Restricted gene flow and local adaptation highlight the vulnerability of high‐latitude reefs to rapid environmental change

Global climate change poses a serious threat to the future health of coral reef ecosystems. This calls for management strategies that are focused on maximizing the evolutionary potential of coral reefs. Fundamental to this is an accurate understanding of the spatial genetic structure in dominant reef‐building coral species. In this study, we apply a genotyping‐by‐sequencing approach to investigate genome‐wide patterns of genetic diversity, gene flow, and local adaptation in a reef‐building coral, Pocillopora damicornis, across 10 degrees of latitude and a transition from temperate to tropical waters. We identified strong patterns of differentiation and reduced genetic diversity in high‐latitude populations. In addition, genome‐wide scans for selection identified a number of outlier loci putatively under directional selection with homology to proteins previously known to be involved in heat tolerance in corals and associated with processes such as photoprotection, protein degradation, and immunity. This study provides genomic evidence for both restricted gene flow and local adaptation in a widely distributed coral species, and highlights the potential vulnerability of leading‐edge populations to rapid environmental change as they are locally adapted, reproductively isolated, and have reduced levels of genetic diversity.     

Thermally tolerant corals have limited capacity to acclimatize to future warming

Thermal stress affects organism performance differently depending on the ambient temperature to which they are acclimatized, which varies along latitudinal gradients. This study investigated whether differences in physiological responses to temperature are consistent with regional differences in temperature regimes for the stony coral Oculina patagonica. To resolve this question, we experimentally assessed how colonies originating from four different locations characterized by >3 °C variation in mean maximum annual temperature responded to warming from 20 to 32 °C. We assessed plasticity in symbiont identity, density, and photosynthetic properties, together with changes in host tissue biomass. Results show that, without changes in the type of symbiont hosted by coral colonies, O. patagonica has limited capacity to acclimatize to future warming. We found little evidence of variation in overall thermal tolerance, or in thermal optima, in response to spatial variation in ambient temperature. Given that the invader O. patagonica is a relatively new member of the Mediterranean coral fauna, our results also suggest that coral populations may need to remain isolated for a long period of time for thermal adaptation to potentially take place. Our study indicates that for O. patagonica, mortality associated with thermal stress manifests primarily through tissue breakdown under moderate but prolonged warming (which does not impair symbiont photosynthesis and, therefore, does not lead to bleaching). Consequently, projected global warming is likely to cause repeat incidents of partial and whole colony mortality and might drive a gradual range contraction of Mediterranean corals.     

Large‐scale longitudinal gradients of genetic diversity: a meta‐analysis across six phyla in the Mediterranean basin

Biodiversity is the diversity of life at all scales, from genes to ecosystems. Predicting its patterns of variation across the globe is a fundamental issue in ecology and evolution. Diversity within species, that is, genetic diversity, is of prime importance for understanding past and present evolutionary patterns, and highlighting areas where conservation might be a priority. Using published data on the genetic diversity of species whose populations occur in the Mediterranean basin, we calculated a coefficient of correlation between within‐population genetic diversity indices and longitude. Using a meta‐analysis framework, we estimated the role of biological, ecological, biogeographic, and marker type factors on the strength and magnitude of this correlation in six phylla. Overall, genetic diversity increases from west to east in the Mediterranean basin. This correlation is significant for both animals and plants, but is not uniformly expressed for all groups. It is stronger in the southern than in the northern Mediterranean, in true Mediterranean plants than in plants found at higher elevations, in trees than in other plants, and in bi‐parentally and paternally than in maternally inherited DNA makers. Overall, this correlation between genetic diversity and longitude, and its patterns across biological and ecological traits, suggests the role of two non‐mutually exclusive major processes that shaped the genetic diversity in the Mediterranean during and after the cold periods of the Pleistocene: east‐west recolonization during the Holocene and population size contraction under local Last Glacial Maximum climate in resident western and low elevation Mediterranean populations.     

