Post on 06-May-2023
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.
References
Anderson, R.B., 1999. Peatland habitat use and selection by woodland
caribou (Rangifer tarandus caribou) in northern Alberta. MSc
Thesis, University of Alberta.
Bishop, M.D., Kappes, S.M., Keele, J.W., Stone, R.T., Sunden,
S.L.F., Hawkins, G.A., Toldo, S.S., Fries, R., Grosz, M.D., Yoo,
J., Beattie, C.W., 1994. A genetic linkage map for cattle. Genetics
136, 619–639.
Boonstra, R., Sinclair, A.R.E., 1984. Distribution and habitat use of
caribou, Rangifer tarandus, and moose, Alces alces andersoni, in the
Spatsizi Plateau Wilderness Area, British Columbia, Canada.
Canadian Field-Naturalist 98, 12–21.
Bradshaw, C.J.A., Hebert, D.M., Rippen, A.B., Boutin, S., 1995.
Winter peatland habitat selection by woodland caribou in north-
eastern Alberta. Canadian Journal of Zoology 73, 1567–1574.
Chekchak, T., Courtois, R., Ouellet, J.P., Breton, L., St. Onge, S.,
1998. Caracteristiques des sites de mise bas de l�original (Alces
alces). Canadian Journal of Zoology 76, 1663–1670.
598 P.D. McLoughlin et al. / Biological Conservation 118 (2004) 593–598
COSEWIC, 2000. Canadian species at risk. Committee on the Status
of Endangered Wildlife in Canada. Available from http://
www.cosewic.gc.ca(Revision date: 13 July 2000).
Courtois, R., Bernatchez, L., Ouellet, J.P., Breton, L., 2003. Signif-
icance of caribou (Rangifer tarandus) ecotypes from a molecular
genetics viewpoint. Conservation Genetics 4, 393–403.
Dyer, S.J., O�Neill, J.P., Wasel, S.M., Boutin, S., 2001. Avoidance of
industrial development by woodland caribou. Journal of Wildlife
Management 65, 531–542.
Dzus, E., 2001. Status of the woodland caribou (Rangifer tarandus
caribou) in Alberta. Alberta Environment, Fisheries and Wildlife
Management Division and Alberta Conservation Association.
Wildlife Status Report No. 30, Edmonton, Alberta.
Ferguson, M.A.D., Gauthier, K.L., 1992. Status and trends of
Rangifer tarandus and Ovibos moschatus populations in Canada.
Rangifer 12, 127–141.
Frankham, R., 1997. Do island populations have less genetic
variability than mainland populations? Heredity 78, 311–327.
Gray, D.R., 1999. Updated status report on the woodland caribou in
Canada. Prepared for the Committee on the Status of Endangered
Wildlife in Canada (COSEWIC) by Grayhound Information
Services, Metcalfe, Ontario.
Guo, S.W., Thompson, E.A., 1992. Performing the exact test of
Hardy–Weinberg proportions for multiple alleles. Biometrics 48,
361–372.
Hartl, D.L., Clark, A.G., 1989. Principles of Population Genetics.
Sinauer Associates, Sunderland, MA.
Hill, W.G., Robertson, A., 1968. Linkage disequilibrium in finite
populations. Theoretical Population Biology 38, 226–239.
James, A.R.C., 1999. Effects of industrial development on the
predator–prey relationship between wolves and caribou in north-
eastern Alberta. PhD Dissertation, University of Alberta.
Kinley, T., 2001. Recovery Action Plan for the South Purcells
Subpopulation of Mountain Caribou. Sylvan Consulting Ltd.,
Invermere, BC.
Kushny, J., Coffin, J., Strobeck, C., 1994. Genetic survey of caribou
populations using microsatellite DNA. Rangifer Special Issue 10,
31–138.
Levine, K., Banks, J., Sadowski, G., Bienvenue, P., Hones, K.C., 1998.
DNA-based Genetic Markers in Black-tailed and Mule Deer for
Forensic Applications. California Department of Fish and Game,
Rancho Cordova, CA.
Mallory, F.F., Hillis, T.L., 1998. Demographic characteristics of
circumpolar caribou populations: ecotypes, ecological constraints,
releases, and population dynamics. Rangifer Special Issue 10, 49–60.
McLoughlin, P.D., Dzus, E., Wynes, B., Boutin, S., 2003. Declines in
populations of woodland caribou. Journal of Wildlife Management
67, 755–761.
Nei, M., Roychoudhury, A.K., 1974. Sampling variances of hetero-
zygosity and genetic distance. Genetics 76, 379–390.
Paetkau, D., Calvert, W., Stirling, I., Strobeck, C., 1995. Microsatellite
analysis of population structure in Canadian polar bears. Molec-
ular Ecology 4, 347–354.
Raymond, M., Rousset, F., 1995. An exact test for population
differentiation. Evolution 49, 1280–1283.
Rice, W.R., 1989. Analyzing tables of statistical tests. Evolution 43,
223–225.
Rettie, W.J., Messier, F., 1998. Dynamics of woodland caribou
populations at the southern limit of their range in Saskatchewan.
Canadian Journal of Zoology 76, 251–259.
Rettie, W.J., Messier, F., 2000. Hierarchical habitat selection by
woodland caribou: its relationship to limiting factors. Ecography
23, 466–478.
Rousset, F., Raymond, M., 1995. Testing heterozygote excess and
deficiency. Genetics 140, 1413–1419.
Smith, K.G., Janet Ficht, E., Hobson, D., Sorenson, T.C., Hervieux,
D., 2000. Winter distribution of woodland caribou in relation to
clear-cut logging in west-central Alberta. Canadian Journal of
Zoology 78, 1433–1440.
Soul�e, M.E., 1980. Conservation biology: an evolutionary perspective.
In: Soul�e, M.E., Wilcox, B.A. (Eds.), Conservation Biology.
Sinauer Associates, Sunderland, MA, pp. 24–44.
Stuart-Smith, A.K., Bradshaw, C.J.A., Boutin, S., Hebert, D.M.,
Rippin, A.B., 1997. Woodland caribou relative to landscape
patterns in northeastern Alberta. Journal of Wildlife Management
61, 622–633.
Van Staaden, M.J., Hamilton, M.J., Chesser, R.K., 1995. Genetic
variation of woodland caribou (Rangifer tarandus) in North
America. Zeitschrift fuer Saeugetierkunde 60, 150–158.
Wahlund, S., 1928. Zusammensetzung von populationen und korre-
lation-serscheinungen vom standpunkt der vererbungslehre aus
betrachtet. Hereditas 11, 65–106.
Weir, B.S., Cockerham, C.C., 1984. Estimating F -statistics for
the analysis of population structure. Evolution 38, 1358–
1370.
Wells, J.V., Richmond, M.E., 1995. Populations, metapopulations,
and species populations: what are they and who should care.
Wildlife Society Bulletin 23, 458–462.
Wilson, G.A., Strobeck, C., Wu, L., Coffin, J.W., 1997. Characteriza-
tion of microsatellite loci in caribou Rangifer tarandus, and their
use in other artiodactyls. Molecular Ecology 6, 697–699.
Wright, S., 1977. Evolution and the Genetics of Populations. Univer-
sity of Chicago Press, Chicago, IL.
Zittlau, K., Coffin, J., Farnell, R., Kuzyk, G., Strobeck, C., 2000.
Genetic relationships of three Yukon woodland caribou herds
determined by DNA typing. Rangifer Special Issue 12, 59–62.