Marked genetic divergence among sky island populations of Sedum lanceolatum (Crassulaceae) in the Rocky Mountains

Climate change during the Quaternary played an important role in the differentiation and evolution of plants. A prevailing hypothesis is that alpine and arctic species survived glacial periods in refugia at the periphery of glaciers. Though the Rocky Mountains, south of the southernmost extent of continental ice, served as an important glacial refuge, little is known about how climate cycles influenced populations within this region. We inferred the phylogeography of Sedum lanceolatum (Crassulaceae) within the Rocky Mountain refugium to assess how this high-elevation plant responded to glacial cycles. We sequenced 884 base pairs (bp) of cpDNA intergenic spacers (tRNA-L to tRNA-F and tRNA-S to tRNA-G) for 333 individuals from 18 alpine populations. Our highly variable markers allowed us to infer that populations persisted across the latitudinal range throughout the climate cycles, exhibited significant genetic structure, and experienced cycles of range expansion and fragmentation. Genetic differentiation in S. lanceolatum was most likely a product of short-distance elevational migration in response to climate change, low seed dispersal, and vegetative reproduction. To the extent that Sedum is a good model system, paleoclimatic cycles were probably a major factor preserving genetic variation and promoting divergence in high-elevation flora of the Rocky Mountains.     

Alpine biogeography of Parnassian butterflies during Quaternary climate cycles in North America

Growth of alpine glaciers during the Pleistocene had profound effects on montane landscapes in North America and the organisms now inhabiting alpine ecosystems. Biogeography of this region has often been viewed as a system of sky islands despite the fact that species richness patterns deviate from a strict island biogeographic model. One explanation is that alpine species are not in equilibrium because of late Quaternary geographic range shifts. Genetic data can provide evidence of nonequilibrium dynamics and the distributional shifts that occur during glaciation events in alpine landscapes. Using mitochondrial and nuclear sequence data, we examine the evolutionary history of butterflies in the Parnassius phoebus complex. We test explicit, alternative models of the biogeographic history of Parnassius smintheus and Parnassius behrii , including an equilibrium island model, ancestral radiation and fragmentation, an expanding alpine archipelago and an alpine archipelago refuge model. Our results support the alpine archipelago refuge model, in which alpine butterflies undergo population contraction during glacial climates followed by population expansion during interglacial phases. While butterflies can disperse between distant mountain ranges during glacial periods, gene flow is rare. We find evidence of recent connectivity between California and Colorado, population expansion events following deglaciation ∼20 000 years B.P., and small population sizes during the last glacial period. An analysis of lineage splitting suggests that morphological differences in P. smintheus and P. behrii are the result of late Pleistocene divergence (∼48 000 years B.P.) with limited gene flow. Our results demonstrate that spatially complex and nonequilibrium population dynamics influence alpine diversity patterns.     

Pleistocene origin and population history of a neoendemic alpine butterfly

Alpine environments underwent dramatic transformation during glacial–interglacial cycles, with the consequence that geographical, ecological and demographic changes of alpine populations provided the opportunity for formation of neoendemic species. Several biogeographical models have been proposed to account for the unique history of alpine populations, with different expectations of genetic divergence and speciation. The expanding alpine archipelago model proposes that alpine populations expand spatially and demographically during glacial events, dispersing between mountain ranges. Under this model, alpine populations are unlikely to diverge in isolation due to substantial interpopulation gene flow. In contrast, the alpine archipelago refuge model proposes that gene flow during glacial phases is limited and populations expand demographically during interglacial phases, increasing genetic isolation and the likelihood of speciation. We assess these models by reconstructing the evolutionary history of Colias behrii, a morphologically and ecologically distinct alpine butterfly restricted to the California Sierra Nevada. C. behrii exhibits very low genetic diversity at mitochondrial and nuclear loci, limited population structure and evidence of population expansion. C. behrii and Rocky Mountain C. meadii share identical mitochondrial haplotypes, while in contrast, nuclear data indicate common ancestry between C. behrii and Cascades Range Colias pelidne. The conflict in gene genealogies may be a result of recent expansion in North American Colias, but an isolation with migration analysis indicates that genetic patterns in C. behrii might result from differential introgression following hybridization. Based on the timing of population expansion and gene flow between mountain ranges, the expanding alpine archipelago model is supported in C. behrii.     