Genomic signatures of host‐associated divergence and adaptation in a coral‐eating snail,Coralliophila violacea (Kiener, 1836)

The fluid nature of the ocean, combined with planktonic dispersal of marine larvae, lowers physical barriers to gene flow. However, divergence can still occur despite gene flow if strong selection acts on populations occupying different ecological niches. Here, we examined the population genomics of an ectoparasitic snail, Coralliophila violacea (Kiener 1836), that specializes on Porites corals in the Indo‐Pacific. Previous genetic analyses revealed two sympatric lineages associated with different coral hosts. In this study, we examined the mechanisms promoting and maintaining the snails’ adaptation to their coral hosts. Genome‐wide single nucleotide polymorphism (SNP) data from type II restriction site‐associated DNA (2b‐RAD) sequencing revealed two differentiated clusters of C. violacea that were largely concordant with coral host, consistent with previous genetic results. However, the presence of some admixed genotypes indicates gene flow from one lineage to the other. Combined, these results suggest that differentiation between host‐associated lineages of C. violacea is occurring in the face of ongoing gene flow, requiring strong selection. Indeed, 2.7% of all SNP loci were outlier loci (73/2,718), indicative of divergence with gene flow, driven by adaptation of each C. violacea lineage to their specific coral hosts.     

Rapid range expansion increases genetic differentiation while causing limited reduction in genetic diversity in a damselfly

Many ectothermic species are currently expanding their geographic range due to global warming. This can modify the population genetic diversity and structure of these species because of genetic drift during the colonization of new areas. Although the genetic signatures of historical range expansions have been investigated in an array of species, the genetic consequences of natural, contemporary range expansions have received little attention, with the only studies available focusing on range expansions along a narrow front. We investigate the genetic consequences of a natural range expansion in the Mediterranean damselfly Coenagrion scitulum, which is currently rapidly expanding along a broad front in different directions. We assessed genetic diversity and genetic structure using 12 microsatellite markers in five centrally located populations and five recently established populations at the edge of the geographic distribution. Our results suggest that, although a marginal significant decrease in the allelic richness was found in the edge populations, genetic diversity has been preserved during the range expansion of this species. Nevertheless, edge populations were genetically more differentiated compared with core populations, suggesting genetic drift during the range expansion. The smaller effective population sizes of the edge populations compared with central populations also suggest a contribution of genetic drift after colonization. We argue and document that range expansion along multiple axes of a broad expansion front generates little reduction in genetic diversity, yet stronger differentiation of the edge populations.     

Diazotrophic community and associated dinitrogen fixation within the temperate coral Oculina patagonica

Dinitrogen (N₂) fixing bacteria (diazotrophs) are an important source of new nitrogen in oligotrophic environments and represent stable members of the microbiome in tropical corals, while information on corals from temperate oligotrophic regions is lacking. Therefore, this study provides new insights into the diversity and activity of diazotrophs associated with the temperate coral Oculina patagonica from the Mediterranean Sea by combining metabarcoding sequencing of amplicons of both the 16S rRNA and nifH genes and ¹⁵N₂ stable isotope tracer analysis to assess diazotroph-derived nitrogen (DDN) assimilation by the coral. Results show that the diazotrophic community of O. patagonica is dominated by autotrophic bacteria (i.e. Cyanobacteria and Chlorobia). The majority of DDN was assimilated into the tissue and skeletal matrix, and DDN assimilation significantly increased in bleached corals. Thus, diazotrophs may constitute an additional nitrogen source for the coral host, when nutrient exchange with Symbiodinium is disrupted (e.g. bleaching) and external food supply is limited (e.g. oligotrophic summer season). Furthermore, we hypothesize that DDN can facilitate the fast proliferation of endolithic algae, which provide an alternative carbon source for bleached O. patagonica. Overall, O. patagonica could serve as a good model for investigating the importance of diazotrophs in coral recovery from bleaching.     

Identifying refugia from climate change using coupled ecological and genetic data in a transitional Mediterranean‐temperate tree species

Populations occurring in areas of overlap between the current and future distribution of a species are particularly important because they can represent “refugia from climate change”. We coupled ecological and range‐wide genetic variation data to detect such areas and to evaluate the impacts of habitat suitability changes on the genetic diversity of the transitional Mediterranean‐temperate tree Fraxinus angustifolia. We sampled and genotyped 38 natural populations comprising 1006 individuals from across Europe. We found the highest genetic diversity in western and northern Mediterranean populations, as well as a significant west to east decline in genetic diversity. Areas of potential refugia that correspond to approximately 70% of the suitable habitat may support the persistence of more than 90% of the total number of alleles in the future. Moreover, based on correlations between Bayesian genetic assignment and climate, climate change may favour the westward spread of the Black Sea gene pool in the long term. Overall, our results suggest that the northerly core areas of the current distribution contain the most important part of the genetic variation for this species and may serve as in situ macrorefugia from ongoing climate change. However, rear‐edge populations of the southern Mediterranean may be exposed to a potential loss of unique genetic diversity owing to habitat suitability changes unless populations can persist in microrefugia that have facilitated such persistence in the past.     

