Clinal Adaptation Research Articles

Detection of the local adaptive and genome-wide associated loci in southeast Nigerian taro (Colocasia esculenta (L.) Schott) populations

BackgroundTaro has a long history of being consumed and remains orphan and on the hand Nigeria farmers. The role of farmer-driven artificial selection is not negligible to fit landraces to a particular ecological condition. Limited study has been conducted on genome-wide association and no study has been conducted on genome-environment association for clinal adaptation for taro. Therefore, the objective of this study was to detect loci that are associated with environmental variables and phenotype traits and forward input to breeders. The study used 92 geographical referred taro landraces collected from Southeast (SE) Nigeria.ResultsThe result indicates that SE Nigerian taro has untapped phenotype and genetic variability with low admixture. Redundancy analysis indicated that collinear explained SNP variation more than single climatic variable. Overall, the results indicated that no single method exclusively was able to capture population confounding effects better than the others for all six traits. Nevertheless, based on overall model performance, Blink seemed to provide slight advantage over other models and was selected for all subsequent assessment of genome-environment association (GEA) and genome-wide association study (GWAS) models. Genome scan and GEA identified local adapted loci and co-located genes. A total of nine SNP markers associated with environmental variables. Some of the SNP markers (such as S_101024366) co-located with genes which previously reported for climatic adaptation such as astringency, diaminopimelate decarboxylase and MYB transcription factor. Genome-wide association also identified 45, 40 and 34 significant SNP markers associated with studied traits in combined, year 1 and year 2 data sets, respectively. Out of these, five SNP markers (S1_18891752 S3_100795476, S1_100584471 S1_100896936 and S2_10058799) were consistent in two different data sets.ConclusionsThe findings from this study improve our understanding of the genetic control of adaptive and phenotypic traits in Nigerian taro. However, the study suggests further study on identification of local adaptive loci and GWAS through collection of more landraces throughout the country, and across different agro-ecologies.

Phenology and plasticity can prevent adaptive clines in thermal tolerance across temperate mountains: The importance of the elevation-time axis.

Critical thermal limits (CTmax and CTmin) decrease with elevation, with greater change in CTmin, and the risk to suffer heat and cold stress increasing at the gradient ends. A central prediction is that populations will adapt to the prevailing climatic conditions. Yet, reliable support for such expectation is scant because of the complexity of integrating phenotypic, molecular divergence and organism exposure. We examined intraspecific variation of CTmax and CTmin, neutral variation for 11 microsatellite loci, and micro‐ and macro‐temperatures in larvae from 11 populations of the Galician common frog (Rana parvipalmata) across an elevational gradient, to assess (1) the existence of local adaptation through a PST‐FST comparison, (2) the acclimation scope in both thermal limits, and (3) the vulnerability to suffer acute heat and cold thermal stress, measured at both macro‐ and microclimatic scales. Our study revealed significant microgeographic variation in CTmax and CTmin, and unexpected elevation gradients in pond temperatures. However, variation in CTmax and CTmin could not be attributed to selection because critical thermal limits were not correlated to elevation or temperatures. Differences in breeding phenology among populations resulted in exposure to higher and more variable temperatures at mid and high elevations. Accordingly, mid‐ and high‐elevation populations had higher CTmax and CTmin plasticities than lowland populations, but not more extreme CTmax and CTmin. Thus, our results support the prediction that plasticity and phenological shifts may hinder local adaptation, promoting thermal niche conservatism. This may simply be a consequence of a coupled variation of reproductive timing with elevation (the “elevation‐time axis” for temperature variation). Mid and high mountain populations of R. parvipalmata are more vulnerable to heat and cool impacts than lowland populations during the aquatic phase. All of this contradicts some of the existing predictions on adaptive thermal clines and vulnerability to climate change in elevational gradients.

Distinct signals of clinal and seasonal allele frequency change at eQTLs in Drosophila melanogaster.

