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Historical Biogeography of Two Alpine Butterflies in the Rocky Mountains

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Historical Biogeography of Two Alpine Butterflies in the Rocky Mountains Journal of Biogeography (J. Biogeogr.) (2005) 32, 1943–1956 ORIGINAL Historical biogeography of two alpine ARTICLE butterflies in the Rocky Mountains: broad-scale concordance and local-scale discordance Eric G. DeChaine1* and Andrew P. Martin2 1Department of Organismic and Evolutionary ABSTRACT Biology, Harvard University, Cambridge, MA, Aim We inferred the phylogeography of the alpine butterfly Colias meadii USA and 2Department of Ecology and Evolutionary Biology, University of Colorado, Edwards (Pieridae) and compared its genetic structure with that of another Boulder, CO, USA 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. 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– *Correspondence: Eric G. DeChaine, contracting archipelago model, suggesting that populations persisted across the Department of Organismic and Evolutionary geographic range throughout the climate cycles, experiencing isolation on ‘sky Biology, Harvard University, 16 Divinity Ave, Biolabs 4081, Cambridge, MA 02138, USA. islands’ during interglacial periods and becoming connected as they migrated E-mail: [email protected] 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 phylogeog- raphy, U.S.A. conditions across the shifting landscape (e.g. West, 1980; INTRODUCTION Coope, 1995; Johansen & Latta, 2003). During unfavourable Quaternary climate oscillations played a central role in periods, species’ distributions contracted and populations were determining the distribution of species and defining the forced to persist in a few fragmented refugia, comprising only a context for evolution (Huntley & Webb, 1989; Webb & fraction of the species’ previous range (e.g. Betancourt et al., Bartlein, 1992; Hewitt, 1996, 2000). Alternation between colder 1990). This oscillation of climatic conditions over the course of glacial periods and warmer interglacial periods (Fig. 1a) has thousands of years has promoted the cyclic expansion and created a temporal and geographic mosaic of continental ice contraction of species ranges in evolutionary time (Avise, 2000; sheets, mountain glaciers, and available habitat (Richmond, Hewitt, 2000). 1965; Winograd et al., 1997). In response to palaeoclimatic Periods of favourable climate that spurred range expansion fluctuations, species’ geographic and elevation ranges have differed among taxa depending on a species’ niche require- tracked preferred habitat and suitable environmental ments. For temperate taxa inhabiting low- to mid-elevation (a) Palaeoclimatic record (b) Populations 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 T3 250 300 (c) Biogeographic regions T4 North Central South 350 T1 400 T5 Time (1000 years bp) Time 450 (d) 500 T6 550 T6 600 -3 -2 -1 0 1 2 3 4 δ18 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 (400,000 yr bp) and establishes a baseline for predicting the interglacial, than during previous glacial periods when species effects of future climate change. were restricted to a few, distant refugia of suitable habitat (Webb & Bartlein, 1992; Comes & Kadereit, 1998; Ayoub & MATERIALS AND METHODS Riechert, 2004; Dobes et al., 2004). By contrast, glacial periods probably connected the alpine tundra and permitted broader Mead’s Sulphur, Colias meadii, inhabits alpine tundra and distributions of high elevation species, while warm interglacials subalpine steppe of the Rocky Mountains from southern caused the fragmentation of habitat and upslope contraction of Colorado, where the effects of interglacial habitat fragmenta- species’ ranges into ‘sky islands’ (Elias, 1996; Hewitt, 2000). tion are most severe, to northern Montana (Fig. 2a; Scott, Because species responded individually to historic climate 1986; Nabokov, 2000), which was completely covered by the changes, the detection of general phylogeographic patterns has Cordilleran and Laurentide ice sheets (Richmond, 1965). proven difficult, even within a habitat-type (Delcourt & Colias meadii is not known from the Rockies of mid-Montana, Delcourt, 1991; FAUNMAP Working Group et al., 1996; nor in the Wyoming Basin (Ferris & Brown, 1981; Opler et al., Comes & Kadereit, 1998; Taberlet et al., 1998). 1995), which, due to its low elevation and xeric habitat, acts as Alpine species could have persisted across an extensive a significant barrier to dispersal of some high elevation insects latitudinal range of the Rocky Mountain cordillera throughout (Noonan, 2001; DeChaine & Martin, 2004). P. smintheus, the several glacial–interglacial climate cycles by shifting elevation. Rocky Mountain Apollo, shares the range of C. meadii, but is The alpine habitat in the Rocky Mountains is highly dissected more broadly distributed (Scott, 1986). Both species of and widely-dispersed, comprising an archipelago of high Lepidoptera are strong flyers, but exhibit short-distance elevation sky islands (Ku¨chler, 1985; Fig. 2a). Many popula- dispersal as revealed through population analyses using genetic tions of alpine arthropods and plants are isolated on mountain markers (Johnson, 1977; Watt et al., 1996; Keyghobadi et al., tops in the current interglacial and probably exhibit different 1999; DeChaine & Martin, 2004). demographic characteristics (Golden & Bain, 2000; Knowles, 2000, 2001; Masta, 2000; DeChaine & Martin, 2004, 2005). In Specimen collection contrast, the Rocky Mountain alpine zone was relatively contiguous during glacial periods, except for a major break Specimens of C. meadii and P. smintheus were collected from associated with the Wyoming Basin (Pewe, 1983; Elias, 1996; eighteen sites throughout their range (Fig. 3a). The number Fig. 2b). Interconnection during the glacial periods could have of sampling locations within a region (north, south, and facilitated genetic and demographic cohesion
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