Late-Quaternary biogeographic scenarios for the brown bear (Ursus arctos), a wild mammal model species

Davison, John; Ho, Simon Y. W.; Bray, Sarah C; Korsten, Marju; Tammeleht, Egle; Hindrikson, Maris; Østbye, Kjartan; Østbye, Eivind; Lauritzen, Stein‐Erik; Austin, Jeremy J.; Cooper, Alan; Saarma, Urmas

doi:10.1016/j.quascirev.2010.11.023

Cited by 146 publications

(211 citation statements)

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“…Our data are compatible with the known phylogeographic structure in mtDNA found in Europe ( Fig. 1D): three major clades can be identified, usually called 1a (Spain and Southern Sweden), 1b (Italy, Balkans, and Southern Carpathians), and 3a (North-Eastern Europe), and usually associated with different glacial refugia and postglacial recolonization processes (36). This pattern was not observed in the nuclear genomes, and it implies a strong genetic barrier in Sweden and a strict affinity between Apennine and Alpine bears.…”

Section: Mtdna Genomessupporting

confidence: 91%

Survival and divergence in a small group: The extraordinary genomic history of the endangered Apennine brown bear stragglers

Benazzo

Trucchi

Cahill

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

156

132

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Survival and divergence in a small group: the extraordinary genomic history of the endangered Apennine brown bear stragglers 2 AbstractAbout 100 km east of Rome, in the Central Apennine mountains, a critically endangered population of approximately fifty brown bears live in complete isolation. Mating outside this population is prevented by several hundred kilometers of bear-free territories. We exploited this natural experiment to better understand the gene and genomic consequences of surviving at extremely small population size. First, we found that brown bear populations in Europe lost connectivity since Neolithic times, when farming communities expanded and forest burning was used for land clearance. In Central Italy, this resulted in a 40-fold population decline. The overall genomic impact of this decline included the complete loss of variation in the mitochondrial genome and along long stretches of the nuclear genome. Several private and deleterious amino acid changes were fixed by random drift; predicted effects include energy deficit, muscle weakness, anomalies in cranial and skeletal development, and reduced aggressiveness. Despite this extreme loss of diversity, Apennine bear genomes show non-random peaks of high variation, possibly maintained by balancing selection, at genomic regions significantly enriched for genes associated with immune and olfactory systems. Challenging the paradigm of increased extinction risk in small populations, we suggest that random fixation of deleterious alleles a) can be an important driver of divergence in isolation, b) can be tolerated when balancing selection prevents random loss of variation at important genes and c) is followed by or results directly in favorable behavioral changes. SignificanceA small and relict population of brown bears lives in complete isolation in the Italian Apennine mountains, providing a unique opportunity to study the impact of drift and selection on the genomes of a large endangered mammal and to reconstruct the phenotypic consequences and the conservation implications of such evolutionary processes. The Apennine bear is highly inbred and harbors very low genomic variation. Several deleterious mutations have been accumulated by drift. We found evidence that this is a consequence of habitat fragmentation in the Neolithic, when human expansion and land clearance shrank its habitat, and that retention of variation at immune system and olfactory receptor genes, as well as changes in diet and behavior, prevented the extinction of the Apennine bear.

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Section: Mtdna Genomessupporting

confidence: 91%

Survival and divergence in a small group: The extraordinary genomic history of the endangered Apennine brown bear stragglers

Benazzo

Trucchi

Cahill

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

156

132

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“…Historically, phylogenetic and phylogeographic research has relied heavily on mitochondrial DNA (mtDNA), with the brown bear (Ursus arctos) as an extensively studied example (Taberlet et al 1998;Purvis 2005;Davison et al 2011). Advantages of analyzing mtDNA include its high mutation rate, availability of markers, high copy number, lack of recombination, and its haploid nature.…”

