The genetic pattern of population threat and loss: a case study of butterflies

Recent decreases in biodiversity in Europe are commonly thought to be due to land use and climate change. However, the genetic diversity of populations is also seen as one essential factor for their fitness. Genetic diversity in species across the continent of Europe has been recognized as being in part a consequence of ice age isolation in southern refugia and postglacial colonization northwards, and these phylogeographical patterns may themselves affect the adaptability of populations. Recent work on butterfly species with different refugia, colonization paths and genetic structures allows this idea to be examined. The 'chalk-hill blue' pattern is one of decreasing genetic diversity from south to north, whereas the 'woodland ringlet' pattern shows greater genetic diversity in eastern than in western lineages. Comparison of population demographic trends in species with these biogeographical patterns reveals higher rates of decrease with lower genetic diversity. This indicates reduced adaptability due to genetic impoverishment as a result of glacial and postglacial range changes. Analysis of phylogeographical pattern may be a useful guide to interpreting demographic trends and in conservation planning.     

Genetic consequences of Pleistocene glaciations for the tundra vole (Microtus oeconomus) in Beringia

Repeated glacial events during the Pleistocene fragmented and displaced populations throughout the northern continents. Different models of the effects of these climate-driven events predict distinct phylogeographic and population genetic outcomes for high-latitude faunas. The role of glaciations in (i) promoting intraspecific genetic differentiation and (ii) influencing genetic diversity was tested within a phylogeographic framework using the rodent Microtus oeconomus. The spatial focus for the study was Beringia, which spans eastern Siberia and northwestern North America, and was a continental crossroads and potential high arctic refugium during glaciations. Variation in mitochondrial DNA (cytochrome b and control region; 214 individuals) and nuclear DNA (ALDH1 intron; 63 individuals) was investigated across the Beringian region. Close genetic relationships among populations on either side of the Bering Strait are consistent with a history of periodic land connections between North America and Asia. A genetic discontinuity observed in western Beringia between members of a Central Asian clade and a Beringian clade is geographically congruent with glacial advances and with phylogeographic discontinuities identified in other organisms. Divergent island populations in southern Alaska were probably initially isolated by glacial vicariance, but subsequent differentiation has resulted from insularity. Tests of the genetic effects of postglacial colonization were largely consistent with expansion accompanied by founder effect bottlenecking, which yields reduced diversity in populations from recently deglaciated areas. Evidence that populations in the Beringian clade share a history of expansion from a low-diversity ancestral population suggests that Beringia was colonized by a small founder population from central Asia, which subsequently expanded in isolation.     

Molecular Markers Reveal Limited Population Genetic Structure in a North American Corvid,Clark’s Nutcracker (Nucifraga columbiana)

The genetic impact of barriers and Pleistocene glaciations on high latitude resident species has not been widely investigated. The Clark’s nutcracker is an endemic North American corvid closely associated with Pinus-dominated forests. The nutcracker’s encompasses known barriers to dispersal for other species, and glaciated and unglaciated areas. Clark’s nutcrackers also irruptively disperse long distances in search of pine seed crops, creating the potential for gene flow among populations. Using the highly variable mitochondrial DNA control region, seven microsatellite loci, and species distribution modeling, we examined the effects of glaciations and dispersal barriers on population genetic patterns and population structure of nutcrackers. We sequenced 900 bp of mitochondrial control region for 169 individuals from 15 populations and analysed seven polymorphic microsatellite loci for 13 populations across the Clark’s nutcracker range. We used species distribution modeling and a range of phylogeographic analyses to examine evolutionary history. Clark’s nutcracker populations are not highly differentiated throughout their range, suggesting high levels of gene flow among populations, though we did find some evidence of isolation by distance and peripheral isolation. Our analyses suggested expansion from a single refugium after the last glacial maximum, but patterns of genetic diversity and paleodistribution modeling of suitable habitat were inconclusive as to the location of this refugium. Potential barriers to dispersal (e.g. mountain ranges) do not appear to restrict gene flow in Clark’s nutcracker, and postglacial expansion likely occurred quickly from a single refugium located south of the ice sheets.     

