to what are polar bears most closely related?

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Mol Ecol. 2015 Mar; 24(6): 1205–1217.

Genomic evidence of geographically widespread result of cistron menstruation from polar bears into brownish bears

James A Cahill

^*Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA, 95064, U.s.a.

Ian Stirling

^†Wildlife Inquiry Division, Department of Environment, Edmonton, AB, Canada

Logan Kistler

^‡Departments of Anthropology and Biological science, The Pennsylvania Country University, 516 Carpenter Edifice, University Park, PA, 16802, U.s.a.

Rauf Salamzade

^§Department of Biomolecular Applied science, University of California, Santa Cruz, CA, 95064, U.s.a.

Erik Ersmark

^¶Section of Bioinformatics and Genetics, Swedish Museum of Natural History, Stockholm, SE-104 05, Sweden

Tara L Fulton

^*Department of Environmental and Evolutionary Biological science, University of California, Santa Cruz, CA, 95064, The states

Mathias Stiller

^*Department of Ecology and Evolutionary Biological science, University of California, Santa Cruz, CA, 95064, United states of america

^**Department of Evolutionary Genetics, Max Planck Constitute for Evolutionary Anthropology, Deutscher Platz 6, Leipzig, D-04103, Germany

Richard E Light-green

^§Department of Biomolecular Applied science, University of California, Santa Cruz, CA, 95064, USA

Beth Shapiro

^*Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA, 95064, USA

Received 2014 Feb 7; Revised 2014 Nov 15; Accepted 2014 Nov 26.

Supplementary Materials

Fig S1: D-statistic tests for brownish bear admixture into individual polar bears.

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Fig S2: Tests for contamination of PB7 by Ken.

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Fig S3: Y chromosome pairwise difference between male bears.

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Tabular array S1: Sample drove details for each bear analyzed in this written report.

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Table S2: D-statistic results for tests of excess allele sharing between one of two brown bears and a polar bear.

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Table S3: D-statistic results for tests of excess allele sharing betwixt one of two polar bears and a brown comport.

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Tabular array S4: estimates measuring the proportion of the each dark-brown deport's genome resulting from polar conduct ancestry.

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Table S5: estimates measuring the proportion of the each polar acquit'due south genome resulting from brown bear beginnings.

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Appendix S1: Methods and results indicating the unsuitability of the PB7 and LS samples for analysis by the methods described here.

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Information Availability Argument

Whole genome shotgun sequencing data produced for this written report are available in the NCBI Short Read Archive as SRX795188, SRX796430 and SRX796442. Data from previously published studies are bachelor at the NCBI Short Read Archive SRX155945–51, SRX155953–62, SRX156012–08, SRX156136, SRX156156–63, SRX265152, SRX265434–36, SRX265452–54, SRX265456, SRX265457, SRX265459.

Abstract

Polar bears are an chill, marine adapted species that is closely related to brown bears. Genome analyses take shown that polar bears are distinct and genetically homogeneous in comparing to dark-brown bears. Yet, these analyses take besides revealed a remarkable episode of polar carry gene flow into the population of brown bears that colonized the Admiralty, Baranof and Chichagof islands (ABC islands) of Alaska. Here, we nowadays an assay of data from a large panel of polar bear and chocolate-brown acquit genomes that includes brown bears from the ABC islands, the Alaskan mainland and Europe. Our results provide clear evidence that gene flow between the ii species had a geographically wide bear on, with polar behave Deoxyribonucleic acid 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 behave ancestry, polar deport genomes appear to be devoid of brown bear ancestry, suggesting the presence of a bulwark to factor flow in that direction.

Keywords: brownish bear, ecological genetics, genomics, hybridization, polar bear, Ursus

Introduction

Polar bears (Ursus maritimus) have evolved numerous morphological, behavioural and physiological specializations for their arctic habitat, including white coat colour, a reduced hibernation government, and a strictly carnivorous nutrition with corresponding changes in tooth morphology and cranial structure (Sacco & Van Valkenburgh ²⁰⁰⁴; Slater et al. ²⁰¹⁰). These adaptations distinguish polar bears from their closely related sister taxon, brown bears (U. arctos), who have a far more than diverse morphology, ecology and geographic range than practise polar bears. Brownish bears vary widely in size, coloration and nutrition regimes that range from primarily herbivorous to populations that are largely dependent on salmon. The historical range of brown bears includes most of northern Eurasia and western North America, while polar bears are found in the continental shelf sea ice regions of the northward Arctic (Fig.​ 1).

Sample Map. Map of the present-twenty-four hours geographic range of brownish bears (red) and polar bears (blue). Messages indicate location from which bears were sampled.

Despite the substantial morphological, behavioural and ecological differences betwixt chocolate-brown bears and polar bears, the ii species share a very close evolutionary relationship. Precisely how shut, however, remains a subject of substantial ongoing debate. At many loci, lineages have not yet sorted betwixt the two species (Hailer et al. ^{2012 , 2013}; Cahill et al. ²⁰¹³), which complicates estimates of when the two species diverged. In addition, polar bears and brown bears produce viable and fertile hybrids both in the wild and in captivity (Preuß et al. ²⁰⁰⁹; Stirling ²⁰¹¹), suggesting a recent divergence betwixt the two lineages.

Published estimates of the time of departure between brown bears and polar bears using genetic data range from 340 thousand to 4–v million years ago (Hailer et al. ²⁰¹²; Miller et al. ²⁰¹²; Cahill et al. ²⁰¹³; Cronin et al. ²⁰¹⁴; Liu et al. ²⁰¹⁴). Not all of these estimates are straight comparable, however. Divergence estimates based on the molecular clock assume express or no gene period and range from ∼600 grand to 3 one thousand thousand years ago, depending largely on how the molecular clock is calibrated (Hailer et al. ²⁰¹²; Cahill et al. ²⁰¹³; Cronin et al. ²⁰¹⁴). Importantly, these estimates are genomic departure times and not population divergence times and will therefore predate the origin of polar bears as a distinct lineage.