Populations of short-lived organisms can respond to spatial and temporal environmental heterogeneity through local adaptation. Local adaptation can be reflected on both phenotypic and genetic levels, and it has been documented in many organisms. Although complex fitness-related phenotypes have been shown to vary across latitudinal clines and seasons in similar ways in Drosophila melanogaster populations, the comparative signals of local adaptation across space and time remain poorly understood. Here, we examined patterns of allele frequency change across a latitudinal cline and between seasons at previously reported expression quantitative trait loci (eQTLs). We divided eQTLs into groups by using differential expression profiles of fly populations collected across latitudinal clines or exposed to different environmental conditions. In general, we find that eQTLs are enriched for clinally varying polymorphisms, and that these eQTLs change in frequency in concordant ways across the cline and in response to starvation and chill-coma. The enrichment of eQTLs among seasonally varying polymorphisms is more subtle, and the direction of allele frequency change at eQTLs appears to be somewhat idiosyncratic. Taken together, we suggest that clinal adaptation at eQTLs is at least partially distinct from seasonal adaptation.

The evolution of thermal performance in native and invasive populations of Mimulus guttatus.

The rise of globalization has spread organisms beyond their natural range, allowing further opportunity for species to adapt to novel environments and potentially become invaders. Yet, the role of thermal niche evolution in promoting the success of invasive species remains poorly understood. Here, we use thermal performance curves (TPCs) to test hypotheses about thermal adaptation during the invasion process. First, we tested the hypothesis that if species largely conserve their thermal niche in the introduced range, invasive populations may not evolve distinct TPCs relative to native populations, against the alternative hypothesis that thermal niche and therefore TPC evolution has occurred in the invasive range. Second, we tested the hypothesis that clines of TPC parameters are shallower or absent in the invasive range, against the alternative hypothesis that with sufficient time, standing genetic variation, and temperature‐mediated selection, invasive populations would re‐establish clines found in the native range in response to temperature gradients. To test these hypotheses, we built TPCs for 18 native (United States) and 13 invasive (United Kingdom) populations of the yellow monkeyflower, Mimulus guttatus. We grew clones of multiple genotypes per population at six temperature regimes in growth chambers. We found that invasive populations have not evolved different thermal optima or performance breadths, providing evidence for evolutionary stasis of thermal performance between the native and invasive ranges after over 200 years post introduction. Thermal optimum increased with mean annual temperature in the native range, indicating some adaptive differentiation among native populations that was absent in the invasive range. Further, native and invasive populations did not exhibit adaptive clines in thermal performance breadth with latitude or temperature seasonality. These findings suggest that TPCs remained unaltered post invasion, and that invasion may proceed via broad thermal tolerance and establishment in already climatically suitable areas rather than rapid evolution upon introduction.

Environmental patterns of adaptation after range expansion in Leontodon longirostris: The effect of phenological events on fitness-related traits.

Because of expected range shifts associated with climate change, there is a renewed interest in the evolutionary factors constraining adaptation, among which are genetic bottlenecks, drift, and increased mutational load after range expansion. Here we study adaptation in the short-lived species Leontodon longirostris showing reduced genetic diversity and increased genetic load along an expansion route. We assessed the phenological patterns of variation, and their effect on fitness-related traits, on 42 L. longirostris populations and six populations of the sister taxa L. saxatilis in a common garden located within the current range of both species. The comparison among L. longirostris populations allowed us to test for genetic clines consistent with local adaptation, whereas the comparison between taxa provided evidence for common adaptive features at the species level. We found significant within-species variability for most traits, as well as differences with its close relative L. saxatilis. In general, seeds from drier, warmer, and unpredictable habitats showed overall lower and more restricted conditions for germination, seedlings emerged later and plants flowered earlier. Consequently, genotypes from arid and unpredictable environments attained smaller reproductive sizes and allocated more biomass to reproduction. Flowering time had the strongest direct effect on total plant size, but seedling emergence also showed an important indirect effect. Our results show the crucial role of phenological patterns in shaping adaptive clines for major life-history stage transitions. Furthermore, the genetic load observed in L. longirostris does not seem to preclude adaptation to the climatic variability encountered along the expansion route.