GENETIC CONSEQUENCES OF PASSIVE DISPERSAL IN POND-DWELLING COPEPODS

Pond-dwelling copepods have colonized habitats throughout North America after glaciers have receded. Most species are passively transported via resting eggs into new habitats. Colonists originating in a glacial refugium could lose some of the ancestral genetic diversity when they establish new populations and the attenuation may be substantial in populations far removed from the refugium due to multiple founder events. Genetic variation was measured in Heterocope septentrionalis from 27 populations at arctic sites near potential refugia and those more recently deglaciated to determine the effects of postglacial dispersal on patterns of genetic relatedness and diversity. Some populations were more distant, genetically, from others within the same site than those from other more distant sites. Eleven polymorphic enzyme loci were significantly more variable (F [1,294 df] = 5.94, P < 0.025) among individuals from populations near the Alaskan refuge than those at the eastern limit of their distribution. Because populations are typically extremely large and stable this loss of genetic diversity is attributed primarily to repeated founder events during colonization. This result suggests profound genetic changes may occur on a continental scale in passively dispersed copepods due to founder events alone. Their potential for divergence and speciation is greater than currently recognized.     

Genetic discontinuity, breeding-system change and population history of Arabis alpina in the Italian Peninsula and adjacent Alps

Arabis alpina is a widespread plant of European arctic and alpine environments and belongs to the same family as Arabidopsis thaliana. It grows in all major mountain ranges within the Italian glacial refugia and populations were sampled over a 1300 km transect from Sicily to the Alps. Diversity was studied in nuclear and chloroplast genome markers, combining phylogeographical and population genetic approaches. Alpine populations had significantly lower levels of nuclear genetic variation compared to those in the Italian Peninsula, and this is associated with a pronounced change in within-population inbreeding. Alpine populations were significantly inbred (F(IS) = 0.553), possibly reflecting a change to the self-incompatibility system during leading edge colonization. The Italian Peninsula populations were approaching Hardy-Weinberg equilibrium (outbreeding, F(IS) = 0.076) and genetic variation was highly structured, consistent with independent local 'refugia within refugia' and the fragmentation of an established population by Quaternary climate oscillations. There is very little evidence of genetic exchange between the Alps and the Italian Peninsula main distribution ranges. The Alps functioned as a glacial sink for A. alpina, while the Italian Peninsula remains a distinct and separate long-term refugium. Comparative analysis indicated that inbreeding populations probably recolonized the Alps twice: (i) during a recent postglacial colonization of the western Alps from a Maritime Alps refugium; and (ii) separately into the central Alps from a source outside the sampling range. The pronounced geographical structure and inbreeding discontinuities are significant for the future development of A. alpina as a model species.     

Phylogeography of lemmings (Lemmus): no evidence for postglacial colonization of Arctic from the Beringian refugium

Beringia is considered as an important glacial refugium that served as the main source for colonization of formerly glaciated Arctic regions. To obtain high resolution views of Arctic refugial history, we examined mitochondrial cytochrome b phylogeography in the northern genus of rodents, Lemmus (true lemmings), sampled across its circumpolar distribution. Strong phylogeographical structure suggests vicariant separation over several glacial-interglacial periods and does not provide evidence supporting the importance of Beringia for extensive colonization of formerly glaciated regions. Rather than a source of postglacial colonization, Beringia represents an area of intraspecific endemism previously undetected by biogeographical analysis. Existing phylogeographical structure suggests that vicariant separation by glacial barriers was an important factor generating genetic divergence and, thus, increasing genetic diversity in lemmings on continental and circumpolar scales. However, there is little evidence for the direct effect of the last glaciation on the level of genetic variation and allele genealogy in lemmings on a regional geographical scale. This finding implies that the population genetic models of postglacial colonization suggested for temperate taxa might have limited applicability for Arctic species.     