Genetic signature of the colonisation dynamics along a coastal expansion front in the damselfly Coenagrion scitulum

1. Many insects are expanding their distribution range polewards as a result of climate change, which has been shown to be associated with founder effects leading to a reduction in genetic diversity and an increase in genetic differentiation. These spatial genetic patterns may arise from colonisation from a broad expansion front or a limited neighbourhood after a stepping stone model of dispersal. The temporal persistence of such founder effects are poorly understood, mainly because studies looking at the fine‐scale initial temporal dynamics of the genetic signature of a range expansion are rare. 2. Using microsatellite markers, we performed a detailed spatiotemporal genetic analysis of the range expanding damselfly Coenagrion scitulum (Rambur) along a coastal axis during the first years after colonisation. 3. A decrease was in (private) allelic richness when going northwards along the coastline, which is consistent with a scenario of cumulative founder events. In spite of the spatiotemporal dynamics in the observation records of the species along the coastline, the spatial genetic data indicated a major contribution from the broad expansion front during the colonisation of the coastline rather than a stepping‐stone colonisation process. 4. The fine‐scale temporal dynamics of the range expansion indicated the absence of persistent founder effects and instead showed considerable temporal instability in genetic indices at the more northern edge populations. This may be explained by genetic immigration and admixture from the broad expansion front in this active disperser.     

The phylogeographical clade trade: tracing the impact of human-mediated dispersal on the colonization of northern Europe by the oak gallwasp Andricus kollari

Human dispersal of organisms is an important process modifying natural patterns of biodiversity. Such dispersal generates new patterns of genetic diversity that overlie natural phylogeographical signatures, allowing discrimination between alternative dispersal mechanisms. Here we use allele frequency and DNA sequence data to distinguish between alternative scenarios (unassisted range expansion and long range introduction) for the colonization of northern Europe by an oak-feeding gallwasp, Andricus kollari. Native to Mediterranean latitudes from Portugal to Iran, this species became established in northern Europe following human introduction of a host plant, the Turkey oak Quercus cerris. Colonization of northern Europe is possible through three alternative routes: (i) unassisted range expansion from natural populations in the Iberian Peninsula; (ii) unassisted range expansion from natural populations in Italy and Hungary; or (iii) descent from populations imported to the UK as trade goods from the eastern Mediterranean in the 1830s. We show that while populations in France were colonized from sources in Italy and Hungary, populations in the UK and neighbouring parts of coastal northern Europe encompass allozyme and sequence variation absent from the known native range. Further, these populations show demographic signatures expected for large stable populations, rather than signatures of rapid population growth from small numbers of founders. The extent and spatial distribution of genetic diversity in the UK suggests that these A. kollari populations are derived from introductions of large numbers of individuals from each of two genetically divergent centres of diversity in the eastern Mediterranean. The strong spatial patterning in genetic diversity observed between different regions of northern Europe, and between sites in the UK, is compatible with leptokurtic models of population establishment.     

Climate‐associated genetic variation in Fagus sylvatica and potential responses to climate change in the French Alps

Local adaptation patterns have been found in many plants and animals, highlighting the genetic heterogeneity of species along their range of distribution. In the next decades, global warming is predicted to induce a change in the selective pressures that drive this adaptive variation, forcing a reshuffling of the underlying adaptive allele distributions. For species with low dispersion capacity and long generation time such as trees, the rapidity of the change could impede the migration of beneficial alleles and lower their capacity to track the changing environment. Identifying the main selective pressures driving the adaptive genetic variation is thus necessary when investigating species capacity to respond to global warming. In this study, we investigate the adaptive landscape of Fagus sylvatica along a gradient of populations in the French Alps. Using a double‐digest restriction‐site‐associated DNA (ddRAD) sequencing approach, we identified 7,000 SNPs from 570 individuals across 36 different sites. A redundancy analysis (RDA)‐derived method allowed us to identify several SNPs that were strongly associated with climatic gradients; moreover, we defined the primary selective gradients along the natural populations of F. sylvatica in the Alps. Strong effects of elevation and humidity, which contrast north‐western and south‐eastern site, were found and were believed to be important drivers of genetic adaptation. Finally, simulations of future genetic landscapes that used these findings allowed identifying populations at risk for F. sylvatica in the Alps, which could be helpful for future management plans.     

