DOI: 10.1111/jbi.13090
RESEARCH ARTICLE
Evolutionary reconstruction supports the presence of a Pleistocene Arctic refugium for a large mammal species €tsch1 Cornelya F. C. Klu
| Micheline Manseau2,3,*
| Morgan Anderson4 |
Peter Sinkins5 | Paul J. Wilson1 1
Biology Department, Trent University, Peterborough, ON, Canada 2
Protected Areas Establishment and Conservation Directorate, Parks Canada, Gatineau, QC, Canada 3
Natural Resources Institute, University of Manitoba, Winnipeg, MB, Canada 4
Department of Environment, Government of Nunavut, Igloolik, NU, Canada 5 Western Arctic Field Unit, Parks Canada, Inuvik, NT, Canada
Correspondence Micheline Manseau, Protected Areas Establishment and Conservation Directorate, Parks Canada, Gatineau, QU, Canada. Email:
[email protected] Present address Micheline Manseau, Landscape Science and Technology, Environment and Climate Change Canada, Ottawa, ON, Canada Funding information Government of Nunavut; Parks Canada; Natural Sciences and Engineering Research Council of Canada; Government of Nunavut; Environment and Climate Change Canada; Polar Continental Shelf Program Editor: Jenny McGuire
Abstract Aim: The presence of refugia in the Canadian High Arctic has been subject to debate for decades. We investigated the potential existence of Arctic refugia during the Pleistocene for a large mammal species in the Canadian Archipelago because if these refugia were present, reconsideration of the evolutionary histories of North American fauna and flora beyond the major refugia of Beringia and south of the Laurentide and Cordilleran Ice Sheets would be required. Peary caribou (Rangifer tarandus pearyi), identified as a subspecies based on morphological characteristics, inhabits the Canadian Arctic Islands and Boothia Peninsula. Previous studies demonstrated incomplete lineage sorting of mitochondrial DNA interpreted as a Beringian origin but were based on small sample sizes. Location: Canadian Arctic. Major taxa studied: Mammals: caribou (Rangifer tarandus). Methods: We used two molecular markers (microsatellites and mitochondrial DNA) and approximate Bayesian computations (ABC) testing the hypotheses of colonization out of Beringia into the Arctic Islands following the Last Glacial Maximum (LGM) or a divergence from Beringia significantly before the end of the LGM within a different refugium. Results: The coalescent-based analyses rejected a recent Beringian origin with subsequent colonization, instead supporting a divergence of Peary caribou from Beringia ~100,000 years ago linking it to the last interglacial/early Wisconsin Glacial Stage (125,000–75,000 years ago). Admixture on Banks Island with Beringian-derived barren-ground caribou is indicative of post-Pleistocene secondary contact; further supporting a divergent history of Peary caribou within a separated Arctic refugium. Main conclusions: Our results offer support for the existence of an Arctic refugium for large mammal species and add to the increasing evidence of such refugia in North America. This has significant implications on understanding the evolution and conservation of Arctic species, particularly in light of sensitivities and adaptive potential to a rapidly changing climate. KEYWORDS
approximate Bayesian computation, Arctic refugium, microrefugia, phylogeography, Pleistocene, Rangifer tarandus, subspecies
Journal of Biogeography. 2017;1–11.
wileyonlinelibrary.com/journal/jbi
© 2017 John Wiley & Sons Ltd
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1 | INTRODUCTION
ET AL.
subspecies (Rangifer tarandus groenlandicus, Borowski, 1780; DU3, COSEWIC, 2011) by relatively smaller body size, more narrowly
Climatic fluctuations during the Pleistocene resulted in geographically
spreading antlers as well as grey antler velvet and bone-coloured
^ te & structured populations (Hewitt, 2000; Shafer, Cullingham, Co
antlers, shorter snouts, lighter fur colour lacking the dark lateral
Coltman, 2010; Soltis, Morris, McLachlan, Manos & Soltis, 2006; Ste-
stripe and larger hooves (Banfield, 1961; COSEWIC, 2011; Manning,
n, 2010; Waltari & Cook, 2005) that experiwart, Lister, Barnes & Dale
1960). These traits are probably adaptations to the Arctic climate.
enced periods of independent evolution because of geographical
Pelage and antler velvet characteristics are clearly different between
isolation in refugia and divergent selection regimes (Hewitt, 2000).