Dynamics in the evolution of sexual traits: losses and gains,radiation and convergence in yellow wagtails (Motacilla flava)

We analyse patterns of genetic diversity and song complexity in the Palaearctic yellow wagtail (Motacilla flava), a highly polytypic species complex. Mitochondrial and nuclear DNA show that the complex is polyphyletic, despite parallel plumage variation in western and eastern clades. In the western clade there is genetic structure among southern subspecies, haplotype diversity decreases with latitude, and northern subspecies show evidence of bottlenecking and rapid expansions, as expected from isolation in glacial refugia followed by postglacial colonization. However, northern subspecies, which have more divergent male plumages, lack genetic structure and sing simpler songs. Loss of song complexity and evolution of plumage in founder populations are consistent with the Kaneshiro model, which posits that variation among species is a consequence of founder-induced shifts in female preference leading to loss of ancestral male sexual traits. Our results suggest possible postglacial founder-effect mechanisms for the morhological diversification of the yellow wagtail complex.     

Unique mitochondrial DNA lineages in Irish stickleback populations: cryptic refugium or rapid recolonization?

Repeated recolonization of freshwater environments following Pleistocene glaciations has played a major role in the evolution and adaptation of anadromous taxa. Located at the western fringe of Europe, Ireland and Britain were likely recolonized rapidly by anadromous fishes from the North Atlantic following the last glacial maximum (LGM). While the presence of unique mitochondrial haplotypes in Ireland suggests that a cryptic northern refugium may have played a role in recolonization, no explicit test of this hypothesis has been conducted. The three‐spined stickleback is native and ubiquitous to aquatic ecosystems throughout Ireland, making it an excellent model species with which to examine the biogeographical history of anadromous fishes in the region. We used mitochondrial and microsatellite markers to examine the presence of divergent evolutionary lineages and to assess broad‐scale patterns of geographical clustering among postglacially isolated populations. Our results confirm that Ireland is a region of secondary contact for divergent mitochondrial lineages and that endemic haplotypes occur in populations in Central and Southern Ireland. To test whether a putative Irish lineage arose from a cryptic Irish refugium, we used approximate Bayesian computation (ABC). However, we found no support for this hypothesis. Instead, the Irish lineage likely diverged from the European lineage as a result of postglacial isolation of freshwater populations by rising sea levels. These findings emphasize the need to rigorously test biogeographical hypothesis and contribute further evidence that postglacial processes may have shaped genetic diversity in temperate fauna.     

Genetic consequences of glacial survival and postglacial colonization in Norway spruce: combined analysis of mitochondrial DNA and fossil pollen

Norway spruce (Picea abies [L.] Karst.) is a broadly distributed European conifer tree whose history has been intensively studied by means of fossil records to infer the location of full‐glacial refugia and the main routes of postglacial colonization. Here we use recently compiled fossil pollen data as a template to examine how past demographic events have influenced the species’ modern genetic diversity. Variation was assessed in the mitochondrial nad1 gene containing two minisatellite regions. Among the 369 populations (4876 trees) assayed, 28 mitochondrial variants were identified. The patterns of population subdivision superimposed on interpolated fossil pollen distributions indicate that survival in separate refugia and postglacial colonization has led to significant structuring of genetic variation in the southern range of the species. The populations in the northern range, on the other hand, showed a shallow genetic structure consistent with the fossil pollen data, suggesting that the vast northern range was colonized from a single refugium. Although the genetic diversity decreased away from the putative refugia, there were large differences between different colonization routes. In the Alps, the diversity decreased over short distances, probably as a result of population bottlenecks caused by the presence of competing tree species. In northern Europe, the diversity was maintained across large areas, corroborating fossil pollen data in suggesting that colonization took place at high population densities. The genetic diversity increased north of the Carpathians, probably as a result of admixture of expanding populations from two separate refugia.     