Using coalescent simulations to test the impact of quaternary climate cycles on divergence in an alpine plant-insect association

The Quaternary climate cycles forced species to repeatedly migrate across a continually changing landscape. How these shifts in distribution impacted the evolution of unrelated but ecologically associated taxa has remained elusive due to the stochastic nature of the evolutionary process and variation in species-specific biological characteristics and environmental constraints. To account for the uncertainty in genealogical estimates, we adopted a coalescent approach for testing hypotheses of population divergence in coevolving taxa. We compared genealogies of a specialized herbivorous insect, Parnassius smintheus (Papilionidae), and its host plant, Sedum lanceolatum (Crassulaceae), from the alpine tundra of the Rocky Mountains to null distributions from coalescent simulations to test whether tightly associated taxa shared a common response to the paleoclimatic cycles. Explicit phylogeographic models were generated from geologic and biogeographic data and evaluated over a wide range of divergence times given calibrated mutation rates for both species. Our analyses suggest that the insect and its host plant responded similarly but independently to the climate cycles. By promoting habitat expansion and mixing among alpine populations, glacial periods repeatedly reset the distributions of genetic variation in each species and inhibited continual codivergence among pairs of interacting species.     

Phylogeography of the mountain chickadee (Poecile gambeli): diversification, introgression, and expansion in response to Quaternary climate change

Since the late 1990s, molecular techniques have fuelled debate about the role of Pleistocene glacial cycles in structuring contemporary avian diversity in North America. The debate is still heated; however, there is widespread agreement that the Pleistocene glacial cycles forced the repeated contraction, fragmentation, and expansion of the North American biota. These demographic processes should leave genetic 'footprints' in modern descendants, suggesting that detailed population genetic studies of contemporary species provide the key to elucidating the impact of the late Quaternary (late Pleistocene-Holocene). We present an analysis of mitochondrial DNA (mtDNA) variation in the mountain chickadee (Poecile gambeli) in an attempt to examine the genetic evidence of the impact of the late Quaternary glacial cycles. Phylogenetic analyses reveal two strongly supported clades of P. gambeli: an Eastern Clade (Rocky Mountains and Great Basin) and a Western Clade (Sierra Nevada and Cascades). Post-glacial introgression is apparent between these two clades in the Mono Lake region of Central California. Within the Eastern Clade there is evidence of isolation-by-distance in the Rocky Mountain populations, and of limited gene flow into and around the Great Basin. Coalescent analysis of genetic variation in the Western Clade indicates that northern (Sierra Nevada/Cascades) and southern (Transverse/Peninsular Ranges) populations have been isolated and evolving independently for nearly 60,000 years.     

Importance of genetic drift during Pleistocene divergence as revealed by analyses of genomic variation

Determining what factors affect the structuring of genetic variation is key to deciphering the relative roles of different evolutionary processes in species differentiation. Such information is especially critical to understanding how the frequent shifts and fragmentation of species distributions during the Pleistocene translates into species differences, and why the effect of such rapid climate change on patterns of species diversity varies among taxa. Studies of mitochondrial DNA (mtDNA) have detected significant population structure in many species, including those directly impacted by the glacial cycles. Yet, understanding the ultimate consequence of such structure, as it relates to how species divergence occurs, requires demonstration that such patterns are also shared with genomic patterns of differentiation. Here we present analyses of amplified fragment length polymorphisms (AFLPs) in the montane grasshopper Melanoplus oregonensis to assess the evolutionary significance of past demographic events and associated drift-induced divergence as inferred from mtDNA. As an inhabitant of the sky islands of the northern Rocky Mountains, this species was subject to repeated and frequent shifts in species distribution in response to the many glacial cycles. Nevertheless, significant genetic structuring of M. oregonensis is evident at two different geographic and temporal scales: recent divergence associated with the recolonization of the montane meadows in individual sky islands, as well as older divergence associated with displacements into regional glacial refugia. The genomic analyses indicate that drift-induced divergence, despite the lack of long-standing geographic barriers, has significantly contributed to species divergence during the Pleistocene. Moreover, the finding that divergence associated with past demographic events involves the repartitioning of ancestral variation without significant reductions of genomic diversity has intriguing implications - namely, the further amplification of drift-induced divergence by selection.     

