Journal of Biogeography (J. Biogeogr.) (2005) 32, 1943–1956
ORIGINAL
ARTICLE
Historical biogeography of two alpine
butterflies in the Rocky Mountains:
broad-scale concordance and local-scale
discordance
Eric G. DeChaine1* and Andrew P. Martin2
1
Department of Organismic and Evolutionary
Biology, Harvard University, Cambridge, MA,
USA and 2Department of Ecology and
Evolutionary Biology, University of Colorado,
Boulder, CO, USA
ABSTRACT
Aim We inferred the phylogeography of the alpine butterfly Colias meadii
Edwards (Pieridae) and compared its genetic structure with that of another
high elevation, co-distributed butterfly, Parnassius smintheus Doubleday
(Papilionidae), to test if the two Rocky Mountain butterflies responded
similarly to the palaeoclimatic cycles of the Quaternary.
Location Specimens were collected from 18 alpine sites in the Rocky Mountains
of North America, from southern Colorado to northern Montana.
Methods We sequenced 867 and 789 nucleotides of cytochrome oxidase I from
an average of 19 and 20 individuals for C. meadii and P. smintheus, respectively,
from each of the same 18 localities. From the sequence data, we calculated
measures of genetic diversity within each population (H, h), genetic divergence
among populations (FST), and tested for geographic structure through an analysis
of molecular variance (amova). Population estimates were compared against
latitude and between species using a variety of statistical tests. Furthermore,
nested clade analysis was implemented to infer historic events underlying the
geographic distribution of genetic variation in each species. Then, we compared
the number of inferred population events between species using a nonparametric
Spearman’s rank correlation test. Finally, we ran coalescent simulations on each
species’ genealogy to test whether the two species of Lepidoptera fit the same
model of population divergence.
Results Our analyses revealed that: (1) measures of within-population diversity
were not correlated with latitude for either species, (2) within-site diversity was
not correlated between species, (3) within a species, nearly all populations were
genetically isolated, (4) both species exhibited significant and nearly identical
partitioning of genetic variation at all hierarchical levels of the amova, including
a strong break between populations across the Wyoming Basin, (5) both species
experienced similar cycles of expansion and contraction, although fewer were
inferred for C. meadii, and (6) data from both species fit a model of three refugia
diverging during the Pleistocene.
*Correspondence: Eric G. DeChaine,
Department of Organismic and Evolutionary
Biology, Harvard University, 16 Divinity Ave,
Biolabs 4081, Cambridge, MA 02138, USA.
E-mail: [email protected]
Main conclusions While our findings supported a shared response of the two
butterfly species to historic climate change across coarse spatial scales, a common
pattern was not evident at finer spatial and temporal scales. The shared
demographic history of the two species is consistent with an expanding–
contracting archipelago model, suggesting that populations persisted across the
geographic range throughout the climate cycles, experiencing isolation on ‘sky
islands’ during interglacial periods and becoming connected as they migrated
down-slope during cool, wet climates.
ª 2005 Blackwell Publishing Ltd www.blackwellpublishing.com/jbi
doi:10.1111/j.1365-2699.2005.01356.x
1943
E. G. DeChaine and A. P. Martin
Keywords
Alpine tundra, coalescent simulations, Colias meadii, Lepidoptera, Parnassius
smintheus, Pleistocene climate cycles, Rocky Mountains, statistical phylogeography, U.S.A.
conditions across the shifting landscape (e.g. West, 1980;
Coope, 1995; Johansen & Latta, 2003). During unfavourable
periods, species’ distributions contracted and populations were
forced to persist in a few fragmented refugia, comprising only a
fraction of the species’ previous range (e.g. Betancourt et al.,
1990). This oscillation of climatic conditions over the course of
thousands of years has promoted the cyclic expansion and
contraction of species ranges in evolutionary time (Avise, 2000;
Hewitt, 2000).
Periods of favourable climate that spurred range expansion
differed among taxa depending on a species’ niche requirements. For temperate taxa inhabiting low- to mid-elevation
INTRODUCTION
Quaternary climate oscillations played a central role in
determining the distribution of species and defining the
context for evolution (Huntley & Webb, 1989; Webb &
Bartlein, 1992; Hewitt, 1996, 2000). Alternation between colder
glacial periods and warmer interglacial periods (Fig. 1a) has
created a temporal and geographic mosaic of continental ice
sheets, mountain glaciers, and available habitat (Richmond,
1965; Winograd et al., 1997). In response to palaeoclimatic
fluctuations, species’ geographic and elevation ranges have
tracked preferred habitat and suitable environmental
Palaeoclimatic record
(a)
Populations
(b)
0
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18
50
T1
100
T2
150
200
Time (1000 years bp)
T3
250
(c)
300
T4
Biogeographic regions
North
350
Central
South
T1
400
T5
450
(d)
500
T6
550
T6
600
-3
-2
-1
0
1
2
3
4
18
δ O
Interglacial
Glacial
Figure 1 Hypotheses of population divergence throughout the Quaternary climate cycles. (a) The palaeoclimatic record over the last
600,000 years based on benthonic foraminifera data from SPECMAP (Imbrie et al., 1989) and Devil’s Hole in Nevada, U.S.A. (Landwehr
et al., 1997). The timeline is given along the y-axis in thousands of years before present (bp). Delta 18O is given in standard deviations and
serves as a proxy for past climates (low ¼ cooler and high ¼ warmer). Interglacial and glacial periods are delineated by grey and white
bands, respectively. The interglacials were used to estimate divergence times (T1 through T6) in the phylogeographic models. For the models
of population divergence (b, c, d), gene trees (shown in black) are constrained within the grey population trees. The null model of a single
population experiencing fragmentation is shown in part b, where each population corresponds to one of the study sites (see Table 1 for
populations details). The 3-refugia model, wherein the three regional populations have been determined through biogeographic and
phylogeographic analyses, is shown for two of the seven different divergence time scenarios in part c and d.
1944
Journal of Biogeography 32, 1943–1956, ª 2005 Blackwell Publishing Ltd
Historical biogeography of Rocky Mountain butterflies
environments, distributions are larger now, in the current
interglacial, than during previous glacial periods when species
were restricted to a few, distant refugia of suitable habitat
(Webb & Bartlein, 1992; Comes & Kadereit, 1998; Ayoub &
Riechert, 2004; Dobes et al., 2004). By contrast, glacial periods
probably connected the alpine tundra and permitted broader
distributions of high elevation species, while warm interglacials
caused the fragmentation of habitat and upslope contraction of
species’ ranges into ‘sky islands’ (Elias, 1996; Hewitt, 2000).
