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

Cahill, James A.; Stirling, Ian; Kistler, Logan; Salamzade, Rauf; Ersmark, Erik; Fulton, Tara L.; Stiller, Mathias; Green, Edward; Shapiro, Beth

doi:10.1111/mec.13038

Cited by 156 publications

(203 citation statements)

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“…There is an emerging consensus that gene flow frequently occurs following speciation despite the establishment of reproductive barriers that otherwise maintain species-level distinctiveness (Roca et al 2005;Good et al 2008;Ellegren et al 2012;Garrigan et al 2012;Toews and Brelsford 2012;Cahill et al 2013Cahill et al , 2014Cui et al 2013;Martin et al 2013;Kutschera et al 2014;Sullivan et al 2014). However, incomplete lineage sorting (ILS) is assumed by default to underpin most cases of phylogenetic discordance.…”

Section: [Supplemental Materials Is Available For This Article]mentioning

confidence: 99%

“…However, incomplete lineage sorting (ILS) is assumed by default to underpin most cases of phylogenetic discordance. Few studies in the literature account for hybridization by analyzing all inheritance patterns (uniparental, sex-biased, biparental) with high-resolution data, or instead have focused on only a few species (Roca et al 2005;Cahill et al 2013Cahill et al , 2014Trigo et al 2013;Khan et al 2014). The cat family Felidae contains 38 recognized species within eight lineages (designated henceforth by a capitalized name, e.g., Puma lineage) that vary in the breadth of their geographic occurrence (Buckley-Beason et al 2006;Johnson et al 2006).…”

Section: [Supplemental Materials Is Available For This Article]mentioning

confidence: 99%

“…ABBA/BABA tests performed on the SNP data set included heterozygous sites by generating pseudohaploid sequences, following Green et al (2010) and Cahill et al (2013Cahill et al ( , 2014. Statistical significance of the Z-score was assessed for each replicate by converting the Z-score into a two-tailed P-value (Eaton and Ree 2013).…”

Section: Detection Of Historical Gene Flowmentioning

confidence: 99%

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Phylogenomic evidence for ancient hybridization in the genomes of living cats (Felidae)

et al. 2015

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Inter-species hybridization has been recently recognized as potentially common in wild animals, but the extent to which it shapes modern genomes is still poorly understood. Distinguishing historical hybridization events from other processes leading to phylogenetic discordance among different markers requires a well-resolved species tree that considers all modes of inheritance and overcomes systematic problems due to rapid lineage diversification by sampling large genomic character sets. Here, we assessed genome-wide phylogenetic variation across a diverse mammalian family, Felidae (cats). We combined genotypes from a genome-wide SNP array with additional autosomal, X-and Y-linked variants to sample ∼150 kb of nuclear sequence, in addition to complete mitochondrial genomes generated using light-coverage Illumina sequencing. We present the first robust felid time tree that accounts for unique maternal, paternal, and biparental evolutionary histories. Signatures of phylogenetic discordance were abundant in the genomes of modern cats, in many cases indicating hybridization as the most likely cause. Comparison of big cat whole-genome sequences revealed a substantial reduction of X-linked divergence times across several large recombination cold spots, which were highly enriched for signatures of selection-driven postdivergence hybridization between the ancestors of the snow leopard and lion lineages. These results highlight the mosaic origin of modern felid genomes and the influence of sex chromosomes and sex-biased dispersal in post-speciation gene flow. A complete resolution of the tree of life will require comprehensive genomic sampling of biparental and sex-limited genetic variation to identify and control for phylogenetic conflict caused by ancient admixture and sex-biased differences in genomic transmission.

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Section: [Supplemental Materials Is Available For This Article]mentioning

confidence: 99%

Section: [Supplemental Materials Is Available For This Article]mentioning

confidence: 99%

Section: Detection Of Historical Gene Flowmentioning

confidence: 99%

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Phylogenomic evidence for ancient hybridization in the genomes of living cats (Felidae)

et al. 2015

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“…Male gene flow has subsequently diluted the original insular polar bear alleles, with higher swamping (lower percentage of polar bear alleles remaining) at loci that show a malebiased inheritance (autosomal > X > mtDNA) (Cahill et al 2013). As subsequently shown by Cahill et al (2015) who sequenced two additional ABC-Island and one European brown bear, brown bears have effectively acted as vectors for polar bear alleles (Hailer 2015): malebiased dispersal by brown bears has carried introgressed polar bear alleles far away from the original zone of admixture into brown bear populations resident on the adjacent North American mainland Liu et al (2014) reported the deep sequencing and de novo assembly of another polar bear genome. The authors used allele frequency and linkage information from 89 sequenced bear genomes for an in-depth demographic modelling of polar/brown bear evolutionary history [see next section for details on aspects of genomic adaptation signals].…”

