Range margin populations show high climate adaptation lags in European trees

How populations of long‐living species respond to climate change depends on phenotypic plasticity and local adaptation processes. Marginal populations are expected to have lags in adaptation (i.e. differences between the climatic optimum that maximizes population fitness and the local climate) because they receive pre‐adapted alleles from core populations preventing them from reaching a local optimum in their climatically marginal habitat. Yet, whether adaptation lags in marginal populations are a common feature across phylogenetically and ecologically different species and how lags can change with climate change remain unexplored. To test for range‐wide patterns of phenotypic variation and adaptation lags of populations to climate, we (a) built model ensembles of tree height accounting for the climate of population origin and the climate of the site for 706 populations monitored in 97 common garden experiments covering the range of six European forest tree species; (b) estimated populations' adaptation lags as the differences between the climatic optimum that maximizes tree height and the climate of the origin of each population; (c) identified adaptation lag patterns for populations coming from the warm/dry and cold/wet margins and from the distribution core of each species range. We found that (a) phenotypic variation is driven by either temperature or precipitation; (b) adaptation lags are consistently higher in climatic margin populations (cold/warm, dry/wet) than in core populations; (c) predictions for future warmer climates suggest adaptation lags would decrease in cold margin populations, slightly increasing tree height, while adaptation lags would increase in core and warm margin populations, sharply decreasing tree height. Our results suggest that warm margin populations are the most vulnerable to climate change, but understanding how these populations can cope with future climates depend on whether other fitness‐related traits could show similar adaptation lag patterns.     

Adaptive population divergence and directional gene flow across steep elevational gradients in a climate‐sensitive mammal

The ecological effects of climate change have been shown in most major taxonomic groups; however, the evolutionary consequences are less well‐documented. Adaptation to new climatic conditions offers a potential long‐term mechanism for species to maintain viability in rapidly changing environments, but mammalian examples remain scarce. The American pika (Ochotona princeps) has been impacted by recent climate‐associated extirpations and range‐wide reductions in population sizes, establishing it as a sentinel mammalian species for climate change. To investigate evidence for local adaptation and reconstruct patterns of genomic diversity and gene flow across rapidly changing environments, we used a space‐for‐time design and restriction site‐associated DNA sequencing to genotype American pikas along two steep elevational gradients at 30,966 SNPs and employed independent outlier detection methods that scanned for genotype‐environment associations. We identified 338 outlier SNPs detected by two separate analyses and/or replicated in both transects, several of which were annotated to genes involved in metabolic function and oxygen transport. Additionally, we found evidence of directional gene flow primarily downslope from high‐elevation populations, along with reduced gene flow at outlier loci. If this trend continues, elevational range contractions in American pikas will likely be from local extirpation rather than upward movement of low‐elevation individuals; this, in turn, could limit the potential for adaptation within this landscape. These findings are of particular relevance for future conservation and management of American pikas and other elevationally restricted, thermally sensitive species.     

The genomic footprint of climate adaptation in Chironomus riparius

The gradual heterogeneity of climatic factors poses varying selection pressures across geographic distances that leave signatures of clinal variation in the genome. Separating signatures of clinal adaptation from signatures of other evolutionary forces, such as demographic processes, genetic drift and adaptation, to nonclinal conditions of the immediate local environment is a major challenge. Here, we examine climate adaptation in five natural populations of the harlequin fly Chironomus riparius sampled along a climatic gradient across Europe. Our study integrates experimental data, individual genome resequencing, Pool‐Seq data and population genetic modelling. Common‐garden experiments revealed significantly different population growth rates at test temperatures corresponding to the population origin along the climate gradient, suggesting thermal adaptation on the phenotypic level. Based on a population genomic analysis, we derived empirical estimates of historical demography and migration. We used an F_ST outlier approach to infer positive selection across the climate gradient, in combination with an environmental association analysis. In total, we identified 162 candidate genes as genomic basis of climate adaptation. Enriched functions among these candidate genes involved the apoptotic process and molecular response to heat, as well as functions identified in studies of climate adaptation in other insects. Our results show that local climate conditions impose strong selection pressures and lead to genomic adaptation despite strong gene flow. Moreover, these results imply that selection to different climatic conditions seems to converge on a functional level, at least between different insect species.     