Because species responded individually to historic climate
changes, the detection of general phylogeographic patterns has
proven difficult, even within a habitat-type (Delcourt &
Delcourt, 1991; FAUNMAP Working Group et al., 1996;
Comes & Kadereit, 1998; Taberlet et al., 1998).
Alpine species could have persisted across an extensive
latitudinal range of the Rocky Mountain cordillera throughout
several glacial–interglacial climate cycles by shifting elevation.
The alpine habitat in the Rocky Mountains is highly dissected
and widely-dispersed, comprising an archipelago of high
elevation sky islands (Küchler, 1985; Fig. 2a). Many populations of alpine arthropods and plants are isolated on mountain
tops in the current interglacial and probably exhibit different
demographic characteristics (Golden & Bain, 2000; Knowles,
2000, 2001; Masta, 2000; DeChaine & Martin, 2004, 2005). In
contrast, the Rocky Mountain alpine zone was relatively
contiguous during glacial periods, except for a major break
associated with the Wyoming Basin (Pewe, 1983; Elias, 1996;
Fig. 2b). Interconnection during the glacial periods could have
facilitated genetic and demographic cohesion within a geographic region.
How did climate cycles of the Quaternary affect the
demographic histories of wide-ranging, high elevation species
in the Rocky Mountains? And, did species respond similarly or
independently to the glacial cycles? If different species shared a
common demographic response to palaeoclimatic cycles, then
geographic partitioning of genetic variation and historic
inferences of population divergence will be correlated between
the species. To address these questions, we inferred the
historical biogeography of the alpine butterfly Colias meadii
Edwards (Pieridae) throughout its range in the Rocky Mountains using mtDNA and compared the results from C. meadii
with data from a co-distributed species, Parnassius smintheus
Doubleday (Papilionidae; DeChaine & Martin, 2004) and with
patterns described for other species (Britten & Brussard, 1992;
Noonan, 1992, 1999; Reiss et al., 1999; Nice & Shapiro, 2001).
Moreover, we tested specific models of Pleistocene divergence
for both species, based on the biogeography of the Rocky
Mountains and previous inferences for P. smintheus (DeChaine
& Martin, 2004): a null hypothesis of fragmentation in a single,
widespread ancestral population and a 3-refugia model
(partitioned into the northern, central, and southern Rockies),
with possible divergence times ranging from 50,000 (most
recent warm period) to 1,700,000 (pre-Pleistocene) yr bp
(Fig. 1). Our comparative approach yielded support for a
general model of how high elevation organisms have responded to climate change over the past four glacial cycles
(400,000 yr bp) and establishes a baseline for predicting the
effects of future climate change.
MATERIALS AND METHODS
Mead’s Sulphur, Colias meadii, inhabits alpine tundra and
subalpine steppe of the Rocky Mountains from southern
Colorado, where the effects of interglacial habitat fragmentation are most severe, to northern Montana (Fig. 2a; Scott,
1986; Nabokov, 2000), which was completely covered by the
Cordilleran and Laurentide ice sheets (Richmond, 1965).
Colias meadii is not known from the Rockies of mid-Montana,
nor in the Wyoming Basin (Ferris & Brown, 1981; Opler et al.,
1995), which, due to its low elevation and xeric habitat, acts as
a significant barrier to dispersal of some high elevation insects
(Noonan, 2001; DeChaine & Martin, 2004). P. smintheus, the
Rocky Mountain Apollo, shares the range of C. meadii, but is
more broadly distributed (Scott, 1986). Both species of
Lepidoptera are strong flyers, but exhibit short-distance
dispersal as revealed through population analyses using genetic
markers (Johnson, 1977; Watt et al., 1996; Keyghobadi et al.,
1999; DeChaine & Martin, 2004).
Specimen collection
Specimens of C. meadii and P. smintheus were collected from
eighteen sites throughout their range (Fig. 3a). The number
of sampling locations within a region (north, south, and
central Rockies; Brouillet & Whetstone, 1993) was proportional to the estimated relative abundance of populations of
C. meadii within that region (Fig. 2a). Seven of the sites were
within national parks: Glacier National Park (permit no.
GLAC-2001-SCI-0020), Yellowstone National Park (permit
no. YELL-2001-SCI-0212), Grand Teton National Park (permit
no. GRTE-2001-SCI-0009), and Rocky Mountain National
Park (permit no. ROMO-2001-SCI-0037), while the remaining eleven sampling locations were on public lands. From
each population, ten to twenty-nine individuals were captured with a hand-net, stored in glassine envelopes, transported
on dry ice and stored at )80 C at the University of
Colorado, Boulder.
Molecular techniques
The cytochrome oxidase I (COI) gene from the mitochondrial
genome was employed for comparative population genetic
analyses because of its rapid rate of evolution and its wide use in
studies of insect phylogeography (Caterino et al., 2000).
Following DNA extraction from thorax tissue using DNeasy
Tissue Extraction Kits (Qiagen, Valencia, CA, USA), we
amplified and sequenced a portion of COI, using specific
primers. The C. meadii primers were: CmF: (5¢-GAGTATCGTCGAGGTATTCC-3¢) and CmR: (5¢-GCAGGAACTGGATGAACAG-3¢). Products from PCR were cleaned
using the Wizard PCR Preps (Promega; Madison, WI, USA).
Sequencing products were generated from the PCR amplicons
Journal of Biogeography 32, 1943–1956, ª 2005 Blackwell Publishing Ltd
1945
E. G. DeChaine and A. P. Martin
(a) Interglacial
49
MT
N
47
Latitude (°N)
C
WY
45
43
ID
W
CO
S
41
39
UT
37
(b) Glacial
49
MT
47
Latitude (°N)
WY
45
43
ID
W
CO
41
39
UT
3500
4500
4000
2500
3000
2000
1500
Elevation (m)
with a Thermo Sequenase DYEnamic Direct Cycle Sequencing
Kit with 7-deaza-dGTP (Amersham Biosciences, Piscataway,
NJ, USA) and nested primers. The nested primers for C. meadii
were CmNF: (5¢-AACGGAGCAGGAACAGGATG-3¢) and
CmNR: (5¢-GGGTAATCTGAATATCGACG-3¢). Forward
and reverse strands were sequenced on a Li-Cor 4200 automated sequencer (Li-Cor, Inc, Lincoln, NE, USA). Reactions for
PCR, cycle sequencing, and thermal cycler profiles, along
with the molecular methods used to collect mitochondrial
sequence data for P. smintheus, are as previously described
(DeChaine & Martin, 2004). Sequences were checked on
1946
1000
37
Distribution of Colias meadii
Distribution of alpine hatitat
Figure 2 The distribution of alpine habitat
in the Rocky Mountains during interglacial
and glacial periods and the known distribution of Colias meadii Edwards. The grey
shaded regions represent the distribution of
alpine habitat during (a) an interglacial,
using the current distribution of alpine habitat (from Küchler, 1985) and (b) a glacial
period, given a 1000 m drop in elevation
(Pewe, 1983). The Wyoming Basin (W) is
labelled. Elevation profiles for each period are
on the right. The transect for the elevation
profiles basically follows the Continental
Divide from the San Juan Range in southern
Colorado to Glacier National Park in Montana, but incorporates study sites and other
locations that emphasize changes in elevation. Latitude and elevation data were
obtained from topographic atlases of the
region (DeLorme, 1998a–d). In part a, the
known distribution of C. meadii (Ferris &
Brown, 1981; Opler et al., 1995) is shaded in
black over the current alpine distribution and
the northern (N), central (C) and southern
(S) regions are labelled.