Phylogeographic structure and postglacial evolutionary history of water voles (Arvicola terrestris) in the United Kingdom

The phylogeographic pattern of mitochondrial DNA variation in water voles (Arvicola terrestris) from 57 localities across the United Kingdom and representative samples from Spain, France, Switzerland and Finland was determined from sequence variation in the central portion of the control region. Twenty-seven different haplotypes were resolved which formed two distinct phylogenetic clades. This major division separated haplotypes found in Scotland from those found in England and Wales. Nested clade analysis of haplotypes indicated that such a division was a consequence of allopatric fragmentation. The haplotypes found in Switzerland, France and Spain clustered with Scottish haplotypes, whereas the haplotype from Finland clustered with the English/Welsh haplotypes. These patterns indicate that contemporary Scottish populations are derived from an Iberian glacial refugium, whereas English and Welsh populations are derived from an eastern European refugium. As such, the postglacial recolonization of the United Kingdom must have involved two colonization events, either in different localities with no subsequent contact, or as two waves separated over time, with the second wave of colonizers displacing the first. An analysis of molecular variance (AMOVA) identified significant population genetic divergence within both the major clades, indicative of restricted gene flow and regional population isolation. The implications of both phylogeographical and population genetic structure are discussed in context with the conservation of water voles in Britain.     

Mitochondrial DNA variation in Pleistocene and modern Atlantic salmon from the Iberian glacial refugium

Current understanding of the postglacial colonization of Nearctic and Palearctic species relies heavily on inferences drawn from the phylogeographic analysis of contemporary generic variants. Modern postglacial populations are supposed to be representative of their Pleistocene ancestors, and their current distribution is assumed to reflect the different colonization success and dispersal patterns of refugial lineages. Yet, testing of phylogeographic models against ancestral genomes from glacial refugia has rarely been possible. Here we compare ND1 mitochondrial DNA variation in late Pleistocene (16,000-40,000 years before present), historical and contemporary Atlantic salmon (Salmo salar) populations from northern Spain and other regions of western Europe. Our study demonstrates the presence of Atlantic salmon in the Iberian glacial refugium during the last 40,000 years and points to the Iberian Peninsula as the likely source of the most common haplotype within the Atlantic lineage in Europe. However, our findings also suggest that there may have been significant changes in the genetic structure of the Iberian refugial stock since the last ice age, and question whether modern populations in refugial areas are representative of ice age populations. A common haplotype that persisted in the Iberian Peninsula during the Pleistocene last glacial maximum is now extremely rare or absent from European rivers, highlighting the need for caution when making phylogeographic inferences about the origin and distribution of modern genetic types.     

Reconstruction of the colonization route from glacial refugium to the northern distribution range of the European butterfly Polyommatus coridon (Lepidoptera: Lycaenidae)

Genetic analyses are useful tools for reconstructing glacial distribution patterns and postglacial expansion corridors. However, little information is available about the latter. We reconstruct the expansion corridors of the butterfly Polyommatus coridon from its glacial refugium to the northern edge of its current distribution by comparing populations from southern Lower Saxony (central Germany) to other existing genetic data sets. The populations from Lower Saxony clearly belonged to a western lineage that expanded postglacially from the Adriatic‐Mediterranean region. They form part of a southern German group passing through the Burgundian Gap. In the southern German group, populations belong to a western subgroup. Therefore, expansion followed the Rhine valley and through Hesse, finally reaching southern Lower Saxony and western Thuringia in central Germany. Thus, we present a complete colonization route from the glacial refugium to the northern distribution range of P. coridon. Such data are useful for understanding the biogeographic structure and migration corridors for other mobile Mediterranean species.     