Genetic differentiation across a latitudinal gradient in two co-occurring butterfly species: revealing population differences in a context of climate change

Genetic differentiation within a species' range is determined by natural selection, genetic drift, and gene flow. Selection and drift enhance genetic differences if populations are sufficiently isolated, while gene flow precludes differentiation and local adaptation. Over large geographical areas, these processes can create a variety of scenarios, ranging from admixture to a high degree of population differentiation. Genetic differences among populations may signal functional differences within a species' range, potentially leading to population or ecotype-specific responses to global change. We investigated differentiation within the geographical range of two butterfly species along a broad latitudinal gradient. This gradient is the primary axis of climatic variation, and many ecologists expect populations at the poleward edge of this gradient to expand under climate change. Our study species inhabit a shared ecosystem and differ in body size and resource specialization; both also find their poleward range limit on an island. We find evidence for divergence of peripheral populations from the core in both taxa, suggesting the potential for genetic distinctiveness at the leading edge of climate change. We also find differences between the species in the extent of peripheral differentiation with the smaller and more specialized species showing greater population divergence (microsatellites and mtDNA) and reduced gene flow (mtDNA). Finally, gene flow estimates in both species differed strongly between two marker types. These findings suggest caution in assuming that populations are invariant across latitude and thus will respond as a single ecotype to climatic change.     

The challenge of separating signatures of local adaptation from those of isolation by distance and colonization history: The case of two white pines

Accurately detecting signatures of local adaptation using genetic‐environment associations (GEAs) requires controlling for neutral patterns of population structure to reduce the risk of false positives. However, a high degree of collinearity between climatic gradients and neutral population structure can greatly reduce power, and the performance of GEA methods in such case is rarely evaluated in empirical studies. In this study, we attempted to disentangle the effects of local adaptation and isolation by environment (IBE) from those of isolation by distance (IBD) and isolation by colonization from glacial refugia (IBC) using range‐wide samples in two white pine species. For this, SNPs from 168 genes, including 52 candidate genes for growth and phenology, were genotyped in 133 and 61 populations of Pinus strobus and P. monticola, respectively. For P. strobus and using all 153 SNPs, climate (IBE) did not significantly explained among‐population variation when controlling for IBD and IBC in redundancy analyses (RDAs). However, 26 SNPs were significantly associated with climate in single‐locus GEA analyses (Bayenv2 and LFMM), suggesting that local adaptation took place in the presence of high gene flow. For P. monticola, we found no evidence of IBE using RDAs and weaker signatures of local adaptation using GEA and F_ST outlier tests, consistent with adaptation via phenotypic plasticity. In both species, the majority of the explained among‐population variation (69 to 96%) could not be partitioned between the effects of IBE, IBD, and IBC. GEA methods can account differently for this confounded variation, and this could explain the small overlap of SNPs detected between Bayenv2 and LFMM. Our study illustrates the inherent difficulty of taking into account neutral structure in natural populations and the importance of sampling designs that maximize climatic variation, while minimizing collinearity between climatic gradients and neutral structure.     

Predicting persistence in a changing climate: flow direction and limitations to redistribution

Synthesis Impending climate changes beg the question: which populations and species will go extinct and which will persist under future environmental conditions? When tolerance in situ is not possible, then species must undergo range shifts to avoid extinction. This synthesis explores ways in which directional air and water flow could impede such redistribution and the characteristics that might allow species to disperse against the flow. Considering flow patterns in tandem with climate and range projections has the potential to improve predictions of persistence for the earth’s many non‐moving foundation and basal species as well as the communities and food webs that they support. Predicting which populations and species will persist (i.e. avoid extinction and continue to exist) in the face of climate change requires an understanding of mechanisms that allow species to cope with altered environmental conditions. When processes of tolerance, acclimation, and adaptation are insufficient to allow persistence in situ, redistribution is required for population or species persistence. Here, I review evidence that directional flows of water and air have the potential to restrict species’ range boundaries under ambient conditions, the spread of introduced species, and the redistribution of native species under changing climatic conditions. I develop the hypothesis that flow patterns, such as the speed and directionality (i.e. poleward vs equatorward) of asymmetric air and water currents, may need to be considered when assessing the vulnerability of populations and species to climate change. To the degree that directional flows are found to limit redistribution, there may be disproportionate losses of diversity where the dominant flow direction opposes that of shifting climate space. Within this context, I highlight flow conditions and life‐history traits that could help the most passively‐dispersed species redistribute to track changing climate. These predictions merit further examination in order to better anticipate which populations, species, and associated communities are likely to persist under climate change.     