Peary and barren-ground caribou and these characteristics do not
Palaeontological and phylogeographical studies have greatly con-
follow a cline but are discontinuous, suggesting that these sub-
tributed to our understanding of the processes of past glacial cycles
species might have different evolutionary origins (McFarlane, Gunn,
and their impact on the diversification of natural populations in North
& Strobeck, 2009). A third DU, the Dolphin Union caribou (DU2,
€ tsch, America (Federov & Stenseth, 2002; Flagstad & Røed, 2003; Klu
COSEWIC, 2011), migrates between Victoria Island and the adjacent
Manseau & Wilson, 2012; Shafer et al., 2010; Sim, Hall, Jex, Hegel &
mainland. Dolphin Union caribou have morphological characteristics
Coltman, 2016; Soltis et al., 2006; Waltari & Cook, 2005; Yannic et al.,
intermediate between barren-ground and Peary caribou (COSEWIC,
2014). Simultaneously, comparative phylogeographical studies (Shafer
2011; Figure 1). Recently, McFarlane, Miller, Barry & Wilson (2014)
et al., 2010; Soltis et al., 2006; Stewart et al., 2010) and ancient DNA
considered this DU to be of admixed origin based on microsatellite
studies (Campos et al., 2010; Heintzman et al., 2016; Shapiro et al.,
data corroborating the presence of morphological characteristics
2004) contributed to the identification of important refugia for plant
from both Peary and barren-ground caribou.
and animal species as well as re-colonization events after the retreat
The early origin of all caribou (Rangifer tarandus) traces back to
of the ice sheets. Two major refugia north and south of the Laurentide
Beringia where Early Pleistocene remains were found in Alaska and
and Cordilleran Ice Sheets, representing the Beringian-Eurasian lineage
the Yukon (Guthrie & Matthews, 1971). During Pleistocene climatic
(BEL) and the North American lineage (NAL), are well-established
fluctuations, caribou migrated to different geographical regions in
based on palaeontological records, phylogeographical and ancient
North America and diversified, resulting in the biological diversity
DNA analyses (Cook et al., 2016; Flagstad & Røed, 2003; Heintzman
€tsch, Manseen today (Banfield, 1961; Flagstad & Røed, 2003; Klu
€tsch et al., 2012; MacPherson, 1965; Polfus, Manseau, et al., 2016; Klu
€tsch et al., 2012; Manning, seau, Trim, Polfus & Wilson, 2016; Klu
€tsch, Simmons & Wilson, 2016; Shapiro et al., 2004; Waltari & Klu
1960; Polfus et al., 2016). In the first comprehensive work on cari-
Cook, 2005). Additional microrefugia and cryptic refugia have been
bou taxonomy, Banfield (1961) suggested, based on morphological
proposed in western Canada (Shafer et al., 2010; Sim et al., 2016) and
characteristics and older glaciation models, that caribou retreated to
in the High Arctic (Dyke, 2004; Dyke et al., 2002; MacPherson, 1965;
two biotic refugia during the Pleistocene: the western Queen Eliza-
Maher, 1968; Stewart & England, 1986). Palaeontological and palaeo-
beth Islands and northern Greenland. Alternatively, Manning (1960),
geographical research suggests that two glacial refugia might have
based on similar lines of evidence, proposed that caribou survived
existed on Arctic Islands: one on Banks Island and the other on the
in a High Arctic refugium with subsequent migration to Banks
north-eastern part of Ellesmere Island and northern Greenland (Maher,
Island. While both of these hypotheses basically state the retreat of
1968; Figure 1). Older quaternary geological surveys indicate that ice-
caribou into one or several High Arctic refugia, an alternative, more
free coastlines in the High Arctic may have been present (Clark & Mix,
recent hypothesis is that a population originating from the Berin-
€ ken, 1966; Steig, Wolfe & 2002; Dyke, 2004; Dyke et al., 2002; Lo
gian mainland migrated northwards to re-colonize the Arctic Islands
Miller, 1998). Furthermore, the presence of ice-free regions on eastern
after the LGM (Flagstad & Røed, 2003), largely based on incomplete
Baffin Island and south-western Greenland has been proposed (Beel,
lineage sorting of mitochondrial control region haplotypes among
Lifton, Briner & Goehring, 2016; Clark & Mix, 2002; Dyke et al., 2002;
northern caribou and limited sample sizes. Only few fossil remains
Margreth, Dyke, Gosse & Telka, 2014; Margreth, Gosse & Dyke, 2016;
have been described in the literature for the Arctic (Dyke, Hooper,
Steig et al., 1998; Figure 1). Other studies have however modelled
Harington & Savelle, 1999; Harington, 1990, 2005; Maher, 1968).
pervasive ice coverage of the High Arctic and Banks Island during the
Among those, a fossilized muskoxen bone on Banks Island was
Last Glacial Maximum (LGM), thereby suggesting the absence of Arctic
dated to 34,000 YBP (Maher, 1968). Mammoth remains found on
, 2009; Vaughan, England & Evans, refugia (England, Furze & Doupe
Banks and Melville islands were radiocarbon dated to ~21,000–
2014). It is therefore not clear if terrestrial species that are currently
22,000 YBP (Harington, 2005) and suggest that large mammals
distributed across the Arctic Islands may have originated from Arctic
could have survived in refugia on Banks Island or other regions in
refugia (Stewart et al., 2010).
the Arctic. However, MacPhee (2007) pointed out that those mam-
Peary caribou (Rangifer tarandus pearyi, Allen, 1902) is one of
moth remains could have been transported on ice rafts from the
four presently described subspecies of caribou in Canada and is rec-
mainland and therefore, do not provide conclusive evidence to the
ognized as a distinct Designatable Unit (DU1, COSEWIC, 2011).
existence of Arctic refugia.
