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.     

Population history of the terrestrial orchid Cremastra appendiculata var. variabilis from Korea,inferred from levels and distribution of genetic diversity

Cremastra appendiculata var. variabilis is a self‐compatible, insect‐pollinated, terrestrial orchid that is a typical member of the warm‐temperate vegetation in the Korean Peninsula. Here we examine levels and partitioning of allozyme diversity (22 loci) in 12 populations of this orchid to gain insight into its genetic structure and post‐glacial colonization history in Korea. It harboured considerably higher levels of genetic variation within populations (%P = 48.1, A = 1.70 and H_e = 0.217) and lower degree of differentiation among populations (F_ST = 0.068) than those typical of allozyme‐based studies in other terrestrial orchid species. These patterns suggest that extant populations were derived from multiple source populations (i.e. from multiple glacial refugia), although further studies are needed to confirm this scenario. In addition to population history, traits such as high potential of seed dispersal, a mixed mating system and its occurrence in large and continuous populations would have contributed to the current levels and distribution of genetic diversity in Korean populations of C. appendiculata var. variabilis. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173 , 721–732.     

Scattered late‐glacial and early Holocene tree populations as dispersal nuclei for forest development in north‐eastern European Russia

Aim Concepts about patterns and rates of post‐glacial tree population migration are changing as a result of the increasing amount of palaeobotanical information being provided by macroscopic plant remains. Here we combine macrofossil, pollen and stomata records from five sites in north‐eastern European Russia and summarize the results for the late‐glacial–early Holocene transition. The late‐glacial–early Holocene transition encompasses the first indications of trees (tree‐type Betula, Picea abies, Abies sibirica and Larix sibirica) and subsequent forest development. Considerable time‐lags between the first macrobotanical and/or stomata finds of spruce (Picea abies) and the establishment of a closed forest are reconsidered. Location Pechora basin, north‐eastern European Russia. Methods We used plant macrofossil, stomata, pollen and radiocarbon analyses to reconstruct late‐glacial and early Holocene tree establishment and forest development. The data were derived from lake sediment and peat archives. Results Palaeobotanical data reveal an early Holocene presence (11,500–10,000 cal. yr bp ) of arboreal taxa at all five sites. One site presently located in the northernmost taiga zone, shows the presence of spruce and reproducing tree birch during the late‐glacial. Given the current view of post‐glacial population dynamics and migration rates, it seems likely that the source area of these early tree populations in north‐eastern European Russia was not located in southern Europe but that these populations had local origins. Results thus support the emerging view that the first post‐glacial population expansions in non‐glaciated regions at high latitudes do not reflect migration from the south but were a result of an increase in the size and density of small persisting outlying tree populations. Main conclusions Results suggest that the area east of the margin of the Scandinavian ice sheet to the Ural Mountains had isolated patches of trees during the late‐glacial and early Holocene and that these small populations acted as initial nuclei for population expansion and forest development in the early Holocene.     

Ancient DNA identifies post‐glacial recolonisation,not recent bottlenecks,as the primary driver of contemporary mtDNA phylogeography and diversity in Scandinavian brown bears

Aim

Brown bear populations in Scandinavia show a strong mitochondrial DNA (mtDNA) phylogeographic structure and low diversity relative to other parts of Europe. Identifying the timing and origins of this mtDNA structure is important for conservation programs aimed at restoring populations to a natural state. Therefore, it is essential to identify whether contemporary genetic structure is linked to post‐glacial recolonisation from divergent source populations or an artefact of demographic impacts during recent population bottlenecks. We employed ancient DNA techniques to investigate the timing and potential causes of these patterns.

Location

Scandinavia and Europe.

Methods

Ancient mtDNA sequences from 20 post‐glacial Scandinavian bears were used to investigate phylogeographic structure and genetic diversity over the last 6000 years. MtDNA from 19 Holocene Norwegian bears was compared with 499 sequences from proximate extant populations in Sweden, Finland, Estonia and western Russia. A single mtDNA sequence from a Holocene Denmark sample was compared with 149 ancient and modern bears from Western Europe.