Historical biogeography of two alpine butterflies in the Rocky Mountains: broad-scale concordance and local-scale discordance

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, θ), genetic divergence among populations (F_ST), 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–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.     

Palaeodistribution modelling and genetic evidence highlight differential post‐glacial range shifts of a rain forest conifer distributed across a latitudinal gradient

Aim We examine the range expansion/contraction dynamics during the last glacial cycle of the late‐successional tropical rain forest conifer Podocarpus elatus using a combination of modelling and molecular marker analyses. Specifically, we test whether distributional changes predicted by environmental niche modelling are in agreement with (1) the glacial maximum contractions inferred from the southern fossil record, and (2) population genetic‐based estimates of range disjunctions and demographic dynamics. In addition, we test whether northern and southern ranges are likely to have experienced similar expansion/contraction dynamics. Location Eastern Australian tropical and subtropical rain forests. Methods Environmental niche modelling was completed for three time periods during the last glacial cycle and was interpreted in light of the known palynology. We collected 109 samples from 32 populations across the entire range of P. elatus. Six microsatellite loci and Bayesian coalescence analysis were used to infer population expansion/contraction dynamics, and five sequenced loci (one plastid and four nuclear) were used to quantify genetic structure/diversity. Results Environmental niche modelling suggested that the northern and southern ranges of P. elatus experienced different expansion/contraction dynamics. In the northern range, the habitat suitable for P. elatus persisted in a small refugial area during the Last Glacial Maximum (LGM, 21 ka) and then expanded during the post‐glacial period. Conversely, in the south suitable habitat was widespread during the LGM but subsequently contracted. These differential dynamics were supported by Bayesian analyses of the population genetic data (northern dispersal) and are consistent with the greater genetic diversity in the south compared with the north. A contact zone between the two genetically divergent groups (corresponding to the Macleay Overlap Zone) was supported by environmental niche modelling and molecular analyses. Main conclusions The climatic fluctuations of the Quaternary have differentially impacted the northern and southern ranges of a broadly distributed rain forest tree in Australia. Recurrent contraction/expansion cycles contributed to the genetic distinction between northern and southern distributions of P. elatus. By combining molecular and environmental niche modelling evidence, this unique study undermines the general assumption that broadly distributed species respond in a uniform way to climate change.     

WHEN COLD IS BETTER: CLIMATE-DRIVEN ELEVATION SHIFTS YIELD COMPLEX PATTERNS OF DIVERSIFICATION AND DEMOGRAPHY IN AN ALPINE SPECIALIST (AMERICAN PIKA, OCHOTONA PRINCEPS)

The genetic consequences of climate-driven range fluctuation during the Pleistocene have been well studied for temperate species, but cold-adapted (e.g., alpine, arctic) species that may have responded uniquely to past climatic events have received less attention. In particular, we have no a priori expectation for long-term evolutionary consequences of elevation shifts into and out of sky islands by species adapted to alpine habitats. Here, we examined the influence of elevation shifts on genetic differentiation and historical demography in an alpine specialist, the American pika ( Ochotona princeps ). Pika populations are divided into five genetic lineages that evolved in association with separate mountain systems, rather than lineages that reflect individual sky islands. This suggests a role for glacial-period elevation shifts in promoting gene flow among high-elevation populations and maintaining regional cohesion of genetic lineages. We detected a signature of recent demographic decline in all lineages, consistent with the expectation that Holocene climate warming has driven range retraction in southern lineages, but unexpected for northern populations that presumably represent postglacial expansion. An ecological niche model of past and future pika distributions highlights the influence of climate on species range and indicates that the distribution of genetic diversity may change dramatically with continued climate warming.     