They inhabit the Arctic Islands and Boothia Peninsula, areas predom-
Here, we investigated the phylogeographical structure and evo-
inantly north of the 74th parallel (COSEWIC, 2011; Figure 1) and
lutionary history of Peary caribou using two genetic markers,
are differentiated from the geographically adjacent barren-ground
specifically microsatellites and mitochondrial DNA, and compared
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F I G U R E 1 Sampling locations for Peary (Rangifer tarandus pearyi) and barrenground caribou (Rangifer tarandus groenlandicus) in the five geographical regions in Canada discussed in the main text. Additionally, the distribution ranges of recognized Designatable Units (COSEWIC, 2011) are shown. The extent of the ice sheets (Dyke et al., 2002; Dyke, 2004) is also displayed
the results to palaeontological and geological findings. As the distri-
The resolution of these two hypotheses has important implica-
bution ranges of the subspecies included in the study are clearly
tions for the Peary subspecies specifically, and to flora and fauna
defined, we applied a coalescent-based approximate Bayesian com-
more generally in providing supporting evidence from the recon-
putation (ABC) approach (Beaumont, 2010; Cornuet et al., 2014) to
struction of evolutionary history for the presence of Arctic refugia
test competing hypotheses for the origin and evolution of Peary
inhabited by a range of species.
caribou: 1. Peary caribou originated from Beringia and re-colonized the Arctic Islands after the LGM where we predicted that a stepping stone colonization model may be the most likely scenario, and that Peary
2 | MATERIALS AND METHODS 2.1 | Sampling collection
caribou evolved more recently than mainland populations coincid-
Faecal pellet samples from the Arctic Islands were collected during
ing with the retreat of the ice sheet during the Holocene.
aerial surveys conducted by the Government of Nunavut, the
2. Alternatively, caribou inhabited an Arctic refugium and colonized
Government of the Northwest Territories, and Parks Canada
the southern Arctic Islands after the end of the LGM where we
between 2004 and 2015 (Figure 1), along with additional oppor-
predict that ABC should identify an ancient lineage correspond-
tunistic collections (pellets, antlers and tissue) in conjunction with
ing to Peary caribou that significantly pre-dates the LGM.
other fieldwork and by community members. Barren-ground samples
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were collected during aerial surveys conducted by the Government
We used hierarchical approximate Bayesian computation analy-
of Manitoba, the Government of the Northwest Territories, Parks
ses (Beaumont, 2010; Cornuet et al., 2014) to test our two main
Canada and the University of Manitoba in collaboration with the
hypotheses. To examine a wide range of models including stepping-
Renewable Resources Board. Samples were labelled and Sahtu
stone, split and admixture models, we prepared sets of models and
shipped on ice to Trent University for genetic analysis.
subsequently selected the top models from each run to be included in successive runs. With this approach, we narrowed down the num-
2.2 | Genetic and statistical analyses
ber of models to a final set of six candidates (Figure 2). Regarding the final six models, the main difference between the models was
Laboratory protocols for the amplification of microsatellites and
the positioning of Banks Island. This population could be a descen-
sequencing of the mitochondrial DNA (mtDNA) control region are
dant from either the mainland lineage or a High Arctic lineage (HAL)
€tsch et al., 2012, 2016). We calcudescribed in detail elsewhere (Klu
or alternatively be a descendant from an admixed population (Fig-
lated summary statistics including number of alleles, observed and
ure 2, model 4). All models were tested three times with a combined
expected heterozygosity, and inbreeding coefficient with the pro-
data set and with microsatellites and mitochondrial DNA separately
gram GENAIEX 6.5 (Peakall & Smouse, 2012). Additionally, we used
to validate model selection.
the program HP-RARE June_2006 (Kalinowski, 2005) to calculate alle-
The software package DIYABC 2.0.4 (Cornuet et al., 2014) was
lic richness and private allelic richness using a rarefaction method to
used to conduct ABC analyses with the following run parameters.
account for uneven sample sizes. Finally, we used the program GENE-
For microsatellites, we selected a stepwise mutation model with an
POP 4.2.2. (Rousset, 2008) to test for heterozygosity deficiency and
average mutation rate of 1 9 10
linkage disequilibrium.
DNA, we determined the proportion of invariable sites and the best
5
to 1 9 10
3
. For mitochondrial
To determine the number of populations present in the current
suited substitution model with the software JMODELTEST 2.1.4 (Dar-
data set, we used the software STRUCTURE 2.3.4 (Pritchard, Stephens
riba, Taboada, Doallo & Posada, 2012). Summary statistics included:
& Donnelly, 2000). Underlying assumptions for model-based cluster-
mean number of alleles, mean size variance of alleles, FST (for both
ing included an admixture model with correlated allele frequencies
microsatellites and haplotypes), shared allele distance, classification
(Falush, Stephens & Pritchard, 2003) and no prior assignment of
index, mean pairwise difference within and between populations,
population information. Run parameters comprised a burn-in of
mean number of haplotypes, mean and variance of pairwise differ-
1 9 106 followed by 1 9 107 permutations to test K = 1 to K = 15
ence of sequences, and mean and variance of number of the rarest
with five iterations each. To summarize run statistics, we ran the
nucleotide at segregating sites. Each ABC run generated about three
program STRUCTURE HARVESTER 0.6.93 (Earl & vonHoldt, 2012). We
million simulated data sets. Model choice was determined by calcu-
used the ΔK method (Evanno, Regnaut & Goudet, 2005) to identify
lating posterior probabilities using the logistic regression analysis
the most probable number of population clusters in the data set.