Intragenomic Conflict between Knob Heterochromatin and B Chromosomes Is the Key to Understand Genome Size Variation along Altitudinal Clines in Maize.

In maize, we studied the causes of genome size variation and their correlates with cultivation altitude that suggests the existence of adaptive clines. To discuss the biological role of the genome size variation, we focused on Bolivian maize landraces growing along a broad altitudinal range. These were analyzed together with previously studied populations from altitudinal clines of Northwestern Argentina (NWA). Bolivian populations exhibited numerical polymorphism for B chromosomes (Bs) (from 1 to 5), with frequencies varying from 16.6 to 81.8 and being positively correlated with cultivation altitude. The 2C values of individuals 0B (A-DNA) ranged between 4.73 and 7.71 pg, with 58.33% of variation. The heterochromatic knobs, detected by DAPI staining, were more numerous and larger in individuals 0B than in those with higher doses of Bs. Bolivian and NWA landraces exhibited the same pattern of A-DNA downsizing and fewer and smaller knobs with increasing cultivation altitude, suggesting a mechanistic link among heterochromatin, genome size and phenology. The negative association between the two types of supernumerary DNA (knob heterochromatin and Bs), mainly responsible for the genome size variation, may be considered as an example of intragenomic conflict. It could be postulated that the optimal nucleotype is the result of such conflict, where genome adjustment may lead to an appropriate length of the vegetative cycle for maize landraces growing across altitudinal clines.

Molecular signatures of local adaptation to light in Norway spruce

Main conclusionTranscriptomic and exome capture analysis reveal an adaptive cline for shade tolerance in Norway spruce. Genes involved in the lignin pathway and immunity seem to play a potential role in contributing towards local adaptation to light.The study of natural variation is an efficient method to elucidate how plants adapt to local climatic conditions, a key process for the evolution of a species. Norway spruce is a shade-tolerant conifer in which the requirement of far-red light for growth increases latitudinally northwards. The objective of the study is to characterize the genetic control of local adaptation to light enriched in far-red in Norway spruce, motivated by a latitudinal gradient for the Red:Far-red (R:FR) ratio to which Norway spruce has been proven to be genetically adapted. We have established the genomic signatures of local adaptation by conducting transcriptomic (total RNA-sequencing) and genomic analyses (exome capture), for the identification of genes differentially regulated along the cline. RNA-sequencing revealed 274 differentially expressed genes in response to SHADE (low R:FR light), between the southern and northern natural populations in Sweden. Exome capture included analysis of a uniquely large data set (1654 trees) that revealed missense variations in coding regions of nine differentially expressed candidate genes, which followed a latitudinal cline in allele and genotype frequencies. These genes included five transcription factors involved in vital processes like bud-set/bud-flush, lignin pathway, and cold acclimation and other genes that take part in cell-wall remodeling, secondary cell-wall thickening, response to starvation, and immunity. Based on these results, we suggest that the northern populations might not only be able to adjust their growing season in response to low R:FR light, but they may also be better adapted towards disease resistance by up-regulation of the lignin pathway that is linked to immunity. This forms a concrete basis for local adaptation to light quality in Norway spruce, one of the most economically important conifer tree species in Sweden.

Climate drives intraspecific differentiation in the expression of growth-defence trade-offs in a long-lived pine species

Intraspecific variation in plant defences is expected to be the result of adaptive and plastic responses to environmental conditions, where trade-offs between growth and defences are thought to play a key role shaping phenotypic patterns in defensive investment. Axial resin ducts are costly defensive structures that remain imprinted in the tree rings of conifers, therefore being a valuable proxy of defensive investment along the trees’ lifespan. We aimed to disentangle climate-driven adaptive clines and plastic responses to both spatial and temporal environmental variation in resin duct production, and to explore growth-defence trade-offs. To that aim, we applied dendrochronological procedures to quantify annual growth and resin duct production during a 31-year-period in a Mediterranean pine species, including trees from nine populations planted in two common gardens. Both genetic factors and plastic responses modulated annual resin duct production. However, we found no evidence of adaptive clines with climate gradients driving population differentiation. Our results revealed a marked physiological trade-off between growth and defences, where the slope of the trade-off was genetically variable and associated with climatic gradients. Our results help to enlighten the evolutionary patterns and genetic basis of defensive allocation within species, particularly revealing a key role of growth-defence trade-offs.

