BIOLOGICAL

CONSERVATION

Biological Conservation 118 (2004) 593–598

www.elsevier.com/locate/biocon

Genetic diversity and relatedness of boreal caribou populationsin western Canada

Philip D. McLoughlin a,*, David Paetkau b, Mary Duda c, Stan Boutin a

a Department of Biological Sciences, CW-405 Biological Sciences Centre, University of Alberta, Edmonton, AB, Canada T6G 2E9b Wildlife Genetics International Inc., Box 274, Nelson, BC, Canada V1L 5P9

c Slocan Forest Products, RR #1, Mile 294 Alaska Hwy, Fort Nelson, BC, Canada V0C 1R0

Received 20 May 2003; received in revised form 15 September 2003; accepted 12 October 2003

Abstract

We studied genetic diversity within and gene flow among six �threatened� populations of boreal caribou (Rangifer tarandus

caribou) inhabiting Alberta and British Columbia, Canada. Mean expected heterozygosity (HE) across 11 loci spanned a narrow

range between 0.74 and 0.79. Estimates of HE were in the mid to high range of those typically observed in natural populations of

large mammals, including caribou, and were not suggestive of any immediate threat to survival. We concluded that recent an-

thropogenic fragmentation of caribou range in western Canada has yet to affect genetic diversity of populations. Analysis of

population structure identified a region of relatively low gene flow corresponding with the valley of the Peace River. The highest

value of FST observed between populations on the same side of the river was 0.025, whereas the lowest value that spanned the river

was 0.044. Confirming this result, an assignment test demonstrated that 96.5% of animals could be assigned to the correct side of the

Peace River, though only 66.0% of animals could, on average, be assigned to populations of actual origin. Taken as a whole, our

results support the existence of two discrete metapopulations bisected by the Peace River, within each of which there exist multiple

populations, or at least multiple regions, which experience considerably higher levels of interchange. For caribou inhabiting

the boreal plains, large rivers such as the Peace and Mackenzie may serve as biologically meaningful boundaries for managing

metapopulations.

� 2003 Elsevier Ltd. All rights reserved.

Keywords: Alberta; Boreal; British Columbia; Canada; Caribou; DNA; Genetics; Microsatellite; Population; Rangifer tarandus caribou

1. Introduction

Boreal caribou are believed to be declining through-

out most of their range in Canada, but especially in the

west (Dzus, 2001; Ferguson and Gauthier, 1992; Gray,

1999; Mallory and Hillis, 1998; McLoughlin et al.,

2003). The species is currently listed as �threatened� bythe Committee on the Status of Endangered Wildlife inCanada (COSEWIC, 2000). Population declines are

thought to proximately result from high levels of

* Corresponding author. Present address: Department of Biology,

University of Saskatchewan, 112 Science Place, Saskatoon, 5K,

Canada S7N 5E2. Tel.: +1-306-966-4451; fax: +1-306-966-4461.

E-mail address: mcloughlin@sask.usask.ca (P.D. McLoughlin).

0006-3207/$ - see front matter � 2003 Elsevier Ltd. All rights reserved.

doi:10.1016/j.biocon.2003.10.008

predation, hunting, and human activity (Dzus, 2001;

Ferguson and Gauthier, 1992; Gray, 1999; Mallory and

Hillis, 1998; McLoughlin et al., 2003). Ultimately, de-

clines may be influenced by habitat alteration (e.g., in-

creased access into caribou range for humans as well as

predators, loss of old growth forests favoring alternate

ungulate prey species; McLoughlin et al., 2003). The

increasingly fragmented nature of caribou range in thewestern boreal forest may also be a factor in generating

population declines.

Although the lichen-dominated diet of boreal cari-

bou restricts the species to large, old-growth patches

(100–10,000 ha) of treed fens and bogs (Anderson,

1999; Bradshaw et al., 1995; James, 1999; Rettie and

Messier, 2000) and variation in hydrology and fire

regime entails that these habitats naturally exist as

Fig. 1. Ranges of boreal caribou examined in this study (shaded re-

gions with range names). WSAR, west side of the Athabasca River;

ESAR, east side of the Athabasca River; CLAWR, Cold Lake Air

Weapons Range. The hatched line approximates the historical south-

ern limit of woodland caribou range.