Topographic,latitudinal and climatic distribution of Pinus coulteri: geographic range limits are not at the edge of the climate envelope

With changing climate, many species are projected to move poleward or to higher elevations to track suitable climates. The prediction that species will move poleward assumes that geographically marginal populations are at the edge of the species' climatic range. We studied Pinus coulteri from the center to the northern (poleward) edge of its range, and examined three scenarios regarding the relationship between the geographic and climatic margins of a species' range. We used herbarium and iNaturalist.org records to identify P. coulteri sites, generated a species distribution model based on temperature, precipitation, climatic water deficit, and actual evapotranspiration, and projected suitability under future climate scenarios. In fourteen populations from the central to northern portions of the range, we conducted field studies and recorded elevation, slope and aspect (to estimate solar insolation) to examine relationships between local and regional distributions. We found that northern populations of P. coulteri do not occupy the cold or wet edge of the species' climatic range; mid‐latitude, high elevation populations occupy the cold margin. Aspect and insolation of P. coulteri populations changed significantly across latitudes and elevations. Unexpectedly, northern, low‐elevation stands occupy north‐facing aspects and receive low insolation, while central, high‐elevation stands grow on more south‐facing aspects that receive higher insolation. Modeled future climate suitability is projected to be highest in the central, high elevation portion of the species range, and in low‐lying coastal regions under some scenarios, with declining suitability in northern areas under most future scenarios. For P. coulteri, the lack of high elevation habitat combined with a major dispersal barrier may limit northward movement in response to a warming climate. Our analyses demonstrate the importance of distinguishing geographically vs. climatically marginal populations, and the importance of quantitative analysis of the realized climate space to understand species range limits.     

Signatures of environmental genetic adaptation pinpoint pathogens as the main selective pressure through human evolution

Previous genome-wide scans of positive natural selection in humans have identified a number of non-neutrally evolving genes that play important roles in skin pigmentation, metabolism, or immune function. Recent studies have also shown that a genome-wide pattern of local adaptation can be detected by identifying correlations between patterns of allele frequencies and environmental variables. Despite these observations, the degree to which natural selection is primarily driven by adaptation to local environments, and the role of pathogens or other ecological factors as selective agents, is still under debate. To address this issue, we correlated the spatial allele frequency distribution of a large sample of SNPs from 55 distinct human populations to a set of environmental factors that describe local geographical features such as climate, diet regimes, and pathogen loads. In concordance with previous studies, we detected a significant enrichment of genic SNPs, and particularly non-synonymous SNPs associated with local adaptation. Furthermore, we show that the diversity of the local pathogenic environment is the predominant driver of local adaptation, and that climate, at least as measured here, only plays a relatively minor role. While background demography by far makes the strongest contribution in explaining the genetic variance among populations, we detected about 100 genes which show an unexpectedly strong correlation between allele frequencies and pathogenic environment, after correcting for demography. Conversely, for diet regimes and climatic conditions, no genes show a similar correlation between the environmental factor and allele frequencies. This result is validated using low-coverage sequencing data for multiple populations. Among the loci targeted by pathogen-driven selection, we found an enrichment of genes associated to autoimmune diseases, such as celiac disease, type 1 diabetes, and multiples sclerosis, which lends credence to the hypothesis that some susceptibility alleles for autoimmune diseases may be maintained in human population due to past selective processes.     

Lineage‐specific adaptation to climate involves flowering time in North American Arabidopsis lyrata

Adaptation to local climatic conditions is commonly found within species, but whether it involves the same intraspecific genomic variants is unknown. We studied this question in North American Arabidopsis lyrata, whose current distribution is shaped by post‐glacial range expansion from two refugia, resulting in two distinct genetic clusters covering comparable climatic gradients. Using pooled whole‐genome sequence data of 41 outcrossing populations, we identified loci associated with three niche‐determining climatic variables in the two clusters and compared these outliers. Little evidence was found for parallelism in climate adaptation for single nucleotide polymorphisms (SNPs) and for genes with an accumulation of outlier SNPs. Significantly increased selection coefficients supported them as candidates of climate adaptation. However, the fraction of gene ontology (GO) terms shared between clusters was higher compared to outlier SNPs and outlier genes, suggesting that selection acts on similar pathways but not necessarily the same genes. Enriched GO terms involved responses to abiotic and biotic stress, circadian rhythm and development, with flower development and reproduction being among the most frequently detected. In line with GO enrichment, regulators of flowering time were detected as outlier genes. Our results suggest that while adaptation to environmental gradients on the genomic level are lineage‐specific in A. lyrata, similar biological processes seem to be involved. Differential loss of standing genetic variation, probably driven by genetic drift, can in part account for the lack of parallel evolution on the genomic level.     