& Estoup, 2010) with a sample size of 30,000 sim(Cornuet, Ravigne
Additionally, the ad-hoc likelihood statistics (Pritchard et al., 2000)
ulated data sets. Model-checking to assess the goodness-of-fit of a
are reported for comparison. Individual and population membership
model parameter posterior combination was also performed (Cornuet
q values over the five iterations were averaged with the programs
et al., 2014). Model-checking was done with the original and a new
CLUMPP 1.1.2 (Jakobsson & Rosenberg, 2007) and DISTRUCT 1.1
set of summary statistics (for microsatellites: mean gene diversity
(Rosenberg, 2004).
across loci, mean M index across loci, (dl)2 distance between two
F I G U R E 2 Final six models tested for Peary caribou (Rangifer tarandus pearyi) and barren-ground caribou (Rangifer tarandus groenlandicus) in Canada with approximate Bayesian computation. BAN, Banks Island; BBH, Bathurst and Bluenose herds; LHA, Lower High Arctic Islands; ELL, Ellesmere; QBH, Qamanirjuaq and Beverly herds. Dotted lines indicate hypothetical, not sampled populations
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samples; mtDNA: number of segregating sites, Tajima’s D, and pri-
Lower High Arctic Islands (LHA) as well as Banks Island (BAN). The
vate segregating sites) for all three data sets. Additionally, new ABC
Dolphin Union DU was not considered because of insufficient sam-
runs with the new summary statistics set were done as well to test
ples sizes.
whether the same model(s) would be chosen with a different set of
Summary statistics showed that Peary caribou on ELL and on the
summary statistics to test the robustness of the results. We selected
LHA (Figure 1) had lower genetic diversity, demonstrated by lower
a generation time of 7 years (COSEWIC, 2002) to retrieve time esti-
(private) allelic richness, and observed and expected heterozygosity
mates in years.
(Table 1) than the mainland populations (i.e., Bathurst and Bluenose herds (BBH), Qamanirjuaq and Beverly herds (QBH)), and BAN. Similarly, haplotype diversity indices (Table 2) confirmed this pattern
3 | RESULTS
showing lower gene and nucleotide diversity on LHA and ELL. After Bonferroni correction, only 3/45 tests for heterozygosity deficiency
Model-based clustering analysis using STRUCTURE 2.3.4 (Pritchard
and none of the 180 pairwise comparisons for linkage disequilibrium
et al., 2000) detected three populations that corresponded to Banks
were significant indicating that there were no substantial deviations
Island, mainland barren-ground, and the High Arctic Islands (Fig-
from Hardy–Weinberg equilibrium or linkage of loci.
ures 3a; Appendices S1a and S2a); however, the DK method
Therefore, five populations were included in the subsequent ABC
(Appendix S1a) identified two populations (K = 2) that corresponded
analysis: ELL, LHA, BAN, and two barren-ground populations (BBH,
to mainland barren-ground and the High Arctic Islands; identifying
QBH). The distinction of two barren-ground populations was justified
Banks Island as an admixed population (Figure 3c). As higher order
because the two groups showed distinct haplotype frequency distribu-
structure can mask fine-scale population structure, a second analysis,
tions (Appendix S3) and the two groups were significantly differenti-
in which barren-ground caribou was taken out of the analysis, was
ated in an AMOVA analysis for mitochondrial DNA (Appendix S4a).
performed to test whether additional population genetic structure
This also allowed for testing of different migration routes either from
could be identified within Peary caribou (Figure 3b; Appendices S1b
the West (Banks Island) or alternatively from the east (via the Boothia
and S2b) and revealed three groups, Ellesmere Island (ELL) and the
Peninsula).