Results

All nineteen Holocene Norwegian samples are identical to or closely related to the most common mtDNA haplotype found in northern Europe today. MtDNA diversity was low and not significantly different from extant populations in northern Europe. In Denmark, we identified a single mtDNA haplotype that is previously unrecorded from Scandinavia.

Main conclusions

The current discrete phylogeographic structure and lack of mtDNA diversity in Scandinavia is attributed to serial founder effects during post‐glacial recolonisation from divergent source populations rather than an artefact of recent anthropogenic impacts. In contrast to previous interpretations, the recolonisation of southern Scandinavia may not have been limited to bears from a single glacial refugium. Results highlight the importance of conserving the long‐term evolutionary separation between northern and southern populations and identify southern Scandinavia as an important reservoir of mtDNA diversity that is under threat in other parts of Europe.

     

Did tree‐Betula,Pinus and Picea survive the last glaciation along the west coast of Norway? A review of the evidence,in light of Kullman (2002)

Aim We discuss the hypotheses proposed by Kullman [Geo‐Öko 21 (2000) 141; Nordic Journal of Botany 21 (2001) 39; Journal of Biogeography 29 (2002) 1117] on the basis of radiocarbon‐dated megafossils of late‐glacial age from the central Swedish mountains that boreal trees survived the glaciation along the south‐west coast of Norway and subsequently migrated eastward early in the late‐glacial to early deglaciated parts of the central Swedish Scandes mountains. Methods We assess these hypotheses on the basis of glacial geological evidence and four lines of palaeoecological evidence, namely macrofossil records of the tree species, vegetation and climate reconstructions from plant evidence, independent climate reconstructions from other proxies for the late‐glacial environment of south‐west Norway, and the patterns of post‐glacial spread of the tree species. Location South and west Norway, central Swedish Scandes mountains (Jämtland). Results and conclusions South‐west Norway and the adjacent continental shelf were under ice at the last‐glacial maximum (LGM). The late‐glacial vegetation of south‐west Norway was treeless and summer temperatures were below the thermal limits for Betula pubescens Ehrh., Pinus sylvestris L. and Picea abies (L.) Karst. Instead of spreading immediately after the onset of Holocene warming, as might have been expected if local populations were surviving, B. pubescens showed a lag of local arrival of 600 to > 1000 years, Pinus lagged by 1500 to > 2000 years, and Picea only reached southern Norway c. 1500 years ago and has not colonized most of south‐west Norway west of the watershed. Glacial geological evidence shows the presence of an ice sheet in the Scandes at the LGM and in the Younger Dryas, which was cold‐based near or at the area where the late‐glacial‐dated megafossils were recovered by Kullman. We conclude that the samples dated by Kullman (2002) should be evaluated carefully for possible sources of contamination. All the available evidence shows that the biogeographical hypotheses, based on these radiocarbon dates taken at face value, of late‐glacial tree survival at the Norwegian coast and subsequent eastwards spread to the mountains, are unsupportable.     

Conservation genetics of small relic populations of silver fir (Abies alba Mill.) in the northern Apennines

Abstract

Small and isolated silver fir populations from the Emilian Apennines (northern Italy) were studied to assess their level of genetic variation and their relationship with Alpine populations. We investigated the variability of two chloroplast microsatellites to analyse the within‐population genetic variability of four peripheral and fragmented Apennine populations and to determine their phylogenetic relatedness to seven Alpine populations covering the entire distribution of silver fir in the Alps. Haplotypic richness and haplotype diversity as well as the fraction of private haplotypes were lower in Apennine populations, evidencing the genetic impoverishment of these stands. The among‐population genetic variability analysis revealed the genetic peculiarity of Apennine populations. Analysis of molecular variance showed that the highest level of the among‐population variation occurs between Alpine and Apennine regions. A neighbour‐joining dendrogram revealed a distinct Apennine cluster that included the closest Alpine population. Our genetic analysis supports a common origin for Emilian Apennine populations, suggesting that these populations are relicts of past large silver fir populations in the northern Apennines. Our results point to a relevant conservation value for these stands, to be considered in their management.     