594 P.D. McLoughlin et al. / Biological Conservation 118 (2004) 593–598

fragments across the landscape, over the past 50 years

forestry and the spread of agriculture, mining, and oil

and gas exploration have substantially added to existing

natural fragmentation throughout much of boreal car-

ibou range. Recent studies of caribou in Alberta showthat caribou rarely cross roads and avoid most an-

thropogenic features, including cutblocks, wellsites, and

the pervasive network of seismic lines cut as part of

geophysical programs (Dyer et al., 2001; Smith et al.,

2000). Radio-monitored caribou demonstrate high fi-

delity to habitat patches, showing little or no seasonal

migration (Stuart-Smith et al., 1997), making move-

ments among population fragments exceedingly rare(Dzus, 2001). It is possible that low genetic diversity

within increasingly isolated population fragments is

acting as an accelerant to negative population growth in

western Canada.

The occurrence of low genetic diversity (e.g., low

expected heterozygosity, HE; Nei and Roychoudhury,

1974) is common to mammal populations inhabiting

islands (Frankham, 1997). In eastern Canada, isolatedpopulations of caribou exhibited values of HE that were

20% less than that of more open populations (Courtois

et al., 2003). Low genetic diversity may affect popula-

tions by impeding fertility, productivity, disease resis-

tance, and survival (Wright, 1977). Genetic diversity

within wild populations is important for maintaining

the ability of organisms to adapt to environmental

change (Soul�e, 1980), which, for caribou in westernCanada, will become ever more important as human

actions alter the natural processes and patterns of the

boreal forest.

Here, we use microsatellite markers to quantify ge-

netic diversity within and gene flow among six spatially

disjunct population fragments (herein referred to as

populations; Wells and Richmond, 1995) of boreal

caribou in Alberta and British Columbia, Canada(Fig. 1). Populations are declining at an average rate of

2.4% annually (McLoughlin et al., 2003). Estimates of

heterozygosity will set a benchmark of existing diver-

sity that may be important for future comparisons, but

also for gauging recent loss of diversity through com-

parisons with previously collected samples (e.g., hides,

trophies, or museum specimens). Identification of the

extent of genetic interchange among populations hasthe potential to alert managers to discrete demographic

units. This will help confirm or deny the status of the

western boreal caribou population as a functional

metapopulation (i.e., a set of spatially disjunct popu-

lations among which there is some immigration; Wells

and Richmond, 1995). Microsatellite analyses may also

form the basis for sound decision-making surrounding

any future supplementation (translocation) programsthat may become necessary, for example to maximize

genetic diversity or maintain genetically similar

populations.

2. Methods

2.1. Study area

The study area encompassed six population ranges

in Alberta and British Columbia (Fig. 1): the west side

of the Athabasca River (WSAR), east side of the

Athabasca River (ESAR), the Royal Canadian Air

Force�s Cold Lake Air Weapons Range (CLAWR),

the Caribou Mountains, and near the communities of

Red Earth and Fort Nelson. Elevation ranged between300 and 700 m, with little topographic variation except

in the Caribou Mountains (Alberta) and northeast

British Columbia (elevation 900 m). Black spruce

(Picea mariana) and tamarack (Larix larcina) domi-

nated fens and bogs (peatlands) in lowlands. Uplands

were dominated by white spruce (Picea glauca), jack

pine (Pinus banksiana), lodgepole pine (Pinus contorta),

and trembling aspen (Populus tremuloides). Bradshawet al. (1995) provides a detailed description of the

landscape typical of boreal caribou range in northern

Alberta.

P.D. McLoughlin et al. / Biological Conservation 118 (2004) 593–598 595

2.2. Animals

Between 1991 and 2002, we physically immobilized

332 caribou using nets projected from a net gun and fired

from a helicopter. Most captured caribou were adultfemales (90%). From these animals we preserved through

freezing 175 unique samples for genetic analysis, with

sample sizes ranging from 15 to 51 per population. Our

captures were purposely distributed evenly across cari-

bou population ranges, with generally no more than two

animals captured within the same group (herd) at the

same time (boreal caribou are scattered at low density in

groups usually numbering fewer than 15 animals; un-published data, J. Nolan, Boreal Caribou Committee,

Vegreville, Alberta). Samples included whole blood

(approximately 10 ml) and tissue and guard hairs with

intact roots where blood samples were not available.