Section: Discovery Of a Pleistocene Polar Bear Jawbone Stimulates Newmentioning

confidence: 94%

Evolutionary History of Polar and Brown Bears

Hailer

Welch

2016

Encyclopedia of Life Sciences

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Taxonomists have long recognised polar and brown bears as separate species with distinct ecological niches and largely nonoverlapping ranges. Surprisingly, phylogenetic studies of maternally inherited mitochondrial DNA (mtDNA) found polar bears nested within brown bears, with an estimated divergence time of <170 000 years. This indicated an unusually rapid speciation and adaptation of polar bears. However, several recent studies of autosomal and Y‐chromosomal DNA have revisited these findings, giving independent perspectives of bear evolutionary history. Results show that polar bears cluster separately from brown bears, and divergence time estimates are older than those based on mtDNA, ranging from >300 000 to 4–5 million years. These studies confirm uniqueness of the polar bear lineage, provide more time for speciation and adaptation, and have uncovered numerous candidate genes for evolutionary adaptations. Several instances of introgressive hybridisation between polar and brown bears have been inferred, revealing trans‐species transmission of mtDNA and some nuclear loci. Key Concepts DNA sequences in conjunction with a calibration of the mutation rate (e.g. inclusion of a previously estimated mutation rate, geological information or inclusion of a radiocarbon‐dated ancient sample) can be used to estimate the timing of speciation between species. Differentially inherited loci can reveal different aspects of evolutionary history. The genome of polar bears contains a wealth of alleles that are not found in brown bears, and vice versa. Polar bears have passed through bottlenecks during their evolutionary history, leaving them much less genetically variable than brown bears. When analysing DNA sequences that have passed through the species boundary due to introgressive hybridisation, studies will obtain information about the hybridisation event rather than the (earlier) speciation event. Brown bears have acted as vectors for polar bear alleles, transporting introgressed genetic material far beyond the species' contact zones. Incomplete lineage sorting (see ‘Glossary’) complicates phylogenetic inferences among rapidly and/or recently diverged taxa. Lineage sorting takes on average four N e generations, which for many taxa can span at least several hundred thousand years (N e being the effective population size). The time needed for lineages to be reciprocally monophyletic can therefore take very long, even under complete reproductive isolation. Molecular studies have found signals of positive selection in polar bear genes that are involved in fat metabolism, energy production and cardiovascular function. These genes are exciting candidates that may help us better understand the genetic basis of polar bear adaptations to Arctic conditions.

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“…The significant D-statistics varied from 0.07 to 0.17, which is slightly higher compared to analyses on recent radiations, such as Darwin's Finches (0.004 -0.092; Lamichhaney et al, 2015) and butterflies of the genera Heliconius (0.04; Dasmahapatra et al, 2012) and Papilio (0.04; Zhang et al, 2013). These values do fall within the range of studies on other hybridizing species, such as pigs (0.11 -0.23; Frantz et al, 2013), bears (0.04 -0.46; Liu et al, 2014, Cahill et al, 2015 and Xiphophorus fish (0.03 -0.56; Cui et al, 2013). A significant D-statistic does not necessarily indicate introgression between the species from which the genomes are being compared.…”

Section: General Patterns Of Introgressionmentioning

confidence: 53%

Crossing species boundaries : the hybrid histories of the true geese

Ottenburghs¹

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. Crossing Species Boundaries: The Hybrid Histories of the True Geese. PhD thesis, Wageningen University, the Netherlands. Hybridization, the interbreeding of different species, is a common phenomenon in birds: about 16% of bird species is known to have hybridized with at least one other species. Numerous avian hybrid zones have been studied from a morphological or genetic perspective, often documenting the interspecific exchange of genetic material by hybridization and backcrossing (i.e. introgression). The incidence of hybridization varies among bird orders with the Anseriformes (waterfowl: ducks, geese and swans) showing the highest propensity to hybridize. In this thesis, I provide a genomic perspective on the role of hybridization in the evolutionary history of one particular anseriform tribe, the Anserini or "True Geese", which comprises 17 species divided over two genera: Anser and Branta . The diversification of this bird group took place in the late Pliocene and the early Pleistocene (between four and two million years ago), conceivably driven by a global cooling trend that led to the establishment of a circumpolar tundra belt and the emergence of temperate grasslands. Most species show a steady population increase during this period, followed by population subdivision during the Last Glacial Maximum about 110,000 to 12,000 years ago. The combination of large effective population sizes and occasional range shifts facilitated contact between the diverging goose species, resulting in high levels of interspecific gene flow. Introgressive hybridization might have enabled these goose populations to quickly adapt to changing environments by transferring of advantageous alleles across species boundaries, increasing standing genetic variation or expanding phenotypic variation of certain traits (e.g., beak morphology). Hybridization seems to be a common and integral component in the evolution and diversification of geese. The pervasiveness of rapid speciation and hybridization in geese complicates the attempt to capture their evolutionary history in a phylogenetic tree, therefore I advocate a phylogenetic network approach. Indeed, trying to capture the complex diversification of the True Geese in a branching tree can be regarded as a wild goose chase. Abstract TABLE OF CONTENTS

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

Cited by 156 publications

References 54 publications

Phylogenomic evidence for ancient hybridization in the genomes of living cats (Felidae)

Phylogenomic evidence for ancient hybridization in the genomes of living cats (Felidae)

Evolutionary History of Polar and Brown Bears

Crossing species boundaries : the hybrid histories of the true geese

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