OR I G I N A L A R T I C L E

Large-scale migrations of brown bears in Eurasia and to NorthAmerica during the Late Pleistocene

Peeter Anijalg1 | Simon Y. W. Ho2 | John Davison1 | Marju Keis1 | Egle Tammeleht1 |

Katalina Bobowik2 | Igor L. Tumanov3 | Alexander P. Saveljev4 | Elena A. Lyapunova5 |

Alexandr A. Vorobiev6 | Nikolai I. Markov6 | Alexey P. Kryukov7 | Ilpo Kojola8 |

Jon E. Swenson9,10 | Snorre B. Hagen11 | Hans Geir Eiken11 | Ladislav Paule12 |

Urmas Saarma1

1Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia

2School of Life and Environmental Sciences, University of Sydney, Sydney, NSW, Australia

3West Branch, Russian Research Institute of Game Management and Fur Farming, Saint Petersburg, Russia

4Russian Research Institute of Game Management and Fur Farming, Kirov, Russia

5N.K. Koltzov Institute of Developmental Biology, Russian Academy of Sciences, Moscow, Russia

6Institute of Plant and Animal Ecology, Ural Branch of Russian Academy of Sciences, Yekaterinburg, Russia

7Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch of the Russian Academy of Sciences, Vladivostok, Russia

8Natural Resources Institute, Rovaniemi, Finland

9Faculty of Environmental Sciences and Natural Resource Management, Norwegian University of Life Sciences, �As, Norway

10Norwegian Institute for Nature Research, Trondheim, Norway

11NIBIO, Norwegian Institute of Bioeconomy Research, Svanvik, Norway

12Faculty of Forestry, Technical University, Zvolen, Slovakia

Correspondence

Urmas Saarma, Department of Zoology,

Institute of Ecology and Earth Sciences,

University of Tartu, Tartu, Estonia.

Email: Urmas.Saarma@ut.ee

Funding information

Seventh Framework Programme, Grant/

Award Number: contracts 247652 and

2096/7. PR UE/2011/2; Estonian Ministry

of Education and Research, Grant/Award

Number: IUT20-32

Editor: Gerald Schneeweiss

Abstract

Aim: Climatic changes during the Late Pleistocene had major impacts on popula-

tions of plant and animal species. Brown bears and other large mammals are likely

to have experienced analogous ecological pressures and phylogeographical pro-

cesses. Here, we address several unresolved issues regarding the Late Pleistocene

demography of brown bears: (1) the putative locations of refugia; (2) the direction

of migrations across Eurasia and into North America; and (3) parallels with the

demographic histories of other wild mammals and modern humans.

Location: Eurasia and North America.

Methods: We sequenced 110 complete mitochondrial genomes from Eurasian

brown bears and combined these with published sequences from 138 brown bears

and 33 polar bears. We used a Bayesian approach to obtain a joint estimate of the

phylogeny and evolutionary divergence times. The inferred mutation rate was com-

pared with estimates obtained using two additional methods.

Results: Bayesian phylogenetic analysis identified seven clades of brown bears, with

most individuals belonging to a very large Holarctic clade. Bears from the wide-

spread clade 3a1, which has a distribution from Europe across Asia to Alaska, shared

a common ancestor about 45,000 years ago.

DOI: 10.1111/jbi.13126

394 | © 2017 John Wiley & Sons Ltd wileyonlinelibrary.com/journal/jbi Journal of Biogeography. 2018;45:394–405.

Main conclusions: We suggest that the Altai-Sayan region and Beringia were impor-

tant Late Pleistocene refuge areas for brown bears and propose large-scale migra-

tion scenarios for bears in Eurasia and to North America. We also argue that brown

bears and modern humans experienced a demographic standstill in Beringia before

colonizing North America.

K E YWORD S

Altai, Beringia, climate change, mitochondrial genome, molecular clock, phylogeography, Ursus

arctos

1 | INTRODUCTION

Climatic fluctuations during the Pleistocene have shaped the distri-

bution, genetic structure, and diversity of present-day species in Eur-

asia and North America. During the Last Glacial Maximum (LGM;

26.5–19 kya), many high-latitude areas were covered by continental

ice sheets and temperate species were largely restricted to warmer

and more hospitable areas known as glacial refugia (Hofreiter & Ste-

wart, 2009). Some southern parts of Europe, such as the Mediter-

ranean peninsulas, have long been recognized as LGM refugia for

temperate species. There is also growing recognition of more north-

erly refugia in Europe, including the Carpathian Mountains (Def-

fontaine et al., 2005; Kotl�ık et al., 2006; Saarma et al., 2007; Schmitt

& Varga, 2012).