Gene Flow Limits Adaptation along Steep Environmental Gradients

When environmental variation is spatially continuous, dispersing individuals move among nearby sites with similar habitat conditions. But as an environmental gradient becomes steeper, gene flow may connect more divergent habitats, and this is predicted to reduce the slope of the adaptive cline that evolves. We compared quantitative genetic divergence of Rana temporaria frog populations along a 2,000-m elevational gradient in eastern Switzerland (new experimental results) with divergence along a 1,550-km latitudinal gradient in Fennoscandia (previously published results). Both studies found significant countergradient variation in larval development rate (i.e., animals from cold climates developed more rapidly). The cline was weaker with elevation than with latitude. Animals collected on both gradients were genotyped at ∼2,000 single-nucleotide polymorphism markers, revealing that dispersal distance was 30% farther on the latitudinal gradient but 3.9 times greater with respect to environmental conditions on the elevational gradient. A meta-analysis of 19 experimental studies of anuran populations spanning temperature gradients revealed that countergradient variation in larval development, while significant overall, was weaker when measured on steeper gradients. These findings support the prediction that adaptive population divergence is less pronounced, and maladaptation more pervasive, on steep environmental gradients.

Rapid growth and defence evolution following multiple introductions.

Rapid adaptation can aid invasive populations in their competitive success. Resource allocation trade‐off hypotheses predict higher resource availability or the lack of natural enemies in introduced ranges allow for increased growth and reproduction, thus contributing to invasive success. Evidence for such hypotheses is however equivocal and tests among multiple ranges over productivity gradients are required to provide a better understanding of the general applicability of these theories.Using common gardens, we investigated the adaptive divergence of various constitutive and inducible defence‐related traits between the native North American and introduced European and Australian ranges, while controlling for divergence due to latitudinal trait clines, individual resource budgets, and population differentiation, using >11,000 SNPs.Rapid, repeated clinal adaptation in defence‐related traits was apparent despite distinct demographic histories. We also identified divergence among ranges in some defence‐related traits, although differences in energy budgets among ranges may explain some, but not all, defence‐related trait divergence. We do not identify a general reduction in defence in concert with an increase in growth among the multiple introduced ranges as predicted trade‐off hypotheses. Synthesis: The rapid spread of invasive species is affected by a multitude of factors, likely including adaptation to climate and escape from natural enemies. Unravelling the mechanisms underlying invasives' success enhances understanding of eco‐evolutionary theory and is essential to inform management strategies in the face of ongoing climate change. OPEN RESEARCH BADGES This article has been awarded Open Materials, Open Data, Preregistered Research Designs Badges. All materials and data are publicly accessible via the Open Science Framework at https://doi.org/10.6084/m9.figshare.8028875.v1, https://github.com/lotteanna/defence_adaptation,https://doi.org/10.1101/435271.

Quantifying the relative contributions of the X chromosome, autosomes, and mitochondrial genome to local adaptation.