Geographical isolation versus dispersal: Relictual alpine grasshoppers support a model of interglacial diversification with limited hybridization

Alpine biotas are paradigmatic of the countervailing roles of geographical isolation and dispersal during diversification. In temperate regions, repeated distributional shifts driven by Pleistocene climatic oscillations produced both recurrent pulses of population fragmentation and opportunities for gene flow during range expansions. Here, we test whether a model of divergence in isolation vs. with gene flow is more likely in the diversification of flightless alpine grasshoppers of the genus Podisma from the Iberian Peninsula. The answer to this question can also provide key insights about the pace of evolution. Specifically, if the data fit a divergence in isolation model, this suggests rapid evolution of reproductive isolation. Genomic data confirm a Pleistocene origin of the species complex, and multiple analytical approaches revealed limited asymmetric historical hybridization between two taxa. Genomic-based demographic reconstructions, spatial patterns of genetic structure and range shifts inferred from palaeodistribution modelling suggest severe range contraction accompanied by declines in effective population sizes during interglacials (i.e., contemporary populations confined to sky islands are relicts) and expansions during the coldest stages of the Pleistocene in each taxon. Although limited hybridization during secondary contact leads to phylogenetic uncertainty if gene flow is not accommodated when estimating evolutionary relationships, all species exhibit strong genetic cohesiveness. Our study lends support to the notion that the accumulation of incipient differences during periods of isolation were sufficient to lead to lineage persistence, but also that the demographic changes, dispersal constraints and spatial distribution of the sky islands themselves mediated species diversification in temperate alpine biotas.     

Phylogeographic structure in long‐tailed voles (Rodentia: Arvicolinae) belies the complex Pleistocene history of isolation,divergence, and recolonization of Northwest North America's fauna

Quaternary climate fluctuations restructured biodiversity across North American high latitudes through repeated episodes of range contraction, population isolation and divergence, and subsequent expansion. Identifying how species responded to changing environmental conditions not only allows us to explore the mode and tempo of evolution in northern taxa, but also provides a basis for forecasting future biotic response across the highly variable topography of western North America. Using a multilocus approach under a Bayesian coalescent framework, we investigated the phylogeography of a wide‐ranging mammal, the long‐tailed vole, Microtus longicaudus. We focused on populations along the North Pacific Coast to refine our understanding of diversification by exploring the potentially compounding roles of multiple glacial refugia and more recent fragmentation of an extensive coastal archipelago. Through a combination of genetic data and species distribution models (SDMs), we found that historical climate variability influenced contemporary genetic structure, with multiple isolated locations of persistence (refugia) producing multiple divergent lineages (Beringian or northern, southeast Alaska or coastal, and southern or continental) during glacial advances. These vole lineages all occur along the North Pacific Coast where the confluence of numerous independent lineages in other species has produced overlapping zones of secondary contact, collectively a suture zone. Finally, we detected high levels of neoendemism due to complex island geography that developed in the last 10,000 years with the rising sea levels of the Holocene.     

Genetic consequences of interglacial isolation in a steppe bird

In response to climate changes that have occurred during Pleistocene glacial cycles, taxa associated to steppe vegetation might have followed a pattern of historical evolution in which isolation and fragmentation of populations occurred during the short interglacials and expansion events occurred during the long glacial periods, in contrast to the pattern described for temperate species. Here, we use molecular genetic data to evaluate this idea in a steppe bird with Palaearctic distribution, the little bustard (Tetrax tetrax). Overall, extremely low genetic diversity and differentiation was observed among eight little bustard populations distributed in Spain and France. Mismatch distribution analyses showed that most little bustard populations expanded during cooling periods previous to, and just after, the last interglacial period (127,000-111,000 years before present), when steppe habitats were widespread across Europe. Coalescent-based methods suggested that glacial expansions have resulted in substantial admixture in Western Europe due to the existence of different interglacial refugia. Our results are consistent with a model of evolution and genetic consequences of Pleistocene cycles with low between-population genetic differentiation as a result of short-term isolation periods during interglacials and long-term exchange during glacial periods.     