In phylogeographical studies of large mammals, the brown bear

(Ursus arctos L.) has been a model species. This is largely due to its

wide past and present distribution, as well as female philopatry (Davi-

son et al., 2011). In historical times, brown bears were common in

most parts of Eurasia and in the western part of North America down

to northern Mexico (Kurt�en, 1968). Present-day bear populations

occupy somewhat smaller areas, with many populations fragmented

mainly because of human persecution and loss of suitable habitat

(Davison et al., 2011; Swenson, Taberlet, & Bellemain, 2011). The lar-

gest brown bear population in northern Eurasia stretches from Scan-

dinavia to the Russian Far East and is associated predominantly with

the occurrence of boreal and temperate forests. The range is

restricted by tundra in the north and by dry steppe in the south

(Servheen, Herrero, & Peyton, 1999). However, the Gobi bear in

Mongolia is desert-dwelling (McCarthy, Waits, & Mijiddorj, 2009),

indicating that brown bears can survive in fairly hostile environments.

For many species, including the brown bear, long-term isolation

of populations in separated glacial refugia resulted in genetic diver-

gence among populations, loss of genetic variability and complex

patterns of migrations during the Late Pleistocene and Holocene

(Davison et al., 2011; Hewitt, 2000; Taberlet, Fumagalli, Wust-Saucy,

& Cosson, 1998). However, despite the wide Eurasian distributions

of many species, including several model species for biogeography,

we lack an equivalent understanding of the processes influencing

populations in Asia.

Analysis of genetic markers has provided a highly informative

means of reconstructing both ancient and contemporary patterns of

diversity and demography. Important insights into geographical varia-

tion among populations of animals, such as those of the brown bear,

have been gained through analyses of autosomal loci (Swenson

et al., 2011; Tammeleht et al., 2010), Y-chromosome markers (Bidon

et al., 2014; Schregel et al., 2015), and other sources of data, such

as diet (Vulla et al., 2009). Based on complete mitogenome

sequences of brown bears in north-western Eurasia, Keis et al.

(2013) identified population structuring, demographic history, and

spatial population processes that had not previously been detected

using shorter sequences.

We expect that a wider analysis of mitogenomes from Eurasia to

North America will help to expose new details of ancient population

processes and their time-frame. Mitochondrial DNA has been a pre-

ferred genetic marker for studying bears for several reasons. Perhaps

the most relevant to phylogeographical studies is that because

female brown bears are philopatric, the phylogeographical signal is

better preserved in mitochondrial DNA than in autosomal markers or

the Y-chromosome. However, the phylogeographic history of the

female lineage does not necessarily coincide with that of the whole

species (Davison et al., 2011). A notable example of this is the mito-

chondrial paraphyly of brown bears (Talbot & Shields, 1996), which

stands in contrast with the clear support for monophyly from male-

specific (Bidon et al., 2014) and biparental markers (Liu et al., 2014).

The present-day European population of brown bears consists of

two main mitochondrial lineages, the eastern (clade 3a) and western

(clade 1), of which the latter is divided into subclades 1a and 1b

(Taberlet & Bouvet, 1994). These clades and subclades exhibit con-

siderable geographical differentiation. Subclade 1a originated from

an Iberian refuge and is now found in southwestern Europe and

southern Scandinavia; however, the recolonization of southern Scan-

dinavia was most likely not limited to migrations from a single refu-

gium (Bray et al., 2013). In contrast, subclade 1b has virtually

remained in its refugial territory in the south and east of Europe

(Italy and Balkans). In North America, four mitochondrial clades have

been identified in contemporary brown bears: clade 2a on the Admi-

ralty, Baranof, and Chichagof (ABC) islands of Alaska, clade 3a1 in

western Alaska, clade 3b in eastern Alaska, and clade 4 in the south-

ern distribution of the species in continental North America (Davison

et al., 2011; Hirata et al., 2013).