Caucasus Mountains divide postulated postglacial colonization routes in the white‐breasted hedgehog,Erinaceus concolor

For many European species, the mountains of the Alps and the Pyrenees have acted as significant barriers to northwards colonization from southern glacial refugia. To the east, the Caucasus Mountains would seem to have been a similar barrier to the white‐breasted hedgehog (Erinaceus concolor). A deep divergence among hedgehog mitochondrial sequences to the north and south of the Caucasus Mountains suggests two colonization routes, originating from separate refugial regions and divided by this mountain barrier. From a Balkan refugium, hedgehogs have colonized northwards into Russia and to the northern foothills of the Caucasus Mountains. The origins of hedgehogs colonizing the southern parts of the Caucasus are not entirely clear, although fossil and climatic data suggest a glacial refugium on the southern shores of the Black Sea. Divergence within the southern group indicates a long‐standing fragmentation within such a refugium or the presence of further cryptic refugia in Turkey and the Near East. The Caucasus barrier would seem to have been an important factor in structuring the late Pleistocene distribution of species.     

Subantarctic flowering plants: pre‐glacial survivors or post‐glacial immigrants?

Aim The aim here was to assess whether the present‐day assemblage of subantarctic flowering plants is the result of a rapid post‐Last Glacial Maximum (LGM) colonization or whether subantarctic flowering plants survived on the islands in glacial refugia throughout the LGM. Location The circumpolar subantarctic region, comprising six remote islands and island groups between latitudes 46° and 55° S, including South Georgia in the South Atlantic Ocean, the Prince Edward Islands, Îles Crozet, Îles Kerguelen, the Heard Island group in the South Indian Ocean and Macquarie Island in the South Pacific Ocean. Methods Floristic affinities between the subantarctic islands were assessed by cluster analysis applied to an up‐to‐date dataset of the phanerogamic flora in order to test for the existence of provincialism within the subantarctic. A review of the primary literature on the palaeobotany, geology and glacial history of the subantarctic islands was carried out and supplemented with additional palaeobotanical data and new field observations from South Georgia, Île de la Possession (Îles Crozet) and Îles Kerguelen. Results First, a strong regionalism was observed, with different floras characterizing the islands in each of the ocean basins, and endemic species being present in the South Indian Ocean and South Pacific Ocean provinces. Second, the majority of the plant species were present at the onset of accumulation of post‐glacial organic sediment and there is no evidence for the natural arrival of new immigrants during the subsequent period. Third, a review of geomorphological data suggested that the ice cover was incomplete during the LGM on the majority of the islands, and ice‐free biological refugia were probably present even on the most glaciated islands. Main conclusions Several independent lines of evidence favour the survival of a native subantarctic phanerogamic flora in local refugia during the LGM rather than a post‐LGM colonization from more distant temperate landmasses in the Southern Hemisphere.     

Topo‐climatic microrefugia explain the persistence of a rare endemic plant in the Alps during the last 21 millennia

Ongoing rapid climate change is predicted to cause local extinction of plant species in mountain regions. However, some plant species could have persisted during Quaternary climate oscillations without shifting their range, despite the limited evidence from fossils. Here, we tested two candidate mechanisms of persistence by comparing the macrorefugia and microrefugia (MR) hypotheses. We used the rare and endemic Saxifraga florulenta as a model taxon and combined ensembles of species distribution models (SDMs) with a high‐resolution paleoclimatic and topographic dataset to reconstruct its potential current and past distribution since the last glacial maximum. To test the macrorefugia hypothesis, we verified whether the species could have persisted in or shifted to geographic areas defined by its realized niche. We then identified potential MR based on climatic and topographic properties of the landscape and applied refined scenarios of MR dynamics and functions over time. Last, we quantified the number of known occurrences that could be explained by either the macrorefugia or MR model. A consensus of two or three SDM techniques predicted absence between 14–10, 3–4 and 1 ka bp , which did not support the macrorefugia model. In contrast, we showed that S. florulenta could have contracted into MR during periods of absence predicted by the SDMs and later re‐colonized suitable areas according to the macrorefugia model. Assuming a limited and realistic seed dispersal distance for our species, we explained a large number of the current occurrences (61–96%). Additionally, we showed that MR could have facilitated range expansions or shifts of S. florulenta. Finally, we found that the most recent and the most stable MR were the ones closest to current occurrences. Hence, we propose a novel paradigm to explain plant persistence by highlighting the importance of supporting functions of MR when forecasting the fate of plant species under climate change.     