Ii studies, Miller et al. ²⁰¹² and Liu et al. ²⁰¹⁴; have besides attempted to gauge the time of population divergence from whole genome information using population-modelling frameworks. Liu et al. estimated population departure to accept occurred 343–479 yard years agone with postdivergence gene flow from polar bears to chocolate-brown bears (Liu et al. ²⁰¹⁴). Miller et al. estimated a much before 4–5 million years ago divergence followed by bidirectional postdivergence factor flow (Miller et al. ²⁰¹²). Given the greater concordance of the 343–479 g years ago population divergence with other genetic difference estimates information technology appears to be a better supported.

Analyses of mitochondrial DNA further complicated interpretation of polar conduct and brown behave history. Near brown bear mitochondrial haplotypes evidence strikingly strong geographic structure, likely resulting from female philopatry (Korsten et al. ²⁰⁰⁹; Davison et al. ²⁰¹¹; Edwards et al. ²⁰¹¹). However, the get-go genetic studies of bear mitochondrial Dna identified a strange exception to this dominion: polar bear mitochondrial haplotypes fall within the range of variety of brown bear mitochondrial haplotypes, rather than outside of brown acquit mitochondrial diversity, as would be expected of dissever species (Cronin et al. ¹⁹⁹¹; Talbot & Shields ¹⁹⁹⁶; Waits et al. ¹⁹⁹⁸; Lindqvist et al. ²⁰¹⁰). The chocolate-brown bear mitochondrial lineage that is most closely related to those of polar bears is found today merely on Alaska'southward ABC islands (Fig.​ 1 Locations G and H). In fact, these brown bear mitochondria are more like to the mitochondria of polar bears than they are to other brown comport mitochondrial lineages. This finding led to early speculation that the ABC islands population was a very ancient population of brown bears and therefore the most closely related population to polar bears (Talbot & Shields ¹⁹⁹⁶).

Afterwards surveys of bear mitochondrial DNA included geographically diverse samples of both living brown bears and extinct populations (Leonard et al. ²⁰⁰⁰; Barnes et al. ²⁰⁰²; Valdiosera et al. ²⁰⁰⁷; Edwards et al. ²⁰¹¹). These analyses farther complicated the scenario by revealing 3 geographically and temporally distinct brownish carry populations that had mitochondrial haplotypes that were very similar to those of polar bears (time to come the brown/polar mtDNA clade). In addition to the ABC islands population, this includes an extinct population that lived on present-solar day Ireland until effectually 9000 years ago (Edwards et al. ²⁰¹¹) and another that lived in Pleistocene Beringia – the in one case-contiguous landmass that continued Alaska to northeastern Siberia – more than 50 000 years ago (Barnes et al. ²⁰⁰²). These findings led to further speculation that the geographic distribution of mitochondrial haplotypes in the brown/polar mitochondrial clade was due not to long-term evolution, but instead to multiple instances of hybridization, during which the mitochondrial lineage was passed between the two species, eventually leading to the geographic pattern of the present day (Edwards et al. ²⁰¹¹).

More recently, analyses of nuclear genomic and Y chromosome data take provided additional insights into the evolutionary relationship betwixt dark-brown and polar bears. Consensus nuclear DNA phylogenies (Hailer et al. ²⁰¹²; Cahill et al. ²⁰¹³; Bidon et al. ²⁰¹⁴; Cronin et al. ²⁰¹⁴) and Y chromosome phylogenies (Bidon et al. ²⁰¹⁴) indicate that, on boilerplate, polar bears and brown bears class ii distinct lineages. Still, many nuclear loci and the mitochondria deviate from this pattern (Hailer et al. ^{2012 , 2013}; Cahill et al. ²⁰¹³). This divergence from the average species tree topology is most likely due to the effects of incomplete lineage sorting and, perchance, admixture.

Nuclear genomic data too reveal a remarkable difference in the corporeality of diversity within the two bear lineages. Mirroring their corresponding levels of ecological and biological variety, polar bears are much more genetically homogenous than are brown bears (Miller et al. ²⁰¹²; Cahill et al. ²⁰¹³). Two polar acquit individuals differ at only about 0.03% of sites, while two dark-brown bears from Alaska differed at 0.sixteen% of sites (Cahill et al. ²⁰¹³). On average, a polar carry differs from a brown behave at approximately 0.24% of sites in the genome (Cahill et al. ²⁰¹³).

We recently proposed that the ABC islands brown bear population descends from an admixture event with polar bears (Cahill et al. ²⁰¹³). We observed that ABC islands brown bears show show of increased polar bear ancestry relative to other brown carry populations throughout their autosomal genomes. Nonetheless, polar bear ancestry is further elevated on ABC island brown bear 10 chromosomes compared to their autosomes (Cahill et al. ²⁰¹³), and they comprise mitochondria that are more similar to those of polar bears than to other brown bears.

These genetic observations and the natural history of the ABC islands are consistent with a model wherein ABC islands brownish bears are the descendants of an original population of polar bears. Immigration of primarily or exclusively male person chocolate-brown bears gradually converted the phenotype and genotype of the ABC islands bears into those of brown bears. This male-biased factor flow did not convert the strictly maternal mitochondrial Deoxyribonucleic acid and was less pronounced in converting Ten chromosome loci, but completely converted the paternal Y chromosome. This outcome overturns the previous hypothesis that polar bears received their mitochondrial haplotype via introgression from a population of brown bears closely related to the ABC island brown bears or ancient Irish gaelic brown bears (Edwards et al. ²⁰¹¹). Rather, the mitochondrial haplotype found in polar bears is of polar bear origin. Under this scenario, brownish bears in the brownish/polar mtDNA clade are the recipients of introgression from polar bears.

