Imprints of glacial refugia in the modern genetic diversity of Pinus sylvestris

Aim To understand the impact of glacial refugia and migration pathways on the modern genetic diversity of Pinus sylvestris. Location The study was carried out throughout Europe. Methods An extended set of data of pollen and macrofossil remains was used to locate the glacial refugia and reconstruct the migrating routes of P. sylvestris throughout Europe. A vegetation model was used to simulate the extent of the potential refugia during the last glacial period. At the same time a genetic survey was carried out on this species. Results The simulated distribution of P. sylvestris during the last glacial period is coherent with the observed fossil data, which showed a patchy distribution of the refugia between c. 40° N and 50° N. Several migrational fronts were detected within the Iberian and the Italian peninsulas, and outside the Hungarian plain and around the Alps. The modern mitochondrial DNA depicted three different haplotypes for P. sylvestris. Two distinct haplotypes were restricted to northern Spain and Italy, and the third haplotype dominated most of the present‐day remaining distribution range of P. sylvestris in Europe. Main conclusions During the last glacial period P. sylvestris was constrained under severe climatic conditions to survive in scattered and restricted refugial areas. Combining palaeoenvironmental data, vegetation modelling and the genetic data, we have shown that the long‐term isolation in the glacial refugia and the migrational process during the Holocene have played a major role in shaping the modern genetic diversity of P. sylvestris in Europe.     

Genetic variation of isolated and peripheral populations of Pinus sylvestris (L.) from glacial refugia

Analysis of variation at 10 polymorphic isoenzyme loci in 51 European populations of Pinus sylvestris both from its main continuous range and from isolated, marginal populations out of the continuous range, revealed differences in genetic structure. The highest genetic richness, measured as mean number of alleles per locus, was recorded for populations from the Iberian Peninsula, followed by those from Scotland and the Balkans. Marginal, isolated populations were characterized by much greater interpopulation variation than populations from the continuous range of the species. The highest mean observed heterozygosity was recorded for the Iberian populations. The highest gene flow was observed among populations in the continuous range of the species. The populations could be classified into five groups based on genetic similarities. Populations from the continuous range formed one group, those from Spain two groups, pines from Scotland one group and those from the Balkans one group. One population from Scotland was found to be most distinct from the other Scottish pines and was found to be grouped with the Balkan populations. The occurrence and frequencies of rare alleles in the populations showed a characteristic pattern, suggesting that populations from the Iberian Peninsula probably did not participate in the colonization of Europe by Pinus sylvestris after the last glaciation. In contrast, the migration of populations from the Balkan refugium into Central and Western Europe had a significant effect on the contemporary gene pools of populations of Pinus sylvestris in its continuous range.     

Inferring the evolutionary history of divergence despite gene flow in a lizard species,Scincella lateralis (Scincidae), composed of cryptic lineages

Although recent radiations are fruitful for studying the process of speciation, they are difficult to characterize and require the use of multiple loci and analytical methods that account for processes such as gene flow and genetic drift. Using multilocus sequence data, we combine hierarchical cluster analysis, coalescent species tree inference, and isolation‐with‐migration analysis to investigate evolutionary relationships among cryptic lineages of North American ground skinks. We also estimate the extent that gene flow has accompanied or followed diversification, and also attempt to account for and minimize the influence of gene flow when reconstructing relationships. The data best support seven largely parapatric populations that are broadly concordant with mitochondrial (mt)DNA phylogeography throughout most of the species range, although they fail to fully represent extensive mtDNA divergence along the Gulf Coast. Relationships within and among three broad geographical groups are well supported, despite evidence of gene flow among them. Rejection of an allopatric divergence model partially depends on the inclusion of samples from near parapatric boundaries in the analyses, suggesting that allopatric divergence followed by recent migration may best explain migration rate estimates. Accounting for geographical variation in patterns of gene flow can improve estimates of migration–divergence parameters and minimize the influence of contemporary gene flow on phylogenetic inference. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

European phylogeography of the epiphytic lichen fungus Lobaria pulmonaria and its green algal symbiont

In lichen symbiosis, fungal and algal partners form close associations, often codispersed by vegetative propagules. Due to the particular interdependence, processes such as colonization, dispersal or genetic drift are expected to result in congruent patterns of genetic structure in the symbionts. To study the population structure of an obligate symbiotic system in Europe, we genotyped the fungal and algal symbionts of the epiphytic lichen Lobaria pulmonaria at eight and seven microsatellite loci, respectively, and analysed about 4300 L. pulmonaria thalli from 142 populations from the species' European distribution range. Based on a centroid approach, which localizes centres of genetic differentiation with a high frequency of geographically restricted alleles, we identified the South Italy–Balkan region as the primary glacial refugial area of the lichen symbiosis. Procrustean rotation analysis and a distance congruence test between the fungal and algal population graphs indicated general concordance between the phylogeographies of the symbionts. The incongruent patterns found in areas of postglacial recolonization may show the presence of an additional refugial area for the fungal symbiont, and the impact that horizontal photobiont transmission and different mutation rates of the symbionts have on their genotypic associations at a continental scale.     