Retention of gene diversity during the spread of a non‐native plant species

Spatial expansion, which is a crucial stage in the process to successful biological invasion, is anticipated to profoundly affect the magnitude and spatial distribution of genetic diversity in novel colonized areas. Here, we show that, contrasting common expectations, Pyrenean rocket (Sisymbrium austriacum), retained SNP diversity as this introduced plant species descended in the Meuse River Basin. Allele frequencies did not mirror between‐population distances along the predominant expansion axis. Reconstruction of invasion history based on the genotypes of historical herbarium specimens indicated no influence of additional introductions or multiple points of entry on this nongradual pattern. Assignment analysis suggested the admixture of distant upstream sources in recently founded downstream populations. River dynamics seem to have facilitated occasional long‐distance dispersal which brought diversity to the expansion front and so maintained evolutionary potential. Our findings highlight the merit of a historical framework in interpreting extant patterns of genetic diversity in introduced species and underscore the need to integrate long‐distance dispersal events in theoretical work on the genetic consequences of range expansion.     

Phylogeography and genetic differentiation along the distributional range of the orchid Epidendrum fulgens: a Neotropical coastal species not restricted to glacial refugia

Aim Phylogeographical studies in the Brazilian Atlantic Forest (BAF) have mostly included species associated with forest habitats, whereas taxa associated with grassland and sand‐dune plant communities have so far been largely overlooked. This study examines the phylogeography of the orchid Epidendrum fulgens, which occurs on coastal sand dunes and granitic outcrops, in order to identify major genetic divergences or disjunctions across the range of the species and to investigate the genetic signatures of past range contractions and expansions. Location Southern and south‐eastern seashore vegetation along the BAF biome, and granitic and arenitic outcrops that occur in the subtropical grassland plant communities located south of the BAF. Methods Nine nuclear and four plastid microsatellite loci were used to genotype 424 individuals from 16 populations across the distributional range of E. fulgens. For both sets of markers, we estimated genetic diversity and population differentiation, testing for a north–south gradient of genetic diversity. The plastid haplotype network and a Bayesian assignment analysis of nuclear markers were used to infer population structure. Past demographic changes were investigated using a coalescence approach. Results A deep disjunction was found between northern populations within the BAF and southern populations outside the BAF that occur on granitic and arenitic outcrops. Recent demographic reductions were detected in northern populations on coastal sands. Such demographic changes were not expected for those populations, as previous studies with forest species had found evidence of population expansion in the same areas. Higher genetic diversity was found in southern populations on granite, in contrast to patterns observed in previous studies of forest species. Main conclusions The results are consistent with the long‐term persistence of E. fulgens. Bottlenecks were detected in populations from areas where population expansion events have been detected in other plant (and animal) species, suggesting that forest expansion after the Last Glacial Maximum played a role in the population fragmentation and decrease in genetic diversity in E. fulgens. A substantial genetic division in E. fulgens corresponds to the ‘Portal de Torres’, a region that demarcates the northern limits of subtropical grassland plant communities and the southern limits of the BAF.     

Ecological and historical determinants of population genetic structure and diversity in the Mediterranean shrub Rosmarinus officinalis (Lamiaceae)

