Late-Quaternary biogeographic scenarios for the brown bear (Ursus arctos), a wild mammal model species
Introduction
Patterns of genetic variation can be used to evaluate the importance of different historical processes affecting populations and species (i.e., phylogeography; Avise, 2000). Information about phylogeographic processes acting upon mammal species has been accumulated in large part through genetic studies of modern populations. However, this approach alone may be insufficient to reveal the influence of historical processes in taxa that have undergone recent demographic bottlenecks, because population reduction increases the loss of genetic diversity through stochastic drift. Analysis of modern samples also provides little information about the timing of evolutionary events (e.g., divergence between taxa), which can be essential for linking phylogeographic patterns with particular historical processes. Indeed, inferences made on the basis of modern samples alone have been characterised as ‘time trapped’ (Pääbo, 2000). In some cases, this trap can be circumvented using DNA from ancient subfossil material to provide direct information about historical phylogeographic patterns and to calibrate molecular clock analyses. However, few species offer a sufficient abundance of ancient samples for this approach to be possible. In this respect, the Quaternary phylogeography of the brown bear Ursus arctos is unusually well-studied, since genetic material from both modern and ancient samples has been extensively sampled across a wide geographic range.
Due to its large size and habit of using caves (especially as hibernacula) the brown bear has left a considerable trace in the fossil record (e.g. Sommer and Benecke, 2005, Østbye et al., 2006). Polar bears are believed to have diverged from brown bears in the late Pleistocene (see discussion below); and prior to this the brown/polar bear branch shared a common ancestor with cave bears Ursus spelaeus. Pioneering paleontological work placed the divergence between brown and cave bear lineages at approximately 1.2–1.7 million years ago (Kurtén, 1968). Evidence from more recently discovered sites (e.g., Vallonet, Atapuerca, Untermaßfeld, Cal Guardiola) has revealed apparently intermediate ancestral forms from the Epivillafranchian – 0.9–1.2 million years ago – providing broad support for Kurtén’s (1968) estimate but raising the possibility of a slightly more recent divergence time (Mazza and Rustioni, 1994, García and Arsuaga, 2001, García, 2004, Madurell-Malapeira et al., 2009). Support for the approximate timing of this divergence event has also been provided by genetic studies (Loreille et al., 2001, Korsten et al., 2009).
Currently, the brown bear is one of the largest extant terrestrial carnivores and has a wide Holarctic distribution (Fig. 1a). The status of the brown bear as a useful animal model in Pleistocene biogeography appears to have come about due to general interest in the biogeography of large mammals and concerns about the conservation of particular local brown bear populations. In addition, the modern brown bear population is widely distributed, and the relative availability of subfossil genetic samples has made large-scale genetic analysis of ancient populations possible. While certain phylogeographic patterns exhibited by modern brown bear populations have been characterised as paradigmatic (Taberlet et al., 1998, Hewitt, 2000, Korsten et al., 2009), there has been little attempt to integrate ancient and modern genetic analysis with molecular-clock timing estimates and paleontological evidence to reveal wide-scale patterns. Such an approach has the potential to shed new light on established theories (Knowles, 2009); including, in the case of the brown bear, those relating to the colonization of North America and population responses to climate change. Moreover, at a time when technological advances are permitting the use of increasingly powerful molecular methods (e.g., high-throughput sequencing), a synthesis of results derived from traditional sequencing of short molecular markers provides a baseline against which to compare new data. More generally, insights gained from the brown bear can serve as a useful guide for studies of species where data are more limited; for example, where only modern DNA sequences are available.
In this review, we synthesise the results of 33 studies published between 1991 and 2010, which to the best of our knowledge represent all matrilineal phylogeographic studies from throughout the brown bear geographical range (Table S1). Furthermore, we present valuable new genetic data from one of the oldest known fossil polar bears (dating to 115 kyBP), a species that shares a paraphyletic association with brown bears on the basis of mitochondrial studies. In order to estimate the timing of evolutionary events within the brown bear lineage, we present a new molecular clock analysis including the new polar bear sequence and a combination of paleontological and ancient DNA calibrations. Using these timing estimates, along with patterns of modern and historical phylogeographic structure, and paleontological records, we propose regional biogeographic scenarios that illustrate different processes acting on brown bears during the late Quaternary.