Section: Introductionmentioning

confidence: 99%

“…Polar bears exhibit low levels of population differentiation at biparentally inherited and mitochondrial markers throughout their range (Paetkau et al 1999;Cronin and MacNeil 2012;Miller et al 2012;Campagna et al 2013). Brown bears, in contrast, show considerable phylogeographic structuring at mitochondrial markers (Davison et al 2011;Edwards et al 2011;Hirata et al 2013;Keis et al 2013), and population structuring can also be discerned at biparentally inherited microsatellites (Paetkau et al 1997;Tammeleht et al 2010;Kopatz et al 2012). Most mtDNA clades are confined to certain geographical regions and are not shared between continents, although one brown bear clade is widespread throughout Eurasia and extends into North America (Korsten et al 2009;Davison et al 2011).…”

Section: Introductionmentioning

confidence: 99%

“…Brown bears, in contrast, show considerable phylogeographic structuring at mitochondrial markers (Davison et al 2011;Edwards et al 2011;Hirata et al 2013;Keis et al 2013), and population structuring can also be discerned at biparentally inherited microsatellites (Paetkau et al 1997;Tammeleht et al 2010;Kopatz et al 2012). Most mtDNA clades are confined to certain geographical regions and are not shared between continents, although one brown bear clade is widespread throughout Eurasia and extends into North America (Korsten et al 2009;Davison et al 2011). Surprisingly, all range-wide phylogeographic studies on brown bears have so far relied on mtDNA.…”

Section: Introductionmentioning

confidence: 99%

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Brown and Polar Bear Y Chromosomes Reveal Extensive Male-Biased Gene Flow within Brother Lineages

Bidon

Janke

Fain

et al. 2014

Molecular Biology and Evolution

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Brown and polar bears have become prominent examples in phylogeography, but previous phylogeographic studies relied largely on maternally inherited mitochondrial DNA (mtDNA) or were geographically restricted. The male-specific Y chromosome, a natural counterpart to mtDNA, has remained underexplored. Although this paternally inherited chromosome is indispensable for comprehensive analyses of phylogeographic patterns, technical difficulties and low variability have hampered its application in most mammals. We developed 13 novel Y-chromosomal sequence and microsatellite markers from the polar bear genome and screened these in a broad geographic sample of 130 brown and polar bears. We also analyzed a 390-kb-long Y-chromosomal scaffold using sequencing data from published male ursine genomes. Y chromosome evidence support the emerging understanding that brown and polar bears started to diverge no later than the Middle Pleistocene. Contrary to mtDNA patterns, we found 1) brown and polar bears to be reciprocally monophyletic sister (or rather brother) lineages, without signals of introgression, 2) male-biased gene flow across continents and on phylogeographic time scales, and 3) male dispersal that links the Alaskan ABC islands population to mainland brown bears. Due to female philopatry, mtDNA provides a highly structured estimate of population differentiation, while male-biased gene flow is a homogenizing force for nuclear genetic variation. Our findings highlight the importance of analyzing both maternally and paternally inherited loci for a comprehensive view of phylogeographic history, and that mtDNA-based phylogeographic studies of many mammals should be reevaluated. Recent advances in sequencing technology render the analysis of Y-chromosomal variation feasible, even in nonmodel organisms.

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“…(iii) An intriguing explanation was recently provided by Hassanin (2015), who argued that all mtDNA lineage belonging to clade 1 ( Fig. 2A; see Leonard et al 2000 andDavison et al 2011 for details about this nomenclature) should be designated as polar bear-derived. Under that hypothesis, not only the current polar bear lineages in clade 2b, but also the clades currently found in brown bear populations on the ABC islands (clade 2a) and Western Europe (clade 1) are ultimately derived from polar bears.…”

Section: (I)mentioning

confidence: 99%

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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Late-Quaternary biogeographic scenarios for the brown bear (Ursus arctos), a wild mammal model species

Cited by 146 publications

References 103 publications

Survival and divergence in a small group: The extraordinary genomic history of the endangered Apennine brown bear stragglers

Survival and divergence in a small group: The extraordinary genomic history of the endangered Apennine brown bear stragglers

Brown and Polar Bear Y Chromosomes Reveal Extensive Male-Biased Gene Flow within Brother Lineages

Evolutionary History of Polar and Brown Bears

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