Putative Glacial Refugia Research Articles

Whole-genome analysis reveals phylogenetic and demographic history of Eurasian perch.

The contemporary diversity and distribution of species are shaped by their evolutionary and ecological history. This can be deciphered with the help of phylogenetic and demographic analysis methods, ideally combining and supplementing information from mitochondrial and nuclear genomes. In this study, we investigated the demographic history of Eurasian perch (Perca fluviatilis), a highly adaptable teleost with a distribution range across Eurasia. We combined whole-genome resequencing data with available genomic resources to analyse the phylogeny, phylogeography, and demographic history of P. fluviatilis populations from Europe and Siberia. We identified five highly diverged evolutionary mtDNA lineages, three of which show a strong signal of admixture in the Baltic Sea region. The estimated mean divergence time between these lineages ranged from 0.24 to 1.42 million years. Based on nuclear genomes, two distinct demographic trajectories were observed in European and Siberian samples reflecting contrasting demographic histories ca. 30,000-100,000 years before the present. A comparison of mtDNA and nuclear DNA evolutionary trees and AMOVA revealed concordances, as well as incongruences, between the two types of data, most likely reflecting recent postglacial colonization and hybridization events. Overall, our findings demonstrate the power and usefulness of genome-wide information for delineating historical processes that have shaped the genome of P. fluviatilis. We also highlight the added value of data-mining existing transcriptomic resources to complement novel sequence data, helping to shed light on putative glacial refugia and postglacial recolonization routes.

Spatial conservation planning of forest genetic resources in a Mediterranean multi-refugial area

The Kunming-Montreal Global Biodiversity Framework recognised the urgency of taking action to conserve intraspecific genetic diversity (IGD) as an insurance against habitat degradation and environmental change. Recent work suggests that 90–99 % of IGD should be conserved to safeguard viability of future generations.Here, we addressed such a conservation issue in three forest tree species in Italy: silver fir (Abies alba Mill.), Heldreich's pine (Pinus heldreichii H. Christ), and pedunculate oak (Quercus robur L.). We used microsatellite markers to measure IGD of 36 (A. alba), 15 (P. heldreichii) and 25 (Q. robur) natural sites, including several putative glacial refugia. We developed a spatial conservation planning (SCP) analysis to quantify the genetic irreplaceability of each site and identify the minimum set coverage ensuring IGD protection. Finally, we compared SCP results with the contributions to allelic diversity within and between sites, total allelic diversity and private allelic richness.We found that between 44 % and 73 % of sites were required to conserve 90–99 % of the alleles, and that this conservation effort held even when targeting lower percentages of alleles to protect (50–75 %). Glacial refugia were often included in the minimum set coverage, confirming biogeographical expectations. Finally, sites with high genetic irreplaceability were found to have higher private allelic richness on average. These results are discussed in the light of the biogeographic history of the species studied and the current policies for the conservation of forest genetic resources.

Phylogeography of Potamon ibericum (Brachyura: Potamidae) identifies Quaternary glacial refugia within the Caucasus biodiversity hot spot.

Refugia are critical for the maintenance of biodiversity during the periods of Quaternary climatic oscillations. The long‐term persistence of refugial populations in a large continuous refugium has resulted in a homogenous pattern of genetic structure among populations, while highly structured evolutionary lineages characterize the restriction of refugial populations to smaller subrefugia. These mechanisms have resulted in the identification of hot spots of biodiversity within putative glacial refugia. We studied phylogeography of Potamon ibericum (Brachyura: Potamidae) in the drainages of the western Caucasus biodiversity hot spot (i.e., Colchis and the Caucasus) to infer spatial genetic structure and potential refugia for a freshwater crab in this region. These areas have traditionally considered as a refugium due to the presence of Tertiary relict species. We integrated population genetic data and historical demographic analysis from cytochrome oxidase subunit I sequences and paleoclimatic data from species distribution modeling (SDM). The results revealed the lack of phylogeographic structure and provided evidence for demographic expansion. The SDM presented a rather homogenous and large refugium that extended from northeast Turkey to Colchis during the last glacial period. In contrast to these findings, previous phylogeographic study on P. ibericum of the eastern Caucasus biodiversity hot spot (i.e., Hyrcania) identified multiple independent refugia. By combining these results, we explain the significance of this important western Palearctic hot spot of biological diversity in shaping the geographic distribution of intraspecific genetic diversity in a freshwater taxon.