Previously, we measured the impact of admixture on the nuclear genomes of ABC bears using the D-statistic test for admixture (Light-green et al. ²⁰¹⁰; Durand et al. ²⁰¹¹). We showed that a dark-brown conduct from the ABC islands carried more polar bear matching alleles than a dark-brown bear from Denali National Park. While the result was statistically well supported, this framework – using a unmarried, non-ABC islands brown bear for comparison – lacks the ability to appraise whether the mainland brown bear is devoid of polar behave ancestry or simply has less polar bear beginnings than does the ABC islands comport. We were therefore unable to explore the geographic extent to which this admixture event affected comport populations or to explore hypotheses nearly frequency of admixture between the two bear lineages. Recently, a study calculated D-statistics suggesting that other ABC islands brown bears and a brown conduct from Glacier National Park in Montana, USA, possessed polar bear beginnings (Liu et al. ²⁰¹⁴).

Here, nosotros examination the extent of polar bear ancestry inside and across the ABC islands population by analysing genomewide information from a more diverse panel of brown bears (Fig.​ 1). Comparisons between bears in this larger console reveal a more widespread pattern of polar bear admixture into brown bears. We discover evidence of polar bear admixture in ABC islands dark-brown bears and in brown bears from the Alaskan mainland. Within the ABC islands, we identify a geographic cline of admixture, with more retained polar acquit ancestry in bears farther from the mainland. Finally, we notice no evidence of cistron menses from brown bears into polar bears, in stark dissimilarity to the widespread indicate of gene menses in the other direction.

Methods

Assembling a large panel of brown comport and polar acquit genome sequences

Previous assay indicated that the genomes of ABC islands dark-brown bears comprise more polar bear ancestry than practice those of mainland Alaskan brown bears. However, this analysis was performed using only a unmarried genome representing each population. To more fully explore the spatial distribution of the signal of polar bear ancestry within the ABC islands, nosotros collected a larger panel of brown and polar comport genomes. Nosotros sequenced three previously unpublished brown bears one from Sweden and two from Chichagof Isle. We analysed these samples forth with samples from two previously published data sets; 2 brown bears, seven polar bears and an American blackness behave published in Cahill et al. ²⁰¹³ (Cahill et al. ²⁰¹³) and iii dark-brown bears and twenty-three polar bears published in Miller et al. ²⁰¹² (Miller et al. ²⁰¹²) (Fig.​ 1, Table S1, Supporting Data).

For many bear genomes, the depth of coverage was insufficient to telephone call heterozygote sites reliably. We therefore used the strategy described previously (Green et al. ²⁰¹⁰; Cahill et al. ²⁰¹³) to sample one high-quality base of operations at each genomic position from each acquit, thereby creating a pseudo-haploid sequence. 2 of the polar bear samples were unsuitable for this approach, and we excluded these from further analysis (Figs S1 and S2, Supporting Information). Equally described previously, nosotros partitioned the polar bear genome associates (Li et al. ²⁰¹¹) to which all sequence data were mapped into scaffolds that are likely to be on autosomes and those likely to be X chromosomes (Cahill et al. ²⁰¹³). No Y chromosome scaffolds were constitute to encounter our minimum scaffold length filtering criteria. To infer the history of the Y chromosome, we therefore assessed separately only the largest Y chromosome scaffold (Supporting Information).

DNA extraction, library preparation and sequencing

We extracted Dna from the Chichagof Island brown bears and the Swedish brown deport using the DNeasy Blood & Tissue Kit (Qiagen) and the QIAmp Micro Kit (Qiagen) according to the manufacturer's specifications. We physically sheared the Dna of the iii new chocolate-brown bear samples using a Diagenode Bioruptor NGS instrument. Extracts were transferred into 1.5-mL tubes and exposed to seven rounds of sonication, using the energy setting 'High' and an 'ON/OFF interval' of xxx/thirty due south. We then purified and full-bodied the extracts using the Agencourt AMPure XP PCR purification kit, according to manufacturer'southward instructions, and eluted in xx μL of 1xTE, with 0.05% Tween20.

We prepared indexed Illumina libraries using 15 μL of each excerpt following the protocol described past Meyer & Kircher (Meyer & Kircher ²⁰¹⁰), with reaction volumes scaled to total book of forty μL. To verify last DNA concentration and the distribution of insert sizes, we ran each library on an Agilent 2100 Bioanalyzer. We and so sequenced each bear upon half of a lane of an Illumina HiSeq 2000 instrument using 150-base pair (bp) paired-end chemistry at the Vincent J. Coates Genomics Sequencing Laboratory at UC Berkeley.

Quality control, mapping and pseudo-haploidization

From the Illumina sequence data, nosotros removed the index and adapter sequence and merged paired reads using a script provided by M. Kircher (Kircher ²⁰¹²). We then trimmed each read to remove low-quality bases past trimming inward from the three′ end of the read until detecting a base with quality score ≥13 (∼95% confidence) (Lohse et al. ²⁰¹²). Nosotros mapped the resulting information to the typhoon polar bear genome (Li et al. ²⁰¹¹) using BWA (Li & Durbin ²⁰¹⁰). We removed duplicated reads created by PCR amplification using the rmdup program from samtools (Li et al. ²⁰⁰⁹).

For all individuals at each position in the genome, we chose a random, single allele from amongst reads that passed the following filtering criteria: (i) read map quality Phred-30 or greater; (ii) Illumina base quality Phred-30 or greater; (iii) genomic position is within a uniquely mappable 35-mers identified using GEM (Derrien et al. ²⁰¹²); (iv) read coverage at that position is betwixt the fifth and 95th percentiles genomewide identified using BEDTools coverageBed (Quinlan & Hall ²⁰¹⁰); and (v) discarding scaffolds <one MB in length. This approach is designed to accept uniform power to detect rare alleles at all mappable positions in all individuals. In contrast, using a genotyping inference programme to telephone call heterozygous sites would have greater ability to detect rare, nonreference alleles in college coverage individuals. This would, however, confound downstream analysis. The result of our approach is that a single base phone call, randomly selected from among the mapped reads, represents the individual at every site in the reference genome. Because bears are diploid, this single base call necessarily simply represents ane of the ii alleles at sites where the comport is heterozygous.