Molecular evidence of the survival of subterranean amphipods (Arthropoda) during Ice Age underneath glaciers in Iceland

Two endemic groundwater arthropod crustacean species, Crangonyx islandicus and Crymostygius thingvallensis, were recently discovered on the mid‐Atlantic volcanic island of Iceland. The extent of morphological differences from closest relatives, endemism, along with the geographic isolation of Iceland and its complete coverage by glaciers 21 000 years ago, suggests that these two species have survived glaciation periods in sub‐glacial refugia. Here we provide strong support for this hypothesis by an analysis of mitochondrial genetic variation within Crangonyx islandicus. Our results show that the species is divided into several distinct monophyletic groups that are found along the volcanic zone in Iceland, which have been separated by 0.5 to around 5 million years. The genetic divergence between groups reflects geographic distances between sampling sites, indicating that divergence occurred after the colonization of Iceland. The genetic patterns, as well as the dependency of genetic variation on distances from the tectonic plate boundary and altitude, points to recent expansion from several refugia within Iceland. This presents the first genetic evidence of multicellular organisms as complex as crustacean amphipods which have survived glaciations beneath an ice sheet. This survival may be explained by geothermal heat linked to volcanic activities, which may have maintained favourable habitats in fissures along the tectonic plate boundary in Iceland during glaciations.     

Intraspecific divergences of Rhodiola alsia (Crassulaceae) based on plastid DNA and internal transcribed spacer fragments

In the present study, we used two maternally inherited plastid DNA intergenic spacers, rpl20‐rps12 and trnS‐trnG, and the biparentally inherited nuclear ribosomal internal transcribed spacer (ITS) region to explore genetic variation and phylogeographical history of Rhodiola alsia, a herb endemic to the Qinghai‐Tibetan Plateau (QTP). Based on range‐wide sampling (18 populations and 227 individuals), we detected 45 plastid DNA haplotypes and 19 ITS sequence types. Only three plastid DNA haplotypes were widespread; most haplotypes were restricted to single sites or to neighbouring populations. Analysis of molecular variance revealed that most of the genetic variance was found within populations (51.24%) but that populations were also distinct (F_ST = 0.48759). We found three areas with relatively high plastid DNA diversity and these could further be recognized as potentially isolated divergence centres based on the ITS sequence type distribution. These represent three potentially isolated glacial refugia for R. alsia: one of them has long been recognized as an important refugium on the south‐eastern edge of the QTP, whereas the others are new and located in the north and south of the Tanggula Mountains on the plateau platform. Divergence time estimates based on ITS suggest that the main lineages of R. alsia diverged from each other 0.35–0.87 Mya, indicating that climatic oscillations during the Pleistocene may have been an important driver of intraspecific divergence in R. alsia. Rhodiola alsia probably experienced a phylogeographical history of retreat to isolated glacial refugia during Quaternary glaciations that led to different degrees of allopatric intraspecific divergence. © 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, 168 , 204–215.     