During local adaptation with gene flow, some regions of the genome are inherently more responsive to selection than others. Recent theory predicts that X-linked genes should disproportionately contribute to local adaptation relative to other genomic regions, yet this prediction remains to be tested. We carried out a multigeneration crossing scheme, using two cline-end populations of Drosophila melanogaster, to estimate the relative contributions of the X chromosome, autosomes, and mitochondrial genome to divergence in four traits involved in local adaptation (wing size, resistance to heat, desiccation, and starvation stresses). We found that the mitochondrial genome and autosomes contributed significantly to clinal divergence in three of the four traits. In contrast, the X made no significant contribution to divergence in these traits. Given the small size of the mitochondrial genome, our results indicate that it plays a surprisingly large role in clinal adaptation. In contrast, the X, which represents roughly 20% of the Drosophila genome, contributes negligibly-a pattern that conflicts with theoretical predictions. These patterns reinforce recent work implying a central role of mitochondria in climatic adaptation, and suggest that different genomic regions may play fundamentally different roles in processes of divergence with gene flow.

Genomic Signatures of Adaptation to a Precipitation Gradient in Nigerian Sorghum.

Evolution of plants under climatic gradients may lead to clinal adaptation. Understanding the genomic basis of clinal adaptation in crops species could facilitate breeding for climate resilience. We investigated signatures of clinal adaptation in the cereal crop sorghum (Sorghum bicolor L. [Moench]) to the precipitation gradient in West Africa using a panel (n = 607) of sorghum accessions from diverse agroclimatic zones of Nigeria. Significant correlations were observed between common-garden phenotypes of three putative climate-adaptive traits (flowering time, plant height, and panicle length) and climatic variables. The panel was characterized at >400,000 single nucleotide polymorphisms (SNPs) using genotyping-by-sequencing (GBS). Redundancy analysis indicated that a small proportion of SNP variation can be explained by climate (1%), space (1%), and climate collinear with space (3%). Discriminant analysis of principal components identified three genetic groups that are distributed differently along the precipitation gradient. Genome-wide association studies were conducted with phenotypes and three climatic variables (annual mean precipitation, precipitation in the driest quarter, and annual mean temperature). There was no overall enrichment of associations near a priori candidate genes implicated in flowering time, height, and inflorescence architecture in cereals, but several significant associations were found near a priori candidates including photoperiodic flowering regulators SbCN12 and Ma6. Together, the findings suggest that a small (3%) but significant proportion of nucleotide variation in Nigerian sorghum landraces reflects clinal adaptation along the West African precipitation gradient.

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 FST 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.

Introgression from Populus balsamifera underlies adaptively significant variation and range boundaries in P.trichocarpa.

Introgression can be an important source of adaptive phenotypes, although conversely it can have deleterious effects. Evidence for adaptive introgression is accumulating but information on the genetic architecture of introgressed traits lags behind. Here we determine trait architecture in Populus trichocarpa under introgression from P.balsamifera using admixture mapping and phenotypic analyses. Our results reveal that admixture is a key driver of clinal adaptation and suggest that the northern range extension of P.trichocarpa depends, at least in part, on introgression from P.balsamifera. However, admixture with P.balsamifera can lead to potentially maladaptive early phenology, and a reduction in growth and disease resistance in P.trichocarpa. Strikingly, an introgressed chromosome 9 haplotype block from P.balsamifera restores the late phenology and high growth parental phenotype in admixed P.trichocarpa. This epistatic restorer block may be strongly advantageous in maximizing carbon assimilation and disease resistance in the southernmost populations where admixture has been detected. We also confirm a previously demonstrated case of adaptive introgression in chromosome 15 and show that introgression generates a transgressive chlorophyll-content phenotype. We provide strong support that introgression provides a reservoir of genetic variation associated with adaptive characters that allows improved survival in new environments.

Breakdown of a geographic cline explains high performance of introduced populations of a weedy invader