Detecting admixture

We used the D-statistic framework (Green et al. ²⁰¹⁰; Durand et al. ²⁰¹¹) to measure the relative amounts of polar bear ancestry between pairs of chocolate-brown bears. The D-statistic is a comparison between four individuals: two conspecific individuals, P1 and P2, a candidate introgressor, P3, and an out-grouping, O. At each site in the genome, nosotros test whether the relationship between these four individuals is inconsistent with the species tree topology. Sites that are considered inconsistent with the species tree are those at which P2 shares a derived allele with P3 but not P1 (ABBA sites) or sites where P1 shares a derived allele with P3 but not P2 (BABA sites). In the absenteeism of bequeathed population construction, processes other than admixture that produce loci inconsistent with the species tree, such every bit incomplete lineage sorting and error, are expected to produce an equal number of ABBA and BABA sites (Green et al. ²⁰¹⁰; Durand et al. ²⁰¹¹). An excess of either ABBA or BABA sites is testify of admixture. In this framework, admixture between P1 and P3, for instance, is expected to produce an excess of BABA sites compared to ABBA sites. As described previously, we used the black behave genome to determine the ancestral state at each polymorphic genomic position (Cahill et al. ²⁰¹³).

We performed analyses for all combinations of pairs of conspecific individuals and candidate admixers. This amounted to 720 comparisons for eight brownish bears with 28 candidate introgressor polar bears (Table​ 1; Fig.​ 2; Table S2, Supporting Data) and 3360 comparisons for 28 polar bears with viii candidate introgressor brown bears (Table S3, Supporting Information). For separate analysis of the X chromosome, nosotros used the X chromosome polar carry genome scaffolds identified in our previous study (Cahill et al. ²⁰¹³). To exist classified as an X chromosome scaffold, a scaffold must encounter two criteria: differences in male vs. female shotgun sequence coverage and the presence of orthologs to 10-linked genes from the dog genome (Lindblad-Toh et al. ²⁰⁰⁵).

Table one

Polar bear ancestry in chocolate-brown behave autosomes

	P2
P1	Sweden	Kenai	Denali	% Polar Acquit
Adm1	0.1258 (12.viii)	0.0685 (5.ix)	0.0160 (1.3)	five.99 (12.2)
Adm2	0.1231 (12.2)	0.0669 (6.one)	0.0139 (1.i)	5.88 (11.7)
Bar	0.1613 (14.vii)	0.1091 (eight.9)	0.0573 (4.3)	7.82 (13.ix)
Chi1	0.1786 (17.7)	0.1278 (11.3)	0.0777 (vi.4)	viii.68 (16.0)
Chi2	0.1819 (eighteen.3)	0.1323 (12.1)	0.0819 (6.7)	8.83 (16.v)
Den	0.1267 (14.iii)	0.0571 (5.six)	N/A	5.38 (12.7)
Ken	0.0719 (9.six)	Northward/A	−0.0571 (5.6)	3.17 (9.two)

D-statistic measure of admixture in brown bears. Distribution of D-statistic tests between two brownish bears and a polar conduct candidate introgressor with an American black bear out-group. Each dot represents an independent test with a different polar bear as the candidate introgressor. ABC islands bears, particularly those from Baranof and Chichagof islands, testify the highest amount of polar bear introgression. Admiralty Island brownish bears testify the greatest bias toward polar behave ancestry on the X chromosome vs. the autosomes. The Denali brown acquit shows the greatest bias toward polar bear beginnings on the autosomes relative to the X chromosome.

The related estimator (Dark-green et al. ²⁰¹⁰; Durand et al. ²⁰¹¹) was used to gauge the proportion of the genome derived from admixture. Ideally, this test requires two individuals of the candidate introgressor species that are non themselves admixed. This was not possible in all cases, yet, because all of the brown bears except the Swedish brown bear were plant to exist admixed with polar bears. To minimize bias, we used the two least admixed brown bears – the Swedish and Kenai individuals – to estimate the fraction of brown bear genomes that had introgressed from polar bears (Table S5, Supporting Information).

For both the D- and statistics, we mensurate D-statistical significance using a weighted cake jackknife using five Mb blocks (Green et al. ²⁰¹⁰; Durand et al. ²⁰¹¹). The weighted block jackknife tests whether admixture signals are uniform across the genome and therefore reflect the same population history. The weighted block jackknife produces a standard error value. The number of standard errors past which the observed value of D or differs from the null expectation of zippo is the Z score. In keeping with Dark-green et al. ²⁰¹⁰ (Greenish et al. ²⁰¹⁰), we define pregnant D- and statistic results as having Z scores greater than 3. Note that we do not perform multiple-test correction, as it is not clear how to correctly business relationship for multiple tests in this exploratory framework in which near tests are not independent.

Results

Admixture analysis

D-statistic comparisons between pairs of brownish bears from different populations revealed statistically meaning differences in all comparisons (Fig.​ 2; Tables​ ane and ​ two, Tabular array S2, Supporting Information). Consistent with previous observations using only a single mainland brown bear, comparison betwixt any ABC islands bear and whatsoever non-ABC islands brown acquit showed an excess of polar bear ancestry in the ABC islands behave. Also as before, the excess of polar deport ancestry in ABC islands bears was greater on the X chromosomes than on the autosomes (Fig.​ 2, Tabular array​ 1). The lower statistical significance of X chromosome results compared to autosomal results (Tables​ 1 and S2–S5, Supporting Information) is due to the much smaller size of the 10 chromosome and corresponding increased influence of removing v MB blocks.