The eastern clade present in Europe (3a) divides further into sub-

clades 3a1 and 3a2 (Hirata et al., 2013). Subclade 3a1 extends from

ANIJALG ET AL. | 395

Fennoscandia to East Asia, and into North America (Keis et al.,

2013; Korsten et al., 2009; Murtskhvaladze, Gavashelishvili, & Tarkh-

nishvili, 2010; Saarma & Kojola, 2007; Waits, Talbot, Ward, &

Shields, 1998). Other clades in Asia appear geographically rather

confined: clade 3a2 to central Hokkaido, 3b to eastern Hokkaido,

the Russian Far East and southern Siberia (Tomsk region), clade 4 to

southern Hokkaido, and clade 5 to Tibet (Guskov, Sheremeteva,

Seredkin, & Kryukov, 2013; Hirata et al., 2013; Salomashkina, Kholo-

dova, Tutenkov, Moskvitina, & Erokhin, 2014).

Although broad patterns of mitogenomic composition are known

for Asian brown bear populations, phylogeographical syntheses of

these patterns remain tentative. The widespread sublineage 3a1 is

believed to have emerged from multiple glacial refugia, but the loca-

tions of putative areas in Asia remain unknown. The Siberian plains

and mountains were largely unglaciated during the LGM, represent-

ing potential refugia (Davison et al., 2011). Indeed, several studies

have suggested that the Altai-Sayan region in south-central Siberia

was one of the most important Asian refugia during the Late Pleis-

tocene, due to its stable climatic conditions and species richness

throughout this period of time (Pavelkov�a �Ri�c�ankov�a, Robovsk�y, &

Riegert, 2014; Pavelkov�a �Ri�c�ankov�a, Robovsk�y, Riegert, & Zrzav�y,

2015). Moreover, modern humans are known to have inhabited the

Altai region for at least 45 kyr (Goebel, 1999) and the area played a

significant role in the peopling of Siberia and North America (Dulik

et al., 2012). Reconstructing the migrations of modern humans dur-

ing the Late Pleistocene and early Holocene (c. 50–10 kya) poses a

major challenge, because of the small population size and low den-

sity of archaeological sites during this period. However, other large

mammal species that shared similar ecological demands as modern

humans, such as the brown bear, wapiti (Cervus canadensis; Meiri

et al., 2014) and grey wolf (Canis lupus; Koblm€uller et al., 2016), rep-

resent a largely unexploited source of information that can also

improve our understanding of the drivers of ancient population pro-

cesses in modern humans.

Several other geographical regions are of potential relevance for

understanding genetic diversity in Asia and links with the adjacent

regions of Europe and North America. First, there is evidence to sug-

gest that the Ural Mountains acted as a glacial refugium for animals

and modern humans at the border of Europe and Asia (Svendsen

et al., 2010). Another refugium is believed to have been located in

Beringia, the area stretching from the Verkhoyansk Mountains and

Lena River Basin in eastern Eurasia to Alaska and the Northwest

Territories of Canada in North America. Compared with areas of sim-

ilar latitude, the climate in Beringia stayed relatively mild and ice-free

during the LGM due to the warm North Pacific circulation (Lambeck,

Yokoyama, & Purcell, 2002). The Bering Land Bridge, which emerged

during times of low sea level, allowed migrations of mammals

between Eurasia and North America several times during the Pleis-

tocene.

The aim of this study was to investigate the Late Pleistocene

phylogeographical history of brown bears in Eurasia and their colo-

nization of North America. We sequenced the complete mitochon-

drial genomes of 110 brown bears across Eurasia and included

publicly available data from Eurasia to North America in a dated phy-

logenetic analysis. We hypothesized that: (1) the widely distributed

clade 3a1 would display Eurasia-wide structure that has not been

apparent using lower-resolution genetic markers; and (2) populations

were restricted to refugia in the areas of Altai, Beringia and the

Urals, such that the ages of the clades containing individuals from

these areas are consistent with the timing of glacial restriction. We

also compared our data with existing information from modern

humans and other mammal species to assess the generality of Late

Pleistocene migration scenarios.

2 | MATERIALS AND METHODS

Tissue samples from 110 brown bears, legally harvested between

1999 and 2010 for purposes other than this study, were used for

full mitochondrial DNA sequencing. These included three from

Romania, five from Estonia, five from Sweden, 10 from Finland and

87 from the Russian Federation (Figure 1). For DNA extraction, we

used the High PCR Template Preparation Kit (Roche Diagnostics,

Mannheim, Germany) following the manufacturer’s instructions.