Abstract What drives the evolution of increased growth and fecundity in plants introduced to a novel range is not well understood. We investigate between‐range differences in performance for Verbascum thapsus, a weedy invader known to grow larger in its introduced than native range. Specifically, we question whether adaptation to herbivory or climate best explains increased performance of introduced populations. We grew 14 native and 22 introduced populations of V. thapsus in two common garden locations: near Prague, Czech Republic (native range) and in Colorado, USA (introduced range). By removing herbivores from half of the plants within each garden we tested the prediction of the evolution of increased competitive ability (EICA) hypothesis: increased performance is driven by an evolutionary shift of resources away from defence against herbivory towards growth and reproduction. We then investigated whether genetically based clines in performance are expressed along climate gradients within both the native and introduced ranges. On average, seeds produce larger rosettes when collected from the introduced vs. native range. While this evolution of increased growth in introduced populations in part matches the prediction of EICA, climate, not herbivory, best explains this between‐range difference. Specifically, seeds collected from the native range produce smaller rosettes as the climate of origin becomes cooler and drier, while there is no cline in performance in rosettes grown from seed collected from the introduced range, which are large regardless of climate of origin. Thus, a climate‐based cline within the native range best explains lower average performance of native compared to introduced populations. Synthesis. The breakdown in a potentially adaptive cline emphasizes the need to more closely investigate the evolutionary processes that shape geographic structuring (or its absence) within the introduced range. In addition, EICA is not universally applicable to all invasion scenarios, and our findings underscore the importance of testing the underlying assumptions alongside the predictions of this hypothesis.

Genomics of clinal variation in Drosophila: disentangling the interactions of selection and demography.

Clines in phenotypes and genotype frequencies across environmental gradients are commonly taken as evidence for spatially varying selection. Classical examples include the latitudinal clines in various species of Drosophila, which often occur in parallel fashion on multiple continents. Today, genomewide analysis of such clinal systems provides a fantastic opportunity for unravelling the genetics of adaptation, yet major challenges remain. A well-known but often neglected problem is that demographic processes can also generate clinality, independent of or coincident with selection. A closely related issue is how to identify true genic targets of clinal selection. In this issue of Molecular Ecology, three studies illustrate these challenges and how they might be met. Bergland etal. report evidence suggesting that the well-known parallel latitudinal clines in North American and Australian D.melanogaster are confounded by admixture from Africa and Europe, highlighting the importance of distinguishing demographic from adaptive clines. In a companion study, Machado etal. provide the first genomic comparison of latitudinal differentiation in D.melanogaster and its sister species D.simulans. While D.simulans is less clinal than D.melanogaster, a significant fraction of clinal genes is shared between both species, suggesting the existence of convergent adaptation to clinaly varying selection pressures. Finally, by drawing on several independent sources of evidence, Božičević etal. identify a functional network of eight clinal genes that are likely involved in cold adaptation. Together, these studies remind us that clinality does not necessarily imply selection and that separating adaptive signal from demographic noise requires great effort and care.

The geography of sex-specific selection, local adaptation, and sexual dimorphism.

Local adaptation and sexual dimorphism are iconic evolutionary scenarios of intraspecific adaptive differentiation in the face of gene flow. Although theory has traditionally considered local adaptation and sexual dimorphism as conceptually distinct processes, emerging data suggest that they often act concurrently during evolutionary diversification. Here, I merge theories of local adaptation in space and sex-specific adaptation over time, and show that their confluence yields several new predictions about the roles of context-specific selection, migration, and genetic correlations, in adaptive diversification. I specifically revisit two influential predictions from classical studies of clinal adaptation and sexual dimorphism: (1) that local adaptation should decrease with distance from the species' range center and (2) that opposing directional selection between the sexes (sexual antagonism) should inevitably accompany the evolution of sexual dimorphism. I show that both predictions can break down under clinally varying selection. First, the geography of local adaptation can be sexually dimorphic, with locations of relatively high local adaptation differing profoundly between the sexes. Second, the intensity of sexual antagonism varies across the species' range, with subpopulations near the range center representing hotspots for antagonistic selection. The results highlight the context-dependent roles of migration versus sexual conflict as primary constraints to adaptive diversification.

