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Nuclear Genomic Sequences Reveal that Polar Bears Are an Old and Distinct Bear Lineage

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Recent studies have shown that the polar bear matriline (mitochondrial DNA) evolved from a brown bear lineage since the late Pleistocene, potentially indicating rapid speciation and adaption to arctic conditions. Here, we present a high-resolution data set from multiple independent loci across the nuclear genomes of a broad sample of polar, brown, and black bears. Bayesian coalescent analyses place polar bears outside the brown bear clade and date the divergence much earlier, in the middle Pleistocene, about 600 (338 to 934) thousand years ago. This provides more time for polar bear evolution and confirms previous suggestions that polar bears carry introgressed brown bear mitochondrial DNA due to past hybridization. Our results highlight that multilocus genomic analyses are crucial for an accurate understanding of evolutionary history.
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DOI: 10.1126/science.1216424
, 344 (2012);336 Science
et al.Frank Hailer
Distinct Bear Lineage
Nuclear Genomic Sequences Reveal that Polar Bears Are an Old and
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CeNA, ANA, and FANA superior to LNA and
TNA (figs. S1 1 and S12 and table S8).
Synthesis and reverse transcription establish
heredity (defined as the ability to encode and
pass on genetic information) in all six XNAs. We
next sought to explore the capacity of such ge-
netic polymers for Darwinian evolution. As a
stringent test for evolution and for acquisition
of higher-order functions such as folding and
specific ligand binding, we initiated aptamer se-
lections directly from diverse HNA sequence
repertoires. We used a modification of the stan-
dard aptamer selection protocol comprising mag-
netic beads for capture and isolation of all-HNA
aptamers against two targets that had previous-
ly been used to generate both DNA and RNA
aptamers (24, 25): the HIV trans-activating re-
sponse RNA (TAR) and hen egg lysozyme (HEL).
After eight rounds (R8) of selection with a
biotinylated [27-nucleotide (nt)] version of the
TAR RNA motif (sTAR) used as bait, clear con-
sensus motifs emerged (fig. S13) from which we
identified an HNA aptamer (T5S8-7) that bound
specifically to sTAR with a dissociation constant
(K
D
) between 28 and 67 nM, as determined by
surface plasmon resonance (SPR), bio-layer inter-
ferometry (BLI), and enzyme-linked oligonucle-
otide assay (ELONA) titration (Fig. 4C, fig. S14,
and table S6). Other anti-T AR HNA aptamers
from the same selection experiment displayed
similar affinities but distinctive fine specificities
with regard to binding TAR loop or bulge re-
gions (Fig. 4A and fig. S14). We initiated selec-
tion against HEL from an N
40
random sequence
repertoire and again observed the emergence of
consensus motifs after R8 (fig. S15). W e iden-
tified specific HEL bind er s with K
D
of 107 to
141 nM, as determined by SPR, BLI, and fluo-
rescence polarization (Fig. 4C, fig. S16, and table
S7). Anti-HEL HNA aptamers cross-reacted with
human lysozy me and, to a minor degree (<10%),
with the highly positively charged cytochrome C
(iso electric point = 9.6), but did not show bind-
ing to unrelated proteins such as bovine serum
albumin and streptavidin (Fig. 4B). Fluorescent-
ly labeled HNA aptamers allowed direct detec-
tion of surface HEL expression by flow cytometry
[fluorescence-activated cell sorting (FACS)] in
a transfected cell line, demonstrating specificity
in a complex biological environment (Fig. 4D).
Our work establishes strategies for the replica-
tion and evolution of synthetic genetic polymers not
found in nature, providing a route to novel sequence
space. The capacity of synthetic polymers for both
heredity and evolution also shows that DNA and
RNA are not functionally unique as genetic mate-
rials. The methodologies developed herein are read-
ily applied to other nucleic acid architectures and
have the potential to enable the replication of genetic
polymers of increasingly divergent chemistry , struc-
tural motifs, and physicochemical properties, as
shown here by the acid resistance of HNA aptamers
(fig. S17). Thus, aspects of the correlations between
chemical structure, evolvability , and phenotypic di-
versity may become amenable to systematic study .