Phylogeography of the bigeye chub Hybopsis amblops (Teleostei: Cypriniformes): early Pleistocene diversification and post‐glacial range expansion

The bigeye chub, Hybopsis amblops, is a member of the Central Highlands ichthyofauna of eastern North America. Phylogenetic analyses of the H. amblops species group based on a 1059 bp fragment of the mitochondrial DNA cytochrome b gene did not recover a monophyletic group. The inclusion of Hybopsis hypsinotus in the species complex is questionable. Within H. amblops, five strongly supported clades were identified; two clades containing haplotypes from the Ozark Highlands and three clades containing haplotypes from the Eastern Highlands and previously glaciated regions of the Ohio and Wabash River drainages. Estimates of the timing of divergence indicated that prior to the onset of glaciation, vicariant events separated populations east and west of the Mississippi River. East of the Mississippi River glacial cycles associated with the blocking and rerouting of the Teays River system caused populations to be pushed southward into refugia of the upper Ohio River. Following the most recent Wisconsinan glaciation, populations expanded northward into previously glaciated regions and southward into the Cumberland River drainage. In the Ozarks, west of the Mississippi River, isolation of clades appears to be maintained by the lack of stream capture events between the upper Arkansas and the White River systems and a barrier formed by the Arkansas River.     

Long‐term survival and diversification of an endemic Melitaea species in mountains of Iran and adjacent areas

Disjunct distribution patterns regularly resulted in the separation of different genetic lineages in glacial refugia. Recent patterns of survival and expansion have been often revealed by climatic niche modelling. We used the combination of genetic markers, geometric morphometry and climatic niche modelling to clear up the taxonomy and reconstruct the potential range of an endemic Iranian, taxonomically disputed Melitaea species in climatically different epochs. Our results show that this species (Melitaea abbas Gross and Ebert 1975, comb. n. = M. zagrosi Tóth and Varga syn. nova) is clearly separated from all taxa of the Melitaea phoebe species group and only occurs in Iran and Azerbaijan but were also predicted for some adjacent regions. Molecular markers and distribution modelling show consistently that this species should have had a long‐term survival in this area, and its range could have been slightly larger during the last glacial maximum than currently. Based on the studied molecular markers, three main groups in M. abbas can be recognized: those of steppic area of Azerbaijan, western Iran and northeastern Iran. Each group is characterized by own mitochondrial haplotypes, but also a high level of genetic diversity appears in the central part of the distribution area (Zagros Mts.).     

Hybridization among Arctic white-headed gulls (Larus spp.) obscures the genetic legacy of the Pleistocene

We studied the influence of glacial oscillations on the genetic structure of seven species of white-headed gull that breed at high latitudes (Larus argentatus, L. canus, L. glaucescens, L. glaucoides, L. hyperboreus, L. schistisagus, and L. thayeri). We evaluated localities hypothesized as ice-free areas or glacial refugia in other Arctic vertebrates using molecular data from 11 microsatellite loci, mitochondrial DNA (mtDNA) control region, and six nuclear introns for 32 populations across the Holarctic. Moderate levels of genetic structure were observed for microsatellites (F(ST)= 0.129), introns (Φ(ST)= 0.185), and mtDNA control region (Φ(ST)= 0.461), with among-group variation maximized when populations were grouped based on subspecific classification. Two haplotype and at least two allele groups were observed across all loci. However, no haplotype/allele group was composed solely of individuals of a single species, a pattern consistent with recent divergence. Furthermore, northernmost populations were not well differentiated and among-group variation was maximized when L. argentatus and L. hyberboreus populations were grouped by locality rather than species, indicating recent hybridization. Four populations are located in putative Pleistocene glacial refugia and had larger τ estimates than the other 28 populations. However, we were unable to substantiate these putative refugia using coalescent theory, as all populations had genetic signatures of stability based on mtDNA. The extent of haplotype and allele sharing among Arctic white-headed gull species is noteworthy. Studies of other Arctic taxa have generally revealed species-specific clusters as well as genetic structure within species, usually correlated with geography. Aspects of white-headed gull behavioral biology, such as colonization ability and propensity to hybridize, as well as their recent evolutionary history, have likely played a large role in the limited genetic structure observed.     