AlignIR v2.0 software (Li-Cor, Inc.) and aligned with Clustal X
(Thompson et al., 1997; Strasbourg, France). A total of 867
and 789 nucleotides of COI were sequenced from an average
of 19 and 20 individuals for C. meadii and P. smintheus
(DeChaine & Martin, 2004), respectively, from 18 alpine
populations.
Population genetic analyses
Estimates of within and among population genetic variation
were calculated for C. meadii and P. smintheus and then
Journal of Biogeography 32, 1943–1956, ª 2005 Blackwell Publishing Ltd
Historical biogeography of Rocky Mountain butterflies
Colias meadii
(a)
Parnassius smintheus
(b)
MT
1 2
3
Private
Alleles
Private
Alleles
MT
1 2
3
CG1
CG3
CY1
CY2
G1
G5
Y1
Y4
Y7
Y8
CY14
CY15
4
5 6
7
8
WY
CC2
CC5
CC8
CC9
CC15
CC16
ID
5 6
4
WY
7
8
ID
CC17
CC27
9
10
12
12
13
14
16
18
UT
CO
11
13
14
15
17
15
UT
9
10
CO
11
16
17
18
R4
R5
R6
R7
C1
C2
C4
C6
C7
C12
C13
C21
C22
C23
C28
C29
C31
Figure 3 Collection sites and haplotype distributions. Sample sites are shown as circles and population numbers correspond to those in
Table 1. (a) Colias meadii Edwards. (b) Parnassius smintheus Doubleday (modified from DeChaine & Martin, 2004). Pie charts show the
proportions of haplotypes within each population. The distributions of wide-ranging haplotypes are denoted by colour, while private alleles
are white. Note that C. meadii and P. smintheus do not share any haplotypes regardless of overlap in colours between the two species. See
Table 1 for the frequency of private alleles within each population.
contrasted between the two species to test for evidence of
similarities in demographic history. For each population,
haplotype diversity (H) and three measures of h, a genealogical
estimate determined with the fluctuate 1.4 software package
(Kuhner et al., 1995), and two others based on the average
within-population pair-wise sequence divergence (p) and the
number of segregating sites (S) were calculated on arlequin
v.2.0 (Schneider et al., 2000). All measures of genetic diversity,
H and h, were regressed against latitude and significance was
assessed using a Mantel test. To test for similarities between
species at the population level, values of H from the two
species were compared using a Wilcoxon sign rank test and
values of h were contrasted using a t-test following logtransformation of the data. We also compared values of h for
each population between species using a nonparametric
Spearmann rank correlation. Finally, Tajima’s D tests of
neutrality (Tajima, 1989) were performed on data for both
species by comparing hp and hS within each population. While
significantly negative D-values are evidence of a recent
population bottleneck (Rogers, 1995), inferences must be
viewed with caution due to the potential for biases to be
introduced by sampling error and population structure
(Hammer et al., 2003).
The degree of genetic divergence, or isolation, at different
geographic scales was assessed using FST, as is commonly done
in studies of population structure (Avise, 2004). Matrices of
pair-wise population FST values for each species were compared using a Mantel test, to evaluate patterns of population
differentiation between the species. To test for genetic
structure at various geographic scales, we subjected the data
to an analysis of molecular variance (amova) with three
hierarchical levels: among regions, among populations within
each region, and within populations. For the amova, regions
were defined as the north (populations 1–3), central (populations 4–8) and southern (populations 9–18) Rocky Mountain
physiographic provinces, following Brouillet & Whetstone
(1993). All calculations were performed using arlequin v.2.0
(Schneider et al., 2000).
Historical inferences based on nested clade analysis
Population processes underlying the geographic distribution of
genetic variation in both species were inferred from intraspecific genealogies. For both species, intraspecific phylogenies
were estimated using statistical parsimony with the aid of the
tcs (acronym for Templeton, Crandall, and Sing from
Templeton et al., 1992) software package (Clement et al.,
2000). From the genealogies, population processes were
inferred through nested clade analysis (NCA; Templeton et al.,
1995) implemented using GeoDis (Posada et al., 2000) and the
inference key in Templeton (1998). Through NCA, phylogenetic clades at all depths, or levels, within the tree are tested
to determine if there is a significant match between genealogy
and geography. Although widely used, inferences gleaned
through NCA must be interpreted with caution because the
analysis is unable to statistically examine alternative scenarios
(Knowles & Maddison, 2002). For this reason, we lumped
inferences into two categories: (1) expansion events that
included contiguous range expansion and long distance
dispersal, and (2) fragmentation events that could have
Journal of Biogeography 32, 1943–1956, ª 2005 Blackwell Publishing Ltd
1947
E. G. DeChaine and A. P. Martin
occurred through past fragmentation or restricted gene flow, as
defined by Templeton (1998). To test whether similar
demographic events occurred at the same time within both
species, we contrasted the number of significant expansion and
fragmentation events within a clade level (depth of phylogeny)
between species using the nonparametric Spearman’s correlation test.
Testing phylogeographic hypotheses using coalescent
simulations
Objective tests of the scenarios resulting from the population
genetic and nested clade approaches were performed in order
to evaluate support for the phylogeographic models (Knowles
& Maddison, 2002). Coalescent simulations of genealogies
constrained within models of population divergence provide a
powerful means of assessing how well observed genetic
patterns fit phylogeographic hypotheses (Knowles, 2001;
Carstens et al., 2005). We tested two general models of
population divergence to determine whether observed patterns
in C. meadii and P. smintheus were consistent with the null
hypothesis of fragmentation from a single, ancestral population (Fig. 1b) or differentiation in three refugia and if
divergence times were concordant between the two species.
Under the alternative hypothesis (Fig. 1c,d), populations of
alpine butterflies were isolated into 3-refugia, corresponding to
the northern, central, and southern biogeographic provinces of
the Rocky Mountains (Fig. 2a; Brouillet & Whetstone, 1993).