Such synthetic genetics (26)that is, the explo-
ration of the informational, structural, and catalytic
potential of synthetic genetic polymersshould
advance our understanding of the parameters of
chemical information encoding and provide a source
of ligands, catalysts, and nanostruc tures with tailor-
made chemistries for applications in biotechnol-
ogy and medicine.
References and Notes
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8. D. Loakes, Nucleic Acids Res. 29, 2437 (2001).
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19. M. J. Fogg, L. H. Pearl, B. A. Connolly, Nat. Struct. Biol.
9, 922 (2002).
20. Single-letter abbreviations for the amino acid residues
are as follows: A, Ala; C, Cys; D, Asp; E, Glu; F, Phe;
G, Gly; H, His; I, Ile; K, Lys; L, Leu; M, Met; N, Asn; P, Pro;
Q, Gln; R, Arg; S, Ser; T, Thr; V, Val; W, Trp; and Y, Tyr.
21. A. F. Gardner, W. E. Jack, Nucleic Acids Res. 30, 605 (2002).
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23. B. Arezi, H. Hogrefe, J. A. Sorge, C. J. Hansen, U.S. Patent
2003/0228616 A1 (2003).
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Int. J. Biol. Macromol. 48, 392 (2011).
25. F. Ducongé, J. J. Toulmé, RNA 5, 1605 (1999).
26. S. A. Benner, Science 306, 625 (2004).
27. Materials and methods are available as supplementary
materials on Science Online.
Acknowledgments: This work was supported by the MRC
(U105178804) (P. Holliger, V.B.P., C.C.) and by grants from
the European Union Framework [FP6-STREP-029092 NEST
(P.Holliger,V.B.P.,M.A.,M.R.,P.Herdewijn)],theEuropean
Science Foundation and the Biotechnology and Biological
Sciences Research Council (BBSRC) UK (09-EuroSYNBIO-OP-013)
(A.I.T.), the European Research Council (ERC-2010-AdG_20100317)
(J.W.), and Katholieke Universiteit Leuven (GOA/IDO programs)
(P. Herdewijn). MRC has filed a patent continuation in part
(U.S. 2010/018407 A1) and a patent application (WO
2011/135280 A2) on the CST selection system and the polymerases
for XNA synthesis and reverse transcription. Polymerases are
available for noncommercial purposes from P. Holliger on
request subject to a material transfer agreement.
Supplementary Materials
www.sciencemag.org/cgi/content/full/336/6079/341/DC1
Materials and Methods
Figs. S1 to S17
Tables S1 to S7
References (2864)
8 December 2011; accepted 6 March 2012
10.1126/science.1217622
Nuclear Genomic Sequences
Reveal that Polar Bears Are an Old
and Distinct Bear Lineage
Frank Hailer,
1
* Verena E. Kutschera,
1
Björn M. Hallström,
1
Denise Klassert,
1
Steven R. Fain,
2
Jennifer A. Leonard,
3
Ulfur Arnason,
4
Axel Janke
1,5
*
Recent studies have shown that the polar bear matriline (mitochondrial DNA) evolved from a
brown bear lineage since the late Pl eistocene, potentially indicating rapid speciation and adaption
to arctic conditions. Here, we present a high-resolution data set from multiple independent
loci across the nuclear genomes of a broad sample of polar, brown, and black bears. Bayesian
coalescent analyses place polar bears outside the brown bear clade and date the divergence
much earlier, in the middle Pleistocene, about 600 (338 to 934) thousand years ago. This provides
more time for polar bear evolution and confirms previous suggestions that polar bears carry
introgressed brown bear mitochondrial DNA due to past hybridization. Our results highlight that
multilocus genomic analyses are crucial for an accurate understanding of evolutionary history.