Evaluating hypotheses of expansion from refugia through comparative phylogeography of south‐eastern Coastal Plain amphibians

AbstractAimEarly genetic studies in the south‐eastern United States provided the foundation for ideas in the field of comparative phylogeography, but few direct comparisons with consistent sampling across taxa exist for this region. We investigate the influence of historical processes and species‐level characteristics on phylogeographic structure within four anuran species, evaluate previously described biogeographic patterns, and test three hypotheses of expansion from putative glacial refugia.LocationSouth‐eastern United States Coastal Plain.MethodsWe sampled four anuran species from the same 36 localities, assembled mitochondrial genomes from Illumina sequence data and estimated phylogenetic relationships and divergence times within each species. We used spatially explicit phylogeographic analyses and ecological niche models (ENMs) to test predictions about expansion from putative glacial refugia and estimate species‐specific parameters including dispersal, migration direction and centre of origin. ENMs for four different time periods were compared within species to assess niche stability.ResultsSpecies differ in patterns of mitochondrial divergence, with only one species displaying a pattern consistent with the previously described Alabama suture zone. Few predictions for hypotheses of expansion from putative glacial refugia were met. ENMs suggest that species have responded differently to historical changes in climate, possibly contributing to discordant genetic patterns. Two species with deep mitochondrial divergences (>2.5 Ma) had low niche stability through time and potentially isolated regions of suitable habitat, whereas the two species with relatively stable, continuous niches exhibit less genetic structure.Main conclusionsThese Coastal Plain anurans appear to have been affected by historical climate change, but were not necessarily isolated in glacial refugia. Different natural history characteristics have likely produced discordant patterns in these species, with more generalist, ephemeral breeders exhibiting greater niche stability and lower phylogeographic structure.

Molecular data and ecological niche modelling reveal the evolutionary history of the common and Iberian moles (Talpidae) in Europe

According to mitochondrial data, the common mole, Talpa europaea, is paraphyletic. This could be explained by either an ancient introgression of mtDNA from the Iberian blind mole T. occidentalis to T. europaea, or the existence of a differentiated taxonomic entity in northern Spain that needs to be described. In this study, we combined mitochondrial (Cytb) and nuclear (HDAC2) data to investigate these two alternative hypotheses. Based on both mitochondrial and nuclear data and an extensive geographical sampling (399 sequenced individuals), we show that the populations of T. europaea from Spain and south‐western France (south of the Loire River) are phylogenetically closer to T. occidentalis than to T. europaea. The Spanish–French lineage has some morphological characters resembling more to T. occidentalis (e.g. eyes) and others resembling more to T. europaea (external measurements, mesostyle of the first upper molar). It also seems to have several distinctive dental characters, suggesting that it should be recognized as a new species. Within the three lineages, we found a marked phylogeographical pattern, with several allopatric or parapatric lineages, dating from the Pleistocene. Our genetic data combined with species distribution models support the presence of several putative glacial refugia during glacial maxima for each species.

Protected areas of Spain preserve the neutral genetic diversity of Quercus ilex L. irrespective of glacial refugia

Quercus ilex L. (holm oak) is a wind-pollinated, sclerophyllous tree that copes with the environmental variability of the Mediterranean climate and that displays flexible ecophysiological adaptability in relation to hydric and thermic stresses. The holm oak dominates Mediterranean woodlands on both acidic and calcareous soils and has been exposed to management (dehesas) for thousands of years. Both protected areas and glacial refugia are supposed to preserve a substantial fraction of the genetic diversity of Iberian species. Genetic diversity was examined for 68 populations sampled throughout Spain using ptDNA SNPs, ptDNA microsatellites, and primarily nuclear AFLPs. Protected populations did not significantly differ from nonprotected populations by any of the measures of levels of genetic diversity. The three-level hierarchical AMOVA indicated that a low number of protected populations harbor most of the species’ genetic diversity. In addition, we found no evidence from either ptDNA or AFLP variation to support that populations from putative glacial refugia are divergent genetic groups as expected during isolation. Outcrossing, anemophilous long-distance pollen dispersal, acorn transport by animals, tree reliance, and habitat availability in Spain probably played a primarily role in homogenizing allele frequency among populations. This result leads us to suggest that extensive gene flow has been prevalent across Spanish populations. We conclude that glacial refugia have not been essential to maintain the neutral genetic makeup of Q. ilex. Nevertheless, conservation of the holm oak in protected areas ensures protection of the species’ genetic diversity, the most widespread woodland ecosystem in Iberia and indirectly the four iconic, endangered animal species (black stork, cinereous vulture, Iberian lynx, western imperial eagle).