2.3. DNA extraction

DNA was extracted using QIAamp (Qiagen Inc.,Mississauga, Ont.) DNA Blood Mini Kits (blood sam-

ples) or DNeasy Tissue Kits (tissue samples). We

amplified each DNA sample at 11 microsatellite loci

(Table 1) using the polymerase chain reaction (PCR).

The markers we chose have origins in (were first cloned

from) caribou (Wilson et al., 1997), cattle (Bos Taurus;

Bishop et al., 1994), and mule deer (Odocoileus hemi-

onus; Levine et al., 1998). All markers were dinucleotidemicrosatellites except OhN, which was a tetranucleotide

microsatellite. Markers excluded due to lack of variation

during preliminary screening included: BM203,

BM4107, BMC1009, CSSM041, FCB193, INRA107,

OhD, OhP, OvA, and OvH. PCR conditions for our

Perkin–Elmer 9700 thermal cycler were 1 min 15 s at 94

�C, followed by 40 cycles of 15 s at 94 �C, 20 s at 54 �Cand 5 s at 72 �C, and then 1 min at 72 �C. One primerfrom each pair of primers was fluorescently labelled.

Whenever possible, we used the primers that were de-

scribed in the first published report of the marker;

Table 1

Genetic markers and source of markers used in this study

Marker HE Reference (GenBank

or publication)

Primers

RT1 0.78 U90737 Modified

RT5 0.82 U90738 Modified

RT7 0.76 U90740 As published

RT13 0.79 U90743 Modified

RT24 0.72 U90746 Modified

BL42 0.77 Bishop et al. (1994) Modified

BM888 0.79 G18484 As published

BM3507 0.78 G18516 Modified

BM4513 0.87 G18507 As published

BM6506 0.80 G18455 Modified

OhN 0.53 AF102244 As published

Markers labelled RT are from caribou, BL and BM are from cattle,

and Oh is from mule deer.

however, in some cases we referred to the sequence that

is archived with GenBank (US Department of Health

and Human Services, National Institutes of Health,

Bethesda, MD), and made our own modifications

(Table 2). Modifications were sometimes made to enablemore markers to be run in the same lane, but were also

done to correct problems that made results difficult to

score. Allele sizes for each locus were determined by

analysis of the PCR products on a 310 Automated Se-

quencer (PE Biosystems, Foster City, CA), using

GeneScan� Analysis Software and Genotyper� Soft-

ware (Applied Biosystems, Foster City, CA).

2.4. Population genetics

After screening for possible duplicate samples, we

proceeded to test for non-random associations between

alleles within loci (Hardy–Weinberg equilibrium; Hartl

and Clark, 1989) and between loci (linkage disequilib-

rium; Hill and Robertson, 1968). These tests were carried

out to provide assurance that null alleles were not presentat a high frequency, and that our sampling areas were not

so large as to include animals from significantly distinct

breeding groups (which would produce aWahlund effect,

or deficit of heterozyogotes; Wahlund, 1928). These tests

(exact tests of Guo and Thompson, 1992) were carried

out using the web-based version of Genepop Version 3.1c

(Rousset and Raymond, 1995). Using Genepop, we also

tested for population differentiation (Raymond andRousset, 1995), combining results across all markers.

We used identified genotypes to measure genetic di-

versity within populations and, subsequently, relation-

ships among populations. Genetic diversity within a

population was measured by an unbiased estimate of

expected heterozygosity (HE; Nei and Roychoudhury,

1974). Interpopulation variation was estimated using

Weir and Cockerham�s, 1984) estimate of FST, a lowvariance statistic based upon a population model with

ongoing gene flow.