Natural genetic variation of Arabidopsis thaliana is geographically structured in the Iberian peninsula

To understand the demographic history of Arabidopsis thaliana within its native geographical range, we have studied its genetic structure in the Iberian Peninsula region. We have analyzed the amount and spatial distribution of A. thaliana genetic variation by genotyping 268 individuals sampled in 100 natural populations from the Iberian Peninsula. Analyses of 175 individuals from 7 of these populations, with 20 chloroplast and nuclear microsatellite loci and 109 common single nucleotide polymorphisms, show significant population differentiation and isolation by distance. In addition, analyses of one genotype from 100 populations detected significant isolation by distance over the entire Iberian Peninsula, as well as among six Iberian subregions. Analyses of these 100 genotypes with different model-based clustering algorithms inferred four genetic clusters, which show a clear-cut geographical differentiation pattern. On the other hand, clustering analysis of a worldwide sample showed a west–east Eurasian longitudinal spatial gradient of the commonest Iberian genetic cluster. These results indicate that A. thaliana genetic variation displays significant regional structure and consistently support the hypothesis that Iberia has been a glacial refugium for A. thaliana. Furthermore, the Iberian geographical structure indicates a complex regional population dynamics, suggesting that this region contained multiple Pleistocene refugia with a different contribution to the postglacial colonization of Europe.     

Phylogeography of the Marsh Fritillary Euphydryas aurinia (Lepidoptera: Nymphalidae) in the UK

We sampled extant (and extinct) populations of Euphydryas aurinia to examine the phylogeography of the species in the UK. We were interested in whether the genetic structuring of populations reflects anything other than a single recent post-glacial colonization event. Four hundred base pairs of the mitochondrial Cytochrome b gene were sequenced from individuals from populations throughout the UK, as well as populations in France and Portugal and seven polymorphic allozyme loci resolved. The mean number of allozyme alleles per locus was 4 and isolation by distance was shown not to be a factor in the geographic structuring of genetic diversity either with or without the inclusion of the French data (Mantel statistic Z = 0.015 and 0.112 respectively, P >0.5). Cytochrome b nucleotide diversity (average number of nucleotide differences per site between two sequences) was low overall (0.003, n = 63) but mean cytochrome b gene diversity over all populations was 0.77. The presence of the Portuguese and French haplotype in Scottish populations indicates that the Iberian peninsula was likely to be one glacial refugium for E. aurinia populations. The pattern of mitochondrial DNA found in the UK could be interpreted in one of two ways: (1) two separate colonization events or (2) a single slow colonization event. Allele frequency distributions followed a similar geographical pattern as mitochondrial DNA haplotypes. An AMOVA assigned just 2.68% of allozyme genetic variation to the grouping tested, providing more support for the single colonization event theory.     

Phylogeographic analysis of the endemic species Sibiraea angustata reveals a marginal refugium in the Qinghai–Tibet Plateau

The phylogeography of Sibiraea angustata, an endemic shrub species, was studied in the Qinghai–Tibet plateau (QTP). We investigated 466 individuals of S. angustata from 39 populations basically covering its total distribution area. Eight haplotypes (A–H) were detected by sequencing the intergenic chloroplast spacer trnS–trnG (600 bp), and one ancestral haplotype (A) was found to be widely distributed. The level of differentiation among populations was very high (G_ST=0.768; N_ST=0.850) and a significant phylogeographical structure was revealed (N_ST>G_ST). Analysis of molecular variance (AMOVA) similarily revealed a high level of differentiation among populations (84%, F_ST=0.842), indicating that little gene flow has occurred among populations mutually isolated by high mountains and rivers in the QTP. On the QTP platform there was only one widespread haplotype (A) in most populations, while populations along the eastern and southeastern edges had high diversity and unique haplotypes. Our results suggest that a glacial refugium may have been located on the eastern or southeastern edges of QTP during the last glaciation, and that interglacial and postglacial range expansion occurred from that refugium. Nested clade analysis (NCA) also suggests this scenario, which indicates that the current spatial distribution of cpDNA haplotypes and populations mainly resulted from long distance colonization, possibly coupled with subsequent or past fragmentation followed by range expansion and allopatric fragmentation.     

