Combined genotype and phenotype analyses reveal patterns of genomic adaptation to local environments in the subtropical oak Quercus acutissima

Understanding the effects of the demographic dynamics and environmental heterogeneity on the genomic variation of forest species is important, not only for uncovering the evolutionary history of the species, but also for predicting their ability to adapt to climate change. In this study, we combined a common garden experiment with range-wide population genomics analyses to infer the demographic history and characterize patterns of local adaptation in a subtropical oak species, Quercus acutissima (Carruthers). We scanned approximately 8% of the oak genome using a balanced representation of both genic and non-genic regions and identified a total of 55 361 single nucleotide polymorphisms (SNPs) in 167 trees. Genomic diversity analyses revealed an east–west split in the species distribution range. Coalescent-based model simulations inferred a late Pleistocene divergence in Q. acutissima between the east and west groups as well as subsequent preglaciation population expansion events. Consistent with observed genetic differentiation, morphological traits also showed east–west differentiation and the biomass allocation in seedlings was significantly associated with precipitation. Environment was found to have a significant and stronger impact on the non-neutral than the neutral SNPs, and also significantly associated with the phenotypic differentiation, suggesting that, apart from the geography, environment had played a role in determining non-neutral and phenotypic variation. Our approach, which combined a common garden experiment with landscape genomics data, validated the hypothesis of local adaptation of this long-lived oak tree of subtropical China. Our study joins the small number of studies that have combined genotypic and phenotypic data to detect patterns of local adaptation.     

Towards identifying genes underlying ecologically relevant traits in Arabidopsis thaliana

A major challenge in evolutionary biology and plant breeding is to identify the genetic basis of complex quantitative traits, including those that contribute to adaptive variation. Here we review the development of new methods and resources to fine-map intraspecific genetic variation that underlies natural phenotypic variation in plants. In particular, the analysis of 107 quantitative traits reported in the first genome-wide association mapping study in Arabidopsis thaliana sets the stage for an exciting time in our understanding of plant adaptation. We also argue for the need to place phenotype-genotype association studies in an ecological context if one is to predict the evolutionary trajectories of plant species.     

Local selection modifies phenotypic divergence among Rana temporaria populations in the presence of gene flow

In ectotherms, variation in life history traits among populations is common and suggests local adaptation. However, geographic variation itself is not a proof for local adaptation, as genetic drift and gene flow may also shape patterns of quantitative variation. We studied local and regional variation in means and phenotypic plasticity of larval life history traits in the common frog Rana temporaria using six populations from central Sweden, breeding in either open‐canopy or partially closed‐canopy ponds. To separate local adaptation from genetic drift, we compared differentiation in quantitative genetic traits (Q_ST) obtained from a common garden experiment with differentiation in presumably neutral microsatellite markers (F_ST). We found that R. temporaria populations differ in means and plasticities of life history traits in different temperatures at local, and in F_ST at regional scale. Comparisons of differentiation in quantitative traits and in molecular markers suggested that natural selection was responsible for the divergence in growth and development rates as well as in temperature‐induced plasticity, indicating local adaptation. However, at low temperature, the role of genetic drift could not be separated from selection. Phenotypes were correlated with forest canopy closure, but not with geographical or genetic distance. These results indicate that local adaptation can evolve in the presence of ongoing gene flow among the populations, and that natural selection is strong in this system.     

Local adaptation and phenotypic plasticity both occurred in <Emphasis Type="Italic">Wedelia trilobata</Emphasis> invasion across a tropical island

The role of the local adaptation and phenotypic plasticity of invasive species in their invasion of new environments has historically been a debatable issue, particularly at small spatial scales (e.g., different habitats within an island). We selected seven field sites across Hainan Island, Hainan Province, China, to investigate the role of local adaptation and/or phenotypic plasticity in the successful invasion of Wedelia trilobata by a field survey, molecular marker analysis, and common garden experiment. In the field survey, the clonal growth characteristics of W. trilobata showed significant differences among the seven sites, suggesting that the species was able to adapt to different environments. The mean phenotypic plasticity index of W. trilobata was higher than that of other invasive plant species (0.61 vs 0.48). The analysis of the inter-simple sequence repeat molecular markers of 420 individuals from the seven sites revealed a Shannon’s index that was similar to those of other invasive plants (0.29 vs 0.25). The nested analysis of the molecular variance in the genetic diversity of the population showed significant differences among the sites. In the common garden experiment, the growth characteristics of plants grown from the seven sites were significantly affected by light and density treatments but not by soil moisture. However, the responses of plants grown from different sites to light treatment varied. Plants from sunny sites had greater clonal traits than those from shady sites, indicating that local adaptation occurred in plant populations grown at some sites. Overall, our results implied that both phenotypic plasticity and local adaptation contributed to the successful invasion of W. trilobata across Hainan Island.     