An assignment test (Paetkau et al., 1995), which as-

signs each individual to the population in which its ge-

notype is most likely to occur, was performed to provide

a more intuitive summary of the relationships between

populations. Likelihoods of occurrence were calculated

for each genotype (individual) in each population andanimals were �assigned� to the population in which their

genotype was most likely to have arisen. These calcu-

lations were made using the calculator available at

www.biology.ualberta.ca/jbrzusto/Doh.html.

3. Results

No significant (P < 0:05) departures from Hardy–

Weinberg equilibrium were detected, and none of the

five significant departures from linkage equilibrium

Table 2

Pairs of primers used for markers in this study

Marker Primer 1 Primer 2

Rt5 CAG CAT AAT TCT GAC AAG TG GTT GAG GGG ACT CGA CTG

Rt24 GTG TAT CCA TCT GGA AGA TTT CAG CAG TTT AAC CAG TCC TCT GTG

OheN GCA ACC AAT AGG ATA GGT CG GCT GGA TGG AAC TGA AAG TC

BM4513 TCA GCA ATT CAG TAC ATC ACC C GCG CAA GTT TCC TCA TGC

BM888 AGG CCA TAT AGG AGG CAA GCT T CTC GGT CAG CTC AAA ACG AG

Rt7 ACT TTT CAC GGG CAC TGG TT CCT GTT CTA CTC TTC TTC TC

BL42 ACA AGT CAA GGT CAA GTC CAA ATG CC GCA TTT TTG TGT TAA TTT CAT GC

BM3507 GCC CAA AGA AAG AAG TAT GTG C GTA GTG CGG AGT CAG TCA TGT G

BM6506 GTG GTA AAG AGA TGG CAT AGC A AAC TTA GCA ACT TGA GCA TGG

Rt1 AGA CCC ATC TTC CCA TCC TCT T TGC CTT CTT TCA TCC AAC AA

Rt13 CAT CCC AGA ACA GGA GTG AG AGA GAA TGG CCC AGT GTT AG

Table 3

The value of FST between population units. The box within the table highlights differences among populations on either side of the valley of the Peace

River

Caribou Fort CLAWR ESAR Red Earth WSAR

Mtns. Nelson

Caribou Mtns.

Fort Nelson 0.023

CLAWR 0.057 0.061

ESAR 0.044 0.054 )0.002Red Earth 0.051 0.065 0.021 0.007

WSAR 0.082 0.071 0.020 0.012 0.025

Table 4

Assignment chart for caribou populations in this study (Paetkau et al., 1995). Boxes within the table highlight differences among populations on the

same side of the Peace River valley

Source Population N Assigned Population

Caribou Mtns. Fort Nelson CLAWR ESAR Red Earth WSAR

Caribou Mtns. 30 23 4 0 3 0 0

Fort Nelson 17 2 14 0 0 1 0

CLAWR 51 0 0 32 7 4 8

ESAR 15 1 0 3 5 5 1

Red Earth 38 1 0 2 9 25 1

WSAR 24 0 0 1 4 1 18

596 P.D. McLoughlin et al. / Biological Conservation 118 (2004) 593–598

remained significant when critical values were adjusted

for the number of tests (Rice, 1989). For the tests of

population differentiation (Raymond and Rousset,

1995), only three pairs of populations failed to producehighly significant results (P < 0:001). All of these pairs

involved ESAR where the sample size, and thus the

power to detect differentiation, was lowest. One pair of

populations (ESAR-Red Earth) produced results that

were not significant (P > 0:10).Genetic diversity within populations as measured by

HE across 11 loci spanned a narrow range between 0.74

(Caribou Mountains and Red Earth) and 0.79 (ESAR).Values of FST showed a clear distinction between pop-

ulations to the east and north and to the south and west

of the Peace River valley (Table 3, Fig. 1). The highest

value observed between populations on the same side of

the Peace River was 0.025, whereas the lowest value that

spans the river was 0.044. The assignment test (Table 4)

demonstrated that there was sufficient differentiation

between populations to allow most animals to be

correctly assigned to their population of origin(�X ¼ 66:0%); however, this varied with sample size and

location of populations (SD¼ 17.5%). Notably, the as-

signment test also showed a clear division in the data

along the Peace River boundary: 96.5% of animals were

assigned to the correct side of the valley.

