Adaptive divergence along environmental gradients in a climate‐change‐sensitive mammal

In the face of predicted climate change, a broader understanding of biotic responses to varying environments has become increasingly important within the context of biodiversity conservation. Local adaptation is one potential option, yet remarkably few studies have harnessed genomic tools to evaluate the efficacy of this response within natural populations. Here, we show evidence of selection driving divergence of a climate‐change‐sensitive mammal, the American pika (Ochotona princeps), distributed along elevation gradients at its northern range margin in the Coast Mountains of British Columbia (BC), Canada. We employed amplified‐fragment‐length‐polymorphism‐based genomic scans to conduct genomewide searches for candidate loci among populations inhabiting varying environments from sea level to 1500 m. Using several independent approaches to outlier locus detection, we identified 68 candidate loci putatively under selection (out of a total 1509 screened), 15 of which displayed significant associations with environmental variables including annual precipitation and maximum summer temperature. These candidate loci may represent important targets for predicting pika responses to climate change and informing novel approaches to wildlife conservation in a changing world.     

Signatures of local adaptation along environmental gradients in a range‐expanding damselfly (Ischnura elegans)

Insect distributions are shifting rapidly in response to climate change and are undergoing rapid evolutionary change. We investigate the molecular signatures underlying local adaptation in the range‐expanding damselfly, Ischnura elegans. Using a landscape genomic approach combined with generalized dissimilarity modelling (GDM), we detect selection signatures on loci via allelic frequency change along environmental gradients. We analyse 13,612 single nucleotide polymorphisms (SNPs), derived from restriction site‐associated DNA sequencing (RADseq), in 426 individuals from 25 sites spanning the I. elegans distribution in Sweden, including its expanding northern range edge. Environmental association analysis (EAA) and the magnitude of allele frequency change along the range expansion gradient revealed significant signatures of selection in relation to high maximum summer temperature, high mean annual precipitation and low wind speeds at the range edge. SNP annotations with significant signatures of selection revealed gene functions associated with ongoing range expansion, including heat shock proteins (HSP40 and HSP70), ion transport (V‐ATPase) and visual processes (long‐wavelength‐sensitive opsin), which have implications for thermal stress response, salinity tolerance and mate discrimination, respectively. We also identified environmental thresholds where climate‐mediated selection is likely to be strong, and indicate that I. elegans is rapidly adapting to the climatic environment during its ongoing range expansion. Our findings empirically validate an integrative approach for detecting spatially explicit signatures of local adaptation along environmental gradients.     

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.     

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.     

Finding needles in a genomic haystack: targeted capture identifies clear signatures of selection in a nonmodel plant species

Teasing apart neutral and adaptive genomic processes and identifying loci that are targets of selection can be difficult, particularly for nonmodel species that lack a reference genome. However, identifying such loci and the factors driving selection have the potential to greatly assist conservation and restoration practices, especially for the management of species in the face of contemporary and future climate change. Here, we focus on assessing adaptive genomic variation within a nonmodel plant species, the narrow‐leaf hopbush (Dodonaea viscosa ssp. angustissima), commonly used for restoration in Australia. We used a hybrid‐capture target enrichment approach to selectively sequence 970 genes across 17 populations along a latitudinal gradient from 30°S to 36°S. We analysed 8462 single‐nucleotide polymorphisms (SNPs) for F_ST outliers as well as associations with environmental variables. Using three different methods, we found 55 SNPs with significant correlations to temperature and water availability, and 38 SNPs to elevation. Genes containing SNPs identified as under environmental selection were diverse, including aquaporin and abscisic acid genes, as well as genes with ontologies relating to responses to environmental stressors such as water deprivation and salt stress. Redundancy analysis demonstrated that only a small proportion of the total genetic variance was explained by environmental variables. We demonstrate that selection has led to clines in allele frequencies in a number of functional genes, including those linked to leaf shape and stomatal variation, which have been previously observed to vary along the sampled environmental cline. Using our approach, gene regions subject to environmental selection can be readily identified for nonmodel organisms.     