The genomic and bioclimatic characterization of Ethiopian barley (Hordeum vulgare L.) unveils challenges and opportunities to adapt to a changing climate

The climate crisis is impacting agroecosystems and threatening food security of millions of smallholder farmers. Understanding the potential for current and future climatic adaptation of local crop agrobiodiversity may guide breeding efforts and support resilience of agriculture. Here, we combine a genomic and climatic characterization of a large collection of traditional barley varieties from Ethiopia, a staple for local smallholder farmers cropping in challenging environments. We find that the genomic diversity of barley landraces can be partially traced back to geographic and environmental diversity of the landscape. We employ a machine learning approach to model Ethiopian barley adaptation to current climate and to identify areas where its existing diversity may not be well adapted in future climate scenarios. We use this information to identify optimal trajectories of assisted migration compensating to detrimental effects of climate change, finding that Ethiopian barley diversity bears opportunities for adaptation to the climate crisis. We then characterize phenology traits in the collection in two common garden experiments in Ethiopia, using genome-wide association approaches to identify genomic loci associated with timing of flowering and maturity of the spike. We combine this information with genotype–environment associations finding that loci involved in flowering time may also explain environmental adaptation. Our data show that integrated genomic, climatic, and phenotypic characterizations of agrobiodiversity may provide breeding with actionable information to improve local adaptation in smallholder farming systems.     

Geographic variation in thermal sensitivity of early life traits in a widespread reptile

Taxa with large geographic distributions generally encompass diverse macroclimatic conditions, potentially requiring local adaptation and/or phenotypic plasticity to match their phenotypes to differing environments. These eco‐evolutionary processes are of particular interest in organisms with traits that are directly affected by temperature, such as embryonic development in oviparous ectotherms. Here we examine the spatial distribution of fitness‐related early life phenotypes across the range of a widespread vertebrate, the painted turtle (Chrysemys picta). We quantified embryonic and hatchling traits from seven locations (in Idaho, Minnesota, Oregon, Illinois, Nebraska, Kansas, and New Mexico) after incubating eggs under constant conditions across a series of environmentally relevant temperatures. Thermal reaction norms for incubation duration and hatchling mass varied among locations under this common‐garden experiment, indicating genetic differentiation or pre‐ovulatory maternal effects. However, latitude, a commonly used proxy for geographic variation, was not a strong predictor of these geographic differences. Our findings suggest that this macroclimatic proxy may be an unreliable surrogate for microclimatic conditions experienced locally in nests. Instead, complex interactions between abiotic and biotic factors likely drive among‐population phenotypic variation in this system. Understanding spatial variation in key life‐history traits provides an important perspective on adaptation to contemporary and future climatic conditions.     

Genomic Shifts,Phenotypic Clines,and Fitness Costs Associated With Cold Tolerance in the Asian Tiger Mosquito

Climatic variation is a key driver of genetic differentiation and phenotypic traits evolution, and local adaptation to temperature is expected in widespread species. We investigated phenotypic and genomic changes in the native range of the Asian tiger mosquito, Aedes albopictus. We first refine the phylogeographic structure based on genome-wide regions (1,901 double-digest restriction-site associated DNA single nucleotide polymophisms [ddRAD SNPs]) from 41 populations. We then explore the patterns of cold adaptation using phenotypic traits measured in common garden (wing size and cold tolerance) and genotype–temperature associations at targeted candidate regions (51,706 exon-capture SNPs) from nine populations. We confirm the existence of three evolutionary lineages including clades A (Malaysia, Thailand, Cambodia, and Laos), B (China and Okinawa), and C (South Korea and Japan). We identified temperature-associated differentiation in 15 out of 221 candidate regions but none in ddRAD regions, supporting the role of directional selection in detected genes. These include genes involved in lipid metabolism and a circadian clock gene. Most outlier SNPs are differently fixed between clades A and C, whereas clade B has an intermediate pattern. Females are larger at higher latitude yet produce no more eggs, which might favor the storage of energetic reserves in colder climate. Nondiapausing eggs from temperate populations survive better to cold exposure than those from tropical populations, suggesting they are protected from freezing damages but this cold tolerance has a fitness cost in terms of egg viability. Altogether, our results provide strong evidence for the thermal adaptation of A. albopictus across its wide temperature range.     