Molecular evidence for Pleistocene glacial cycles driving diversification of a North American desert spider, Agelenopsis aperta

The influence of historical climatic vs. geological changes on species diversification patterns was investigated in a widely distributed North American desert spider, Agelenopsis aperta (Araneae: Agelenidae), with particular reference to Pleistocene glacial cycles and earlier patterns of mountain building. Levels of sequence divergence obtained from the mitochondrial gene, cytochrome oxidase I, dated to the Pleistocene, eliminating Rocky Mountain orogeny as a cause of diversification, as orogeny ended 4 million years ago. The results of phylogenetic and network analyses showed the presence of three geographically defined clades, which were consistent with the presence of at least three glacial refugia: (i) east of the Rocky Mountains; (ii) between the Rocky Mountains and Sierra Nevadas; and (iii) west of the Sierra Nevadas. In addition, populations within the Rocky Mountains exhibited significantly lower genetic diversity than populations east of the Rocky Mountains and the haplotypes found within the Rockies were a subset of eastern haplotypes. These patterns suggest that a post-Pleistocene range expansion occurred out of an eastern glacial refugium into the Rocky Mountains. Examination of phylogeographical studies of other North American desert taxa indicated that mountain building explained diversification patterns more effectively for some taxa but Pleistocene climate change was more important for others, including A. aperta.     

Phylogeography of halophytes from European coastal and inland habitats

The repeated advance and retreat of glaciers during the Pleistocene ice ages have played a major role in shaping the present patterns of genetic variation within and among plant and animal populations of the temperate zone. In Europe, the geographic ranges of many species were confined to a few, mostly southern refugia during periods of full glaciation. Distribution ranges then reexpanded, and uninhabited northern areas were recolonized during the interglacials. These contraction–expansion cycles were repeated at least four times. Paleontological and molecular phylogeographic studies during the last decade have greatly increased our knowledge of refugial areas and postglacial recolonization patterns of European trees, shrubs and Alpine plants since the last glacial maximum about 20,000 years ago. Much less is known yet about non-Alpine herbaceous plants. In the present review, we summarize recent phylogeographic work on halophytic (salt-adapted) plants from coastal and inland habitats in Europe. Major refugial areas for these plants have been identified along the Mediterranean coasts, but some species could also have survived in saline inland localities. In general, recolonization of N and NW Europe occurred in a stepwise fashion along the Atlantic coastline. For a number of species, molecular studies revealed concordant genetic discontinuities on the background of an essentially continuous geographic distribution. Such congruency could be explained by the preferential seed dispersal through sea currents. However, phylogeographic patterns of halophytes also proved to be influenced by other factors like sea-level fluctuations during the Pleistocene, secondary contact between divergent lineages, long-distance dispersal, clonal growth, and special habitat and temperature requirements.     

Late‐glacial recolonization and phylogeography of European red deer (Cervus elaphus L.)