Postglacial dispersal of the European rabbit (Oryctolagus cuniculus) on the Iberian peninsula reconstructed from nested clade and mismatch analyses of mitochondrial DNA genetic variation

Nested clade analysis was applied to cytochrome b restriction site data previously obtained on 20 natural populations of the European rabbit across the Iberian Peninsula to test the hypothesis of postglacial dispersal from two main refugia, one in the northeast and the other in the southwest. Apart from historical fragmentation that resulted in geographic discontinuity of two distinct mitochondrial DNA (mtDNA) clades A and B, patterns of haplotype genetic variability have been shaped mostly by restricted gene flow via isolation by distance. The distribution of tip versus interior haplotypes suggests that dispersal occurred from both the southwestern and northeastern groups. Dispersal from the southwest had a north and northwest direction, whereas from the northeast it had mostly a western and southern orientation, with subsequent overlap in a southeastern-northwestern axis across the Iberian Peninsula. The analysis of the pairwise mismatch distribution of a 179-181-bp fragment of the mtDNA control region, for seven of those populations, further supports the idea that major patterns of dispersal were in the direction of central Iberia. Additionally, rabbit populations do not show signs of any significant loss of genetic diversity in the recent past, implying that they maintained large population sizes and structure throughout the ice ages. This is congruent with the fact that the Iberian Peninsula was itself a glacial refugium during Quaternary ice ages. Nonetheless, climatic oscillations of this period, although certainly milder than in northern Europe, were sufficient to affect the range distributions of Iberian organisms.     

Postglacial colonization of Europe by the barbastelle bat: agreement between molecular data and past predictive modelling

The barbastelle (Barbastella barbastellus) is a rare forest bat with a wide distribution in Europe. Here, we combine results from the analysis of two mtDNA fragments with species distribution modelling to determine glacial refugia and postglacial colonization routes. We also investigated whether niche conservatism occurs in this species. Glacial refugia were identified in the three southern European peninsulas: Iberia, Italy and the Balkans. These latter two refugia played a major role in the postglacial colonization process, with their populations expanding to England and central Europe, respectively. Palaeo‐distribution models predicted that suitable climatic conditions existed in the inferred refugia during the last glacial maximum (LGM). Nevertheless, the overlap between the current and the LGM distributions was almost inexistent in Italy and in the Balkans, meaning that B. barbastellus populations were forced to shift range between glacial and interglacial periods, a process that probably caused some local extinctions. In contrast, Iberian populations showed a ‘refugia within refugium’ pattern, with two unconnected areas containing stable populations (populations that subsisted during both glacial and interglacial phases). Moreover, the match between LGM models and the refugial areas determined by molecular analysis supported the hypothesis of niche conservatism in B. barbastellus. We argue that geographic patterns of genetic structuring, altogether with the modelling results, indicate the existence of four management units for conservation: Morocco, Iberia, Italy and UK, and Balkans and central Europe. In addition, all countries sampled possessed unique gene pools, thus stressing the need for the conservation of local populations.     

Postglacial colonisation patterns and the role of isolation and expansion in driving diversification in a passerine bird

Pleistocene glacial cycles play a major role in diversification and speciation, although the relative importance of isolation and expansion in driving diversification remains debated. We analysed mitochondrial DNA sequence data from 15 great reed warbler (Acrocephalus arundinaceus) populations distributed over the vast Eurasian breeding range of the species, and revealed unexpected postglacial expansion patterns from two glacial refugia. There were 58 different haplotypes forming two major clades, A and B. Clade A dominated in Western Europe with declining frequencies towards Eastern Europe and the Middle East, but showed a surprising increase in frequency in Western and Central Asia. Clade B dominated in the Middle East, with declining frequencies towards north in Central and Eastern Europe and was absent from Western Europe and Central Asia. A parsimonious explanation for these patterns is independent postglacial expansions from two isolated refugia, and mismatch distribution analyses confirmed this suggestion. Gene flow analyses showed that clade A colonised both Europe and Asia from a refugium in Europe, and that clade B expanded much later and colonised parts of Europe from a refugium in the Middle East. Great reed warblers in the eastern parts of the range have slightly paler plumage than western birds (sometimes treated as separate subspecies; A. a. zarudnyi and A. a. arundinaceus, respectively) and our results suggest that the plumage diversification took place during the easterly expansion of clade A. This supports the postglacial expansion hypothesis proposing that postglacial expansions drive diversification in comparatively short time periods. However, there is no indication of any (strong) reproductive isolation between clades and our data show that the refugia populations became separated during the last glaciation. This is in line with the Pleistocene speciation hypothesis invoking that much longer periods of time in isolation are needed for speciation to occur.     