4. Discussion

4.1. Diversity and relatedness

Despite declining populations and the �threatened�status of boreal caribou in Canada, genetic diversity

P.D. McLoughlin et al. / Biological Conservation 118 (2004) 593–598 597

among and within populations continues to lack ade-

quate documentation throughout most of the species�range. Studies to report genetic diversity for caribou

populations include Courtois et al. (2003), Kushny et al.

(1994), Van Staaden et al. (1995), and Zittlau et al.(2000), and a handful of unpublished accounts and

government reports (e.g., Kinley, 2001). Our study adds

to the documentation of current genetic diversity for

boreal caribou. The level of diversity observed within

caribou populations (HE) was in the mid to high range

of that typically observed in natural populations of large

mammals, and was comparable to estimates of HE ob-

tained for caribou in the Yukon (Zittlau et al., 2000) andQu�ebec (Courtois et al., 2003). Our results do not sug-

gest the sort of genetic impoverishment that would be

associated with threats to survival (Wright, 1977).

There was no meaningful variation in HE between any

single population versus combinations of other popu-

lations, ruling out the possibility that caribou of any

individual range had a history of strong genetic isola-

tion. However, inter-population analyses identified aclear division in genetic relatedness along the natural

boundary of the Peace River (Fig. 1), with relatively

little population structure on either side of the river, but

substantially more differentiation between the two sides.

For example, the value of FST between the Caribou

Mountains and Red Earth was more than double that

between Red Earth and the physically more distant

CLAWR. Consistent with FST results, the differentiationacross the Peace River stands out in the assignment test,

with almost all animals assigned to a population on the

correct side of the valley (Table 4). Individuals from the

Caribou Mountains and Red Earth, to take again as an

example, had almost completely non-overlapping like-

lihood distributions – such that origin could be assigned

with some confidence – but there was substantially more

overlap between the Red Earth and CLAWR distribu-tions (not shown). Taken as a whole, our results support

the existence of two discrete metapopulations, within

each of which there exist multiple populations, or at

least multiple regions, which experience considerably

higher levels of interchange.

4.2. Conservation implications

Relatively high levels of heterozygosity lead us to

conclude that observed population declines for boreal

caribou in western Canada have not been the result of

inbreeding depression or other effects of low genetic

diversity. This conclusion is supported by consistent

observations of healthy, disease-free caribou for several

boreal populations in western Canada and typically high

rates of pregnancy and calf production (e.g., centralSaskatchewan, Rettie and Messier, 1998 and northern

Alberta, McLoughlin et al., 2003; Stuart-Smith et al.,

1997). Of particular importance, it appears that the

recent anthropogenic fragmentation of caribou range in

our study area has yet to affect the genetic makeup of

populations. That we see no loss of genetic diversity

from what we might expect naturally – our values of HE

are comparable to that of Yukon and barren-groundcaribou where anthropogenic disturbance is very low

(Courtois et al., 2003; Zittlau et al., 2000) – sets

a benchmark of diversity for us to maintain into the

future.

Our results further suggest that for caribou inhabiting

the boreal plains, large rivers such as the Peace and

Mackenzie may serve as biologically meaningful

boundaries for managing metapopulations. Boreal car-ibou may naturally avoid large river corridors because

they provide for higher densities of alternate prey spe-

cies, such as moose (Alces alces) and their primary

predator, the gray wolf (Canis lupus). James (1999)

demonstrated that wolf pack territories in northern Al-

berta centered on river valleys. Moose preference for

river valleys has been noted by Boonstra and Sinclair

(1984) and Chekchak et al. (1998). As populationsbecome more isolated due to anthropogenic fragmen-

tation, HE may be maintained through physical trans-

locations of caribou previously identified to belong to

the same metapopulation.

Acknowledgements

Funding for this project was provided by the Boreal

Caribou Committee (BCC) of Alberta, Alberta Re-

search Council Inc., Slocan Forest Products Ltd., Forest

Renewal BC, and the Natural Science and Engineering

Research Council of Canada (NSERC). All genetic

analyses were performed in cooperation with WildlifeGenetics International Inc.

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