The
AMOVA
analysis
for
both
microsatellites
5 ELL
4 LHA
3 BAN
3
3
4
5
BAN
LHA
ELL
ELL
2 2
LHA BBH
1 1 QB
(c)
H
(b)
BAN
QB H
BBH
2
1
(a)
F I G U R E 3 STRUCTURE bar plots for Peary caribou (Rangifer tarandus pearyi) and barren-ground caribou (Rangifer tarandus groenlandicus) in Canada. (a) Shows the results of the Bayesian cluster analysis for K = 3. Populations included: QBH, Qamanirjuaq and Beverly herds; BBH, Bathurst and Bluenose herds; BAN, Banks Island; LHA, Lower High Arctic Islands; ELL, Ellesmere Island. (b). STRUCTURE results for additional run including only Peary caribou (R.t. pearyi) samples. Bar plot for K = 3. Populations included: BAN, Banks Island; LHA, Lower High Arctic Islands; ELL, Ellesmere Island. (c). This figure shows the results for K = 2 for the entire data set. Populations included: QBH, Qamanirjuaq and Beverly herds; BBH, Bathurst and Bluenose herds; BAN, Banks Island; LHA, Lower High Arctic Islands; ELL, Ellesmere Island
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T A B L E 1 Summary of genetic diversity estimates for Peary caribou (Rangifer tarandus pearyi) and barren-ground caribou (Rangifer tarandus groenlandicus) in Canada. Number of samples (N), number of alleles (NA), allelic richness (AR), private allelic richness (ARP), expected (HE) and observed heterozygosity (HO), FIS estimates, and standard errors (SE) for each of the estimates N
Group
NA
SE
AR
ARP
HO
SE
HE
SE
FIS
SE
QBH
97
14.78
1.10
12.4
1.33
0.84
0.02
0.86
0.01
0.03
0.02
BBH
211
18.33
2.27
12.7
1.33
0.85
0.02
0.87
0.01
0.02
0.01
BAN
122
13.78
3.24
10.5
0.99
0.79
0.02
0.79
0.02
0.001
0.01
LHA
48
7.33
1.87
7.1
0.91
0.66
0.05
0.65
0.03
0.01
0.04
ELL
113
9.00
3.53
7.1
0.85
0.66
0.03
0.69
0.03
0.05
0.02
QBH, Qamanirjuaq and Beverly herds; BBH, Bathurst and Bluenose herds; BAN, Banks Island; LHA, Lower High Arctic Islands; ELL, Ellesmere.
T A B L E 2 Summary statistics for mitochondrial DNA data for Peary caribou (Rangifer tarandus pearyi) and barren-ground caribou (Rangifer tarandus groenlandicus) in Canada. Number of samples (N), nucleotide diversity (p) and gene diversity (gene div) plus respective standard deviations are shown Group
N
p
SD
Gene div
SD
QBH
90
0.019
0.010
0.984
0.005
BBH
179
0.015
0.008
0.933
0.012
BAN
121
0.012
0.006
0.796
0.028
LHA
31
0.009
0.005
0.733
0.061
ELL
111
0.008
0.005
0.763
0.018
QBH, Qamanirjuaq and Beverly herds; BBH, Bathurst and Bluenose herds; BAN, Banks Island; LHA, Lower High Arctic Islands; ELL, Ellesmere.
conservative. The Last Interglacial period was between 125,000 and 75,000 years ago, so the separation between the lineages corresponded to that time period. The contemporary population on Banks Island evolved from an admixture event of the two ancient lineages ~8,330 years ago (CI: 1,064–24,430) based on the combined data set. This ABC time estimate corresponds to the opening of a passage along the coastline in the High Arctic >8,000 years ago (Dyke, 2004) while the northern ice sheet retreated. The opening of a passage is a prerequisite for gene flow between the two ancient lineages to occur if Arctic refugia existed. The alignment of the ABC time estimates with the timing of the retreat of the ice sheet contributes to the plausibility of the selected ABC model. Additional ABC runs with a different set of summary statistics resulted in the same model choice and model-checking with the original and a new set of summary statistics were comparable as well.
(Appendix S4b) and mitochondrial DNA (Appendix S4a) indicated that
This indicated that the results were robust and not depended on
Peary caribou populations from Ellesmere Island and the Lower High
summary statistic choice. Differentiation processes within each of
Arctic Islands were most differentiated from the mainland populations
the ancient lineages led to two barren-ground caribou populations
and that Banks Island had equally low genetic differentiation values to
and two Peary caribou populations. This is consistent with a median-
all other populations in microsatellites but showed a closer relationship
joining network (Appendix S6) that shows evolutionary relationships
to Peary caribou on the Lower High Arctic Islands and Ellesmere Island
of mitochondrial DNA control region haplotypes. The most common
in mitochondrial DNA.
haplotype in Peary caribou (H99) and a few rare Peary caribou hap-
In total, 65 models (data not shown) were tested using a hierarchical approximate Bayesian computation approach, resulting in six
lotypes are located on a different branch than the majority of the haplotypes found in barren-ground caribou.