PCR and sequencing of the complete mitochondrial genomes

was done as described by Keis et al. (2013), with a modified set of

primers; we replaced six primers with newly designed ones to

improve mitogenome assembly (Table S1 in Appendix S1). All

sequences have been deposited in GenBank (accession numbers

KY419593–KY419702). For phylogenetic analysis, we added

sequences from 138 brown bears and 33 polar bears (U. maritimus)

from GenBank (Table S4 in Appendix S1). In total, our data set con-

tained 281 mitogenome sequences from brown bears and polar

bears.

To estimate the matrilineal phylogeny and evolutionary time-

scale of brown bears, we analysed complete mitogenomes using a

Bayesian approach in BEAST 1.8.4 (Drummond, Suchard, Xie, & Ram-

baut, 2012). The best-fitting partitioning scheme was chosen based

on the Bayesian information criterion using PartitionFinder (Lanfear,

Calcott, Ho, & Guindon, 2012), which partitioned the alignment

into six subsets: D-loop, rRNA genes, tRNA genes, and the three

codon positions of all 13 protein-coding genes. We compared con-

stant-size and skyride coalescent models for the tree prior using

Bayes factors in BEAST, calculated using the stepping-stone estimator

of the marginal likelihood (Xie, Lewis, Fan, Kuo, & Chen, 2011).

The constant-size model was decisively favoured (BF > 100) and

we used this to provide the prior for the tree topology and relative

node times.

We analysed the partitioned alignment using a strict molecular

clock, owing to the intraspecific nature of the data. Preliminary anal-

yses using a more parameter-rich uncorrelated lognormal relaxed

clock led to poor mixing and convergence in our analyses. A rate

multiplier was specified for each data subset. The molecular clock

was calibrated by the inclusion of a sequence from an ancient polar

bear (age 120,000 years; GU573488). Estimates of posterior distri-

butions were obtained via Markov chain Monte Carlo sampling, with

396 | ANIJALG ET AL.

samples drawn every 5,000 steps over a total of 50,000,000 steps.

Each analysis was run in duplicate and the samples were combined

after removing the first 10% as burn-in. We checked that the effec-

tive sample sizes of all parameters were >200.

We performed a date-randomization test to investigate the

performance of the sequence ages as calibrations for the molecu-

lar clock (Ramsden, Holmes, & Charleston, 2009) and generated

10 replicate data sets in which the sequence ages were randomly

reassigned. The mean rate estimate from the original data set was

not included in the 95% credibility intervals (CI) of the rate esti-

mates from any of the 10 date-randomized replicates. Further-

more, the rate estimates from the date-randomized replicates had

long lower tails that spanned multiple orders of magnitude. In

combination, these features suggest that the original data set has

sufficient temporal structure and spread for calibrating the esti-

mate of the rate (Duchene, Duchene, Holmes, & Ho, 2015; Ho

et al., 2011).

As an independent check on the reliability of the rate estimate,

we analysed the data using two other tip-dating methods: root-to-

tip regression and least-squares dating. For both of these methods,

we inferred a phylogenetic tree using maximum likelihood with 100

random starts in RAxML 8.2.4 (Stamatakis, 2014). The inferred phy-

logram was then used for regression of root-to-tip distances against

sampling time in TempEst (Rambaut, Lam, Carvalho, & Pybus, 2016)

and for least-squares dating in LSD (To, Jung, Lycett, & Gascuel,

2016).

3 | RESULTS

Our Bayesian phylogenetic analysis of 281 mitogenome sequences

from brown bears to polar bears distinguished eight clades (Fig-

ure 2). According to the prevailing terminology (Davison et al., 2011;

Hirata et al., 2013), these clades are: 1 and 2a (and 2b for polar

bears) representing the western lineage; and 3a1, 3a2, 3b, 4 and 5

representing the eastern lineage. All newly sequenced samples fell

into the widely distributed clade 3a1, except for one sample from

Sweden which belonged to western clade 1.

In our Bayesian phylogenetic analysis, the mitogenomic mutation

rate was estimated at 2.48 9 10�8 mutations per site per year, with a

95% CI of 1.93 9 10�8 to 3.04 9 10�8 mutations per site per year.

This estimate was slightly lower than the estimate based on regression

of root-to-tip distances against sample age (3.35 9 10�8 mutations

per site per year), but similar to the rate estimated using least-squares

dating (2.84 9 10�8 mutations per site per year).