Population genetic studies of widespread Mediterranean shrubs are scarce compared with those of trees and narrow endemics or studies from phylogeographical perspectives, despite the key role these species may play in Mediterranean ecosystems. Knowledge on the effect of ecological factors in shaping their genetic patterns is also limited. In this study we investigate genetic diversity and population structure across 18 populations of Rosmarinus officinalis, a Mediterranean shrubland plant. Populations were sampled along two elevational gradients, one each on calcareous and siliceous soils in a mountain system in the eastern Iberian Peninsula, to decipher the effect of ecological factors on the genetic diversity and structure based on 11 microsatellite loci. We found overall high levels of genetic diversity and weak population structure. Genetic diversity increased with elevation, whereas population differentiation was stronger among populations growing on siliceous soils. The nested analysis of elevational gradients within soil types revealed that these general patterns were mostly driven by siliceous populations, whereas calcareous populations were more homogeneous along elevational belts. Bayesian analysis of population structure revealed genetic membership of lowland and high‐elevation populations to different genetic clusters and a higher admixture of intermediate‐elevation populations to both clusters. High‐elevation populations were less differentiated from a hypothetical ancestral cluster, suggesting the persistence of their gene pool during the Pleistocene glaciations. In contrast, lowland populations resulted from more recent divergence. We propose that life‐history and reproductive traits mostly contribute to explain the high levels of genetic diversity and weak population structure, whereas ecological and historical factors mostly contribute to the stronger differentiation of siliceous populations and a rapid expansion of R. officinalis on calcareous soils possibly mediated by human landscape transformations, © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016, 180 , 50–63.     

Adaptation to reef habitats through selection on the coral animal and its associated microbiome

Spatially adjacent habitats on coral reefs can represent highly distinct environments, often harbouring different coral communities. Yet, certain coral species thrive across divergent environments. It is unknown whether the forces of selection are sufficiently strong to overcome the counteracting effects of the typically high gene flow over short distances, and for local adaptation to occur. We screened the coral genome (using restriction site‐associated sequencing) and characterized both the dinoflagellate photosymbiont‐ and tissue‐associated prokaryote microbiomes (using metabarcoding) of a reef flat and slope population of the reef‐building coral, Pocillopora damicornis, at two locations on Heron Island in the southern Great Barrier Reef. Reef flat and slope populations were separated by <100 m horizontally and ~5 m vertically, and the two study locations were separated by ~1 km. For the coral host, genetic divergence between habitats was much greater than between locations, suggesting limited gene flow between the flat and slope populations. Consistent with environmental selection, outlier loci primarily belonged to the conserved, minimal cellular stress response, likely reflecting adaptation to the different temperature and irradiance regimes on the reef flat and slope. The prokaryote community differed across both habitat and, to a lesser extent, location, whereas the dinoflagellate photosymbionts differed by habitat but not location. The observed intraspecific diversity associated with divergent habitats supports that environmental adaptation involves multiple members of the coral holobiont. Adaptive alleles or microbial associations present in coral populations from the environmentally variable reef flat may provide a source of adaptive variation for assisted evolution approaches, through assisted gene flow, artificial cross‐breeding or probiotic inoculations, with the aim to increase climate resilience in the slope populations.     

Genetically diverse but with surprisingly little geographical structure: the complex history of the widespread herb Carex nigra (Cyperaceae)

Aim Based on extensive range‐wide sampling, we address the phylogeographical history of one of the most widespread and taxonomically complex sedges in Europe, Carex nigra s. lat. We compare the genetic structure of the recently colonized northern areas (front edge) and the long‐standing southern areas (rear edge), and assess the potential genetic basis of suggested taxonomic divisions at the rank of species and below. Location Amphi‐Atlantic, central and northern Europe, circum‐Mediterranean mountain ranges, central Siberia, Himalayas. Methods A total of 469 individuals sampled from 83 populations, covering most of the species’ range, were analysed with amplified fragment length polymorphism (AFLP) and chloroplast DNA (cpDNA) markers. Bayesian clustering, principal coordinates analysis, and estimates of diversity and differentiation were used for the analysis of AFLP data. CpDNA data were analysed with statistical parsimony networks and maximum parsimony and Bayesian inference of phylogenetic trees. Results Overall genetic diversity was high, but differentiation among populations was limited. Major glacial refugia were inferred in the Mediterranean Basin and in western Russia; in addition, there may have been minor refugia in the North Atlantic region. In the southern part of the range, we found high levels, but geographically quite poorly structured genetic diversity, whereas the levels of genetic diversity varied among different areas in the north. North American populations were genetically very similar to the European populations. Main conclusions The data are consistent with extensive gene flow, which has obscured the recent history of the taxon. The limited differentiation in the south probably results from the mixing of lineages expanding from several local refugia. Northward post‐glacial colonization resulted in a leading‐edge pattern of low diversity in the Netherlands, Belgium, Scotland and Iceland, whereas the observed high diversity levels in Fennoscandia suggest broad‐fronted colonization from the south as well as from the east. The patterns found in the American populations are consistent with post‐glacial colonization, possibly even with anthropogenic introduction from Europe. Our data also suggest that the tussock‐forming populations of C. nigra, often referred to as a distinct species (Carex juncella), represent an ecotype that has originated repeatedly from different populations with creeping rhizomes.     