Section snippets
Mitochondrial sequence analysis
Currently, three basic genetic marker systems are available for animal phylogeography studies: (i) mitochondrial DNA (mtDNA), which can be used to characterise the evolution of female lineages; (ii) autosomal markers such as microsatellites, which reflect the combined history of female and male lineages; and (iii) sex chromosome markers, such as male-specific Y-chromosome microsatellites in mammals, which can be used to characterise the evolution of male lineages. In common with many animal
Sampling of modern brown bear mtDNA diversity
To provide an indication of the confidence with which conclusions about large-scale biogeographic scenarios can be drawn, it is informative to consider sampling effort throughout the brown bear range. Modern mtDNA sequences have been characterised from 22 out of the 48 countries in which the species currently occurs (Table S1; McLellan et al., 2008), with continental-scale variation existing in sampling effort. It is currently estimated that there are close to 200 000 brown bears worldwide, of
Sampling and analysis of ancient brown bear DNA
To date, ancient DNA sampling has largely focused on putative glacial refuge areas in the south and west of Europe (44 individuals) and the north-west of North America (44 individuals), with further samples derived from North Africa and the Middle East (27 individuals; Table S1). In common with analysis of modern sequences, ancient DNA analysis has concentrated on the CR; however, due to the particular challenges posed by degradation of samples (Lindahl, 1993, Willerslev and Cooper, 2005,
Global genetic diversity
An important aspect of phylogeography is the identification of monophyletic groups of individuals (i.e., clades) that share closer common ancestry with one another than with members of any other group. Among modern bear populations, a number of divergent and for the most part geographically distinct clades have been identified, largely on the basis of CR data but generally also supported by analysis of cytb (Fig. 3; node support values in Table 1). The nomenclature for the clades proposed by
The phylogenetic placement of polar bears
Mitochondrial DNA analysis of North American ursids has revealed that polar and brown bears share a paraphyletic relationship (Cronin et al., 1991, Shields and Kocher, 1991, Talbot and Shields, 1996). Thus, brown bears of subclade 2a are more closely related to polar bears (subclade 2b) than to other brown bear clades (Fig. 3). Nonetheless, the polar bear possesses many derived characters that have been used to assign species status, and its range is generally separate from that of the brown
Estimating time-scales for population divergence
In order to infer phylogeographic processes from patterns of genetic diversity, it is essential to understand the time-scales during which evolutionary events may have occurred. With such information, it becomes possible to link genetic patterns with historical parameters, such as climatic fluctuations (Hundertmark et al., 2002, Shapiro et al., 2004, Saarma et al., 2007) or domestication (Ho et al., 2008b). Various attempts have been made to estimate the timing of splits between brown bear
Regional biogeographic scenarios
The following sections combine information derived from modern and ancient mtDNA analysis, multiple-calibration estimates of divergence times and paleontological data to create regional biogeographic scenarios for brown bears during the mid-late Pleistocene and Holocene. Greatest detail is reserved for the two best-studied regions: North America and Europe.
Brown bear phylogeography in other regions
Brief summaries of brown bear phylogeography in other regions are presented here. Further discussion can be found in the Supplementary Material.
Implications for phylogeographic study and future approaches
Aside from Homo sapiens, the brown bear is arguably the best-studied extant mammal in terms of its Pleistocene–Holocene biogeography. Decades of research have revealed in considerable detail the spatial and temporal dynamics of different populations and genetic lineages. Complex patterns of migration, colonization and vicariance have been described, and inferred population responses to climate change have challenged the prevailing paradigm.
The case of the brown bear also provides a cautionary
Acknowledgements
We thank Dr G. Baryshnikov for his advice concerning interpretation of paleontological evidence. This work was supported by grants from the Estonian Ministry of Education and Sciences (target financing project SF0180122s08), the Estonian Science Foundation (grants 7040 and GLOOM0058J) and from the European Union through the European Regional Development Fund (Centre of Excellence FIBIR). SYWH was supported by the Australian Research Council.
References (127)
- et al.
On Beringian climate during the Late Pleistocene and Holocene
Quaternary Science Reviews
(2001) - et al.
Ice sheets and sea level at the last glacial maximum
Quaternary Science Reviews
(2002) - et al.
Paleomagnetism and radiochemical age estimates for Late Brunhes polarity episodes
Earth and Planetary Science Letters
(1977) Beringian paleoecology: results from the 1997 workshop
Quaternary Science Reviews
(2001)- et al.
Ursus dolinensis: a new species of Early Pleistocene ursid from Trinchera Dolina, Atapuerca (Spain)
Comptes Rendus de l’Académie des Sciences, Sciences de la Terre et des planètes
(2001) - et al.
An Ice Age refugium for large mammals in the Alexander Archipelago, southeastern Alaska
Quaternary Research
(1996) Some genetic consequences of ice ages, and their role in divergence and speciation
Biological Journal of the Linnean Society
(1996)Post-glacial re-colonization of European biota
Biological Journal of the Linnean Society
(1999)Sea level history in Beringia during the past 250,000 years
Quaternary Research
(1973)- et al.