The most recent common ancestor (MRCA) of clade 3a1 lived

c. 45 kya (95% CI: 31–58 kya) (Figure 2; see also Table S2 and

Table S3 for 95% CIs, in Appendix S1). This split separated brown

bears currently inhabiting Romania and Bulgaria from the rest of the

3a1 clade. The latter diverged 37 kya (95% CI: 27–48 kya) into two

large subclades: (1) a Kamchatkan–Alaskan subclade comprising bears

from Alaska and Kamchatka (34 kya, 95% CI: 24–44 kya); and (2) a

Eurasian subclade that includes bears inhabiting the vast area from

eastern Europe to the Russian Far East (32 kya, 95% CI 23–42 kya).

F IGURE 1 Map showing locations ofEurasian and North American brown bearsanalysed in this study: 110 newlysequenced mitogenomes (circles) and 138from databases (triangles). Colourscorrespond to clades in Figure 2[Colour figure can be viewed atwileyonlinelibrary.com]

ANIJALG ET AL. | 397

Following the formation of the Kamchatkan-Alaskan subclade,

the Alaskan bears separated from the Kamchatkan bears (27 kya,

95% CI 19–36 kya). The latter formed two clusters: “to E-Kam-

chatka” (14 kya, 95% CI 7–21 kya), consisting mostly of bears

inhabiting the north-eastern part of the peninsula; and “to W-Kam-

chatka” (25 kya, 95% CI 17–33 kya), largely represented by bears

from the south-western part of the peninsula. The Eurasian subclade

divided into lineages that reached Primorye, Sakhalin, and Kam-

chatka (27 kya, 95% CI 18–37 kya) and one that spread widely in

Eurasia (29 kya, 95% CI 21–38 kya). The latter divided further into

two: bears that eventually reached Europe and bears that migrated

to the Urals and to Magadan region, with only minimal overlap in

the Perm and Sverdlovsk regions.

4 | DISCUSSION

Although the phylogeography of European mammals has been stud-

ied fairly extensively, we have only a fragmentary understanding of

the phylogeographical processes affecting mammals in the vast terri-

tory of northern Eurasia. An important step towards improving this

knowledge is to gain a reliable estimate of the evolutionary rate and

time-scale of each species (Ho, Saarma, Barnett, Haile, & Shapiro,

2008). Our analyses confirm previous suggestions that a single

ancient DNA sequence can be sufficient for calibrating the molecular

clock, provided that it is sufficiently old in comparison with the evo-

lutionary time-scale of the samples in the data set (Molak, Lorenzen,

Shapiro, & Ho, 2013). This is further supported by the consistency in

our estimates of the mutation rate using three different methods.

To date, only shallow regional genetic structure has been

detected among several mammal species occurring across northern

Eurasia (e.g. Hindrikson et al., 2017; Korsten et al., 2009). However,

that emerging picture is by no means definitive, as these compar-

isons were made using relatively short mitochondrial sequences

(Davison et al., 2011). Based on our analyses of complete mitogen-

ome data, we propose several scenarios of brown bear migration

across Eurasia and to North America during the last 50 kyr

(Figure 3).

F IGURE 2 Bayesian phylogenetic tree of brown bears inferred from mitochondrial genomes. The numbers on nodes and after cladesrepresent posterior mean estimates of the ages of different bear lineages, with numbers in parentheses representing the 95% credibilityintervals. Red circles at nodes represent posterior probabilities >0.95. The blue vertical columns represent long cold periods according to Ahnand Brook (2014). The tree is drawn to a time-scale, with node ages given in thousands of years before present. Colours indicate differentmitochondrial clades. Colours of clades correspond to those in Figure 1 [Colour figure can be viewed at wileyonlinelibrary.com]

398 | ANIJALG ET AL.

4.1 | Spatial distribution of bear clade 3a in theLate Pleistocene

The full distribution of clade 3a bears around 50 kya remains

unknown, but existing data indicate that the distribution could have

been wide. Two radiocarbon-dated 3a bear samples are known from

this period, both c. 47 ky old: one from Ramesch Cave, Austria

(Hofreiter et al., 2004) and the other from Tain Cave in the Urals,

Russia (Bray, 2010). The distribution of clade 3a probably reached

even farther east. One of the arguments to support this is the

F IGURE 3 Possible distribution and migration scenarios of brown bears from clade 3a1 in the Late Pleistocene. Colours correspond tothose in Figures 1 and 2. Excerpts of the corresponding parts of the phylogenetic tree (according to Figure 2) are shown on the right of eachpanel. Subfossils are marked by large brown circles [Colour figure can be viewed at wileyonlinelibrary.com]