Postglacial recolonization in a cold climate specialist in western Europe: patterns of genetic diversity in the adder (Vipera berus) support the central-marginal hypothesis.

Understanding the impact of postglacial recolonization on genetic diversity is essential in explaining current patterns of genetic variation. The central-marginal hypothesis (CMH) predicts a reduction in genetic diversity from the core of the distribution to peripheral populations, as well as reduced connectivity between peripheral populations. While the CMH has received considerable empirical support, its broad applicability is still debated and alternative hypotheses predict different spatial patterns of genetic diversity. Using microsatellite markers, we analysed the genetic diversity of the adder (Vipera berus) in western Europe to reconstruct postglacial recolonization. Approximate Bayesian Computation (ABC) analyses suggested a postglacial recolonization from two routes: a western route from the Atlantic Coast up to Belgium and a central route from the Massif Central to the Alps. This cold-adapted species likely used two isolated glacial refugia in southern France, in permafrost-free areas during the last glacial maximum. Adder populations further from putative glacial refugia had lower genetic diversity and reduced connectivity; therefore, our results support the predictions of the CMH. Our study also illustrates the utility of highly variable nuclear markers, such as microsatellites, and ABC to test competing recolonization hypotheses.

Tracing the evolutionary history of the mole,Talpa europaea, through mitochondrial DNA phylogeography and species distribution modelling

Our understanding of the effect of Pleistocene climatic changes on the biodiversity of European mammals mostly comes from phylogeographical studies of non-subterranean mammals, whereas the influence of glaciation cycles on subterranean mammals has received little attention. The lack of data raises the question of how and to what extent the current amount and distribution of genetic variation in subterranean mammals is the result of Pleistocene range contractions/expansions. The common mole (Talpa europaea) is a strictly subterranean mammal, widespread across Europe, and represents one of the best candidates for studying the influence of Quaternary climatic oscillation on subterranean mammals. Cytochrome b sequences, as obtained from a sampling covering the majority of the distribution area, were used to evaluate whether Pleistocene climate change influenced the evolution of T. europaea and left a trace in the genetic diversity comparable to that observed in non-subterranean small mammals. Subsequently, we investigated the occurrence of glacial refugia by comparing the results of phylogeographical analysis with species distribution modelling. We found three differentiated mitochondrial DNA lineages: two restricted to Spain and Italy and a third that was widespread across Europe. Phylogenetic inferences and the molecular clock suggest that the Spanish moles represent a highly divergent and ancient lineage, highlighting for the first time the paraphyly of T. europaea. Furthermore, our analyses suggest that the genetic break between the Italian and the European lineages predates the last glacial phase. Historical demography and spatial principal component analysis further suggest that the Last Glacial Maximum left a signature both in the Italian and in the European lineages. Genetic data combined with species distribution models support the presence of at least three putative glacial refugia in southern Europe (France, Balkan Peninsula and Black Sea) during the last glacial maximum that likely contributed to post-glacial recolonization of Europe. By contrast, the Italian lineage remained trapped in the Italian peninsula and, according to the pattern observed in other subterranean mammals, did not contribute to the recolonization of northern latitudes.