A
daptation to novel environmental con-
ditions is an important driver of niche
specialization and speciation (1). Ex-
cept for special cases such as hybrid speci-
ation (2), the speciation process is generally
considered to be rather slow in mammals: Pa-
leontological and genetic evidence indicate
that most species pairs or sister lineages of
mammals diverged at least 1 million years
ago (3, 4). One notable exception seems to
be the polar bear (Ursus maritimus), a unique-
ly adapted high-arctic s pecialist (5, 6)for
which recent studies have suggest ed a sur-
prisingly modern matrilineal origin at less than
111 to 166 thous and y ears ago (ka) (79).
These studies found extant polar bears rooted
1
Biodiversity and Climate Research Centre (BiK-F), Senckenberg
Gesellschaft r Naturforschung, Senckenberganlage 25, 60325
Frankfurt am Main, Germany.
2
National Fish and Wildlife Foren-
sic Laboratory, 1490 East Main Street, Ashland, OR, USA.
3
Con-
servation and Evolutionary Genetics Group, Estación Biológica
de Doñana (EBD-CSIC), Avenida Américo Vespucio, s/n, 41092
Seville, Spain.
4
Lund University Hospital, Box 117, 221 00 Lund,
Sweden.
5
Goethe University Frankfurt, Institute for Ecology,
Evolution and Diversity, 60438 Frankfurt am Main, Germany.
*To whom correspondence should be addressed. E-mail:
frashai@gmx.net (F.H.); ajanke@senckenberg.de (A.J.)
20 APRIL 2012 VOL 336 SCIENCE www.sciencemag.org344
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Fig. 1. Ancientoriginofpolarbearsandsubsequent introgre ssive replacement of
their mitochondrial DNA withabrownbearhaplotype.(A) Species tree of nuclear
intron data. Polar and brown bears are sister groups, with their divergence time
estimated at 603 (338 to 934) ka. Numbers next to nodes indicate statistical support,
and gray bars are 95% highest credibility ranges for node ages. (B)MtDNA
phylogeny. Polar bears are nested within the brown bear clade. The circular arrow
denotes mtDNA replacement in polar bears before 166 to 111 ka [upper and lower
95% confidence limits from (9)]. Clades are named according to previously identified
mtDNA lineages in brown bears (8, 18). (C) Temperature curve since the Pleistocene
[modified from (32)], and evolutionary events in bears. a denotes the origination of
the polar bear lineage and b the diversification of extant brown bear lineages.
Shaded gray bars are 95% credibility intervals; black lines denote median estimates.
(D) Schematic scenario for mtDNA inheritance in bears. Speciation occurred in the
middle Pleistocene, but hybridization during the late Pleistocene led to mtDNA
similarity between extant polar bears and brown bears from the ABC islands (7, 8)and
Ireland (9). The star denotes the brown bear ancestor of extant polar bear mtDNA and
the X a hypothesized disappearance of the ancestral matriline in polar bears.
mtDNA data from ancient remains indicate additional instances of hybridization (9).
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within brown bear (U. arctos) diversity, as a
sister lineage to brown bears from the Alas-
kan Admiralty, Baranof, and Chichagof (ABC)
islands or Ireland (79). Those results would
render brown bears paraphyletic and are con-
sistent with the absence of polar bear fossils
before the late Pleistocene (710).
To date, the evolutionary history of polar
and brown bears ha s primarily been studied
using mitochondrial DNA (mtDNA) (79, 11 ).