Table 2

Polar conduct ancestry in brown bear Ten chromosomes

	P2
P1	Sweden	Kenai	Denali	% Polar Bear
Adm1	0.2226 (one.9)	0.2285 (ii.7)	0.2330 (4.5)	vii.63 (one.8)
Adm2	0.221 (1.8)	0.2323 (2.nine)	0.2388 (three.2)	7.53 (1.7)
Bar	0.2538 (i.8)	0.2632 (2.half dozen)	0.2785 (2.7)	9.35 (one.5)
Chi1	0.2654 (two.ii)	0.2736 (3.3)	0.2787 (4.0)	9.59 (one.9)
Chi2	0.2669 (2.6)	0.2769 (4.1)	0.2826 (iii.9)	9.71 (2.3)
Den	0.0364 (0.4)	−0.0041 (0.1)	North/A	one.04 (0.3)
Ken	0.0360 (0.seven)	N/A	0.0041 (0.1)	1.04 (0.vii)

The brown behave from Sweden had the lowest rate of matching polar bear alleles in all pairwise comparisons with other brown bears. The Kenai brown behave had the adjacent lowest charge per unit, with estimated polar comport beginnings of 3.17% on the autosomes and ane.04% on the X chromosome. The Denali brown carry, which was the only mainland brown conduct sample from our previous study, had the highest rate of polar bear allele matching among all non-ABC islands brown bears in this larger sample of brown bears (Fig.​ 2). Using , we estimate polar bear ancestry in the Denali carry to be at to the lowest degree 5.38% on the autosomes and 1.04% on the X chromosome.

D-statistic measurements of polar bear ancestry on the X chromosome vs. autosomes reveal a striking difference between ABC islands bears and non-ABC islands bears. The pattern of enriched polar bear beginnings on the X chromosome of ABC islands brownish bears is reversed in non-ABC islands brown bears (Fig.​ 2, Table​ ane); that is, non-ABC island brown bears have less polar bear ancestry on the 10 chromosome relative to their autosomes.

Within the ABC islands, the brownish bears from Baranof and Chichagof islands have more than polar behave ancestry than the chocolate-brown bears from Admiralty Island (Fig.​ 2, Tables​ 1 and ​ 2). estimates of polar acquit ancestry in ABC islands brown bears ranges from 5.9% to 8.8% of the autosomes and 7.5 to ix.vii% of the X chromosome. As noted above, all of the ABC islands dark-brown bears' Ten chromosomes are enriched for polar bear beginnings compared to their autosomes. Within the ABC islands, 10 chromosome bias of polar bear ancestry increases as total polar bear beginnings decreases. The brown bears of Admiralty Island, the island closest to the mainland, take the least polar bear beginnings, and polar bear ancestry is the near X chromosome biased (Tables​ one and ​ two).

We as well tested for a indicate of admixture within polar bear genomes. D-statistic tests between pairs of polar bear genomes for unequal rates of matching derived brown acquit alleles resulted in no D-statistics that differed statistically from zero (weighted block jackknife Z>3) (Fig.​ 3; Table S3; Fig. S1, Supporting Information). estimators too indicated an absenteeism of detectable gene flow from brown bears into polar bears, with no comparisons deviating statistically from nothing ( statistics with weighted block jackknife Z>iii).

D-statistic measure of admixture in polar bears. Box-and-whisker plots showing the range of D-statistic values for a single polar bear (Sample), bundled along the x-centrality by geographic location (Population), compared to every other polar behave with every chocolate-brown bear as a candidate introgressor. For each box-and-whisker-plot, boxes range from the 25th to 75th percentiles, whiskers are 1.5 times the distance from the 25th to 75th percentile, or the nearly extreme effect if information technology is less than one.5 times the distance from the 25th to 75th percentile. Circles indicate information that fall outside of 25th to 75th percentile (outliners). Statistically meaning D-statistic values point that the subject polar bear shares an backlog of derived alleles with brown bears. None of the comparisons, including the outliners, resulted in D-statistic values that differed significantly from nothing (Z>iii).

Discussion

Uneven amounts of polar bear beginnings among dark-brown bears

Our previous observations nearly polar bear ancestry inside ABC islands bears relied on comparison to a single mainland brownish bear from Denali National Park, Alaska. While the comparisons were consistently and strongly in the direction of backlog polar comport ancestry in ABC islands bears, employ of a unmarried comparing genome is limiting in an of import way. Quantifying the absolute amount of polar bear ancestry requires making an assumption most the amount of polar bear ancestry in the comparison brown bear. For our previous work, we made the assumption that the Denali acquit was costless of polar carry beginnings. Following this assumption, the excess polar bear ancestry in ABC islands brown bears was interpreted as a mensurate of the absolute amount of polar deport ancestry in the ABC islands brown bears.

Our new results indicate that this supposition was incorrect – the Denali brown bear is not gratuitous of polar comport ancestry. In fact, among the non-ABC islands brown bears analysed here, the Denali conduct has the greatest polar comport ancestry: at least five.38% of the autosomes and one.04% of the X chromosome derives from polar bear. The Swedish brown bear has the least polar behave beginnings in all pairwise comparisons and thus establishes a new baseline for admixture-free brown acquit.

A further unexpected result is that in contrast to the excess of polar bear ancestry on the 10 chromosomes relative to autosomes among ABC islands bears, we see the opposite design inside non-ABC island chocolate-brown bears; that is, these bears have lower levels of polar acquit beginnings inside their X chromosomes vs. their autosomes (Fig.​ ii).