Mitochondrial phylogeography of the European wild boar: the effect of climate on genetic diversity and spatial lineage sorting across Europe

AbstractAimClimate changes in the past had a deep impact on the evolutionary history of many species and left genetic signatures that are often still detectable today. We investigated the geographical pattern of mitochondrial DNA diversity in the European wild boar (Sus scrofa). Our final aims were to clarify the influence of present and past climatic conditions, infer the geographical position of glacial refugia, and suggest post‐glacial spatial dynamics.LocationEurope.MethodsD‐loop sequences were obtained for 763 individuals from Portugal to western Russia. Phylogenetic, multivariate and interpolation methods were used to describe the genetic and geographical patterns. Climatic suitability during the Last Glacial Maximum (LGM) was predicted using MaxEnt. The effect of present and past suitability on the observed patterns of diversity was evaluated by multiple linear regression.ResultsWe confirmed the existence of a ubiquitous mitochondrial clade in Europe (E1), an endemic clade in Italy (E2) and a few East Asian haplotypes (A), presumably introgressed from domestic pigs. No Near Eastern haplotypes were detected. Genetic divergence was not simply related to geographical distance. A clear south–north decreasing gradient of diversity was observed, with maximum levels in putative glacial refugia. Latitudinal variation in climatic conditions during the LGM was shown to be a good predictor of current genetic diversity. Moreover, an unexpected similarity between Iberia and eastern Europe was observed, while central European populations showed a higher affinity to the Italian gene pool.Main conclusionsThe current distribution of mitochondrial genetic diversity was highly influenced by past climatic events, especially those related to the LGM, and is consistent with a major contribution of the Italian peninsula and the Balkans to the post‐glacial recolonization of northern areas. More recent processes, such as restocking and extensive hunting, probably acted at rather local scales, without great impact on the global pattern of mitochondrial diversity.

Was Jeju Island a glacial refugium for East Asian warm‐temperate plants? Insights from the homosporous fern Selliguea hastata (Polypodiaceae)

We posed two hypotheses for broad scenarios of postglacial recolonization of Korea by the warm-temperate vegetation: (1) that extant Korean populations are derived from a single refugium, or (2) that they are derived from multiple refugia. We chose a homosporous fern typical of East Asian warm-temperate vegetation, Selliguea hastata, to test which of the two scenarios is more likely and to check whether Japan contained putative glacial refugia. Using 16 allozyme loci, we obtained genotypes of 756 individuals from 20 populations, representative of the whole distribution area in Korea (including Jeju Island), Japan, and Taiwan. We assessed genetic variability within and among populations, Wright's F-statistics, and conducted analysis of molecular variance, model-based Bayesian clustering, and bottleneck tests. We found no allozyme variation within populations of S. hastata in mainland Korea, whereas genetic polymorphism was detected for populations from Jeju Island, Japan (in particular a population from southeastern Shikoku), and Taiwan. The levels of inbreeding within populations were high, consistent with the potential of S. hastata for intragametophytic selfing. Data on allelic richness together with Bayesian clustering methods suggest a pattern of postglacial recolonization of mainland Korea from a single refugium, probably located either on Jeju Island or in Japan. Jeju Island should merit the highest priority for conservation biogeography, as it played a role as a Quaternary refugium for arctic-alpine, boreal, temperate as well as warm-temperate plants, as suggested here.

Phylogeographical Pattern and Evolutionary History of an Important Peninsular Malaysian Timber Species, Neobalanocarpus heimii (Dipterocarpaceae)

Tectonic movements, climatic oscillations, and marine transgressions during the Cenozoic have had a dramatic effect on the biota of the tropical rain forest. This study aims to reveal the phylogeography and evolutionary history of a Peninsular Malaysian endemic tropical timber species, Neobalanocarpus heimii (Dipterocarpaceae). A total of 32 natural populations of N. heimii, with 8 samples from each population were investigated. Fifteen haplotypes were identified from five noncoding chloroplast DNA (cpDNA) regions. Overall, two major genealogical cpDNA lineages of N. heimii were elucidated: a widespread southern and a northern region. The species is predicted to have survived in multiple refugia during climatic oscillations: the northwestern region (R1), the northeastern region (R2), and the southern region (R3). These putative glacial refugia exhibited higher levels of genetic diversity, population differentiation, and the presence of unique haplotypes. Recolonization of refugia R1 and R2 could have first expanded into the northern region and migrated both northeastwards and northwestwards. Meanwhile, recolonization of N. heimii throughout the southern region could have commenced from refugia R3 and migrated toward the northeast and northwest, respectively. The populations of Tersang, Pasir Raja, and Rotan Tunggal exhibited remarkably high haplotype diversity, which could have been the contact zones that have received an admixture of gene pools from the northerly and also southerly regions. As a whole, the populations of N. heimii derived from glacial refugia and contact zones should be considered in the conservation strategies in order to safeguard the long-term survival of the species.