The alternative model was developed from phylogeographic
patterns for P. smintheus (DeChaine & Martin, 2004) and
patterns of genetic diversity inferred for C. meadii in this study
(see Results). Because high elevation taxa are expected to
experience population fragmentation during warm, interglacials, the seven divergence times that were tested for each
model correspond to interglacials over the last 600,000 years
(Fig. 1a; T1 ¼ 50,000, T2 ¼ 100,000, T3 ¼ 200,000, T4 ¼
300,000, T5 ¼ 400,000, T6 ¼ 500,000 yr bp) and include a
pre-Pleistocene date (1,700,000 yr bp).
In order to determine the probability that a species’
genealogy was generated under each hypothesis of population
divergence, we first estimated the genealogy and population
size (Ne) for a species and then evaluated how well the
observed data fit the expectations generated by coalescent
simulations of each model. modeltest 3.6 (Posada &
Crandall, 1998) was employed to evaluate models of DNA
substitution for both species individually and to select the
model that best fitted the data based on the Akaike
Information Criterion (AIC). The best-fit model for a species
was used to generate two genealogies in paup* 4.10b
(Swofford, 2003), one with and one without a molecular clock
enforced. The two trees were compared with a Likelihood
Ratio Test (LRT; Felsenstein, 1988) to determine if the data
were consistent with a molecular clock.
The sequence data were also subjected to additional
population genetic analyses in MDIV (Nielsen & Wakeley,
2001), which simultaneously estimates h (¼ 2Nel) and
1948
divergence time (T/2Ne). The program was run, using the
HKY. finite sites model, three times for each species to evaluate
convergence for each parameter. From the results, the effective
population size (Ne) was estimated using a 2.3% sequence
divergence per million years for COI in Lepidoptera (Brower,
1994).
Coalescent simulations, incorporating the species’ genealogy and estimate of Ne, were performed on mesquite 1.05
(Maddison & Maddison, 2003) to test how well the observed
data fit each model of divergence. To test the null
hypothesis, whether fragmentation in a widespread ancestral
population could explain the observed genealogy, 100 gene
trees were simulated by coalescence within the null model
(Fig. 1b). First, a set of gene matrices was simulated for
each of the hypothetical divergence times [where the
branch length ¼ the number of generations, and 1 generation ¼ 1 year for these species of Lepidoptera (Scott, 1986)],
using the species-specific model of DNA substitution
determined by MODELTEST 3.6 (Posada & Crandall,
1998) and the estimate of Ne. Trees were then reconstructed
from the simulated gene matrices in PAUP* 4.10b
(Swofford, 2003). The resulting gene trees were contained
within the 3-refugia model with the corresponding divergence time (Fig. 1a,c,d) and the amount of discordance, as
measured by S, the minimum number of sorting events
required to produce the genealogy within a given model of
divergence (Slatkin & Maddison, 1989), was determined. The
S-value for the observed tree constrained within the
3-refugia model was compared to the distribution of
S-values from the simulations to determine if the observed
genealogy could have been generated under the null model.
A similar approach was adopted to test the 3-refugia model
over a range of different divergence times. One hundred gene
matrices were simulated under the chosen model of DNA
substitution and constrained within the population history
predicted by the 3-refugia model for a given time of
divergence. Trees were reconstructed in PAUP* 4.10b (Swofford, 2003) and the S-distribution from the simulated gene
trees constrained by the 3-refugia model was compared with
that of the observed tree for each divergence time (T1 through
T7). In so doing, we were able to test whether the observed
genealogies were consistent with the 3-refugia model and
estimate a range of times during which divergence could have
occurred.
RESULTS
The COI gene was highly polymorphic in both species. In
C. meadii, 35 variable sites defined 52 unique haplotypes
(Genbank accession numbers DQ105804 through DQ105855);
by contrast, 53 variable sites defined 74 haplotypes in
P. smintheus (DeChaine & Martin, 2004). For both species,
all polymorphisms occurred at synonymous nucleotide positions. The observed genetic variation illustrates the sensitivity
of this marker to population processes and its utility in
intraspecific phylogenetic analyses of insects.
Journal of Biogeography 32, 1943–1956, ª 2005 Blackwell Publishing Ltd
Historical biogeography of Rocky Mountain butterflies
sampled from a single locality (Table 1; Fig. 3), implying
isolation among sky islands (Slatkin, 1985). In addition, only a
few haplotypes were common among physiographic provinces
in P. smintheus and only one (CC16) in C. meadii (Figs 3 & 4).
Overall, these patterns of haplotype diversity imply geographic
isolation of populations in both species.
Similarly, the three-level analyses of molecular variance
(amova) revealed significant partitioning of genetic variation
at all spatial scales (Table 2). This result, combined with
significant genetic divergence based on pair-wise population
comparisons using FST and in plots of the normalized pair-wise
FST values [FST/(1 ) FST)] against the log of distance (C. meadii
r2 ¼ 0.05, P < 0.005; P. smintheus r2 ¼ 0.14, P < 0.001),
implies a history of restricted gene flow for both species.
However, the magnitudes and patterns of pair-wise population
genetic divergence were not similar between species (Mantel test,
P < 0.01), a result that reflects lack of significant correlation in
levels of within population genetic variation between species.
The percent of variation explained at each hierarchical level of
the amova analyses were nearly identical between species
(Table 2), suggesting that gene flow, and thus dispersal barriers,
are similar between the species. But, the regional pattern of
sequence diversity differed between C. meadii and P. smintheus.
In C. meadii, levels of variation, as measured by h, were greater in
the north whereas P. smintheus exhibited more variation in the
south than in the central and northern Rockies (Table 1). These
Population genetics
Estimates of within population genetic diversity varied widely
among sites within a species and were not correlated between
species. The average haplotype diversity (H) was significantly
greater in P. smintheus than in C. meadii (Wilcoxon sign rank
test, P ¼ 0.045), with estimates of H ranging from 0.00 to 0.89
and from 0.59 to 0.91 in C. meadii and P. smintheus, respectively
(Table 1). In contrast, estimates of h did not differ between the
species, C. meadii (h mean ¼ 0.00307) and P. smintheus
(h mean ¼ 0.00331), based on a paired t-test (h t ¼ 0.35,
P ¼ 0.73), but ranged widely in both species (Table 1). For both
species, estimates of h were highly variable among collecting
localities at similar latitudes and were not correlated with
latitude (for C. meadii h r2 ¼ 0.11, P ¼ 0.18; for P. smintheus
h r2 ¼ 0.08, P ¼ 0.24). Importantly, in a comparison of withinsite diversity, values of h were not correlated between the two
lepidopterans based on Spearman’s rank correlation test
(rs ¼ 153, P > 0.5). Tests of neutrality based on Tajima’s D
showed that nearly all populations in both species were stable,
but that in C. meadii, the Sundance Mountain population
(population 9) probably experienced a recent contraction.