Local adaptation across a complex bioclimatic landscape in two montane bumble bee species

Understanding evolutionary responses to variation in temperature and precipitation across species ranges is of fundamental interest given ongoing climate change. The importance of temperature and precipitation for multiple aspects of bumble bee (Bombus) biology, combined with large geographic ranges that expose populations to diverse environmental pressures, make these insects well‐suited for studying local adaptation. Here, we analyzed genome‐wide sequence data from two widespread bumble bees, Bombus vosnesenskii and Bombus vancouverensis, using multiple environmental association analysis methods to investigate climate adaptation across latitude and altitude. The strongest signatures of selection were observed in B. vancouverensis, but despite unique responses between species for most loci, we detected several shared responses. Genes relating to neural and neuromuscular function and ion transport were especially evident with respect to temperature variables, while genes relating to cuticle formation, tracheal and respiratory system development, and homeostasis were associated with precipitation variables. Our data thus suggest that adaptive responses for tolerating abiotic variation are likely to be complex, but that several parallels among species can emerge even for these complex traits and landscapes. Results provide the framework for future work into mechanisms of thermal and desiccation tolerance in bumble bees and a set of genomic targets that might be monitored for future conservation efforts.     

Ecological genomics of local adaptation in Cornus florida L. by genotyping by sequencing

Discovering local adaptation, its genetic underpinnings, and environmental drivers is important for conserving forest species. Ecological genomic approaches coupled with next‐generation sequencing are useful means to detect local adaptation and uncover its underlying genetic basis in nonmodel species. We report results from a study on flowering dogwood trees (Cornus florida L.) using genotyping by sequencing (GBS). This species is ecologically important to eastern US forests but is severely threatened by fungal diseases. We analyzed subpopulations in divergent ecological habitats within North Carolina to uncover loci under local selection and associated with environmental–functional traits or disease infection. At this scale, we tested the effect of incorporating additional sequencing before scaling for a broader examination of the entire range. To test for biases of GBS, we sequenced two similarly sampled libraries independently from six populations of three ecological habitats. We obtained environmental–functional traits for each subpopulation to identify associations with genotypes via latent factor mixed modeling (LFMM) and gradient forests analysis. To test whether heterogeneity of abiotic pressures resulted in genetic differentiation indicative of local adaptation, we evaluated F_st per locus while accounting for genetic differentiation between coastal subpopulations and Piedmont‐Mountain subpopulations. Of the 54 candidate loci with sufficient evidence of being under selection among both libraries, 28–39 were Arlequin–BayeScan F_st outliers. For LFMM, 45 candidates were associated with climate (of 54), 30 were associated with soil properties, and four were associated with plant health. Reanalysis of combined libraries showed that 42 candidate loci still showed evidence of being under selection. We conclude environment‐driven selection on specific loci has resulted in local adaptation in response to potassium deficiencies, temperature, precipitation, and (to a marginal extent) disease. High allele turnover along ecological gradients further supports the adaptive significance of loci speculated to be under selection.     

Use of intraspecific variation in thermal responses for estimating an elevational cline in the timing of cold hardening in a sub‐boreal conifer

To avoid winter frost damage, evergreen coniferous species develop cold hardiness with suitable phenology for the local climate regime. Along the elevational gradient, a genetic cline in autumn phenology is often recognised among coniferous populations, but further quantification of evolutionary adaptation related to the local environment and its responsible signals generating the phenological variation are poorly understood. We evaluated the timing of cold hardening among populations of Abies sachalinensis, based on time series freezing tests using trees derived from four seed source populations × three planting sites. Furthermore, we constructed a model to estimate the development of hardening from field temperatures and the intraspecific variations occurring during this process. An elevational cline was detected such that high‐elevation populations developed cold hardiness earlier than low‐elevation populations, representing significant genetic control. Because development occurred earlier at high‐elevation planting sites, the genetic trend across elevation overlapped with the environmental trend. Based on the trade‐off between later hardening to lengthen the active growth period and earlier hardening to avoid frost damage, this genetic cline would be adaptive to the local climate. Our modelling approach estimated intraspecific variation in two model components: the threshold temperature, which was the criterion for determining whether the trees accumulated the thermal value, and the chilling requirement for trees to achieve adequate cold hardiness. A higher threshold temperature and a lower chilling requirement could be responsible for the earlier phenology of the high‐elevation population. These thermal responses may be one of the important factors driving the elevation‐dependent adaptation of A. sachalinensis.     