Western Palaearctic phylogeography of an inquiline oak gall wasp, Synergus umbraculus

Insect-induced galls on plants comprise species-rich but self-contained communities of herbivores and natural enemies. In the present study, we focus on galls induced by cynipid gall wasps on oaks, and on the least-known trophic level that these galls contain: inquilines. These insects, also cynipids, feed on gall tissue and are an abundant but taxonomically poorly understood part of an otherwise well-studied system. We used DNA sequence data to examine spatial patterns in the genetic diversity of Synergus umbraculus Olivier 1791 (Hymenoptera: Cynipidae: Synergini), a widespread species attacking many host galls across the Western Palaearctic. Analysis of 239 cytochrome b sequences revealed eight haplogroups showing significant phylogeographic pattern across the Western Palaearctic, corresponding to putative glacial refugia in Iberia, Central Europe, Turkey, and Iran. There were significant genetic discontinuities across the Pyrenees and the Anatolian diagonal but no impact of the Alps, suggesting that significant discontinuities have biotic rather than physical causes. Detailed analysis of sites in the Carpathian Basin reveal a high diversity and low spatial structure, and identify Central Europe as the source of colonists for Quaternary colonization of Germany, France, and Britain. We found no evidence for host-associated differentiation of S. umbraculus lineages associated with the most common cynipid host galls, suggesting frequent shifts within the host gall assemblage by inquiline lineages. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102, 750–764.

The influence of Wisconsinan glaciation and contemporary stream hydrology on microsatellite DNA variation in rainbow trout (Oncorhynchus mykiss)

Microsatellite DNA variation was examined in rainbow trout ( Oncorhynchus mykiss ) populations from throughout British Columbia, Canada, to address the roles of historical isolation, postglacial dispersal, and contemporary geomorphology in structuring genetic variation and differentiation. We detected signatures of historical isolation and postglacial recolonization in the form of “interior” and “coastal” population groupings, a decline in genetic variation as distance increased from putative glacial refugia, and different extents of isolation-by-distance in different regions. Rainbow trout populations were structured genetically into major regions and into smaller watersheds and then into drainages. Within drainages, high levels of dispersal and gene flow were inferred between geographically proximate and contiguous lakes. Elevation, stream branching points (nodes), fluvial distance, migration barriers, and stream and lake order influenced genetic diversity within, and differentiation among, populations. Habitat characteristics, particularly lake surface area and perimeter, were poor predictors of genetic variation. Although founder events and postglacial dispersal influenced broadscale patterns of genetic diversity in rainbow trout, our results suggest that contemporary factors can strongly modulate historical patterns.

AFLPs reveal an absence of geographical genetic structure among remnant populations of pohutukawa (Metrosideros excelsa, Myrtaceae)

Ten populations spanning the natural geographical range of Metrosideros excelsa (pohutukawa) were analysed using AFLP. All populations were highly variable showing levels of genetic diversity similar to other long‐lived outcrossing tree species. UPGMA analysis of interpopulation genetic distances and multivariate analysis of individual multilocus genotype data showed genetic differentiation among populations, but there was no obvious relationship between genetic structure and geographical location. There was also no evidence of greater genetic variation in areas of New Zealand that have been proposed to be glacial refugia. These data provide a contrast to previously published observations on M. excelsa using chloroplast DNA, which showed that plants from putative glacial refugia exhibited higher levels of variation than those from non‐refugial areas.