The geographic distribution of haplotypes suggests little
gene flow among populations at local and regional scales.
Populations of both species harboured a relatively high and
variable frequency of private alleles, or haplotypes that were
Table 1 Sampling and distribution of genetic variation in Colias meadii Edwards and Parnassius smintheus Doubleday
n
Locality
C
h
H
P
C
1 Gunsight Pass
10 27 0.89
2 Triple Divide Pass, 22 21 0.65
3 Dawson Pass
17 13 0.70
4 Hyndman Pk
13 32 0.59
5 Mt. Washburn
20 27 0.89
6 Amethyst Mt.
26 20 0.88
7 Moose Pass
12 20 0.48
8 Static Pk
12 15 0.62
9 Sundance Mt.
19 13 0.45
10 Long’s Pk
17 35 0.84
11 Quandary Pk
19 10 0.84
12 Maroon Bells
20 10 0.70
13 Mt. Elbert
16 15 0.40
14 Mt. Shavano
25 21 0.72
15 American Basin
20 33 0.36
16 San Luis Pk
29 28 0.78
17 Humboldt Pk
12 13 0.00
18 Iron Nipple
19 10 0.74
Average
19 20 0.64
Among regions
Northern
50 65 0.77
Central
83 121 0.87
Southern
196 188 0.82
hp
hS
%p
P
C
P
C
P
C
P
0.67
0.85
0.85
0.80
0.80
0.75
0.91
0.59
0.81
0.88
0.69
0.73
0.83
0.83
0.88
0.75
0.73
0.80
0.79
0.0064
0.0020
0.0028
0.0011
0.0073
0.0052
0.0022
0.0027
0.0017
0.0039
0.0049
0.0022
0.0010
0.0025
0.0025
0.0026
0.0000
0.0043
0.0031
0.0009
0.0029
0.0045
0.0026
0.0030
0.0014
0.0063
0.0013
0.0033
0.0053
0.0005
0.0025
0.0024
0.0043
0.0045
0.0045
0.0044
0.0050
0.0033
3.76
4.43
4.44
0.95
6.02
4.91
4.36
4.95
1.09
4.85
4.40
1.12
1.60
3.66
1.62
3.75
0.00
4.39
3.35
1.91
2.28
2.63
1.72
1.79
1.85
2.67
1.18
2.17
3.54
0.91
1.67
1.85
2.08
3.77
2.70
2.98
3.12
2.28
4.10
2.47
3.25
0.97
4.79
3.41
2.98
3.31
2.29
3.55
3.72
1.81
1.21
2.12
2.82
2.29
0.00
3.15
2.68
1.81
1.95
2.66
1.78
1.81
1.41
2.27
0.92
2.00
3.08
0.71
1.77
1.54
2.50
2.96
2.54
2.65
2.73
2.06
C
60
9
17
38
40
39
0
8
5
0
16
18
25
12
10
66
0
42
22.5
0.79 0.0037 0.0028 4.52 2.24 3.27 2.14 60
0.90 0.0037 0.0029 5.43 2.24 2.96 1.70 100
0.96 0.0026 0.0036 4.67 4.46 2.30 2.28 85
P
Private alleles in C. meadii
4
24
24
48
7
30
53
7
16
32
0
40
33
71
27
24
8
27
26.4
CG6, CG7, CG8, CG10
CG4
CG5, CG9
CI1, CI2
CY4, CY8, CY9, CY13, CY16, CY17, CY18
CY3, CY7, CY10, CY11, CY12, CY19
n/a
CY5
n/a
CC22, CC28
CC4, CC13, CC14
CC26
CC10, CC30
CC20, CC29
CC11, CC12, CC19, CC21
n/a
CC18, CC23
48
55
84
Collection sites, numbers of individuals surveyed, haplotype diversity (H), genetic diversity (h), and percentage of private alleles (%p) for both species
are shown. The private alleles from each population of C. meadii are given, while those for P. smintheus were previously published (DeChaine &
Martin, 2004). Abbreviations are as follows: C ¼ C. meadii, P ¼ P. smintheus.
Journal of Biogeography 32, 1943–1956, ª 2005 Blackwell Publishing Ltd
1949
E. G. DeChaine and A. P. Martin
Species
Source
n
d.f.
SS
Variance
%
Colias meadii Edwards
Among Regions
Among Populations
Within Populations
Total
3
18
325
325
2
15
307
324
198.2
245.3
541.2
984.7
0.90
0.82
1.76
3.48
25.9
23.4
50.7
Parnassius smintheus
Doubleday
Among Regions
Among Populations
Within Populations
Total
3
18
374
374
2
15
356
373
185.1
200.8
424.4
810.3
0.67
0.60
1.19
2.47
27.3
24.4
48.3
Table 2 Tests of genetic subdivision using a
three level amova; among regions, among
populations within regions, and within populations
Regions were defined as the northern, central, and southern Rocky Mountain biogeographic
provinces following Brouillet & Whetstone (1993). Values for the sum of squares based on pairwise distances (SS), the variance components (variance), and the percentage of variation at each
hierarchical level (%) are shown.
analyses of differentiation indicate that genetic diversity is
structured in both species, but that similarities between species
depend on the geographic scale of the analyses.
Inferences from nested clade analyses
The intraspecific phylogenies revealed a pattern of genetic
divergence associated with known geographic provinces in the
Rocky Mountains (Fig. 4). We did not determine the ancestral
root, and thus geographic origin, for either species, but we were
able to make inferences of geographic transitions from the
phylogenies (Wares et al., 2001). Colias meadii exhibited a
geographically structured genealogy (Fig. 4a), including a
southern clade (3-1), a central clade (3-3), and a clade
harbouring haplotypes from all regions (3-7). Northern
haplotypes in C. meadii were derived from two or three
separate transitions (CG1, CG10, and CG3) from the central
and southern Rockies. A similar history is apparent in the
genealogy of P. smintheus (Fig. 4b), with a southern clade (4-1),
a central clade (4-2) with one transition to the south, and a
clade including haplotypes from all regions (4-3), with two
switches to the north. In general, deeper clades (i.e. clade levels
(b)
(a) Colias meadii
3-7
CG6
CG8
Parnassius smintheus
4-3
CG4
G6
CG1
G4
4-2
CG10
CG9
Y13
Y12
Y4
Y3
Y8
CY13
CC16
Y5
CY3
Y9
I2
CY4
CY11
CY1
CY19
CC11
CY7
CY14
Y16
Y17
CY16
Y10
Y7
Y11
R8
G1
CY17
CI2
CC18
Y6
R6
R7
Y14
R9
CY15
CY12
CY8
CY9
R11
G2
R4
CY18
CI1
3-1
R12
CY10
Y15
3-4
R5
R3
R1
R2
CC4
CC29
CC27
C4
CC13
C13
CC8
CC9
C9
C6
C11
CC2
CC30 CC22
CC20
C32
C18
C17
C2
C15 C16
C12
CC26
C10
C31
C24
C14
C8
CC10
C23
C1
C7
CC28
CC14
C3
C5
C25
C27
C19
C21
C26
C22
Haplotype location
North
Central
C33
C29 C28
4-1
CC23
CC19
C34
C30
R10
CC12 CC21
I4
I3
I1
CY5
CY2
CC17
G9
G8
Y1
CG3
3-3
CC15
G5
G7
G3
CG5
CG7
C20
Haplotype frequency
South
Shared
Unsampled
1
2-5
6-10
11-15
15-20
21-50
51+
Figure 4 TCS-inferred mtDNA genealogies of sampled haplotypes for (a) Colias meadii Edwards and (b) Parnassius smintheus Doubleday.