Range position and climate sensitivity: The structure of among‐population demographic responses to climatic variation

Species’ distributions will respond to climate change based on the relationship between local demographic processes and climate and how this relationship varies based on range position. A rarely tested demographic prediction is that populations at the extremes of a species’ climate envelope (e.g., populations in areas with the highest mean annual temperature) will be most sensitive to local shifts in climate (i.e., warming). We tested this prediction using a dynamic species distribution model linking demographic rates to variation in temperature and precipitation for wood frogs (Lithobates sylvaticus) in North America. Using long‐term monitoring data from 746 populations in 27 study areas, we determined how climatic variation affected population growth rates and how these relationships varied with respect to long‐term climate. Some models supported the predicted pattern, with negative effects of extreme summer temperatures in hotter areas and positive effects on recruitment for summer water availability in drier areas. We also found evidence of interacting temperature and precipitation influencing population size, such as extreme heat having less of a negative effect in wetter areas. Other results were contrary to predictions, such as positive effects of summer water availability in wetter parts of the range and positive responses to winter warming especially in milder areas. In general, we found wood frogs were more sensitive to changes in temperature or temperature interacting with precipitation than to changes in precipitation alone. Our results suggest that sensitivity to changes in climate cannot be predicted simply by knowing locations within the species’ climate envelope. Many climate processes did not affect population growth rates in the predicted direction based on range position. Processes such as species‐interactions, local adaptation, and interactions with the physical landscape likely affect the responses we observed. Our work highlights the need to measure demographic responses to changing climate.     

Climatic breadth of calling behaviour in two widespread Neotropical frogs: Insights from humidity extremes

Climate change is severely altering precipitation regimes at local and global scales, yet the capacity of species to cope with these changes has been insufficiently examined. Amphibians are globally endangered and particularly sensitive to moisture conditions. For mating, most amphibian species rely on calling behaviour, which is a key weather‐dependent trait. Using passive acoustics, we monitored the calling behaviour of two widespread Neotropical frogs in 12 populations located at the humidity extremes but thermal mean of the species distribution. Based on 2,554 hr of recordings over a breeding season, we found that both the aquatic species Pseudis paradoxa and the arboreal species Boana raniceps exhibited calling behaviour at a wide range of relative humidity. Calling humidity was significantly lower in conspecific populations subjected to drier conditions, while calling temperature did not differ between populations or species. Overall, no variation in climatic breadth was observed between large and small choruses, and calling behaviour was scarcely detected during the driest, hottest and coldest potential periods of breeding. Our results showed that calling humidity of the studied species varies according to the precipitation regime, suggesting that widespread Neotropical anurans may have the capacity to exhibit sexual displays in different climatic environments. Regardless of the underlying mechanism (plasticity or local adaptation), which should be determined by common garden experiments, a wide and population‐specific climatic breadth of calling behaviour may assist species to deal with changing humidity conditions. To our knowledge, this is the first study to explore the response capacity of anurans to perform calling behaviour under contrasting precipitation regimes.     

Signatures of local adaptation in candidate genes of oaks (Quercus spp.) with respect to present and future climatic conditions

Testing how populations are locally adapted and predicting their response to their future environment is of key importance in view of climate change. Landscape genomics is a powerful approach to investigate genes and environmental factors involved in local adaptation. In a pooled amplicon sequencing approach of 94 genes in 71 populations, we tested whether >3500 single nucleotide polymorphisms (SNPs) in the three most common oak species in Switzerland (Quercus petraea, Q. pubescens, Q. robur) show an association with abiotic factors related to local topography, historical climate and soil characteristics. In the analysis including all species, the most frequently associated environmental factors were those best describing the habitats of the species. In the species‐specific analyses, the most important environmental factors and associated SNPs greatly differed among species. However, we identified one SNP and seven genes that were associated with the same environmental factor across all species. We finally used regressions of allele frequencies of the most strongly associated SNPs along environmental gradients to predict the risk of nonadaptedness (RONA), which represents the average change in allele frequency at climate‐associated loci theoretically required to match future climatic conditions. RONA is considerable for some populations and species (up to 48% in single populations) and strongly differs among species. Given the long generation time of oaks, some of the required allele frequency changes might not be realistic to achieve based on standing genetic variation. Hence, future adaptedness requires gene flow or planting of individuals carrying beneficial alleles from habitats currently matching future climatic conditions.     