Mitochondrial phylogeography of moose (Alces alces): late Pleistocene divergence and population expansion
Molecular Phylogenetics and Evolution
(2002)
Pleistocene Maximum and Late Wisconsin glacier extents across Alaska, U.S.A
Ancient DNA analysis reveals divergence of the cave bear, Ursus spelaeus, and brown bear, Ursus arctos, lineages
Current Biology
Late Quaternary palaeoenvironments of northwestern North America
Quaternary Science Reviews
New developments in ancient genomics
Trends in Ecology and Evolution
Les faunes de grands mammifères de la Caune de l’Arago (Tautavel) dans le cadre biochronologique des faunes du Pléistocène moyen italien
Anthopologie
Paviland cave: contextualizing the Red Lady
Antiquity
Phylogeography: The History and Formation of Species
Dynamics of Pleistocene population extinctions in Beringian brown bears
Science
Assessing the causes of Late Pleistocene extinctions on the continents
Science
Funds enough, and time: mtDNA, nuDNA and the discovery of divergence
Molecular Ecology
Fauna of Russia and Neighbouring Countries
Chronology and correlation of Quaternary magnetostratigraphy and nannofossil biostratigraphy in Norwegian-Greenland sea sediments
Geologische Rundschau
Deciphering the complete mitochondrial genome and phylogeny of the extinct cave bear in the Paleolithic painted cave of Chauvet
Proceedings of the National Academy of Sciences of the United States of America
Palaeomagnetic and U-series dating of cave sediments in Baradla cave, Hungary
Acta Carsologica
Holarctic phylogeography of the root vole Microtus oeconomus: implication for late Quaternary biogeography of high latitudes
Molecular Ecology
Ancient DNA evidence for the loss of a highly divergent brown bear clade during historical times
Molecular Ecology
Genetic diversity of endangered brown bear Ursus arctos populations at the crossroads of Europe, Asia and Africa
Diversity and Distributions
Map of Glacial Limits and Possible Refugia in the Southern Alexander Archipelago, Alaska
Possible refugia in the Alexander Archipelago in southeastern Alaska during the Wisconsin glaciation
Canadian Journal of Earth Sciences
Revealing the history of sheep domestication using retrovirus integrations
Science
Grizzly bear (Ursus arctos)
Genetic relationships of grizzly bears Ursus arctos in the Prudhoe Bay region of Alaska: inference from microsatellite DNA, mitochondrial DNA, and field observations
Journal of Heredity
Interspecific and intraspecific mitochondrial-DNA variation in North-American bears (Ursus)
Canadian Journal of Zoology
Genetic variation and relatedness of grizzly bears in the Prudhoe Bay region and adjacent areas in northern Alaska
Ursus
Ice age terrestrial carbon changes revisited
Global Biogeochemical Cycles
Theriofauna formation in the Late Pleistocene and Holocene on the territory of the Republic of Moldova
Archäologie in Eurasien
Late Pleistocene mammal fauna from the Late Palaeolithic butchering site Cos uti 1, Moldova
Acta Zoologica Cracoviensa
Looking forwards or looking backwards in avian phylogeography? A comment on Zink and Barrowclough
Molecular Ecology
The life and times of the Bering land bridge
Nature
Karyotype variability in Sorex araneus L. Insectivora, Mammalia
Chromosomes Today
Genetic resolution of the composition and phylogenetics placement of the Isabelline bear
Ursus
New results on the remains of Ursidae from Untermassfeld: comparisons with Ursus dolinensis from Atapuerca and other early and middle pleistocene sites
Intraspecific phylogenetic analysis of Siberian woolly mammoths using complete mitochondrial genomes
Proceedings of the National Academy of Sciences of the United States of America
Refugia within refugia: patterns of phylogeographic concordance in the Iberian Peninsula
Fossil grizzly bears (Ursus arctos) from Prince of Wales Island, Alaska, offer new insights into animal dispersal, interspecific competition, and age of deglaciation
Current Research in the Pleistocene
The Late Wisconsin vertebrate history of Prince of Wales Island, Southeast Alaska
Hybrid zones – natural laboratories for evolution studies
Trends in Ecology and Evolution
The genetic legacy of the Quaternary ice ages
Nature
Chronologie Th/U des concrétions calcaires des varves du lac glaciaire de Deschaillon (Wisconsinien inférieur)
Canadian Journal of Earth Sciences
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2020, Encyclopedia of the World's Biomes