Haplotypes are shown as labelled circles, with the size of the circle indicating the relative frequency of each haplotype. Circle shading denotes
the geographic region from which the haplotype was sampled; pie charts designate the frequency of a haplotype within each region. Each line
connecting haplotypes represents a one-step mutational change between the haplotypes. Boxes delineate major NCA-clades referred to in the
text.
1950
Journal of Biogeography 32, 1943–1956, ª 2005 Blackwell Publishing Ltd
Historical biogeography of Rocky Mountain butterflies
cies: A ¼ 0.2984, C ¼ 0.1400, G ¼ 0.1433, T ¼ 0.4183; pinvar ¼ 0.8439; gamma shape parameter ¼ 0.9071; rA-C ¼ 1,
rA-G ¼ 3.3568, rA-T ¼ 0.3184, rC-G ¼ 0.3184, rC-T ¼
3.3568, rG-T ¼ 1). These models were used to generate
intraspecific phylogenies with and without enforcing a
molecular clock. Because the LRT failed to reject the clock in
both species (C. meadii LRT ¼ 63.08 df ¼ 50, P > 0.10;
P. smintheus LRT ¼ 79.2, df ¼ 73, P > 0.25), the rate of
2.3% substitutions per million years (Brower, 1994) was
applied to MDIV (Nielsen & Wakeley, 2001) estimates of h
(¼ 2Nel) to calculate Ne (C. meadii h ¼ 8.1, Ne ¼ 203,099;
P. smintheus h ¼ 11.1, Ne ¼ 305,836). Multiple data analyses
on MDIV (Nielsen & Wakeley, 2001) converged on similar
estimates for each parameter. The intraspecific genealogies and
estimates of Ne were incorporated into the testing of
phylogeographic hypotheses.
The single and 3-refugia hypotheses were tested with
coalescent simulations in MESQUITE 1.05 (Maddison &
Maddison, 2003). We computed S-values for C. meadii
(S ¼ 10) and P. smintheus (S ¼ 6) by constraining their
genealogies within the 3-refugia model. The null model of a
single ancestral population could be rejected for both species
for all time periods tested (P < 0.01). Not only did the two
alpine butterflies fit the 3-refugia model, but the range of
divergence times was nearly identical for both species. For the
3-refugia model, C. meadii, divergence times ranging from
100,000 to 400,000 yr bp (T2 P ¼ 0.25, T3 P ¼ 0.30, T4
P ¼ 0.10, T5 P ¼ 0.07) could not be rejected, but divergence
times at T1 (P ¼ 0.02), T6 (P ¼ 0.01), and T7 (P < 0.01) were
all rejected. Likewise, for P. smintheus, population divergence
times of 100,000 to 300,000 yr bp (T2 P ¼ 0.30, T3 P ¼ 0.22,
T4 P ¼ 0.07) could not be rejected for the 3-refugia model,
but more recent and later divergence times were rejected (T1
P < 0.01, T5 P ¼ 0.03, T6 P < 0.01, T7 P < 0.01). Thus, a
3-refugia model with population divergence occurring between
100,000 to 300,000 yr bp is strongly supported for both species
by the coalescent simulations.
4 or 5) included haplotypes from broad geographic distributions, while haplotypes in the more derived clades (lower
clade number) were geographically restricted. The genealogies
corroborate the amova findings of geographic structure.
A nested clade analysis (NCA) of the intraspecific genealogies revealed that the two species were affected similarly by
historic events (the Spearman’s r ¼ 0.93, P < 0.001). The
geographic distributions of the major clades illustrate the
cycles of expansion and fragmentation experienced by both
species (Fig. 5). NCA of C. meadii uncovered evidence for
eight clades that experienced fragmentation or restricted gene
flow and three clades that underwent contiguous range
expansion or long-distance colonization (Table 3; Fig. 5a).
Fewer clades were inferred to have undergone demographic
events in C. meadii than for P. smintheus, which experienced
11 fragmentations and seven expansions (Table 3; Fig. 5b), a
result that stems, in part, from the greater number of distinct
haplotypes in P. smintheus than in C. meadii. Note that for
both species haplotypes from northwestern Colorado cluster
with the central and northern clades as opposed to the
southern clades. Moreover, both species showed evidence for
recent and more ancient range expansions and a series of
fragmentation events and restricted gene flow across the three
lowest levels of the trees.
Tests of the phylogeographic hypotheses
In preparation for testing the phylogeographic hypotheses,
genealogies and population parameters were inferred for both
species. Results from the modeltest 3.6 (Posada & Crandall,
1998) analyses revealed that the best model of substitution
for C. meadii corresponded to a TrN + I + G model (AIC ¼
3199.3228; nucleotide frequencies: A ¼ 0.3121, C ¼ 0.1278,
G ¼ 0.1437, T ¼ 0.4164; pinvar ¼ 0.8526; gamma shape
parameter ¼ 0.2283; rA-C ¼ 1, rA-G ¼ 17.0302, rA-T ¼ 1,
rC-G ¼ 1, rC-T ¼ 9.4366, rG-T ¼ 1) and P. smintheus fit a
K81uf + I + G model (AIC ¼ 3423.8008; nucleotide frequen-
(a) Colias meadii
(b) Parnassius smintheus
MT
1
2
Figure 5 Geographic patterns of NCAinferences for (a) Colias meadii Edwards and
(b) Parnassius smintheus Doubleday. Ellipses
designate clades that experienced expansion
(solid lines, white interior) or fragmentation
(dashed lines, grey interior) as inferred
through NCA. The thickness of the ellipse
lines corresponds to clade depth with thicker
lines representing deeper clades. For simplicity, not all clades that exhibited significant
geographic structure are shown. A complete
list of all NCA-inferences is given in Table 3.