models that were included in a final run (Figure 2). These six models did not include a stepping-stone model because those models received low support once other split models and/or admixture mod-
4 | DISCUSSION
els were included. The selected model (scenario 4) with highest posterior probabilities (Figure 2, Table 3) showed that populations from
A reconstruction of the evolutionary history of Peary caribou
Ellesmere Island and the Lower High Arctic Islands evolved from an
rejected a stepping-stone model for the colonization of the Arctic
independent HAL, without significant gene flow from other popula-
from Beringia following the LGM. Instead, a more ancient divergence
tions and barren-ground populations originated from a different lin-
of Peary caribou from Beringian-evolved caribou was supported. The
eage in all three data sets. Thus, the two sub-specific lineages
split of this HAL was estimated to ~96,000–185,000 YBP (based on
corresponding to the HAL and barren-ground caribou separated at
the three data sets used), suggesting divergence pre-dating the LGM
least ~100,000 years ago (CI: 25,550–193,900; node t4 in scenario
that was subsequently phylogeographically maintained. Therefore,
4, Figure 2) based on mitochondrial DNA, the genetic marker that
previous glacial cycles contributed to isolation and prolonged diver-
gave
HAL
gent evolution of lineages/populations in caribou. The median-joining
(Appendix S5a). The combined and microsatellite data sets (Appen-
network supported the ABC modelling results and identified a lin-
dices S5b and S5c) estimated the split to be even older; thus, the
eage that diverged from the main body of the network. This lineage
mitochondrial DNA estimate of ~100,000 YBP seems to be
included the most common haplotype found in Peary caribou (H99)
the youngest time estimates for
the origin of
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T A B L E 3 Posterior probabilities ABC and credible interval (CI) for the three ABC runs (i.e., microsatellite, mtDNA, and combined data set) for Peary caribou (Rangifer tarandus pearyi) and barren-ground caribou (Rangifer tarandus groenlandicus) in Canada Scenario 1
Scenario 2
Scenario 3
Scenario 4
Scenario 5
Scenario 6
Microsatellite data set
0.044 (0.020–0.068)
0.000 (0.000–0.001)
0.000 (0.000–0.001)
0.933 (0.9–0.966)
0.023 (0.010–0.036)
0.000 (0.000–0.001)
mtDNA data set
0.000 (0.000–0.005)
0.219 (0.202–0.236)
0.000 (0.000–0.005)
0.017 (0.012–0.022)
0.000 (0.000–0.005)
0.763 (0.746–0.781)
Combined data set
0.000 (0.000–0.707)
0.000 (0.000–0.707)
0.000 (0.000–0.707)
1.0 (0.9997–1.000)
0.000 (0.000–0.707)
0.000 (0.000–0.707)
that is found on Ellesmere (ELL), the most northern part of the Peary
different lineages were also found in the Daphnia pulex complex
caribou distribution range, but that is not found in Beringian-derived
(Weider & Hobæk, 2003) suggesting that Banks Island is a region
caribou supporting the hypothesis that Peary caribou has an inde-
where different lineages of various species came into contact. Inter-
pendent evolutionary history. The finding that Peary caribou has this
estingly the Daphnia complex is a system also supporting LGM Arctic
and other private haplotypes (e.g., H126, H268, H269, and H270) is
refugia (Weider & Hobæk, 2003).
unlikely to be a sampling artifact because haplotype data sets for
Beyond this study and the Daphnia findings, there is increasing
the two subspecies were comparable (barren-ground: 269 samples
molecular evidence of past Arctic glacial refugia. Phylogenetic analy-
and Peary caribou: 263 samples). A few shared common mtDNA
ses in collared lemmings, Arctic hares, and ptarmigans (Federov &
control region haplotypes (e.g., H14, H26) might have been dis-
Stenseth, 2002; Holder, Montgomerie & Friesen, 2000; Waltari &
tributed by the admixture event—common haplotypes are statisti-
Cook, 2005) showed that haplotypes from the High Arctic form
cally the first to be shared between groups. Interestingly, even these
monophyletic groups that are differentiated from Beringian hap-
common and shared haplotypes are yet to be found in Alaska/Eura-
logroups. In collared lemmings, divergence time between the two
sia and therefore, are unlikely of Beringian origin. Finally, the molec-
phylogenetic clades was estimated to be ~100,000 YBP (Federov &
ular results are further supported by the considerable morphological
Stenseth, 2002) and therefore, rejected the possibility of post-glacial
differentiation of Peary caribou from barren-ground that does not
re-colonization. In rock ptarmigan (Lagopus mutus), divergence times
seem to follow a cline as would be expected by a stepwise coloniza-
ranged from 135,000 to 11,000 YBP between multiple lineages
tion of the islands from the mainland but that was found to be dis-
(Holder et al., 2000), suggesting that multiple glacial cycles con-
continuous in characters like breeding pelage and antler velvet
tributed to phylogeographical patterns seen in this species. These
(McFarlane et al., 2009); suggesting independent evolution of bar-
time frames are fairly consistent with time estimates for population
ren-ground and Peary caribou.
expansions
Small refugial populations might have experienced severe reductions in genetic variation caused by genetic drift (Widmer & Lexer,
found
in
the
literature
for
caribou
of
around
115,000 YBP for population expansions (Flagstad & Røed, 2003 and the current study).