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.     

Numts help to reconstruct the demographic history of the ocellated lizard (Lacerta lepida) in a secondary contact zone

In northwestern Iberia, two largely allopatric Lacerta lepida mitochondrial lineages occur, L5 occurring to the south of Douro River and L3 to the north, with a zone of putative secondary contact in the region of the Douro River valley. Cytochrome b sequence chromatograms with polymorphisms at nucleotide sites diagnostic for the two lineages were detected in individuals in the region of the Douro River and further north within the range of L3. We show that these polymorphisms are caused by the presence of four different numts (I-IV) co-occurring with the L3 genome, together with low levels of heteroplasmy. Two of the numts (I and II) are similar to the mitochondrial genome of L5 but are quite divergent from the mitochondrial genome of L3 where they occur. We show that these numts are derived from the mitochondrial genome of L5 and were incorporated in L3 through hybridization at the time of secondary contact between the lineages. The additional incidence of these numts to the north of the putative contact zone is consistent with an earlier postglacial northward range expansion of L5, preceding that of L3. We show that genetic exchange between the lineages responsible for the origin of these numts in L3 after secondary contact occurred prior to, or coincident with, the northward expansion of L3. This study shows that, in the context of phylogeographic analysis, numts can provide evidence for past demographic events and can be useful tools for the reconstruction of complex evolutionary histories.     

How lizards survived blizzards: phylogeography of the Liolaemus lineomaculatus group (Liolaemidae) reveals multiple breaks and refugia in southern Patagonia and their concordance with other codistributed taxa

Patagonia was shaped by a complex geological history, including the Miocene uplift of the Andes, followed by volcanism, marine introgressions, and extreme climatic oscillations during Pliocene–Pleistocene glaciation–deglaciation cycles. The distributional patterns and phylogenetic relationships of southern patagonian animals and plants were affected in different ways, and those imprints are reflected in the seven phylogeographic breaks and eight refugia that have been previously proposed. In this study, we estimated time‐calibrated phylogenetic/phylogeographic patterns in lizards of the Liolaemus lineomaculatus group and relate them to historical Miocene‐to‐Pleistocene events of Patagonia and the previously proposed phylogeographic patterns. Individuals from 51 localities were sequenced for the mitochondrial marker (cyt‐b) and a subsample of individuals from each mitochondrial lineage was sequenced for one nuclear (LDA12D) and one slow evolving mitochondrial gene (12S). Our analyses revealed strong phylogeographic structure among lineages and, in most cases, no signal of demographic changes through time. The lineomaculatus group is composed of three strongly supported clades (lineomaculatus, hatcheri and kolengh + silvanae), and divergence estimates suggested their origins associated with the oldest known Patagonian glaciation (7–5 Ma); subsequent diversification within the lineomaculatus clade coincided with the large Pliocene glaciations (~3.5 Ma). The lineomaculatus clade includes nine strongly genetically and geographically structured lineages, five of which are interpreted as candidate species. Our findings suggest that some Liolaemus lineages have persisted in situ, each of them in a different refugium, through several glaciation–deglaciation cycles without demographic fluctuations. We also summarize and update qualitative evidence of some shared phylogeographic breaks and refugia among plants, rodents and lizards.     

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.     

Salicaceae detoxification abilities in Florida tiger swallowtail butterflies (Papilio glaucus maynardi Gauthier): Novel ability or Pleistocene holdover?

Abstract Florida populations of the eastern tiger swallowtail butterfly, Papilio glaucus L., have unique morphological features and ecological adaptations that have contributed to their subspecies status (P. g. maynardi Gauthier). We describe geographically unique abilities for detoxification of Carolina willow, Salix caroliniana Michx. (Salicaceae), for several Florida populations of P. g. maynardi. Of all the approximately 570 worldwide species of the Papilionidae, such Salicaceae detoxification abilities exist only in the allopatric North American western and northernmost species (P. rutulus Lucas, P. eurymedon Lucas and P. canadensis Rothschild & Jordan). Females of P. glaucus collected from populations in southeastern USA were examined for oviposition preference in 5‐choice assays, and displayed a low preference for Salicaceae (<5%), but larvae from Florida populations exhibited a high survival (>60%) on these plants. Detoxification abilities have previously shown to be autosomally inherited, and can be transferred via natural or hand‐paired interspecific hybrid introgression. However, these Florida populations are at least 700–1 500 km from the nearest hybrids or the hybrid species, P. appalachiensis Pavulaan & Wright, which possess these detoxification abilities. In any case, the Z ( = X)‐linked oviposition preferences for Salicaceae are lacking in these Florida populations, illustrating genetic independence of oviposition preference determination and larval survival/performance abilities. The origins of detoxification abilities are unlikely to be due to recent climate‐driven introgression, and may represent ancestral trait carry‐overs from interglacial refugium populations of the Pleistocene epoch.