Riverscape genomics of a threatened fish across a hydroclimatically heterogeneous river basin

Understanding how natural selection generates and maintains adaptive genetic diversity in heterogeneous environments is key to predicting the evolutionary response of populations to rapid environmental change. Detecting selection in complex spatial environments remains challenging, especially for threatened species where the effects of strong genetic drift may overwhelm signatures of selection. We carried out a basinwide riverscape genomic analysis in the threatened southern pygmy perch (Nannoperca australis), an ecological specialist with low dispersal potential. High‐resolution environmental data and 5162 high‐quality filtered SNPs were used to clarify spatial population structure and to assess footprints of selection associated with a steep hydroclimatic gradient and with human disturbance across the naturally and anthropogenically fragmented Murray–Darling Basin (Australia). Our approach included F_ST outlier tests to define neutral loci, and a combination of spatially explicit genotype–environment association analyses to identify candidate adaptive loci while controlling for the effects of landscape structure and shared population history. We found low levels of genetic diversity and strong neutral population structure consistent with expectations based on spatial stream hierarchy and life history. In contrast, variables related to precipitation and temperature appeared as the most important environmental surrogates for putatively adaptive genetic variation at both regional and local scales. Human disturbance also influenced the variation in candidate loci for adaptation, but only at a local scale. Our study contributes to understanding of adaptive evolution along naturally and anthropogenically fragmented ecosystems. It also offers a tangible example of the potential contributions of landscape genomics for informing in situ and ex situ conservation management of biodiversity.     

Environmental drivers interactively affect individual tree growth across temperate European forests

Forecasting the growth of tree species to future environmental changes requires a better understanding of its determinants. Tree growth is known to respond to global‐change drivers such as climate change or atmospheric deposition, as well as to local land‐use drivers such as forest management. Yet, large geographical scale studies examining interactive growth responses to multiple global‐change drivers are relatively scarce and rarely consider management effects. Here, we assessed the interactive effects of three global‐change drivers (temperature, precipitation and nitrogen deposition) on individual tree growth of three study species (Quercus robur/petraea, Fagus sylvatica and Fraxinus excelsior). We sampled trees along spatial environmental gradients across Europe and accounted for the effects of management for Quercus. We collected increment cores from 267 trees distributed over 151 plots in 19 forest regions and characterized their neighbouring environment to take into account potentially confounding factors such as tree size, competition, soil conditions and elevation. We demonstrate that growth responds interactively to global‐change drivers, with species‐specific sensitivities to the combined factors. Simultaneously high levels of precipitation and deposition benefited Fraxinus, but negatively affected Quercus’ growth, highlighting species‐specific interactive tree growth responses to combined drivers. For Fagus, a stronger growth response to higher temperatures was found when precipitation was also higher, illustrating the potential negative effects of drought stress under warming for this species. Furthermore, we show that past forest management can modulate the effects of changing temperatures on Quercus’ growth; individuals in plots with a coppicing history showed stronger growth responses to higher temperatures. Overall, our findings highlight how tree growth can be interactively determined by global‐change drivers, and how these growth responses might be modulated by past forest management. By showing future growth changes for scenarios of environmental change, we stress the importance of considering multiple drivers, including past management and their interactions, when predicting tree growth.     