These results take several important implications for understanding the admixture outcome on the ABC islands. Almost importantly, nosotros now guess a much greater corporeality of polar deport ancestry in each ABC islands brown bear than previously reported. Recalculating the accented corporeality of polar bear ancestry for the five ABC islands bears using the Swedish conduct every bit the nonadmixed standard results in higher estimated proportions of polar bear beginnings than when using the Denali bear (Table​ one). Whereas we previously reported an absolute amount of half-dozen.5% polar bear ancestry on the X chromosome and 0.5% polar bear ancestry on the autosomes of the bear from Admiralty Island, estimates based on the Swedish acquit betoken that seven.six% of the Ten chromosomes of this bear are derived from polar bear ancestry, as is half-dozen.0% of the autosomes. These results may explain the very high 10: autosome ratio of polar carry ancestry that was estimated while using the Denali brown bear equally standard, which cruel exterior of the distribution of ratios predicted by demographic simulation (Cahill et al. ²⁰¹³). Considering the Denali deport has a significant amount of polar deport ancestry on the autosomes, this led to an underestimate of the amount of polar bear ancestry on the autosomes of the ABC islands brown bear.

We notice a geographic bespeak wherein bears from the islands less accessible from the mainland – Baranof and Chichagof islands – have more polar comport ancestry than the bears of Admiralty Isle (Fig.​ ii). A previous assay of microsatellite data from a large sample of Alaskan brownish bears similarly reported more gene flow between Admiralty Isle and the Alaskan mainland than between the more distant Baranof and Chichagof islands and the Alaskan mainland, and very footling gene flow between Baranof and Chichagof islands and Admiralty Island (Paetkau et al. ^{1998 , 1999}). These data support a model of brown bear dispersal from the Alaskan mainland that is limited mainly by long-altitude water crossings (Fig.​ 2).

Notably, Baranof and Chichagof islands brown bears' polar bear ancestry is less 10 chromosome biased than Admiralty Island bears' polar bear ancestry (Fig.​ 2). This upshot is consistent with and extends the model we proposed previously wherein male-dominated gene flow from the mainland onto these islands carries chocolate-brown acquit genetic material into a population that was initially polar bears. More distal bears are further from the source of this gene period and thus less impacted by migration from the mainland. In this style, the dark-brown bears of Baranof and Chichagof islands retain more of their polar bear genetic ancestry, merely exhibit comparatively less bias toward the X chromosome. Lending further back up to this hypothesis of female-biased polar bear beginnings and male-biased brown deport ancestry, a contempo study by Bidon and colleagues found Y chromosome ancestry on the ABC islands to be exclusively dark-brown behave (Bidon et al. ²⁰¹⁴). Similarly, we discover no evidence of polar comport ancestry in any brown bears when analysing the largest Y chromosome scaffold in the polar bear assembly (Supporting Information).

Polar bear ancestry in non-ABC islands brown bears

For each of the not-ABC islands Alaskan brown bears nosotros analysed, excess polar bear ancestry is observed on the autosomes over the Ten chromosome when compared to the Swedish brown bear. The reverse is observed in the ABC islands chocolate-brown bears. This X chromosome depletion is more pronounced than the 10 chromosome enrichment on the ABC islands. There are multiple plausible hypotheses that could explain this outcome, both demographic and selective.

Demographically, brown bear dispersal is primarily male-mediated (McLellan & Reiner ¹⁹⁹⁴; Støen et al. ²⁰⁰⁶). Populations that are located further from the site of hybridization would be expected therefore to have less polar deport ancestry on the female-biased X chromosome than on the autosomes. This behavioural process is supported by genetic evidence: while brownish bear mitochondrial haplotypes, which are exclusively maternally inherited, bear witness strong geographic structuring (Korsten et al. ²⁰⁰⁹; Davison et al. ²⁰¹¹; Edwards et al. ²⁰¹¹), Y chromosome haplotypes, which are exclusively paternally inherited, show no such geographic structure (Bidon et al. ²⁰¹⁴). Thus, i hypothesis that is consistent with our data is that brown bears from the ABC islands, and perhaps other regions of polar bear admixture, will take their polar conduct ancestry dispersed primarily by male brown bears. Every bit males carry fewer X chromosomes than autosomes, polar bear ancestry will go increasingly less visible on the X chromosome than on autosomes equally one samples brown bears farther from the site of admixture.

From a selective standpoint, it has been suggested that loci involved in hybrid incompatibility are overrepresented on the 10 chromosome (Masly & Presgraves ²⁰⁰⁷). This is because, in the heterogametic sex activity, the presence of simply 1 copy of any incompatible allele prevents a homologous compatible allele from masking the incompatibility. In theory, this should lead to a reduction in introgressed ancestry on the X chromosome relative to the balance of the genome. Such an effect was recently observed in the case of Neandertal introgression into non-African humans, where Neandertal ancestry is almost absent on the Ten chromosome (Sankararaman et al. ²⁰¹⁴). In that case, the authors' simulations appeared to reject a demographic explanation.

These processes are not mutually exclusive, and both biased dispersal and selection confronting polar bear ancestry on the X chromosome may play a function in explaining the lower polar conduct ancestry on the Ten chromosome of non-ABC islands chocolate-brown bears. At this stage, it seems likely that at that place is bereft understanding of the demography of bears throughout Alaska and northern Canada to brand a definitive assessment of the role of each.

Our results showing backlog polar bear ancestry in every dark-brown bear we sampled compared with the Swedish brownish bear, whose own polar comport ancestry we cannot reliably estimate for the reasons noted higher up, advise a higher charge per unit of introgression of polar bear DNA into brown carry genomes than previously calculated. It may be that the epicentre of this introgression is in the ABC islands and the surrounding area. Following the initial introgression result, predominantly male migration could have then carried polar bear ancestry abroad from the Islands. This model is simple and not obviously contradictory to the data. However, further study will be required to refine the number, timing and geographic locations of polar bear admixture into Alaskan brown bears. I peculiarly intriguing possibility concerns the other brown bears that were plant with a mitochondrial haplotype like to the polar behave haplotype: some Beringian brown bears that lived more than 50 grand years ago (Barnes et al. ²⁰⁰²) and a population of now extinct Irish gaelic brown bears (Edwards et al. ²⁰¹¹). It will be interesting to know whether these results are due to a similar process of male person-mediated cistron period from dark-brown bears into other polar acquit populations in the by and, if so, whether in that location is whatsoever remaining polar bear ancestry from those introgression events in brown bear populations today.