4
MT
1
2
3
3
5
7
8
6
WY
4
5
7
8
WY
6
ID
ID
9
10
11
12
12
Expansion
Journal of Biogeography 32, 1943–1956, ª 2005 Blackwell Publishing Ltd
15
16
CO
13
14
13
14
UT
9
10
11
CO
17
18
UT
15
16
17
18
Fragmentation
1951
E. G. DeChaine and A. P. Martin
Table 3 Inferences of historical processes in Colias meadii
Edwards and Parnassius smintheus Doubleday
Clade
Colias meadii
4-1
4-2
4-3
3-1
3-3
3-7
2-1
2-4
2-9
2-13
1-1
1-18
Parnassius smintheus
5-1, total
4-1
4-2
3-1
3-2
3-6
3-7
2-2
2-3
2-6
2-7
2-13
2-17
1-9
1-28
1-32
1-41
Inferred event
Contiguous range expansion
Long distance colonization
Contiguous range expansion
Restricted gene flow with isolation-by-distance
Restricted gene flow with isolation-by-distance
Past fragmentation
Restricted gene flow with isolation-by-distance
Contiguous range expansion
Restricted gene flow with isolation-by-distance
Past fragmentation
Restricted gene flow with isolation-by-distance
Restricted gene flow with isolation-by-distance
Past fragmentation
Contiguous range expansion
Long distance colonization
Restricted gene flow with isolation-by-distance
Past fragmentation
Contiguous range expansion
Restricted gene flow with isolation-by-distance
Restricted gene flow with isolation-by-distance
Restricted gene flow with isolation-by-distance
Past fragmentation
Past fragmentation
Past fragmentation
Contiguous range expansion
Long distance colonization
Restricted gene flow with isolation-by-distance
Past fragmentation
Long distance colonization
Summary
Parnassius
smintheus
Colias meadii
Clade level
E
F
E
F
Fifth
Fourth
Third
Second
First
0
2
0
1
0
0
0
3
3
2
0
3
1
1
2
1
0
3
5
2
DISCUSSION
Analysis of mitochondrial DNA sequences from eighteen sky
islands spanning about 12 of latitude in the Rocky Mountain
cordillera revealed an intriguing pattern of genetic divergence
for the co-distributed alpine butterflies, C. meadii and
P. smintheus. Populations of both species are geographically
structured at all spatial scales and both species probably
persisted across most of the latitudinal range throughout the
glacial cycles. At the scale of biogeographic regions, populations of both species are relatively isolated within north,
1952
central, and southern provinces, which implies a shared history
of restricted gene flow among the regions. Moreover, palaeoclimatic changes of the Quaternary likely influenced genetic
divergence in the two species in a similar way, through
repeated cycles of down-slope population expansion and
upslope contraction. But, across more limited geographic
scales and over shorter time periods, population parameters
are not correlated between the species. Overall, the demographic histories of these two alpine butterflies are marked by
broad-scale concordance and local-scale disparities.
Clear large-scale geographic patterns of genetic divergence
were shared by both species. For instance, C. meadii and
P. smintheus exhibited a strong genetic break across the
Wyoming Basin, a region of low elevation and dry habitat that
lies on the Continental Divide at approximately 42 N and
separates the southern from the central Rockies (Fig. 2a;
Brouillet & Whetstone, 1993). A similar pattern was evident
for other high elevation Lepidoptera (Britten & Brussard, 1992;
Nice & Shapiro, 2001) and Coleoptera (Noonan, 1992, 1999;
Reiss et al., 1999) suggesting that this region is a major
biogeographic boundary for alpine insects. But, the tighter
association between populations in northwestern Colorado
(numbers 9, 10, and 11) with northern populations (Figs 4 & 5)
as opposed to other southern populations suggests a secondary
colonization of the south from the central and/or northern
populations for both species. Although less distinct, a genetic
break was detected in both species between the most northern
collection sites from the previously glaciated area of Montana
and the central Rocky Mountains in Wyoming and Idaho. This
part of the Rocky Mountains is also marked by lower elevation
and reduced alpine habitat (Fig. 2a, elevation profile). Genetic
divergence across regions was most pronounced in C. meadii, in
which only one haplotype was found in more than one
geographic region (Fig. 3a; haplotype CC16). For the few
P. smintheus haplotypes that were widespread, frequencies
differed dramatically among the three regions. Moreover, the
amova revealed that about 26% of the genetic variation
sampled was distributed among regions in both species. This
distribution of haplotype diversity suggests that, within both
species, genetic divergence among regions is due to restricted
gene flow across low-elevation geographic barriers.
Demographic histories inferred for C. meadii and
P. smintheus were similar throughout the climate cycles of
the Quaternary. Both species showed evidence of multiple
cycles of population expansion and fragmentation over a
period defined by the 5-level nested cladograms. Moreover, the
cycles of population expansion and contraction were correlated between the species with respect to clade depth (level), even
though the number of demographic events was greater in
P. smintheus. These results suggest that both species may have
responded to climate cycles similarly.
Testing phylogeographic hypotheses through coalescent
simulations provided strong support for concordance between
the biogeographic histories of the two butterflies. Data from
both species were consistent with divergence among three
refugia occurring during the Pleistocene, from 100,000 to
Journal of Biogeography 32, 1943–1956, ª 2005 Blackwell Publishing Ltd
Historical biogeography of Rocky Mountain butterflies
400,000 yr bp, a period including three to four major glacial–
interglacial cycles (Winograd et al., 1997). Because gene
divergence times generally overestimate population divergence
times (Edwards & Beerli, 2000), the more ancient divergences
(T4 and T5) with low statistical support (P < 0.1) probably do
not accurately reflect the ages of population divergence, but do
provide a maximum confidence limit for the inferences.
Moreover, since high elevation populations are expected to
have diverged during interglacial periods when the alpine
tundra was fragmented and xeric, low elevation regions like the
Wyoming Basin were impassable, the populations of alpine
butterflies in the northern, central, and southern regional
refugia likely diverged during one of the more recent
interglacials at approximately 100,000 or 200,000 yr bp (T2
or T3). These findings, like those for alpine grasshoppers in the
Rocky Mountains (Knowles, 2001), suggest that the palaeoclimatic cycles of the Quaternary promoted divergence among
high elevation insects.