Refugial origins of reindeer (Rangifer tarandus L.) inferred from mitochondrial DNA sequences

The glacial-interglacial cycles of the upper Pleistocene have had a major impact on the recent evolutionary history of Arctic species. To assess the effects of these large-scale climatic fluctuations to a large, migratory Arctic mammal, we assessed the phylogeography of reindeer (Rangifer tarandus) as inferred from mitochondrial DNA (mtDNA) sequence variation in the control region. Phylogenetic relationships among haplotypes seem to reflect historical patterns of fragmentation and colonization rather than clear-cut relationships among extant populations and subspecies. Three major haplogroups were detected, presumably representing three separate populations during the last glacial. The most influential one has contributed to the gene pool of all extant subspecies and seems to represent a large and continuous glacial population extending from Beringia and far into Eurasia. A smaller, more localized refugium was most likely isolated in connection with ice expansion in western Eurasia. A third glacial refugium was presumably located south of the ice sheet in North America, possibly comprising several separate refugial populations. Significant demographic population expansion was detected for the two haplogroups representing the western Eurasian and Beringian glacial populations. The former apparently expanded when the ice cap retreated by the end of the last glacial. The large continuous one, in contrast, seems to have expanded by the end of the last interglacial, indicating that the warm interglacial climate accompanied by marine transgression and forest expansion significantly confined population size on the continental mainland. Our data demonstrate that the current subspecies designation does not reflect the mtDNA phylogeography of the species, which in turn may indicate that morphological differences among subspecies have evolved as adaptive responses to postglacial environmental change.     

Genome‐wide set of SNPs reveals evidence for two glacial refugia and admixture from postglacial recolonization in an alpine ungulate

Past glaciation events have played a major role in shaping the genetic diversity and distribution of wild sheep in North America. The advancement of glaciers can isolate populations in ice‐free refugia, where they can survive until the recession of ice sheets. The major Beringian refugium is thought to have held thinhorn sheep (Ovis dalli) populations during times of glacial advance. While isolation in the major refugium can account for much of the genetic and morphological diversity seen in extant thinhorn sheep populations, mounting evidence suggests the persistence of populations in smaller minor refugia. We investigated the refugial origins of thinhorn sheep using ~10 000 SNPs obtained via a cross‐species application of the domestic sheep ovine HD BeadChip to genotype 52 thinhorn sheep and five bighorn sheep (O. canadensis) samples. Phylogenetic inference revealed a distinct lineage of thinhorn sheep inhabiting British Columbia, which is consistent with the survival of a group of thinhorn sheep in a minor refugium separate from the Beringian refugium. Isolation in separate glacial refugia probably mediated the evolution of the two thinhorn sheep subspecies, the white Dall's sheep (O. d. dalli), which persisted in Beringia, and the dark Stone's sheep (O. d. stonei), which utilized the minor refugium. We also found the first genetic evidence for admixture between sheep from different glacial refugia in south‐central Yukon as a consequence of post glacial expansion and recolonization. These results show that glaciation events can have a major role in the evolution of species inhabiting previously glaciated habitats and the need to look beyond established refugia when examining the evolutionary history of such species.