during summer, black bears were displaced by brown bears, which supports distribution theory in that black bears appeared to be partially constrained from areas containing salmon, resulting in their use of areas containing less nutritious forage. Spatial segregation of brown and American black bears apparently occurs when high-quality resources are spatially restricted and alternate resources are available to the subordinate species. This and previous work suggest that individual interactions between species can result in seasonal population-level responses.     

Polar bears of western Hudson Bay and climate change: Are warming spring air temperatures the “ultimate” survival control factor?

Long-term warming of late spring (April–June) air temperatures has been proposed by Stirling et al. [Stirling, I., Lunn, N.J., Iacozza, J., 1999. Long-term trends in the population ecology of polar bears in western Hudson Bay in relation to climatic change. Arctic 52, 294–306] as the “ultimate” factor causing earlier sea-ice break-up around western Hudson Bay (WH) that has, in turn, led to the poorer physical and reproductive characteristics of polar bears occupying this region. Derocher et al. [Derocher, A.E., Lunn, N.J., Stirling, I., 2004. Polar bears in a warming climate. Integr. Comp. Biol. 44, 163–176] expanded the discussion to the whole circumpolar Arctic and concluded that polar bears will unlikely survive as a species should the computer-predicted scenarios for total disappearance of sea-ice in the Arctic come true. We found that spring air temperatures around the Hudson Bay basin for the past 70 years (1932–2002) show no significant warming trend and are more likely identified with the large-amplitude, natural climatic variability that is characteristic of the Arctic. Any role of external forcing by anthropogenic greenhouse gases remains difficult to identify. We argue, therefore, that the extrapolation of polar bear disappearance is highly premature. Climate models are simply not skilful for the projection of regional sea-ice changes in Hudson Bay or the whole Arctic. Alternative factors, such as increased human–bear interaction, must be taken into account in a more realistic study and explanation of the population ecology of WH polar bears. Both scientific papers and public discussion that continue to fail to recognize the inherent complexity in the adaptive interaction of polar bears with both human and nature will not likely offer any useful, science-based, preservation and management strategies for the species.     

Phylogeny of the bears (Ursidae) based on nuclear and mitochondrial genes

The taxomic classification and phylogenetic relationships within the bear family remain argumentative subjects in recent years. Prior investigation has been concentrated on the application of different mitochondrial (mt) sequence data, herein we employ two nuclear single-copy gene segments, the partial exon 1 from gene encoding interphotoreceptor retinoid binding protein (IRBP) and the complete intron 1 from transthyretin (TTR) gene, in conjunction with previously published mt data, to clarify these enigmatic problems. The combined analyses of nuclear IRBP and TTR datasets not only corroborated prior hypotheses, positioning the spectacled bear most basally and grouping the brown and polar bear together but also provided new insights into the bear phylogeny, suggesting the sister-taxa association of sloth bear and sun bear with strong support. Analyses based on combination of nuclear and mt genes differed from nuclear analysis in recognizing the sloth bears as the earliest diverging species among the subfamily ursine representatives while the exact placement of the sun bear did not resolved. Asiatic and American black bears clustered as sister group in all analyses with moderate levels of bootstrap support and high posterior probabilities. Comparisons between the nuclear and mtDNA findings suggested that our combined nuclear dataset have the resolving power comparable to mtDNA dataset for the phylogenetic interpretation of the bear family. As can be seen from present study, the unanimous phylogeny for this recently derived family was still not produced and additional independent genetic markers were in need.     

Sex-biased natal dispersal in Hokkaido brown bears revealed through mitochondrial DNA analysis

Understanding natal dispersal patterns is fundamental in the ecology and conservation biology of large wild carnivores. In this study, we used two approaches to determine genetic variation and dispersal patterns of brown bears in the Shiretoko Peninsula, eastern Hokkaido, Japan. The first approach was a large-scale genetic analysis. We analyzed haplotypes from the mitochondrial DNA (mtDNA) control region of 760 individual samples collected throughout the peninsula during 1998–2016. We detected seven haplotypes, including two that were confirmed for the first time. In females, the distribution of haplotypes was geographically structured, whereas haplotypes in males were distributed widely throughout the peninsula. Only some males in the lower peninsula had haplotypes that were not detected within the peninsula. The second approach was a local-scale genetic analysis, including intensive focal sampling in the Rusha area, a special wildlife protection area on the peninsula. Proportions of mtDNA haplotypes in adult bears were investigated and compared between the sexes. Although more than half of the females had the same haplotype, males had more diverse haplotypes, suggesting that they came to the Rusha area from other regions. Thus, our study revealed that mtDNA haplotype distribution has been maintained by female philopatry, and that bears exhibit male-biased dispersal. Furthermore, the lower peninsula appears to act as a contact zone between the peninsula and mainland Hokkaido, which is important for maintaining genetic diversity.     