Behavioural response to combined insecticide and temperature stress in natural populations of Drosophila melanogaster

Insecticide resistance evolves extremely rapidly, providing an illuminating model for the study of adaptation. With climate change reshaping species distribution, pest and disease vector control needs rethinking to include the effects of environmental variation and insect stress physiology. Here, we assessed how both long‐term adaptation of populations to temperature and immediate temperature variation affect the genetic architecture of DDT insecticide response in Drosophila melanogaster. Mortality assays and behavioural assays based on continuous activity monitoring were used to assess the interaction between DDT and temperature on three field‐derived populations from climate extremes (Raleigh for warm temperate, Tasmania for cold oceanic and Queensland for hot tropical). The Raleigh population showed the highest mortality to DDT, whereas the Queensland population, epicentre for derived alleles of the resistance gene Cyp6g1, showed the lowest. Interaction between insecticide and temperature strongly affected mortality, particularly for the Tasmanian population. Activity profiles analysed using self‐organizing maps show that the insecticide promoted an early response, whereas elevated temperature promoted a later response. These distinctive early or later activity phases revealed similar responses to temperature and DDT dose alone but with more or less genetic variance depending on the population. This change in genetic variance among populations suggests that selection particularly depleted genetic variance for DDT response in the Queensland population. Finally, despite similar (co)variation between traits in benign conditions, the genetic responses across population differed under stressful conditions. This showed how stress‐responsive genetic variation only reveals itself in specific conditions and thereby escapes potential trade‐offs in benign environments.     

On the roles of landscape heterogeneity and environmental variation in determining population genomic structure in a dendritic system

Dispersal and natural selection are key evolutionary processes shaping the distribution of phenotypic and genetic diversity. For species inhabiting complex spatial environments however, it is unclear how the balance between gene flow and selection may be influenced by landscape heterogeneity and environmental variation. Here, we evaluated the effects of dendritic landscape structure and the selective forces of hydroclimatic variation on population genomic parameters for the Murray River rainbowfish, Melanotaenia fluviatilis across the Murray–Darling Basin, Australia. We genotyped 249 rainbowfish at 17,503 high‐quality SNP loci and integrated these with models of network connectivity and high‐resolution environmental data within a riverscape genomics framework. We tested competing models of gene flow before using multivariate genotype–environment association (GEA) analysis to test for signals of adaptive divergence associated with hydroclimatic variation. Patterns of neutral genetic variation were consistent with expectations based on the stream hierarchy model and M. fluviatilis’ moderate dispersal ability. Models incorporating dendritic network structure suggested that landscape heterogeneity is a more important factor determining connectivity and gene flow than waterway distance. Extending these results, we also introduce a novel approach to controlling for the unique effects of dendritic network structure in GEA analyses of populations of aquatic species. We identified 146 candidate loci potentially underlying a polygenic adaptive response to seasonal fluctuations in stream flow and variation in the relative timing of temperature and precipitation extremes. Our findings underscore an emerging predominant role for seasonal variation in hydroclimatic conditions driving local adaptation and are relevant for informing proactive conservation management.     

Molecular divergence in tropical tree populations occupying environmental mosaics

Unveiling the genetic basis of local adaptation to environmental variation is a major goal in molecular ecology. In rugged landscapes characterized by environmental mosaics, living populations and communities can experience steep ecological gradients over very short geographical distances. In lowland tropical forests, interspecific divergence in edaphic specialization (for seasonally flooded bottomlands and seasonally dry terra firme soils) has been proven by ecological studies on adaptive traits. Some species are nevertheless capable of covering the entire span of the gradient; intraspecific variation for adaptation to contrasting conditions may explain the distribution of such ecological generalists. We investigated whether local divergence happens at small spatial scales in two stands of Eperua falcata (Fabaceae), a widespread tree species of the Guiana Shield. We investigated Single Nucleotide Polymorphisms (SNP) and sequence divergence as well as spatial genetic structure (SGS) at four genes putatively involved in stress response and three genes with unknown function. Significant genetic differentiation was observed among sub‐populations within stands, and eight SNP loci showed patterns compatible with disruptive selection. SGS analysis showed genetic turnover along the gradients at three loci, and at least one haplotype was found to be in repulsion with one habitat. Taken together, these results suggest genetic differentiation at small spatial scale in spite of gene flow. We hypothesize that heterogeneous environments may cause molecular divergence, possibly associated to local adaptation in E. falcata.     