The few studies that employed nuclear mark-
ers included only single representations per
species, therefore lacking power to assess
paraphyly (9, 1214). Although mtDNA anal-
yses are routine ly used in phylogenetics and
phylogeography, they have well-k nown limi-
tations, especially in cases of sex bias and/ or
introgressive hybridization (15). Its mat ernal
inheritance renders mtDNA sensitive t o ran-
dom genetic drift but insensitive to male-biased
gene flow. Moreover, its inheritance as a sin-
gle linked molecule prevents the estimation
of genome-wide population genetic parame-
ters (16). To test the mt DNA-based observa-
tion of brown bear paraphyly (some brown
bears being more closely related to polar bears
than to some conspecifics), nuclear sequen-
ces from a diversity of brown and polar bears
are required. Studies using multiple unlinked
nuclear loci from a broad population sample
allow the analysis of autonomously inherited
genetic markers. These yield statistically in-
dependent information and are therefore es-
sential for recovering an unbiased picture of
evolutionary relationships (e.g., species trees)
and for obtaining accurate estimates of diver-
gence times (16).
We sequenced and analyzed 9116 nucleo-
tides from 14 independent nuclear loci (in-
trons) across the genome in 45 individuals of
polar, brown, and black bears (tables S1 and
S2) (17), using the giant panda as an outgroup
(17). A species tree was reconstructed using a
Bayesian multilocus coalescent approach (Fig.
1A) (16) that embeds the gene trees for each
locus in a separately estimated species tree.
With high statistical support (P > 0.99), polar
bears were recovered as a sister lineage to all
brown bears, and their divergence time was
estimated at 603 ka (median estimate), with
95% credibility intervals (338 to 934 ka) that
exclude the time frame determined for the
extant matriline (111 to 166 ka) (9). A phylo-
genetic analysis of the concatenated data (fig.
S2) and a neighbor-joining tree of pairwise
differentiation estimates (F
ST
) (fig. S3) con-
firmed this multilocus analysis. Our results
thus provide a fundamentally different picture
of the polar bears evolutionary history, com-
pared with the recent-origin scenario sug-
gested for its mtDNA (7, 8).
Due to the contrasting evolutionary scena-
rios provided by our nuclear versus published
mtDNA data, we analyzed (17) a 640base
pair section of the mitochondrial control re-
gion to verify that our samples represent the
main lineages of extant brown and polar bears
and that their evolutionary relationships re-
flect the current view of bear mtDNA phy-
logeny. Indeed, following the nomenclature
of Leonard et al.(18), our sampli ng covers
brow n bear clades 1, 2, 3, and 4, encompas-
sing individuals from northern and central
Europe as well as the Alaskan ABC islands
and across continental North America (Fig.
1B). Consistent with previous mtDNA studies
(79, 11), all polar bears clustered together
with high posterior node support (P > 0.99)
within the diversity of brown bears, sharing a
most recent common ancestor with the ABC
island lineage (clade 2a). Our sampling in-
cludes two of the most strongly differentiated
microsatellite clusters in polar bears (19) (east
versus west Gree nland), as well as continen-
tal North America and Iceland (17). There-
fore, this study represents a high-resolution
data set that compares nuclear genomic var-
iation in multiple polar and brown bear in-
dividuals, providing an independent view of
their evolutionary history.
Recently diverged species still share many
all ele s in their nuclear genomes because of
retained ancestral polymorphisms (20, 21).
Therefore, given the rece nt mtDNA diver-
gence among extant polar and brown bears,
one might expect the two spec ies to share a
majority of nucle ar haplot ypes. However,
numerous nuclear haplotypes were unique to
polar bears. Across all polar and brown bear
samples, we encountered a total of 114 hap-
lotypes at the 14 intron loci (table S3). Out of
35 haplotypes in polar bears and 79 in brown
bears, only 6 were shared (table S3 and fig.
S1), and most of these were rare in at least
one taxon. For the majority of nuclear loci,
polar bear sequences were distinct from those
in brown bears (fig. S1), and at least 20 sites
were fixed. Nucleotide di versity in polar bears
was only about 20% of that in brown bears
(Table 1), with 22 single-nucleotide polymor-
phisms in polar bears and 95 in brow n bears.