Habitat use by black bears in relation to conspecifics and competitors

Sympatric black bears (Ursus americanus) and brown bears (Ursus arctos) are common in many boreal systems; however, few predator assemblages are known to coexist on a single seasonally abundant large prey item. In lowland southwestern interior Alaska, black bears and brown bears are considered the primary cause of moose (Alces alces) calf mortality during the first 6 weeks of life. The objective of this study was to document habitat use of global-positioning system (GPS)-collared black bears during peak and non-peak seasons of black bear-induced and brown bear-induced moose calf mortality within southwestern interior Alaska, in spring 2002. We compared habitats of GPS-collared black bears to those of presumably uncollared black bears and brown bears at their moose calf mortality sites. Results from this study suggest that GPS-collared black bears use similar habitat as conspecifics more than expected during the peak period of black bear predation on moose calves, whereas they use habitat in proportion to home range availability during the peak in brown bear predation on moose calves. Sex-specific Ivlev's electivity indices describe greater than expected use of mixed-deciduous forest and needleleaf forest by male GPS-collared black bears during the peak of moose calf predation, whereas females have a tendency to use these habitats less than expected. Juvenile GPS-collared black bears largely use the same habitat as other sympatric predators during the peak of moose calf predation, whereas during the non-peak period juveniles use opposite habitats as adult GPS-collared black bears. The outcome of this study offers possible explanations (e.g., sex, age) for spatial overlap or segregation in one member of a complex predator guild in relation to a seasonal pulse of preferred prey.     

Mitogenetic structure of brown bears (Ursus arctos L.) in northeastern Europe and a new time frame for the formation of European brown bear lineages

We estimated the phylogenetic relationships of brown bear maternal haplotypes from countries of northeastern Europe (Estonia, Finland and European Russia), using sequences of mitochondrial DNA (mtDNA) control region of 231 bears. Twenty-five mtDNA haplotypes were identified. The brown bear population in northeastern Europe can be divided into three haplogroups: one with bears from all three countries, one with bears from Finland and Russia, and the third composed almost exclusively of bears from European Russia. Four haplotypes from Finland and European Russia matched exactly with haplotypes from Slovakia, suggesting the significance of the current territory of Slovakia in ancient demographic processes of brown bears. Based on the results of this study and those from the recent literature, we hypothesize that the West Carpathian Mountains have served either as one of the northernmost refuge areas or as an important movement corridor for brown bears of the Eastern lineage towards northern Europe during or after the last ice age. Bayesian analyses were performed to investigate the temporal framework of brown bear lineages in Europe. The molecular clock was calibrated using Beringian brown bear sequences derived from radiocarbon-dated ancient samples, and the estimated mutation rate was 29.8% (13.3%-47.6%) per million years. The whole European population and Western and Eastern lineages formed about 175,000, 70,000 and 25,000 years before present, respectively. Our approach to estimating the time frame of brown bear evolution demonstrates the importance of using an appropriate mutation rate, and this has implications for other studies of Pleistocene populations.     

Mercury in polar bears from Alaska

Alaskan polar bear (Ursus maritimus) muscle and liver samples collected in 1972 were analyzed for total mercury. Bears north of Alaska had more mercury than bears west of Alaska. The only difference between young and adult animals was in the northern area where adults had more mercury in liver tissue than young animals. Levels were probably not high enough to be a serious threat to bears.     