ANIJALG ET AL. | 399

divergence of 3a1 and 3a2 that started c. 53 kya (95% CI: 38–

71 kya). As 3a2 bears are found only in Hokkaido (Hirata et al.,

2013), the likely distribution of 3a bears before the split extended to

eastern Asia. The vast distribution is also supported by the biotope

map in Hoogakker et al. (2016) which shows that around 54 kya

boreal and temperate forests covered a continuous area from west-

ern Europe to the Russian Far East (Figure 4c). The wide distribution

of the 3a lineage might have been ruptured by significant global cli-

mate cooling about 48–54 kya (Kindler et al., 2014), with these

bears potentially restricted to different refugia (Figure 3a).

The most recent common ancestor of clade 3a1 lived 45 kya

(95% CI: 31–58 kya). This clade split into two mitochondrial lineages,

the first of which is represented by bears from Romania to Bulgaria.

These might be descendants of ancient bears that lived in central

Europe c. 50 kya (e.g. the individual from Ramesch Cave) that found

refuge south of the Carpathian Mountains. The Carpathian region

probably acted as a glacial refugium for brown bears, as previously

suggested by Sommer and Benecke (2005) and Saarma et al. (2007),

and also for other species, such as the common vole (Microtus arva-

lis) (Stojak, McDevitt, Herman, Searle, & W�ojcik, 2015) and weasel

(Mustela nivalis) (McDevitt et al., 2012). Two other Romanian sam-

ples belonged to the much larger second lineage of 3a1 (Figure 2),

which moved across Eurasia and to North America. This suggests

that bears made their way to the Carpathians (Romania) not only

from the north (central Europe), but also from the east (from the

Altai-Sayan region, discussed below).

The clade that spread throughout Eurasia and part of North

America shared a most recent common ancestor about 37 kya (95%

CI: 27–48 kya; Figure 3b). Several lines of evidence suggest that this

ancestral population was restricted to a refuge area in the mountain-

ous Altai-Sayan region of Central Asia. This region is known as a bio-

diversity hotspot for temperate flora and fauna, having maintained

high ecological stability since the Late Pleistocene (Allen et al., 2010;

Huntley et al., 2013). Detailed analysis of the Late Pleistocene mam-

mal assemblages in the Altai region has shown that no significant

changes in composition or ecological structure occurred between the

F IGURE 4 Maps showing the extent ofdifferent biotopes (a) 6 kya, (b) 21 kya and(c) 54 kya (modified from Hoogakker et al.,2016). Note that the precise distribution ofbiotypes – for example the extent of forestin central Eurasia in periods (b) and (c) –comes with a degree of uncertainty (seeHoogakker et al., 2016 for discussion)Potential refuge areas are shown withdashed lines [Colour figure can be viewedat wileyonlinelibrary.com]

400 | ANIJALG ET AL.

Late Pleistocene and the Holocene, providing a modern analogue for

the Pleistocene communities (Agadjanian & Serdyuk, 2005;

Pavelkov�a �Ri�c�ankov�a et al., 2014, 2015).

The Altai-Sayan region is at the geographical centre of the brown

bear 3a1 distribution, making it the most parsimonious location for

the ancestral refuge area. Furthermore, historical bear samples exhi-

bit higher genetic diversity in this region than elsewhere in northern

Eurasia (Hirata, Abramov, Baryshnikov, & Masuda, 2014). The Altai-

Sayan region is likely to have served as an important glacial refugium

for modern humans and as an important route for the peopling of

northern Asia (Derenko et al., 2014).

4.2 | Colonizing North America

One of the major subclades of 3a1 bears headed towards Beringia,

eventually colonizing Kamchatka and Alaska. Bears from the other

major subclade of 3a1 dispersed widely throughout Eurasia. Interest-

ingly, bears in the Magadan area, a region close to Kamchatka, were

neither part of the migration wave that colonized the Kamchatka

Peninsula, nor part of the wave that entered North America. Rather,

these bears apparently did not move farther north-east. However,

we found a bear from the east Asian migration in Kamchatka (Fig-

ure 3c), suggesting that some bears from this population eventually

reached Kamchatka, perhaps somewhat later than bears that were

part of the earlier migration that colonized North America.