These anal yses suppo rt that polar bears are
a distinct and geneti cally differentiated spe-
cies, rather than a lineage that evolved re-
cently from a brown bear genotype. Although
the polar bear genome thus harbors an un-
expected abundance of unique genetic varia-
tion, effective population size is lower than
that of its southern relative. This commonly
observed biogeographic pattern likely reflects
smaller long-term population sizes and stron-
ger population bottlenecks in arctic than in
temperate species (22).
Overal l nuclear genomic differentiation
(multilocus F
ST
) between polar and brown
bears (0.692) was similar to that between each
of these and black bears (brown-black 0.685,
polar-black 0.893) (table S4), consistent with
long-term genetic distinctiveness of polar bears.
These findings agree with the nuclear species
tree (Fig. 1A) but differ from the matrilineal
scenario. A recent estimate of the polar/brown
bear divergence time (0.4 to 2 million years)
Table 1. Mitochondrial and nuclear genetic
diversity in bears. n, number of analyzed individ-
uals; p, Tamura-Nei corrected nucleotide diversity.
Species n
p (mtDNA)
(×10
3
)
p (nuclear DNA)
(×10
3
)
Polar 19 5.45 0.575
Brown 18 25.13 2.496
Black 7 17.75 1.437
Fig. 2. Individual-based cluster-
ing results from nuclear varia-
tion in bears. Vertical bars show
the cluster membership of each
individual, for a clustering into
five groups (indicated by sepa-
rate colors). Polar bears (blue)
appear to be genetically more
homogeneous than brown bears,
within which a subclustering is
discernible (light and dark brown).
Note the absence of multilocus
introgression signals among brown
and polar bears, indicating that
much of the polar bear genome is
unaffected by (recent) hybridization.
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based on nuclear loci and single representations
per species supports our results (9). Previous
studies provided an older time frame for the
black/brown bear divergence (7, 17) than our
data (Fig. 1A). Therefore, our dating of the
polar/brown bear divergence could prove an
underestimate, which would strengthen our
main conclusions. Our nuclear dating closely
resembles the time frame for speciation of
another high-arctic specialist, the arctic fox,
which diverged from its sister lineage about
900 ka (23). In accordance with matrilineal
data (9), our nuclear gene analyses place the
origin of extant brown bear diversity at ap-
proximately 125 (65 to 207) ka. The warm
Eemian interglacial period at 125 ka and the
ensuing onset of late Pleistocene glacial cy-
cles (Fig. 1C) may explain the fragmentation
and origin of modern brown bear line ages.
Extant genetic diversity in the gray wolf also
dates back to thi s time (24). Our dating of
evolution ary events in bears therefore co-
inci des with analogous events in other Eur-
asian and North American carnivores. Kurténs
allometry-based suggesti on (10) that polar
bears could have evolved during the middle
Pleistocene supports our finding, although
the oldest known polar bear fossils date to
less than 110 to 130 ka (710). The life of po-
lar bears on coastal ice, an ephemeral habi tat
shaped by multiple glacial advances and re-
treats, may explain why older fossils have
not been found.
An e arlier evolutionary origin of the polar
bear lineage requires a reinterpretation of the
established branching pattern of mtDNA lin-
eages (79, 11 ). In principle, all extant brown
and polar bear mtDNA could be of polar bear
origin, but this would require several events of
hybridization and subsequent mtDNA replace-
ment (9), which appears unlikely in a wide-
spread generalist species like the brown bear.
More parsimoniously, introgressed brown bear
material may have replaced the original polar
bear mtDNA (Fig. 1D). This would imply that
female brown bears mated with male polar
bears and that the offspring backcrossed into
the polar bear population [consistent with re-
cent observations of fertile hybrids in the wild
(25)]. Polar and brown bears are not generally
codistributed, but polar bears colonizing coast-
al land due to sea ice melting during the last
interglacial could have been susceptible to in-
trogression from resident brown bears (25, 26).