A changing climate is eroding the geographical range of the Namib Desert tree Aloe through population declines and dispersal lags

While poleward species migration in response to recent climatic warming is widely documented, few studies have examined entire range responses of broadly distributed sessile organisms, including changes on both the trailing (equatorward) and the leading (poleward) range edges. From a detailed population census throughout the entire geographical range of Aloe dichotoma Masson, a long-lived Namib Desert tree, together with data from repeat photographs, we present strong evidence that a developing range shift in this species is a 'fingerprint' of anthropogenic climate change. This is explained at a high level of statistical significance by population level impacts of observed regional warming and resulting water balance constraints. Generalized linear models suggest that greater mortalities and population declines in equatorward populations are virtually certainly the result, due to anthropogenic climate change, of the progressive exceedance of critical climate thresholds that are relatively closer to the species' tolerance limits in equatorward sites. Equatorward population declines are also broadly consistent with bioclimatically modelled projections under anticipated anthropogenic climate change but, as yet, there is no evidence of poleward range expansion into the area predicted to become suitable in future, despite good evidence for positive population growth trends in poleward populations. This study is among the first to show a marked lag between trailing edge population extinction and leading edge range expansion in a species experiencing anthropogenic climate change impacts, a pattern likely to apply to most sessile and poorly dispersed organisms. This provides support for conservative assumptions of species' migration rates when modelling climate change impacts for such species. Aloe dichotoma 's response to climate change suggests that desert ecosystems may be more sensitive to climate change than previously suspected.     

Population genomic footprints of selection and associations with climate in natural populations of Arabidopsis halleri from the Alps

Natural genetic variation is essential for the adaptation of organisms to their local environment and to changing environmental conditions. Here, we examine genomewide patterns of nucleotide variation in natural populations of the outcrossing herb Arabidopsis halleri and associations with climatic variation among populations in the Alps. Using a pooled population sequencing (Pool‐Seq) approach, we discovered more than two million SNPs in five natural populations and identified highly differentiated genomic regions and SNPs using F_ST‐based analyses. We tested only the most strongly differentiated SNPs for associations with a nonredundant set of environmental factors using partial Mantel tests to identify topo‐climatic factors that may underlie the observed footprints of selection. Possible functions of genes showing signatures of selection were identified by Gene Ontology analysis. We found 175 genes to be highly associated with one or more of the five tested topo‐climatic factors. Of these, 23.4% had unknown functions. Genetic variation in four candidate genes was strongly associated with site water balance and solar radiation, and functional annotations were congruent with these environmental factors. Our results provide a genomewide perspective on the distribution of adaptive genetic variation in natural plant populations from a highly diverse and heterogeneous alpine environment.     

The response of two butterfly species to climatic variation at the edge of their range and the implications for poleward range shifts

To predict changes in species' distributions due to climate change we must understand populations at the poleward edge of species' ranges. Ecologists generally expect range shifts under climate change caused by the expansion of edge populations as peripheral conditions increasingly resemble the range core. We tested whether peripheral populations of two contrasting butterflies, a small-bodied specialist (Erynnis propertius) and a large-bodied generalist (Papilio zelicaon), respond favorably to warmer conditions. Performance of populations related to climate was evaluated in seven peripheral populations spanning 1.2 degrees latitude (160 km) using: (1) population density surveys, an indirect measure of site suitability; and (2) organismal fitness in translocation experiments. There was evidence that population density increased with temperature for P. zelicaon whose population density declined with latitude in 1 of 3 sample years. On the other hand, E. propertius showed a positive relationship of population density with latitude, apparently unrelated to climate or measured habitat variables. Translocation experiments showed increased larval production at increased temperatures for both species, and in P. zelicaon, larval production also increased under drier conditions. These findings suggest that both species may increase at their range edge with warming but the preference for core-like conditions may be stronger in P. zelicaon. Further, populations of E. propertius at the range boundary may be large enough to act as sources of colonists for range expansions, but range expansion in this species may be prevented by a lack of available host plants further north. In total, the species appear to respond differently to climate and other factors that vary latitudinally, factors that will likely affect poleward expansion.     