Brown bears belonging to the Kamchatkan-Alaskan mitochondrial

subclade apparently entered western Beringia before the beginning

of the LGM, because north-eastern territories outside Beringia were

mainly polar desert during the LGM and unsuitable for brown bears

(Ray & Adams, 2001). Indeed, Pitulko et al. (2004) described c. 34-

kyr-old brown bear remains at the Yana site (Yana RHS), whereas

Bray (2010) was able to sequence a 135-bp mitochondrial fragment

of a c. 30-kyr-old brown bear sample from Indigirka area that

belonged to clade 3a. Both sites are in western Beringia, providing

evidence that brown bears were present there before the LGM.

Moreover, our data suggest that the Kamchatkan-Alaskan subclade

also reached western Beringia around that time (see discussion

about Kamchatka below). There is no biotope map relating to this

time period, but the 54 kya map shows an almost continuous distri-

bution of boreal forest from Eurasia to central Beringia (Figure 4c).

Around 37 kya this distribution was probably interrupted by abrupt

climate change, thus separating the Kamchatkan-Alaskan subclade.

The MRCA of the Alaskan brown bears lived 22 kya (95% CI:

13–32 kya; Figure 2). The most likely location of these bears was

west of the current Bering Strait, where they remained for about 6–

7 thousand years (Beringian Standstill), before crossing the Bering

Land Bridge and reaching Alaska c. 15 kya. The Beringian Standstill

hypothesis was originally proposed for migrations of modern

humans, whereby the ancestors of Native Americans remained in

western Beringia for thousands of years before migrating to North

America (Tamm et al., 2007). During this time the climatic conditions

were unsuitable for modern humans at higher latitudes outside the

land bridge (Hoffecker, Elias, & O’Rourke, 2014). The biotope map

describing the LGM (Figure 4b) shows that central Beringia was cov-

ered by boreal forest, providing suitable habitat for brown bears.

There has been growing genetic support for the standstill hypothesis

(Watson, 2017), including evidence from ancient mitochondrial gen-

omes from modern humans (Llamas et al., 2016). A study of wapiti

also found that this species was present in western Beringia

c. 50 kya, but did not advance to North America until 15 kya (Meiri

et al., 2014).

The favourable conditions for many plant and animal species in

western and central Beringia during the LGM are believed to have

been caused by the North Pacific circulation, which brought warm

and moist air to the area (Brubaker, Anderson, Edwards, & Lozhkin,

2005; Hoffecker et al., 2014; Willerslev et al., 2014). However, such

good conditions were not available in eastern Beringia before

15 kya. Here the environment was apparently a cold, semi-arid, and

treeless steppe-tundra, suitable only for species adapted to extreme

cold, such as woolly mammoths (Mammuthus primigenius) (Guthrie,

2001).

Synchrony in the timing of colonization and expansion implies

that the ecology of large mammals, such as the wapiti and brown

bear, includes key limiting factors that can enhance our understand-

ing of the ancient movements of modern humans (Meiri et al.,

2014). However, despite similarities between the migrations of

brown bears and modern humans towards North America c. 15 kya,

there are also some important differences. Brown bears are known

to have colonized North America earlier; clades 2c, 3c, and 4 were

already in North America before the last glaciation (Barnes, Matheus,

Shapiro, Jensen, & Cooper, 2002; Davison et al., 2011). The genetic

diversity of Beringian brown bears in the pre-glacial period

(c. 40 kya) was higher than that of modern North American popula-

tions, but by 15 kya the genetic diversity was similar to that of con-

temporary bears in the New World (Leonard, Wayne, & Cooper,

2000).

4.3 | Colonizing the Kamchatka Peninsula

The extent and timing of the last glaciation in Kamchatka were lar-

gely influenced by the Laurentide Ice Sheet (Barr & Solomina, 2014).

The ice is believed to have advanced in two major stages in Late

Pleistocene Kamchatka: the first advance was extensive and

occurred between 60 and 31 kya; the more recent advance was less

extensive, characterized primarily by mountain glaciation, and coin-

cided with the LGM. The MRCA of brown bears that colonized

North America and Kamchatka was dated to 34 kya (95% CI: 24–

44 kya), coinciding with the end of the major glaciation on Kam-

chatka. At this point, bears would have been able to occupy the ter-

ritory in the vicinity of the peninsula, or even enter the peninsula to

some extent. The biotope map (Figure 4b) shows that boreal forests

were present to a limited extent in northern Kamchatka during the

LGM, making it a suitable habitat for brown bears that later colo-

nized the peninsula.