Regardless of the direction of mtDNA replace-
ment, such a process has been described for
other mammals (27, 28).
A Bayesian multilocus genotype cluster-
ing analysis (17, 29) revealed n o detectable
signal of recent or ongoing nuclear gene flow
between the polar and brown bear individ-
uals (Fig. 2 and fig. S5). Similarly, migra-
tion rates among polar and brown bear groups
did not differ significantly from zero, as shown
by coalescent-based multilocus simulations
(table S5 and fig. S4) (30). This suggests that
polar/brown bear hybridization is currently
infrequent and/or limited to a few geographic
regions (25). Nevertheless, mtDNA yields a
signal of at least one or two hybridization
events during the late Pleistocene (9), illus-
trating the usefulness of haploid, uniparen-
tally inherited loci and ancient DNA studies
to track reticulate evolutionary relationships
(79). To obtain the overall species tree and
associated timing estimates, however, t he use
of multiple independent loci is crucial. This
study therefore highlights that mtDNA does
not always reflect the species overall (genome-
wide) evolutionary h istory.
Despite the lack of average, multilocus
signals of frequent or recent bear hybridi-
zation (Fig. 2 and fig. S4), indications of ad-
mixture are not limited to mtDNA. Some loci
can remain informative about past hybridiza-
tion events even when most of the genome is
unaffected (31). We found a candidate locus
for introgression by polar/brown bear hybrid-
ization. At the intron locus 11080, bears clus-
tered in species-specific haplogroups (fig. S1),
with one notable outlier: ABC island brown
bears carried the (fixed) polar bear haplotype.
If this pattern reflects introgression, it could
represent evidence of polar bear genetic ma-
terial in brown bears, suggesting gene flow in
the opposite direction relative to mtDNA (9).
Because the process of lineage sorting is slow,
spanning time scales relevant to speciation
(20, 21), linkage mapping studies like those in
canids (31) will be necessary to pinpoint the
phylogenetic origins of individual alleles in
bears. Adaptive introgression not only may
have helped polar bears to withstand intergla-
cial warm phases (9) and potentially counter-
acted inbreeding but also may have facilitated
the persistence of brown bear populations in
subarctic landscapes.
In conclusion, our data suggest that polar
bears are a genetically distinct lineage that is
older than previously recognized. An evolu-
tionary origin several hundred thousand years
ago implies that polar bears as a species have
experienced multiple glacial cycles and have
had considerable time to adapt to arctic con-
ditions. However, the low genetic diversity in
polar bears suggests that changes in the envi-
ronment, such as warm phases, caused popu-
lation bottlenecks. Although polar bears have
persisted through previous warm phases, mul-
tiple human-mediated stressors (e.g., habitat
conversion, persecution, and accumulation of
toxic substances in the food chain) could mag-
nify the impact of current climate change, pos-
ing a novel and likely profound threat to polar
bear survival.
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Acknowledgments: The study was supported by
Hesses LOEWE, Landes-Offensive zur Entwicklung
Wissenschaftlich-ökonomischer Exzellenz. We thank
E. W. Born, H.-G. Eiken, C. Frosch, S. Hagen, A. Kopatz,
C. Nowak, M. Onucsán, M. Pfenninger, K. Skírnisson,
F. Zachos, and P. Beerli for providing samples and for
discussions. Obtained sequences have been deposited in the
EMBL database (accession nos. HE657192 to HE657234
and HE657776 to HE658979). The authors declare no
competing financial interests.
Supplementary Materials
www.sciencemag.org/cgi/content/full/336/6079/344/DC1
Materials and Methods
Figs. S1 to S5
Tables S1 to S5
References (3361)
Supplemental Files S1 and S2
9 November 2011; accepted 13 March 2012
10.1126/science.1216424
www.sciencemag.org SCIENCE VOL 336 20 APRIL 2012 347
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