Molecular phylogeography of the microturbellarian Monocelis lineata (Platyhelminthes: Proseriata) in the North‐East Atlantic

Monocelis lineata is a complex of cryptic species (three in the Mediterranean and one in the Atlantic) widespread in midlittoral habitats. Throughout the range, populations with or without an ocular pigmented shield are found. We investigated the genetic structure of the North‐East Atlantic populations with the aim of shedding light on their phylogeography and reconstructing possible patterns of recolonization after the Würmian glaciation. Fourteen samples were investigated using cytochrome c oxidase subunit I (COI) and 13 by inter‐simple sequence repeats (ISSRs). COI did not exhibit a clear pattern of decreased genetic diversity along a latitudinal gradient. Populations from Ferrol (Spain), Doolin (Ireland), and Helsingør (Denmark) showed a higher genetic variability, whereas a reduction in the number of haplotypes was found at the northernmost edge of the distribution and in northern Ireland and Scotland. Two genetically differentiated areas (southern Europe and south‐western Ireland versus northern Atlantic) were revealed by ISSR data. The results obtained provided evidence of three refugia (Iberian Peninsula, south‐western Ireland, and North Sea), and the occurrence of secondary contacts that shaped the genetic variability of some of the populations examined. Two different recolonization pathways of north‐western Europe during the post‐Würmian glaciations have been detected. Furthermore, ISSR analysis provided evidence of genetic divergence among populations with and without pigmented eyespot, suggesting the action of ecological differentiation. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 117–135.     

Phylogeography,historical demography and habitat suitability modelling of freshwater fishes inhabiting seasonally fluctuating Mediterranean river systems: a case study using the Iberian cyprinid Squalius valentinus

The Mediterranean freshwater fish fauna has evolved under constraints imposed by the seasonal weather/hydrological patterns that define the Mediterranean climate. These conditions have influenced the genetic and demographic structure of aquatic communities since their origins in the Mid‐Pliocene. Freshwater species in Mediterranean‐type climates will likely constitute genetically well‐differentiated populations, to varying extents depending on basin size, as a consequence of fragmentation resulting from drought/flood cycles. We developed an integrative framework to study the spatial patterns in genetic diversity, demographic trends, habitat suitability modelling and landscape genetics, to evaluate the evolutionary response of Mediterranean‐type freshwater fish to seasonal fluctuations in weather. To test this evolutionary response, the model species used was Squalius valentinus, an endemic cyprinid of the Spanish Levantine area, where seasonal weather fluctuations are extreme, although our findings may be extrapolated to other Mediterranean‐type species. Our results underscore the significant role of the Mediterranean climate, along with Pleistocene glaciations, in diversification of S. valentinus. We found higher nuclear diversity in larger drainage basins, but higher mitochondrial diversity correlated to habitat suitability rather than basin size. We also found strong correlation between genetic structure and climatic factors associated with Mediterranean seasonality. Demographic and migration analyses suggested population expansion during glacial periods that also contributed to the current genetic structure of S. valentinus populations. The inferred models support the significant contribution of precipitation and temperature to S. valentinus habitat suitability and allow recognizing areas of habitat stability. We highlight the importance of stable habitat conditions, fostered by typical karstic springs found on the Mediterranean littoral coasts, for the preservation of freshwater species inhabiting seasonally fluctuating river systems.     