Behavioral response of polar bears to aircraft activity on the northern coast of Alaska

The rapid loss of arctic sea ice is forcing a larger proportion of the Southern Beaufort Sea polar bear (Ursus maritimus) population to spend more time on land, increasing chances of negative interactions between people and bears. In the United States, the Marine Mammal Protection Act (MMPA) protects polar bears from incidental disturbance from human activities. For the remote and roadless areas of northern Alaska, USA, effective management of small aircraft activity is necessary to limit disturbance, but effects of overflights on polar bear behavior are largely unknown. During 2021 and 2022, we intentionally exposed polar bears (n = 115) to systematic aircraft activity (helicopter, fixed-wing) until we observed a disruption of behavior that qualified as a level B take response (e.g., abrupt change in activity or movement) under the MMPA. We used a Bayesian logistic regression to determine what factors influence and can be used to predict when a polar bear will exhibit a level B take response and estimate the probability of an aircraft eliciting a level B take response at different altitudes above the polar bear. Aircraft type, flight altitude, landscape (barrier islands vs. mainland), and bear behavior (active vs. inactive) upon initial aircraft encounter were all important predictors of take. Probability of take rapidly increased with a decrease in flight altitude starting at 450 m for helicopter and 300 m for fixed-wing aircraft. Active (e.g., standing, walking) polar bears on barrier-island landscapes were more likely to experience take than inactive (e.g., bedded) bears on mainland landscapes. Our findings can help with assessments and management plans by quantifying disturbance to polar bears from current and future human activity that involves aircraft use.     

Recent observations of intraspecific predation and cannibalism among polar bears in the southern Beaufort Sea

Intraspecific killing has been reported among polar bears (Ursus maritimus), brown bears (U. arctos), and black bears (U. americanus). Although cannibalism is one motivation for such killings, the ecological factors mediating such events are poorly understood. Between 24 January and 10 April 2004, we confirmed three instances of intraspecific predation and cannibalism in the Beaufort Sea. One of these, the first of this type ever reported for polar bears, was a parturient female killed at her maternal den. The predating bear was hunting in a known maternal denning area and apparently discovered the den by scent. A second predation event involved an adult female and cub recently emerged from their den, and the third involved a yearling male. During 24 years of research on polar bears in the southern Beaufort Sea region of northern Alaska and 34 years in northwestern Canada, we have not seen other incidents of polar bears stalking, killing, and eating other polar bears. We hypothesize that nutritional stresses related to the longer ice-free seasons that have occurred in the Beaufort Sea in recent years may have led to the cannibalism incidents we observed in 2004.Electronic Supplementary Material Supplementary material is available for this article at and is accessible for authorized users.     

Stable isotope differences of polar bears in the Southern Beaufort Sea and Chukchi Sea

The life-history, genetic, and habitat use differences between the 2 polar bear (Ursus maritimus) subpopulations in Alaska, USA, have been used to determine the geographic border separating them, but it has sparked a debate of the correct placement of the border for several years. Recently, the Southern Beaufort Sea (SBS) polar bear subpopulation has declined because of sea ice loss, while the Chukchi Sea (CS) subpopulation appears stable. To provide additional information about potential differences between the SBS and CS subpopulations, such as differences in prey sources, we used stable isotope analysis of carbon and nitrogen from bone collagen of polar bears in these 2 neighboring subpopulations. We analyzed polar bear bones from 112 individuals collected from 1954–2019. Our purpose was to determine if the SBS and CS subpopulations could be distinguished based on the stable isotope signatures of bone collagen. A difference >1‰ in stable carbon isotope (δ¹³C) values suggests a change in carbon sources, such as nearshore to offshore, while a 3‰ change in stable nitrogen isotope (δ¹⁵N) values equates to a change of about 1 trophic level. Our study indicated a difference in δ¹³C values (P ≤ 0.001) but not δ¹⁵N values (P = 0.654) between the CS (−13.0 ± 0.3‰ and 22.0 ± 0.9‰, respectively) and SBS bears (−14.7 ± 1.3‰ and 22.2 ± 1.0‰, respectively). Our findings indicate that the 2 subpopulations are consuming similar high trophic level prey, while feeding in ecosystems with different δ¹³C baselines. We performed a logistic regression analysis using δ¹³C and δ¹⁵N values of the polar bears to predict their placement into these 2 subpopulations. Using Icy Cape, Alaska as the geographical boundary, the analysis correctly placed polar bears in their respective subpopulations 82% of the time. Overall accuracy of placement changed to 84% when using the current geographical boundary at Utqiaġvik, Alaska. We predicted samples collected from the Wainwright, Alaska region as 58% CS and 42% SBS polar bears. This suggests that the area between Wainwright and Icy Cape is a polar bear mixing zone that includes bears from both subpopulations. Bone collagen has a long-term, potentially life-long, stable isotope turnover rate, and our results could be used to determine the association of harvested polar bears to Alaska subpopulations, thus aiding in transboundary harvest quota management.