Evidence for a large‐scale population structure among accessions of Arabidopsis thaliana: possible causes and consequences for the distribution of linkage disequilibrium

The existence of a large-scale population structure was investigated in Arabidopsis thaliana by studying patterns of polymorphism in a set of 71 European accessions. We used sequence polymorphism surveyed in 10 fragments of approximately 600 nucleotides and a set of nine microsatellite markers. Population structure was investigated using a model-based inference framework. Among the accessions studied, the presence of four groups was inferred using genetic data, without using prior information on the geographical origin of the accessions. Significant genetic isolation by geographical distance was detected at the group level, together with a geographical gradient in allelic richness across groups. These results are discussed with respect to the previously proposed scenario of postglacial colonization of Europe from putative glacial refugia. Finally, the contribution of the inferred structure to linkage disequilibrium among 171 pairs of essentially unlinked markers was also investigated. Linkage disequilibrium analysis revealed that significant associations detected in the whole sample were mainly due to genetic differentiation among the inferred groups. We discuss the implication of this finding for future association studies in A. thaliana.

Genetic diversity of core and peripheral Sitka spruce ( Picea sitchensis (Bong.) Carr) populations: implications for conservation of widespread species

This study investigated levels of genetic diversity and population differentiation among Sitka spruce ( Picea sitchensis) populations classified as core or peripheral based on ecological niche, and continuous or disjunct based on species distribution. Large numbers of trees ( N = 200) were sampled from each of eight populations to evaluate the distribution of rare as well as common alleles across the species range. Codominant alleles for eight sequence-tagged site loci were classified based on frequency and geographic distribution in order to develop appropriate sampling strategies to target specific classes of alleles. An important finding of this study is the similarity in genetic diversity as measured by expected heterozygosity between core populations (mean H E = 0.58) and peripheral populations (mean H E = 0.56). However, there was significant inbreeding in peripheral ( F IS = 0.17) but not in core ( F IS = 0.03) populations. Large differences in gene flow estimates were observed between core (Nm = 9.0) and peripheral populations (Nm = 3.5). Irrespective of population classification, over 75% of the alleles were common and widespread. Only one allele was classified as rare and localized, and this allele was limited to one core, disjunct and two peripheral, disjunct populations. There was stronger evidence of past bottlenecks in peripheral, disjunct populations than in core, continuous populations. Results are used to suggest sampling strategies for capture of maximum level of genetic diversity and conservation of rare alleles. The conservation of peripheral, particularly disjunct, populations as well as populations in putative glacial refugia may present the best opportunity for conserving rare alleles.

Microsatellites for use in Nothofagus cunninghamii (Nothofagaceae) and related species

Abstract Nothofagus cunninghamii (myrtle) has a widespread distribution through the temperate rainforest of southeastern Australia with some disjunct populations existing in putative glacial refugia. Polymorphic nuclear markers are required to resolve the biogeographical history of the species and will also be useful for conservation and forestry applications in this and other species of Nothofagus. Fourteen polymorphic microsatellite loci were isolated from N. cunninghamii, with four to 10 alleles amplified in 15 individuals tested. Transferability to other species of Nothofagus was successful, with six loci transferring to all eight other species tested.

Population genetic structure, phylogeography and spawning philopatry in walleye (Stizostedion vitreum) from mitochondrial DNA control region sequences.

Mitochondrial (mt) DNA control region sequences were used to test the genetic and phylogeographic structure of walleye Stizostedion vitreum populations at different geographical scales: among spawning sites, lake basins, lakes, and putative glacial refugia in the Great Lakes region. Sequencing 199 walleye revealed nucleotide substitutions and tandemly repeated sequences that varied in copy number, as well as in sequence composition, in approximately 1200 bp of the mtDNA control region. Variable numbers of copies of an 11-bp tandem repeat showed no geographical patterning and were not used in further analyses. Substitutions in the other areas of the control region yielded 19 haplotypes, revealing phylogeographic structure and significant differences among glacial refugia, lakes, basins and some spawning sites. Differences among spawning populations were consistent with reduced gene flow, philopatry and possible natal homing. Analysis of spawning populations showed consistency of genotypic frequencies among years and between males and females, supporting philopatry in both sexes. The unglaciated plateau in southern Ohio, USA housed a very different haplotype that diverged prior to the Missouri, Mississippi and Atlantic glacial refugia types. Haplotypes from the three refugia colonized the Great Lakes after retreat of the Wisconsin glaciers, and their present distribution reflects the geography of their prior isolation and differential colonization. Populations that became associated with spawning localities appear to have diverged further due to philopatry, resulting in fine-scale phylogeographic structuring.