Preliminary Study on Effects of Glacial Retreat on the Dominant Glacial Snow Bacteria in Laohugou Glacier No. 12

One impact of climate change is the rapid shrinking of glaciers, resulting in microorganisms deposited into glacial snow or ice being exposed to new environments such as glacier foreland. A pyrosequencing analysis based on the bacterial 16S rRNA gene showed that bacterial diversity was the highest in proglacial soil, followed by that of glacial snow in ablation zone, then by that of glacial snow in the accumulation area, finally by that of glacial snow in glacier terminus, with the combination of Chao1, ACE, Shannon and Simpson analysis. Eighteen phyla were detected from the 7 samples, but mainly composed of Proteobacteria, Actinobacteria and Bacteroidetes. Flavobacterium, Massilia, Pedobacter, Polaromonas were more abundant in glacial snow samples than in glacial soil sample. Massilia was rarely reported in other environments, implying the necessity for its conservation under scenarios of glacier and snowpack loss induced by climate change.     

Differentiation and speciation in mountain streams: a case study in the caddisfly Rhyacophila aquitanica (Trichoptera)

Few studies have analysed the biogeography of mountain aquatic organisms, although this habitat provides stable conditions in which many species survived Pleistocene climatic oscillations, usually in the geographical vicinity of their present distribution ranges. The mountain caddisfly Rhyacophila aquitanica was selected as a model organism for this habitat type. Morphological measurements of genitalia and external characters of male individuals were obtained from almost the entire range of distribution of the species. Morphometric results were analysed by cluster analysis and multivariate statistics. Important differences were discovered among three population groups of R. aquitanica inhabiting different European mountain ranges: (i) mountain ranges north‐west of the Alps (Massif Central, Vosges, Schwarzwald and Fribourg); (ii) the southern Alps (Lombardia and Carinthia); and (iii) the western part of the southern Carpathians. This divergence suggests a long‐term isolation among these groups, which presumably took place long before the last Pleistocene glaciation, with no secondary contact among these populations. The differentiation centres of the southern Alps and Carpathian groups may have been mostly homotopic to their actual ranges, whereas the western group must have been distributed in the areas west or north‐west of the Alps with secondary expansions and disjunctions.     

Late Pleistocene and Holocene development of the felid fauna (Felidae) of Europe: a review

In the fossil deposits of the Late Pleistocene ( c . 115 000–11 500 years ago), five felid species are recorded in Europe: the wildcat Felis silvestris , Eurasian lynx Lynx lynx , Iberian lynx Lynx pardinus , leopard Panthera pardus and cave lion Panthera leo spelaea . In the Holocene, Europe was colonized by F. silvestris , L. lynx and L. pardinus as well as the lion Panthera leo . The status of P. pardus in post-glacial Europe is unknown. So far, only sparse records indicate that P. pardus survived into the early Holocene. During the Late Glacial, both L. lynx and L. pardinus occurred on the Iberian Peninsula. However, from the Holocene, only the Iberian lynx is recorded in this region. There are subfossil records that indicate that L. pardinus also occurred in central and western France until c . 3000 years ago. Surprisingly, with reservations on the determination of the bones (by J. Altuna), both lions and cave lions seem to be recorded in the Iberian Peninsula in the Late Glacial. There are published records of the lion P. leo in the northern Iberian Peninsula from the early Holocene. However, its presence in Europe on the basis of subfossil records was proven initially from the Atlantic period. In Ponto-Mediterranean regions of Europe, the lion is recorded from the Atlantic to the younger sub-Atlantic.     

Mitochondrial DNA variation and genetic population structure of chum salmon Oncorhynchus keta around the Pacific Rim

A survey of mtDNA variation among populations of chum salmon Oncorhynchus keta around the Pacific Rim revealed four large population groups: Rim of the Sea of Japan, the Rim of the Okhotsk Sea and West Bering Sea, North‐west Alaska and Gulf of Alaska. The observed population structure appears to reflect isolation by distance with limited gene flow between regions and larger amounts of gene flow between populations within these four regions.