The Pleistocene was an epoch of extreme climatic and environmental changes. How individual species responded to the repeated cycles of warm and cold stages is a major topic of debate. For the European fauna and flora, an expansion–contraction model has been suggested, whereby temperate species were restricted to southern refugia during glacial times and expanded northwards during interglacials, including the present interglacial (Holocene). Here, we test this model on the red deer (Cervus elaphus) a large and highly mobile herbivore, using both modern and ancient mitochondrial DNA from the entire European range of the species over the last c. 40 000 years. Our results indicate that this species was sensitive to the effects of climate change. Prior to the Last Glacial Maximum (LGM) haplogroups restricted today to South‐East Europe and Western Asia reached as far west as the UK. During the LGM, red deer was mainly restricted to southern refugia, in Iberia, the Balkans and possibly in Italy and South‐Western Asia. At the end of the LGM, red deer expanded from the Iberian refugium, to Central and Northern Europe, including the UK, Belgium, Scandinavia, Germany, Poland and Belarus. Ancient DNA data cannot rule out refugial survival of red deer in North‐West Europe through the LGM. Had such deer survived, though, they were replaced by deer migrating from Iberia at the end of the glacial. The Balkans served as a separate LGM refugium and were probably connected to Western Asia with genetic exchange between the two areas.     

Phylogeography of spruce beetles (Dendroctonus rufipennis Kirby) (Curculionidae: Scolytinae) in North America

Tree-feeding insects that are widespread in north temperate regions are excellent models for studying how past glaciations have impacted differentiation and speciation. We used mitochondrial DNA (mtDNA) sequences and allele frequencies at nine microsatellite loci to examine genetic population structure across the current range of the spruce beetle (Dendroctonus rufipennis), an economically important insect in North America. Two major haplotype groups occur across northern North America, from Newfoundland to Alaska, on white spruce (Picea glauca), and a third distinctive haplotype group occurs throughout the Rocky Mountains on Engelmann spruce (Picea engelmannii). The two mtDNA lineages found in northern populations are 3-4% divergent from each other and from the lineages found in the Rocky Mountains. Analyses of microsatellite data also suggest the existence of major population groupings associated with different geographical regions. In the Pacific Northwest, concordant contact zones for genetically distinct populations of spruce beetles and their principal hosts appear to reflect recent secondary contact. Although we could detect no evidence of historical mtDNA gene flow between allopatric population groups, patterns of variation in the Pacific Northwest suggest recent hybridization and introgression. Together with the pollen record for spruce, they also suggest that beetles have spread from at least three glacial refugia. A minimum estimate of divergence time between the Rocky Mountain and northern populations was 1.7 Myr (million years), presumably reflecting the combined effects of isolation during multiple glacial cycles.     

Environmental drivers of subalpine and alpine fen vegetation in the Southern Rocky Mountains,Colorado, USA

Fens are widely distributed wetlands worldwide and provide vital habitat for plant and animal species in mountainous regions. Alpine fens are rare in the Rocky Mountains and concentrated in the San Juan Mountains where broad regions at high elevation have relatively level topography and suitable climate to favor peat accumulation. Studies of montane and boreal peatlands have identified water chemistry as a main driver of vegetation composition. This study investigated whether similar drivers of vegetation composition are important for alpine and subalpine fens in the San Juan Mountains of Colorado, USA. Water chemistry variables were most important in structuring subalpine and alpine fen vegetation. However, these variables explained considerably less variation in alpine than subalpine fen vegetation. In addition, lower variance of water chemistry in alpine fens did not lead to lower beta diversity of vegetation in alpine than in subalpine fens. Although alpine and subalpine fen vegetation supports similar beta diversity, key differences occur in the environmental drivers of their vegetation composition.     

Genotyping‐by‐sequencing and ecological niche modeling illuminate phylogeography,admixture, and Pleistocene range dynamics in quaking aspen (Populus tremuloides)