Adaptive cyanogenesis clines evolve recurrently through geographical sorting of existing gene deletions

Identifying the genetic basis of parallel phenotypic evolution provides insight into the process of adaptation and evolutionary constraint. White clover (Trifolium repens) has evolved climate-associated adaptive clines in cyanogenesis (the ability to produce hydrogen cyanide upon tissue damage) in several world regions where it has been introduced. Gene-deletion polymorphisms at the CYP79D15 and Li loci underlie the presence/absence of the cyanogenic phenotype. Both loci have undergone multiple independent gene-deletion events, which are identifiable through molecular signatures in flanking regions. To investigate whether cyanogenesis clines in introduced populations have evolved through the sorting of standing genetic variation or de novo gene deletions, we examined cyanogenesis gene-flanking regions in three world regions. In comparison with native Eurasian populations, we find no evidence for novel gene deletion events in any introduced region, which suggests that these adaptive clines have evolved through the geographical sorting of pre-existing genetic variation.

Differentiating genetic and environmental drivers of plant–pathogen community interactions

Summary Plant genotypic variation can shape associated arthropod and microbial communities locally, as has been demonstrated in controlled common garden experiments. However, the relative roles of plant genetics and the environment in defining communities at larger spatial scales are not well known. The environmental heterogeneity hypothesis maintains that plant genetic effects on associated communities diminish across the landscape as environmental variation predominates. Alternatively, the local adaptation hypothesis argues that plant genetic effects change across landscapes as a result of species interactions being locally adapted. Thus, very different mechanisms could produce similar patterns. Using replicated common gardens located along an elevation and distance gradient, observational studies in the wild, and a greenhouse inoculation experiment, we examined these two non‐mutually exclusive hypotheses for Populus angustifolia and its fungal leaf pathogen community. Supporting the environmental heterogeneity hypothesis, plant genotypic effects on fungal leaf pathogen communities were two to three times stronger within than among gardens. Consistent with the local adaptation hypothesis, plant genotypic effects on pathogens also varied significantly among gardens (i.e. G × E interaction effect). Observational data from the wild and our greenhouse inoculation experiment unveiled clinal adaptation in plant genetic resistance that is correlated with disease risk along the elevation gradient, but did not support local pathogen adaptation to plants or vice versa. Synthesis. While our study found that plant genotype plays a significant role in shaping associated pathogen communities at local and geographic scales, the environment most strongly influenced P. angustifolia leaf pathogens at the geographic scale. Plant genetic effects on pathogens were also influenced by the environment, highlighting the potential for environmental (e.g. climate) change to trigger local evolutionary responses in plant–pathogen community interactions.

Genetically based latitudinal variation in Artemisia californica secondary chemistry

Steep climatic gradients may select for clinal adaptation in plant functional traits with implications for interspecific interactions and response to future climate change. Terpenes are common in Mediterranean environments and mediate plant interactions with both the abiotic and biotic environment, including herbivores. Clines in traits such as terpenes have received much attention because they are linked to plant fitness and experience strong selection from the abiotic and biotic environment. In this study, we tested for intraspecific variation in Artemisia californica terpene chemistry in a common garden of plants sourced from populations spanning a large precipitation gradient (6° latitude) and grown in treatments of high and low precipitation. We found genetic variation in terpene richness, diversity, concentration and composition among A. californica populations spanning this species’ range. Of these traits, terpene composition and monoterpene concentration varied clinally with respect to source site latitude. Regarding terpene composition, pairwise dissimilarity among populations increased in parallel with geographic distance between source sites. At the same time, monoterpene concentration decreased monotonically from plants of southern origin (source sites with high temperature, aridity, and precipitation variability) to plants of northern origin. Our precipitation manipulation suggests that phenotypic selection by precipitation may underlie this clinal variation in monoterpene concentration, and that monoterpene concentration and other aspects of terpene chemistry are not phenotypically plastic. In summary, this study provides novel evidence for a genetically based latitudinal cline in plant secondary chemistry and suggests that adaptation to a key aspect of the abiotic environment may contribute to this intraspecific variation. Accordingly, changes in terpene chemistry under projected future climates will likely occur solely through the relatively slow process of adaptation, with important consequences for plant interactions with the abiotic environment and a diverse community of associates.