Kurt�en (1968) mentioned that the American broad-skulled bears

morphologically resemble the Kamchatkan bears, whereas the

ANIJALG ET AL. | 401

American narrow-skulled bears are more similar to the bears from

north-eastern Siberia. The morphological resemblance might be the

result of diet, because the largest bears occur in regions where they

have access to large amounts of meat, especially salmon (Hilderbrand

et al., 1999). Another mammal species, the northern red-backed vole

(Myodes rutilus), exhibits a similar Kamchatkan-Alaskan clade (Kohli,

Fedorov, Waltari, & Cook, 2015). The close phylogenetic association

between Alaskan and Kamchatkan populations in these two species

points to a migration pattern that might also be shared by other

mammals.

4.4 | Large-scale migrations across Siberia andexpansion to Europe

The MRCA of the Eurasian subclades was dated to 32 kya (95% CI:

23–42 kya). At this point, most of the Eurasian bears split from the

branch that today can be found in the Primorye region, Sakhalin

Island and Kamchatka, suggesting that at least some bears managed

to reach Kamchatka after the initial colonization of the peninsula

(Figure 3c). Bears from this subclade were probably restricted to a

refuge area in the Far East during the LGM, a plausible region being

the Manchurian Plain. According to the climate model by Hoogakker

et al. (2016), around 21 kya the Manchurian Plain was suitable for

boreal and temperate forests, making it potentially habitable for

brown bears (Figure 4b).

The other Eurasian branch split into two around 29 kya (95% CI:

21–38 kya; Figure 3d). One of the lineages moved west towards the

Ural Mountains and the other eastward. The Ural Mountains have

been suggested as a LGM refugium for several animal species, such

as the field vole (Microtus agrestis) (Jaarola & Searle, 2002). The

MRCA of European bears lived around 25 kya (95% CI: 17–32 kya)

and, as conditions improved, this lineage colonized eastern and

northern Europe, reaching Romania (Figure 3d). The clade that

remained east of the Ural Mountains started to diverge about

25 kya (95% CI: 17–34 kya; Figure 3d). One lineage migrated

towards the Ural Mountains and the other towards Magadan region.

Although the western migration reached the Ural Mountains, this lin-

eage has not been found farther west than the Perm region on the

western slopes of the Urals. As with the 3a1 clade in brown bears,

the common juniper (Juniperus communis) also has a dominant and

widespread clade in Eurasia (Hantemirova et al., 2017), although it

does not reach as far east.

In conclusion, our mitogenome analysis of brown bears in Eurasia

and North America demonstrates that this species shared several

population processes in common with wapiti and modern humans

during the last 50 thousand years, including the Beringian Standstill.

This suggests that wild mammal species and modern humans

responded to the same key limiting factors in the Late Pleistocene.

ACKNOWLEDGEMENTS

The authors thank three anonymous reviewers for their insightful

comments and suggestions, and Dr. Frank Zachos for his generous

help. We also thank Eline Lorenzen for providing sequence data. This

work was supported by the institutional research funding (grant

IUT20-32) from the Estonian Ministry of Education and Research;

BIOGEAST – Biodiversity of East-European and Siberian large mam-

mals on the level of genetic variation in populations, 7th Framework

Programme (contracts 247652 and 2096/7. PR UE/2011/2); Aus-

tralian Research Council; Swedish Environmental Protection Agency;

Norwegian Environment Agency; Research Council of Norway; and

the Finnish Ministry of Agriculture and Forestry.

ORCID

Urmas Saarma http://orcid.org/0000-0002-3222-571X

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BIOSKETCH

Peeter Anijalg is interested in brown bear phylogeography and

population genetics, and the impact of climate change on ancient

and contemporary animal population processes. The remaining

authors have broad interests in molecular ecology, phylogeogra-

phy and biogeography, particularly relating to animals of the Late

Pleistocene and Holocene.

Author contributions: U.S. and P.A conceived the original idea;

all authors collected the data; P.A., S.Y.W.H., K.B., J.D. and U.S.

analysed the data; P.A., S.Y.W.H., J.D. and U.S. wrote the first

draft of the manuscript and all authors contributed to writing

the final version.

SUPPORTING INFORMATION

Additional Supporting Information may be found online in the sup-

porting information tab for this article.

How to cite this article: Anijalg P, Ho SYW, Davison J, et al.

Large-scale migrations of brown bears in Eurasia and to

North America during the Late Pleistocene. J Biogeogr.

2018;45:394–405. https://doi.org/10.1111/jbi.13126

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