Populus tremuloides is the widest‐ranging tree species in North America and an ecologically important component of mesic forest ecosystems displaced by the Pleistocene glaciations. Using phylogeographic analyses of genome‐wide SNPs (34,796 SNPs, 183 individuals) and ecological niche modeling, we inferred population structure, ploidy levels, admixture, and Pleistocene range dynamics of P. tremuloides, and tested several historical biogeographical hypotheses. We found three genetic lineages located mainly in coastal–Cascades (cluster 1), east‐slope Cascades–Sierra Nevadas–Northern Rockies (cluster 2), and U.S. Rocky Mountains through southern Canadian (cluster 3) regions of the P. tremuloides range, with tree graph relationships of the form ((cluster 1, cluster 2), cluster 3). Populations consisted mainly of diploids (86%) but also small numbers of triploids (12%) and tetraploids (1%), and ploidy did not adversely affect our genetic inferences. The main vector of admixture was from cluster 3 into cluster 2, with the admixture zone trending northwest through the Rocky Mountains along a recognized phenotypic cline (Utah to Idaho). Clusters 1 and 2 provided strong support for the “stable‐edge hypothesis” that unglaciated southwestern populations persisted in situ since the last glaciation. By contrast, despite a lack of clinal genetic variation, cluster 3 exhibited “trailing‐edge” dynamics from niche suitability predictions signifying complete northward postglacial expansion. Results were also consistent with the “inland dispersal hypothesis” predicting postglacial assembly of Pacific Northwestern forest ecosystems, but rejected the hypothesis that Pacific‐coastal populations were colonized during outburst flooding from glacial Lake Missoula. Overall, congruent patterns between our phylogeographic and ecological niche modeling results and fossil pollen data demonstrate complex mixtures of stable‐edge, refugial locations, and postglacial expansion within P. tremuloides. These findings confirm and refine previous genetic studies, while strongly supporting a distinct Pacific‐coastal genetic lineage of quaking aspen.     

Distribution and population structure of the anther smut Microbotryum silenes‐acaulis parasitizing an arctic–alpine plant

Cold‐adapted organisms with current arctic–alpine distributions have persisted during the last glaciation in multiple ice‐free refugia, leaving footprints in their population structure that contrast with temperate plants and animals. However, pathogens that live within hosts having arctic–alpine distributions have been little studied. Here, we therefore investigated the geographical range and population structure of a fungus parasitizing an arctic–alpine plant. A total of 1437 herbarium specimens of the plant Silene acaulis were examined, and the anther smut pathogen Microbotryum silenes‐acaulis was present throughout the host's geographical range. There was significantly greater incidence of anther smut disease in more northern latitudes and where the host locations were less dense, indicating a major influence of environmental factors and/or host demographic structure on the pathogen distribution. Genetic analyses with seven microsatellite markers on recent collections of 195 M. silenes‐acaulis individuals revealed three main genetic clusters, in North America, northern Europe and southern Europe, likely corresponding to differentiation in distinct refugia during the last glaciation. The lower genetic diversity in northern Europe indicates postglacial recolonization northwards from southern refugia. This study combining herbarium surveys and population genetics thus uniquely reveals the effects of climate and environmental factors on a plant pathogen species with an arctic–alpine distribution.     

The impact of Pleistocene climate change on an ancient arctic-alpine plant: multiple lineages of disparate history in Oxyria digyna

The ranges of arctic-alpine species have shifted extensively with Pleistocene climate changes and glaciations. Using sequence data from the trnH-psbA and trnT-trnL chloroplast DNA spacer regions, we investigated the phylogeography of the widespread, ancient (>3 million years) arctic-alpine plant Oxyria digyna (Polygonaceae). We identified 45 haplotypes and six highly divergent major lineages; estimated ages of these lineages (time to most recent common ancestor, T(MRCA)) ranged from ～0.5 to 2.5 million years. One lineage is widespread in the arctic, a second is restricted to the southern Rocky Mountains of the western United States, and a third was found only in the Himalayan and Altai regions of Asia. Three other lineages are widespread in western North America, where they overlap extensively. The high genetic diversity and the presence of divergent major cpDNA lineages within Oxyria digyna reflect its age and suggest that it was widespread during much of its history. The distributions of individual lineages indicate repeated spread of Oxyria digyna through North America over multiple glacial cycles. During the Last Glacial Maximum it persisted in multiple refugia in western North America, including Beringia, south of the continental ice, and within the northern limits of the Cordilleran ice sheet. Our data contribute to a growing body of evidence that arctic-alpine species have migrated from different source regions over multiple glacial cycles and that cryptic refugia contributed to persistence through the Last Glacial Maximum.