2001). The results of this study suggest that only a small population
The time period of ~96,000–185,000 YBP links the isolation of
with low genetic diversity survived in an Arctic refugium. This is con-
the Peary caribou lineage to the Last Interglacial period, the Sanga-
gruent with some palaeogeographical surveys (Beel, Lifton, Briner &
monian Interglacial, which lasted from 125,000–75,000 YBP (sensu
Goehring, 2016; Dyke, 2004; Dyke et al., 2002; Margreth et al.,
lato, Lisiecki & Raymo, 2005). The Sangamonian Interglacial was cli-
2014, 2016; Steig et al., 1998) that indicate that only fairly small
matically characterized by temperatures up to 5°C warmer than
geographical regions remained ice-free in the Arctic. Hence, the
today in Oxygen Isotope Stage-5e (~125,000–119,000 YBP; Funder
lower genetic diversity found in Peary caribou could in part reflect
et al., 1998), OIS 5c (around 95,000 YBP), and OIS 5a (around
the limited size of ice-free patches that supported small population
85,000 YBP; Lisiecki & Raymo, 2005); however, the remainder of
sizes in addition to generally lower population sizes found in this
the Sangamonian Interglacial, especially the early Wisconsinan (OIS
subspecies. Finally, the higher genetic diversity estimates found on
4) in North America was characterized by rapid cooling (Berger,
Banks Island are consistent with the selected ABC model because
Yasuda, Bickert & Wefer, 1996). It has been proposed that cold-
admixture in secondary contact zones are expected to increase
n et al., 2005), lemmings (Fedadapted species like Arctic fox (Dale
genetic diversity estimates (Weider & Hobæk, 2003). The time esti-
erov & Stenseth, 2002), Arctic hares (Waltari & Cook, 2005), and
mate derived from the combined data set for the caribou admixture
caribou (Flagstad & Røed, 2003) likely responded in the opposite
event on Banks Island is ~8,330 YBP which corresponds to when
way to glacial cycles than temperate species. This means that these
Peary caribou came into contact with expanding barren-ground cari-
species contracted into Arctic refugia (Stewart et al., 2010) during
bou onto Banks Island and adjacent Lower High Arctic islands after
interglacial periods whereas during glacial maxima, those taxa might
the retreat of the ice sheets. Previous studies have suggested that
have had larger distribution ranges (Stewart et al., 2010). In numer-
intergrades between Peary and mainland barren-ground caribou are
ous species, a signature of population expansion during the begin-
found on Banks Island (Banfield, 1961) and potential hybrids of
ning of the last glaciation was found indicating that population sizes
8
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ET AL.
were small during interglacials (Stewart et al., 2010). This might par-
Briner & Goehring,
tially explain the lower molecular diversity found in Peary caribou in
ice-free patches on eastern Baffin Island and western Greenland
this study (Table 2) as low effective population size generally led to
indicate that the reconstruction of palaeoclimatic models remains
lower genetic diversity. For Arctic foxes (Alopex lagopus), a mismatch
contradictory. Ultimately, the empirical molecular and more limited
distribution
at
fossil evidence supports one or more glacial refugia in the Arctic
n et al., 2005). The authors proposed that inter~118,000 YBP (Dale
promoting the need of future studies consolidating the different
glacials led to isolation of Arctic populations because cold-adapted
lines of evidence on confirming the existence of Arctic refugia dur-
traits were selected against in warmer periods, so survival of cold-
ing the LGM of the Pleistocene.
indicated
a
sudden
demographic
expansion
(2016) and Margreth et al. (2016) supporting
adapted populations/species was more likely in Arctic refugia. Since
This study adds to an increasing body of literature on the impact
temperatures dropped in the early Wisconsin Glacial Stage, cold-
of the Pleistocene and Holocene on the evolution of northern and
adapted species likely saw expanding ranges and population sizes.
€tsch Arctic species (Flagstad & Røed, 2003; Harington, 2005; Klu
To conclude, the Last Interglacial might have led to the retreat of
et al., 2012; MacPherson, 1965; Polfus et al., 2016). An emerging
caribou to regions where their cold-adapted traits were advanta-
pattern from these recent studies and the current study is that
geous. Future genomic studies may help identify genes responsible
regional populations are descendants from ancient lineages and
for thermal adaptations to different climatic conditions in caribou
those northern refugia may have played a significant role in diversifi-
and other species.
cation of northern populations at the subspecies level. These inde-
The presence of multiple refugia within Beringia has recently
pendent evolutionary paths may have led to the accumulation of
been proposed (Galbreath, Cook, Eddingsaas & DeChaine, 2011;
local adaptations that provide essential genetic diversity to face cli-
Shafer et al., 2010; Sim et al., 2016). Hence, an alternative scenario
mate change. Alternatively, evolution in divergent northern refugia
explaining the current results could be that two ancient lineages
may have resulted in differential sensitivities to a changing climate,
evolving in two different microrefugia within Beringia remained iso-
particularly warming trends. The results of the current study further
lated while recolonizing the Arctic Islands after the LGM. The (HAL)
suggest that a HAL was separated from other caribou populations
colonized the Arctic region first and subsequently BEL recolonized
during the Sangamonian Interglacial/Early Wisconsin Glacial Stage
the lower island belt resulting in admixture seen on Banks Island.
indicating that Peary caribou have retreated to an Arctic refugium
However, the predisposition of barren-ground and Peary to inter-
during periods of warmer climate. Consequently, Peary caribou may
breed, as evidenced by Banks Island, makes it unlikely that the two
be especially vulnerable to the effects of climate change with
ancient lineages remained separated while colonizing the Arctic
increasing temperatures and higher frequencies of extreme weather
Islands. If both lineages originated from Beringia, then microrefugia
conditions. More generally, numerous Arctic species show distinct
separated them for up to ~100,000 YBP with these divergent lin-
evolutionary histories and genetic diversity that require special
eages subsequently having taken the same northward migration
attention and particularly in light of potential sensitivities and adap-
routes simultaneously. Only a few Peary caribou haplotypes are
tive potential to a rapidly changing climate.