Absence of detectable chocolate-brown carry ancestry in polar bears

Admixture is more easily detected by the D-statistic when the population receiving cistron flow is small (Durand et al. ²⁰¹¹). Given that the effective population size of polar bears is and likely has been small for many thousands of years (Miller et al. ²⁰¹²), our observation that none of the 28 polar bear genomes used in this assay take detectable dark-brown acquit ancestry is even more striking and has of import implications for understanding both the relationship between the two species and for predicting the long-term consequences of hybridization.

Despite the widespread touch of admixture on chocolate-brown bear genomes, the genetic data point no corresponding effect on polar bears. The absenteeism of detectable gene menstruation into polar bears may therefore reverberate an ecological barrier to admixed individuals surviving every bit polar bears, where whatever introduction of brownish deport DNA into polar bears may be strongly deleterious (Schluter ²⁰⁰⁹). Within the polar behave lineage, there is testify of powerful episodes of positive selection (Liu et al. ²⁰¹⁴). One possibility is that the extremely specialized adaptations of polar bears may quickly place phenotypically intermediate hybrids at more of a disadvantage in the polar bear surroundings than the brown bear environment.

1 simple example of this could be coat colour – a trait that would likely play a more than severe role in decreasing fitness of F1 hybrids in the polar bear habitat than the brown bear habitat. Similar other arctic predators hunting on snow or ice, such as arctic wolves (Canis lupus arctos) or arctic foxes (Vulpes lagopus) in winter, polar bears are uniformly white except for their optics and nose. In contrast, hybrids have darker patches and sometimes overall coloration (Gray ¹⁹⁷¹; Stirling ²⁰¹¹). When a polar bear stalks a seal on the ice, it holds the head down low and walks in a straight line toward the intended prey (Stirling ¹⁹⁷⁴), presumably because that minimizes contrasting dark spots that a seal may detect. An important time for polar comport feeding is late jump when the new ingather of young ringed seals, with footling experience with predators, is weaned (Stirling & Øristland ¹⁹⁹⁵) and later on in the spring, as the snow melts that covers animate holes and nascency lairs when a loftier proportion of seals are out on the ice basking and moulting (Kelly & Quakenbush ¹⁹⁹⁰). Much of the hunting of these seals is performed by stalking (Stirling ¹⁹⁷⁴). Hybrid bears with patches or darker pelage, or darker shades would be more visible to the seals and therefore less successful hunters. In contrast, variation in coloration may be less of a constraint for a hybrid acquit feeding on brown deport food sources: vegetation, salmon or carrion. While this model – extreme reduction in F1 hybrid fitness in the polar bear ecological environment – is speculative and simplistic, it would suffice to explain the striking absence of brown acquit genetic introgression into polar comport populations.

Another possible explanation for the observed imbalance in admixture proportions may exist that dark-brown bear Deoxyribonucleic acid did introgress into polar bears, but that all polar bears take equivalent levels of brown comport ancestry. The D-statistic, which is a pairwise comparison method, has no ability to find admixture in this unique scenario. Such a scenario could manifest in two ways. Outset, all of the polar bears sampled here may have received an exactly equal corporeality of brown carry ancestry via introgression more recently than the time of the polar bear populations shared mutual ancestor. This scenario seems unlikely due to the size and geographic diversity of the panel of polar bears analysed here. Widespread brownish comport into polar acquit introgression might be expected to result in at least some variation in the amount of introgressed brown deport beginnings in 1 of these bears. 2d, brown comport Deoxyribonucleic acid may accept introgressed into the polar bear population that was bequeathed to all extant populations of polar bears. In this second scenario, all polar bears would have exactly the same brown bear ancestry, thereby masking the signal of admixture. Under this scenario, no living polar behave would have detectable excess brown bear ancestry.

One way to investigate this second scenario is to examine the number of D-statistic informative sites. D-statistic informative sites are incongruous with the species tree and tin can ascend from a variety of processes including incomplete lineage sorting, sequencing errors, multiple mutations at a site and admixture. If two conspecific individuals, P1 and P2, received the same amount of introgression from P3, then the D-statistic for D(P1, P2, P3, O) would exist zero. However, the number of species tree incongruous sites would be greater than if no introgression had occurred. In improver to D-statistics of zip, we discover very few sites that are incongruous with the species tree (Fig.​ four) when comparing two polar bears for dark-brown conduct matching alleles. This suggests that the second scenario – brown acquit admixture into the ancestral population of polar bears – is also unlikely.

Frequency of sites informative to the D-statistic. The frequency of ABBA sites (grey bars) and BABA sites (coloured bars) for each D-statistic comparison. Both ABBA and BABA sites are considered species tree-incongruent sites. Processes other than admixture, such as incomplete lineage sorting and sequencing error, are expected to produce an equal number of ABBA and BABA sites. Any difference between the number of ABBA and BABA sites – here, the deviation between coloured and grayness confined – is interpreted as evidence of admixture. Comparisons involving pairs of polar bears testify very few tree-incongruent sites and no prove of admixture from dark-brown bears.