Exploring genomic variation associated with drought stress in Picea mariana populations

Predicted increases in drought and heat stress will likely induce shifts in species bioclimatic envelopes. Genetic variants adapted to water limitation may prove pivotal for species response under scenarios of increasing drought. In this study, we aimed to explore this hypothesis by investigating genetic variation in 16 populations of black spruce (Picea mariana) in relation to climate variables in Alaska. A total of 520 single nucleotide polymorphisms (SNPs) were genotyped for 158 trees sampled from areas of contrasting climate regimes. We used multivariate and univariate genotype‐by‐environment approaches along with available gene annotations to investigate the relationship between climate and genetic variation among sampled populations. Nine SNPs were identified as having a significant association with climate, of which five were related to drought stress response. Outlier SNPs with respect to the overall environment were significantly overrepresented for several biological functions relevant for coping with variable hydric regimes, including osmotic stress response. This genomic imprint is consistent with local adaptation of black spruce to drought stress. These results suggest that natural selection acting on standing variation prompts local adaptation in forest stands facing water limitation. Improved understanding of possible adaptive responses could inform our projections about future forest dynamics and help prioritize populations that harbor valuable genetic diversity for conservation.     

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.     

Local environment,not local adaptation,drives leaf‐out phenology in common gardens along an elevational gradient in Acadia National Park,Maine

Premise of the Study

Climate‐driven changes in phenology are substantially affecting ecological relationships and ecosystem processes. The role of variation among species has received particular attention; for example, variation among species’ phenological responses to climate can disrupt trophic interactions and can influence plant performance. Variation within species in phenological responses to climate, however, has received much less attention, despite its potential role in ecological interactions and local adaptation to climate change.

Methods

We constructed three common gardens across an elevation gradient on Cadillac Mountain in Acadia National Park, Maine, to test population‐level responses in leaf‐out phenology in a reciprocal transplant experiment. The experiment included three native species: low bush blueberry (Vaccinium angustifolium), sheep's laurel (Kalmia angustifolia), and three‐toothed cinquefoil (Sibbaldiopsis tridentata).

Key Results

Evidence for local adaptation of phenological response to temperature varied among the species, but was weak for all three. Rather, variation in phenological response to temperature appeared to be driven by local microclimate at each garden site and year‐to‐year variation in temperature.

Conclusions

Population‐level adaptations in leaf‐out phenology appear to be relatively unimportant for these species in Acadia National Park, perhaps a reflection of strong genetic mixing across elevations, or weak differences in selection on phenological response to spring temperatures at different elevations. These results concur with other observational data in Acadia and highlight the utility of experimental approaches to understand the importance of annual and local site variation in affecting phenology both among and within plant species.     

An integrated framework to identify wildlife populations under threat from climate change

Climate change is a major threat to global biodiversity that will produce a range of new selection pressures. Understanding species responses to climate change requires an interdisciplinary perspective, combining ecological, molecular and environmental approaches. We propose an applied integrated framework to identify populations under threat from climate change based on their extent of exposure, inherent sensitivity due to adaptive and neutral genetic variation and range shift potential. We consider intraspecific vulnerability and population‐level responses, an important but often neglected conservation research priority. We demonstrate how this framework can be applied to vertebrates with limited dispersal abilities using empirical data for the bat Plecotus austriacus. We use ecological niche modelling and environmental dissimilarity analysis to locate areas at high risk of exposure to future changes. Combining outlier tests with genotype–environment association analysis, we identify potential climate‐adaptive SNPs in our genomic data set and differences in the frequency of adaptive and neutral variation between populations. We assess landscape connectivity and show that changing environmental suitability may limit the future movement of individuals, thus affecting both the ability of populations to shift their distribution to climatically suitable areas and the probability of evolutionary rescue through the spread of adaptive genetic variation among populations. Therefore, a better understanding of movement ecology and landscape connectivity is needed for predicting population persistence under climate change. Our study highlights the importance of incorporating genomic data to determine sensitivity, adaptive potential and range shift potential, instead of relying solely on exposure to guide species vulnerability assessments and conservation planning.