Despite evidence for shared history across large spatial scales
and over the last few hundred thousand years, there is little
evidence for a common demographic pattern when the
analyses were focused at the level of individual localities. For
instance, estimates of genetic diversity for C. meadii and
P. smintheus were not correlated. A similar pattern of
discordance between species was evident from the pair-wise
FST values. This independent biogeographic response of species
to climate cycles has been repeatedly demonstrated through
palynological records (West, 1980; Whitlock & Bartlein, 1997),
fossil insect assemblages (Coope, 1995; Elias, 1996) and
molecular phylogeographic studies (Taberlet et al., 1998;
Stewart & Lister, 2001; Kropf et al., 2003). For C. meadii and
P. smintheus, the lack of correlation detected from pair-wise
comparisons of the species is probably not due to stochastic
variance associated with the coalescent process (Edwards &
Beerli, 2000) because broad-scale genetic patterns correspond
to geographic barriers and indicate a common cause. Rather,
local extinction and re-colonization dynamics, which greatly
influence the magnitude of within-population genetic variation and the genetic divergence among populations (Slatkin,
1977; Pannell, 2003), may be responsible for the differences
observed between the species. Our findings corroborate
previous records showing that, at fine geographic scales, the
individual response of a species governs population size, spatial
structure, and genetic structure, and depends on the magnitude of climate change (Webb, 1987; Bennett, 1990; Davis &
Shaw, 2001).
Similarity of large-scale geographic patterns and inferences
of population expansions and fragmentation over the last
400,000 years suggests a general model for alpine and subalpine biogeography for the Rocky Mountains south of the
Cordilleran Ice sheet. The basis for this model was outlined
by Hewitt (1996): the hypothetical response of high elevation
taxa to the shifting environment associated with climate
cycles is to track alpine habitat by migrating up and down in
elevation, rather than dispersing over great distances. As with
Hewitt’s (1999, 2000) work, most phylogeographic studies of
alpine systems have been performed on European plants and
arthropods, where mountain ranges that run along an eastwest axis were mostly covered by ice during glacial periods.
This implies that in Europe, alpine species were forced to
persist in a few isolated refugia during glacial periods, as has
been shown for several taxa (Taberlet et al., 1998; Stehlik,
2000; Garnier et al., 2004; Schmitt & Hewitt, 2004). The
disjunct pattern of glacial refugia in Europe lies in stark
contrast to the hypothetical wide distribution of alpine
habitat in the Rocky Mountains during glacial periods
(Fig. 2b), and underscores the need for a phylogeographic
model that accounts for the prevalence of alpine habitat
throughout the Quaternary climate cycles along the northsouth spanning cordillera.
DeChaine & Martin (2004) hypothesized that populations of
alpine and sub-alpine organisms have existed on an expanding
and contracting archipelago of sky islands, along the Rocky
Mountain cordillera. The Rocky Mountains are one of the
longest terrestrial mountain ranges on the planet, and are
marked by topographic and climatological heterogeneity,
abrupt changes in elevation, resources, and a mosaic of alpine
habitat. For inhabitants of the Rocky Mountain alpine tundra,
we imagine a dynamic process, as did Hewitt (1996), in which
a species is subdivided into small, isolated populations
(contraction phase) punctuated by periods when populations
are large and span vast geographic ranges (expansion phase).
But, specific to the north-south running mountain ranges,
local habitat is available throughout the climate cycles,
obviating the need for long distance migration or glacial
refugia. Rather, it is during interglacials, like the current
conditions, that populations contracted and fragmented as
they moved up in elevation with the warming climate.
Throughout these contraction periods, populations were
isolated and underwent genetic divergence [as shown for
Melanoplus grasshoppers in the central and northern Rockies
(Knowles, 2000)], and many populations probably went
extinct. With the return of cool, wetter climates, the alpine
and sub-alpine habitats expanded and became connected, as
did populations of high elevation organisms. Throughout
expansion periods, gene flow was more extensive, and habitats
in which populations had gone extinct during the interglacials
were probably re-colonized. The current study and those of
DeChaine & Martin (2004, 2005) provide empirical evidence
for repeated cycles of population expansion and contraction
within mountain blocks along a vast latitudinal range of the
Rocky Mountains.
The distribution of genetic variation in C. meadii and
P. smintheus is undoubtedly due to a combination of historic
and current ecological factors. At broad geographic and
temporal scales, the two species exhibited concordant patterns
of genetic divergence, but at finer scales, demographic histories
were not correlated between the species. Inferences from our
study suggest that the general response of alpine taxa in the
Rocky Mountains to palaeoclimatic oscillations of the
Quaternary fits an expanding–contracting archipelago model.
According to this hypothesis, populations persisted across the
Journal of Biogeography 32, 1943–1956, ª 2005 Blackwell Publishing Ltd
1953
E. G. DeChaine and A. P. Martin
latitudinal range of the Rockies throughout the climate cycles
by expanding down-slope during glacial periods, and contracting upslope into a fragmented archipelago of sky islands
during warm, interglacials. While the palaeoclimatic cycles of
the Quaternary governed the general distribution of genetic
diversity in high elevation taxa, biological characteristics
peculiar to each species probably promoted different patterns
of genetic variation between the species on finer spatial and
temporal scales as biologically relevant environmental variables
changed independently; sometimes in concert, at other times
in opposition (Jackson & Overpeck, 2000). Further examination of data for other Rocky Mountain alpine taxa will help to
determine the generality of our findings and identify the
potential effects of future climate change on diversity at high
elevations.
ACKNOWLEDGEMENTS
Permission to collect butterflies was generously provided by
Glacier National Park (permit no. GLAC-2001-SCI-0020),
Yellowstone National Park (permit no. YELL-2001-SCI-0212),
Grand Teton National Park (permit no. GRTE-2001-SCI0009), and Rocky Mountain National Park (permit no.
ROMO-2001-SCI-0037). The work was funded by the National
Science Foundation, the University of Colorado, the Beverly
Sears Graduate Student Grants, the John W. Marr Ecology
Fund, the Indian Peaks Wilderness Association, CanonNational Parks Scholarships, the Edna Bailey Sussman Fellowship, the Colorado Mountain Club Academic Fellowship, and
the Southern Rockies Ecosystem Project. For help collecting
specimens, we thank Gerald DeChaine, Mathew Burt, and
Thomas Walla. We also thank Deane Bowers, William
Bowman, Yan Linhart, and Tom Veblen for valuable discussions and feedback.
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BIOSKETCHES
Eric DeChaine earned a doctorate for his research on the
comparative phylogeography of the Rocky Mountain alpine
tundra and is currently a postdoctoral fellow at Harvard
University. His work focuses on the historical biogeography
and diversification of species involved in co-evolutionary
associations.
Andrew Martin, a Professor of Ecology and Evolutionary
Biology at the University of Colorado, Boulder, is interested in
biological diversity and the underlying factors driving diversification across a wide range of taxa, from microbes to
mammals, butterflies to fishes.
Editor: Brett Riddle
Journal of Biogeography 32, 1943–1956, ª 2005 Blackwell Publishing Ltd