If brown bear introgression were very ancient and took identify prior to the most recent common ancestor of polar bears, then it would be incommunicable to detect this admixture event every bit all polar bears would carry these introgressed and stock-still alleles. However, estimates of the timing of both the genetic time to most recent common ancestor between polar bears (130–650 chiliad years agone; Cahill et al. ²⁰¹³) and speciation between polar bears and chocolate-brown bears (343–479 thousand years ago; Liu et al. ²⁰¹⁴) point that these two events were nearly simultaneous, making this situation unlikely. While it is not possible to exclude the possibility of minimal, evenly distributed brown bear introgression into polar bears, any introgression that did occur must have been express and makes no affect on the extant genetic diverseness of polar bears.

Wider implications of disproportionate gene catamenia

Geneflow disproportion is not an obvious or expected outcome of admixture. Nonetheless, testify for asymmetric factor flow has been presented in other instances, notably between modern humans and Neandertals (Green et al. ²⁰¹⁰), between subspecies of house mouse (Mus musculus) (Expert et al. ²⁰⁰⁸; Teeter et al. ²⁰⁰⁸) and amongst some Darwin'due south finches (Grant & Grant ²⁰¹⁰). The disproportionate hybridization nosotros discover between polar bears and brown bears differs in important means from these examples. While the touch on of human and Neandertal admixture was geographically widespread, information technology is currently non possible to know the extent of factor flow into Neandertal populations as population information from this extinct species are scarce. In any case, it is possible that the disproportion observed thus far is due to demographic phenomenon – a growing, expanding human population entering and replacing a dwindling Neandertal population (Mellars & French ²⁰¹¹; Prüfer et al. ²⁰¹⁴).

Hybridization betwixt house mouse subspecies M. m. musculus and M. chiliad. domesticus occurs in a large hybrid zone beyond central Europe, in which genes flow more than readily from M. m. domesticus introgressing into M. m. muscle than they do in the reverse management (Teeter et al. ²⁰⁰⁸; Wang et al. ²⁰¹¹; Staubach et al. ²⁰¹²). However, unlike the strictly disproportionate gene menstruation from polar bears into dark-brown bears, genes are also known to catamenia from Thousand. m. muscle into M. thou. domesticus (Teeter et al. ²⁰⁰⁸; Wang et al. ²⁰¹¹; Staubach et al. ²⁰¹²). Thus, the disproportion is a quantitative and non a qualitative phenomenon. Among Darwin's finches, F1 hybrids exhibit biased backcrossing into the paternal species, whichever that may be. This bias is believed to be mediated by imprinting of paternal song (Grant & Grant ¹⁹⁹⁷) and in any case is not a strict bulwark to factor flow in either direction (Grant et al. ²⁰⁰⁴).

Our observation of farthermost asymmetry in gene menstruation betwixt polar bears and chocolate-brown bears suggests that the impacts of admixture may differ considerably amidst these closely related species. More generally, these results may present a new challenge to the concept of species. The model of past hybridization and gene period that we present is consistent with a biological species definition of brownish bears that includes polar bears, merely inconsistent with a biological species definition of polar bears that includes brownish bears. To our noesis, there is no current species concept that fully accommodates an disproportionate definition of species.

Understanding why brown bear alleles exercise not introgress into polar bear populations may provide of import insights into how polar bears survive in their farthermost, arctic habitat. The consequences of this observation for conservation of polar bears are articulate: polar bears have very little genetic diversity, and this design has persisted despite geographically widespread signals of admixture within brownish bears. Information technology seems unlikely therefore that hybridization or the paucity of genetic diverseness among polar bears represents the principle threat to the long-term survival of polar bears. Rather, the rapid rate of contempo climate modify and consequent disappearance of their habitat (Stirling & Derocher ²⁰¹²) remain the most proximate and serious threats to polar bears.

Decision

Hybridization between polar bears and brown bears has exerted a surprisingly large and asymmetrical influence on the genomes of polar bears and brown bears carrying polar acquit genes into chocolate-brown bears inhabiting a broad geographic area. Interestingly, while chocolate-brown bears possess polar bear ancestry across meaning portions of their genomes, brown bear ancestry appears absent-minded from polar bears. This suggests that an every bit nevertheless unidentified bulwark to gene flow exists that prevents hybrid individuals from successfully backcrossing with the polar bear population. This i-way barrier to gene flow provides an interesting new framework for the study of the interactions between climate, ecology and speciation.

Acknowledgments

JC and BS were supported by the Packard Foundation and by NSF ARC-09090456 and ARC-1203990. REG was supported by the Searle Scholars Program. BS and REG were additionally supported by the Gordon and Betty Moore Foundation. We thank the University of Alaska at Fairbanks Museum of Natural History and the Natural History Museum in Stockholm for providing brown bear specimens.

Data accessibility

Whole genome shotgun sequencing data produced for this study are available in the NCBI Short Read Archive as SRX795188, SRX796430 and SRX796442. Data from previously published studies are available at the NCBI Short Read Annal SRX155945–51, SRX155953–62, SRX156012–08, SRX156136, SRX156156–63, SRX265152, SRX265434–36, SRX265452–54, SRX265456, SRX265457, SRX265459.

Supporting Data

Additional supporting information may be found in the online version of this article.

Fig S1

D-statistic tests for brown bear admixture into individual polar bears.

Fig S2

Tests for contamination of PB7 past Ken.

Fig S3

Y chromosome pairwise departure between male bears.

Tabular array S1

Sample collection details for each carry analyzed in this report.

Table S2

D-statistic results for tests of excess allele sharing between i of two brown bears and a polar acquit.

Tabular array S3

D-statistic results for tests of excess allele sharing between one of two polar bears and a brown behave.

Tabular array S4

estimates measuring the proportion of the each brown behave's genome resulting from polar acquit ancestry.

Table S5

estimates measuring the proportion of the each polar bear'south genome resulting from brown bear ancestry.

Appendix S1

Methods and results indicating the unsuitability of the PB7 and LS samples for analysis by the methods described here.

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Source: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4409089/

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