more closely related to those more commonly found in barrenground caribou in the MJ-network (Appendix S6) and none of the most common Peary caribou haplotypes are found in Alaska, north-
ACKNOWLEDGEMENTS
ern Europe or Russia (i.e., Beringia) as determined by comparison of
We thank Marina Kerr, Jill Lalor, and Bridget Redquest for techni-
Peary caribou mtDNA control region haplotypes to data available on
cal support in the laboratory and Samantha McFarlane and Pauline
GenBank (number of haplotypes: >240) from those regions. There-
Priadka for map preparations. We are grateful to the Resolute Bay
fore, we currently view the possibility of a Beringian origin of HAL
Hunters and Trappers Association and the Iviq Hunters and Trap-
as improbable.
pers Association (Grise Fiord) for their guidance and support. We
Molecular evidence of a High Arctic refugium for Peary caribou
are indebted to the facilities of the Shared Hierarchical Academic
and other species contradicts some recent palaeoclimatic models
Research Computing Network (SHARCNET: www.sharcnet.ca) and
(England et al., 2009; Vaughan et al., 2014) that suggest northern
Compute Canada/Calcul Canada for providing high-performance
ice sheets covered the High Artic Archipelago entirely, thereby pre-
computing services. We thank Arthur Dyke and John England for
venting the inhabitation of floral and faunal species in Arctic refu-
helpful discussions and comments on an earlier version of the
gia during the glacial maxima. While fossil evidence for mammal
manuscript. Finally, we are thankful to Grant Zazula and two
remains is scare or specimens are relatively recent, i.e. post-LGM
anonymous referees for helpful comments that greatly improved
(Harington, 1990), there is evidence of two mammoth fossils dating
this manuscript. This work was funded by the Government of
20,700 270 YBP
and
Nunavut, Parks Canada, Environment and Climate Change Canada,
21,000 320 YBP (Harington, 2005). The caveat to this finding is
the Polar Continental Shelf Program and NSERC through the Col-
the potential for contamination in radiocarbon dating assays as
laborative, Strategic, Discovery and Canada Research Chair Pro-
observed with mastodon fossils (Zazula et al., 2014) and the possi-
grams. We also thank the following individuals and institutions for
bility of transport of mammoth fossils from other geographical
contributing to samples collection: Gary Mouland, Doug Stern, Rene
regions (MacPhee, 2007). The most recent results by Beel, Lifton,
Wissink from Parks Canada, Mitch Campbell, Grigor Hope and
to
the
LGM
approximately
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ET AL.
Tabitha Mullen from the Government of Nunavut, Etuangat Akeeagok from Grise Fiord, Tabitha Mullin, Samson Simeonie, Tommy Salluviniq and James Iqaluk from Resolute Bay, Judith Eger and Lim Burton from the Royal Ontarian Museum, Guy Savard and Mary Gamberg
from
Environment
Canada,
the
Sahtu
Renewable
Resources Board and the Ɂehdzo Got’ı̨ nez (Renewable Resources Councils), Heather Sayine-Crawford and Brett Elkin from the Government of the Northwest Territories, and Jean Polfus from the University of Manitoba.
CONFLICT OF INTERESTS We declare that we have no conflict of interest.
DATA ACCESSIBILITY The microsatellite data set supporting this article can be found on Dryad:
https://doi.org/10.5061/dryad.t1 cc5.
Newly
generated
mtDNA sequences have been deposited on GenBank (accession numbers: MF547418 – MF547447).
ORCID €tsch Cornelya F. C. Klu Micheline Manseau
http://orcid.org/0000-0001-8238-2484 http://orcid.org/0000-0003-0199-3668
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11
SUPPORTING INFORMATION BIOSKETCH The multidisciplinary research team focusses on the genetic and
Additional Supporting Information may be found online in the supporting information tab for this article.
ecological analyses of wildlife populations applying phylogeographical tools and landscape genetics as well as modelling approaches to understand the evolution and differentiation of
€tsch CFC, Manseau M, Anderson How to cite this article: Klu
biodiversity across landscapes. One major aim of the group is to
M, Sinkins P, Wilson PJ. Evolutionary reconstruction supports
integrate this knowledge into biologically meaningful conserva-
the presence of a Pleistocene Arctic refugium for a large
tion and management strategies to preserve biological variation
mammal species. J Biogeogr. 2017;00:1–11. https://doi.org/
in changing environments.
10.1111/jbi.13090
Author contributions: C.K., M.M. and P.W. conceived the study. C.K. assembled and analyzed the data and wrote up a first manuscript draft, M.M., A.M. and P.S. helped with sample collection and technical assistance. All authors contributed considerably to data interpretation and final manuscript preparation.