Reduced variability in range‐edge butterfly populations over three decades of climate warming

Populations at the high latitude edge of species’ geographical ranges are thought to show larger interannual population fluctuations, with subsequent higher local extinction risk, than those within the ‘core’ climatic range. As climate envelopes shift northward under climate warming, however, we would expect populations to show dampened variability. We test this hypothesis using annual abundance indices from 19 butterfly species across 79 British monitoring sites between 1976 and 2009, a period of climatic warming. We found that populations in the latter (warmer) half of the recording period show reduced interannual population variability. Species with more southerly European distributions showed the greatest dampening in population variability over time. Our results suggest that increases in population variability occur towards climatic range boundaries. British sites, previously existing at the margins of suitable climate space, now appear to fall closer to the core climatic range for many butterfly species.     

Latitudinal gradients in butterfly population variability are influenced by landscape heterogeneity

The variability of populations over time is positively associated with their risk of local extinction. Previous work has shown that populations at the high‐latitude boundary of species’ ranges show higher inter‐annual variability, consistent with increased sensitivity and exposure to adverse climatic conditions. However, patterns of population variability at both high‐ and low‐latitude species range boundaries have not yet been concurrently examined. Here, we assess the inter‐annual population variability of 28 butterfly species between 1994 and 2009 at 351 and 18 sites in the United Kingdom and Catalonia, Spain, respectively. Local population variability is examined with respect to the position of the species’ bioclimatic envelopes (i.e. whether the population falls within areas of the ‘core’ climatic suitability or is a climatically ‘marginal’ population), and in relation to local landscape heterogeneity, which may influence these range location – population dynamic relationships. We found that butterfly species consistently show latitudinal gradients in population variability, with increased variability in the more northerly UK. This pattern is even more marked for southerly distributed species with ‘marginal’ climatic suitability in the UK but ‘core’ climatic suitability in Catalonia. In addition, local landscape heterogeneity did influence these range location – population dynamic relationships. Habitat heterogeneity was associated with dampened population dynamics, especially for populations in the UK. Our results suggest that promoting habitat heterogeneity may promote the persistence of populations at high‐latitude range boundaries, which may potentially aid northwards expansion under climate warming. We did not find evidence that population variability increases towards southern range boundaries. Sample sizes for this region were low, but there was tentative evidence, in line with previous ecological theory, that local landscape heterogeneity may promote persistence in these retracting low‐latitude range boundary populations.     

Adaptation to climate through flowering phenology: a case study in Medicago truncatula

Local climatic conditions likely constitute an important selective pressure on genes underlying important fitness‐related traits such as flowering time, and in many species, flowering phenology and climatic gradients strongly covary. To test whether climate shapes the genetic variation on flowering time genes and to identify candidate flowering genes involved in the adaptation to environmental heterogeneity, we used a large Medicago truncatula core collection to examine the association between nucleotide polymorphisms at 224 candidate genes and both climate variables and flowering phenotypes. Unlike genome‐wide studies, candidate gene approaches are expected to enrich for the number of meaningful trait associations because they specifically target genes that are known to affect the trait of interest. We found that flowering time mediates adaptation to climatic conditions mainly by variation at genes located upstream in the flowering pathways, close to the environmental stimuli. Variables related to the annual precipitation regime reflected selective constraints on flowering time genes better than the other variables tested (temperature, altitude, latitude or longitude). By comparing phenotype and climate associations, we identified 12 flowering genes as the most promising candidates responsible for phenological adaptation to climate. Four of these genes were located in the known flowering time QTL region on chromosome 7. However, climate and flowering associations also highlighted largely distinct gene sets, suggesting different genetic architectures for adaptation to climate and flowering onset.     

Population genetic differentiation and genomic signatures of adaptation to climate in an abundant lizard

Species distributed across climatic gradients will typically experience spatial variation in selection, but gene flow can prevent such selection from causing population genetic differentiation and local adaptation. Here, we studied genomic variation of 415 individuals across 34 populations of the common wall lizard (Podarcis muralis) in central Italy. This species is highly abundant throughout this region and populations belong to a single genetic lineage, yet there is extensive phenotypic variation across climatic regimes. We used redundancy analysis to, first, quantify the effect of climate and geography on population genomic variation in this region and, second, to test if climate consistently sorts specific alleles across the landscape. Climate explained 5% of the population genomic variation across the landscape, about half of which was collinear with geography. Linear models and redundancy analyses identified loci that were significantly differentiated across climatic regimes. These loci were distributed across the genome and physically associated with genes putatively involved in thermal tolerance, regulation of temperature-dependent metabolism and reproductive activity, and body colouration. Together, these findings suggest that climate can exercise sufficient selection in lizards to promote genetic differentiation across the landscape in spite of high gene flow.Subject terms: Genetic variation, Genetic variation