Northern glacial refugia and altitudinal niche divergence shape genome‐wide differentiation in the emerging plant model Arabidopsis arenosa

Quaternary climatic oscillations profoundly impacted temperate biodiversity. For many diverse yet undersampled areas, however, the consequences of this impact are still poorly known. In Europe, particular uncertainty surrounds the role of Balkans, a major hotspot of European diversity, in postglacial recolonization of more northerly areas, and the Carpathians, a debatable candidate for a northern ‘cryptic’ glacial refugium. Using genome‐wide SNPs and microsatellites, we examined how the interplay of historical processes and niche shifts structured genetic diversity of diploid Arabidopsis arenosa, a little‐known member of the plant model genus that occupies a wide niche range from sea level to alpine peaks across eastern temperate Europe. While the northern Balkans hosted one isolated endemic lineage, most of the genetic diversity was concentrated further north in the Pannonian Basin and the Carpathians, where it likely survived the last glaciation in northern refugia. Finally, a distinct postglacial environment in northern Europe was colonized by populations of admixed origin from the two Carpathian lineages. Niche differentiation along altitude‐related bioclimatic gradients was the main trend in the phylogeny of A. arenosa. The most prominent niche shifts, however, characterized genetically only slightly divergent populations that expanded into narrowly defined alpine and northern coastal postglacial environments. Our study highlights the role of eastern central European mountains not only as refugia for unique temperate diversity but also sources for postglacial expansion into novel high‐altitude and high‐latitude niches. Knowledge of distinct genetic substructure of diploid A. arenosa also opens new opportunities for follow‐up studies of this emerging model of evolutionary biology.     

The east‐west‐north colonization history of the Mediterranean and Europe by the coastal plant Carex extensa (Cyperaceae)

Coastal plants are ideal models for studying the colonization routes of species because of the simple linear distributions of these species. Carex extensa occurs mainly in salt marshes along the Mediterranean and European coasts. Variation in cpDNA sequences, amplified fragment length polymorphisms (AFLPs) and simple sequence repeats (SSRs) of 24 populations were analysed to reconstruct its colonization history. Phylogenetic relationships indicate that C. extensa together with the South American Carex vixdentata and the southern African Carex ecklonii form a monophyletic group of halophilic species. Analyses of divergence times suggest that early lineage diversification may have occurred between the late Miocene and the late Pliocene (Messinian crisis). Phylogenetic and network analyses of cpDNA variation revealed the monophyly of the species and an ancestral haplotype contained in populations of the eastern Mediterranean. The AFLP and SSR analyses support a pattern of variation compatible with these two lineages. These analyses also show higher levels of genetic diversity and differentiation in the eastern population group, which underwent an east‐to‐west Mediterranean colonization. Quaternary climatic oscillations appear to have been responsible for the split between these two lineages. Secondary contacts may have taken place in areas near the Ligurian Sea in agreement with the gene flow detected in Corsican populations. The AFLP and SSR data accord with the ‘tabula rasa’ hypothesis in which a recent and rapid colonization of northern Europe took place from the western Mediterranean after the Last Glacial Maximum. The unbalanced west‐east vs. west‐north colonization may be as a result of ‘high density blocking’ effect.     

Latitudinal divergence in a widespread amphibian: Contrasting patterns of neutral and adaptive genomic variation

Stochastic effects from demographic processes and selection are expected to shape the distribution of genetic variation in spatially heterogeneous environments. As the amount of genetic variation is central for long‐term persistence of populations, understanding how these processes affect variation over large‐scale geographical gradients is pivotal. We investigated the distribution of neutral and putatively adaptive genetic variation, and reconstructed demographic history in the moor frog (Rana arvalis) using 136 individuals from 15 populations along a 1,700‐km latitudinal gradient from northern Germany to northern Sweden. Using double digest restriction‐site associated DNA sequencing we obtained 27,590 single nucleotide polymorphisms (SNPs), and identified differentiation outliers and SNPs associated with growing season length. The populations grouped into a southern and a northern cluster, representing two phylogeographical lineages from different post‐glacial colonization routes. Hybrid index estimation and demographic model selection showed strong support for a southern and northern lineage and evidence of gene flow between regions located on each side of a contact zone. However, patterns of past gene flow over the contact zone differed between neutral and putatively adaptive SNPs. While neutral nucleotide diversity was higher along the southern than the northern part of the gradient, nucleotide diversity in differentiation outliers showed the opposite pattern, suggesting differences in the relative strength of selection and drift along the gradient. Variation associated with growing season length decreased with latitude along the southern part of the gradient, but not along the northern part where variation was lower, suggesting stronger climate‐mediated selection in the north. Outlier SNPs included loci involved in immunity and developmental processes.