Different gardens, different results: native and introduced populations exhibit contrasting phenotypes across common gardens

Invasive plants may respond through adaptive evolution and/or phenotypic plasticity to new environmental conditions where they are introduced. Although many studies have focused on evolution of invaders particularly in the context of testing the evolution of increased competitive ability (EICA) hypothesis, few consistent patterns have emerged. Many tests of the EICA hypothesis have been performed in only one environment; such assessments may be misleading if plants that perform one way at a particular site respond differently across sites. Single common garden tests ignore the potential for important contributions of both genetic and environmental factors to affect plant phenotype. Using a widespread invader in North America, Cynoglossum officinale, we established reciprocal common gardens in the native range (Europe) and introduced range (North America) to assess genetically based differences in size, fecundity, flowering phenology and threshold flowering size between native and introduced genotypes as well as the magnitude of plasticity in these traits. In addition, we grew plants at three nutrient levels in a pot experiment in one garden to test for plasticity across a different set of conditions. We did not find significant genetically based differences between native and introduced populations in the traits we measured; in our experiments, introduced populations of C. officinale were larger and more fecund, but only in common garden experiments in the native range. We found substantial population-level plasticity for size, fecundity and date of first flowering, with plants performing better in a garden in Germany than in Montana. Differentiation of native populations in the magnitude of plasticity was much stronger than that of introduced populations, suggesting an important role for founder effects. We did not detect evidence of an evolutionary change in threshold flowering size. Our study demonstrates that detecting genetically based differences in traits may require measuring plant responses to more than one environment.     

Adaptive phenotypic plasticity contributes to divergence between lake and river populations of an East African cichlid fish

Adaptive phenotypic plasticity and fixed genotypic differences have long been considered opposing strategies in adaptation. More recently, these mechanisms have been proposed to act complementarily and under certain conditions jointly facilitate evolution, speciation, and even adaptive radiations. Here, we investigate the relative contributions of adaptive phenotypic plasticity vs. local adaptation to fitness, using an emerging model system to study early phases of adaptive divergence, the generalist cichlid fish species Astatotilapia burtoni. We tested direct fitness consequences of morphological divergence between lake and river populations in nature by performing two transplant experiments in Lake Tanganyika. In the first experiment, we used wild‐caught juvenile lake and river individuals, while in the second experiment, we used F1 crosses between lake and river fish bred in a common garden setup. By tracking the survival and growth of translocated individuals in enclosures in the lake over several weeks, we revealed local adaptation evidenced by faster growth of the wild‐caught resident population in the first experiment. On the other hand, we did not find difference in growth between different types of F1 crosses in the second experiment, suggesting a substantial contribution of adaptive phenotypic plasticity to increased immigrant fitness. Our findings highlight the value of formally comparing fitness of wild‐caught and common garden‐reared individuals and emphasize the necessity of considering adaptive phenotypic plasticity in the study of adaptive divergence.     

GENE FLOW AND SELECTION ON PHENOTYPIC PLASTICITY IN AN ISLAND SYSTEM OF RANA TEMPORARIA

Gene flow is often considered to be one of the main factors that constrains local adaptation in a heterogeneous environment. However, gene flow may also lead to the evolution of phenotypic plasticity. We investigated the effect of gene flow on local adaptation and phenotypic plasticity in development time in island populations of the common frog Rana temporaria which breed in pools that differ in drying regimes. This was done by investigating associations between traits (measured in a common garden experiment) and selective factors (pool drying regimes and gene flow from other populations inhabiting different environments) by regression analyses and by comparing pairwise F_ST values (obtained from microsatellite analyses) with pairwise Q_ST values. We found that the degree of phenotypic plasticity was positively correlated with gene flow from other populations inhabiting different environments (among‐island environmental heterogeneity), as well as with local environmental heterogeneity within each population. Furthermore, local adaptation, manifested in the correlation between development time and the degree of pool drying on the islands, appears to have been caused by divergent selection pressures. The local adaptation in development time and phenotypic plasticity is quite remarkable, because the populations are young (less than 300 generations) and substantial gene flow is present among islands.     

基于野外调查和同质种植园实验的芦苇植物功能性状变异研究

研究表型可塑性和遗传变异在植物表型分化中的相对作用,有助于预测全球环境变化下的植物群落组成和生态系统功能的变化。芦苇（Phragmites australis）是全球性广布的草本植物,种内变异丰富,在我国西北和东部均存在多个分化稳定的生态型,但中国芦苇在更大尺度上的表型研究还非常匮乏。将位于黄河上游的宁夏平原和黄河下游的黄河三角洲作为研究区域,通过野外调查和同质种植园实验对芦苇自然种群的植物功能性状变异进行观测。结果表明,无论在野外还是同质种植园,黄河三角洲芦苇的基径、叶长和叶宽均显著大于宁夏平原芦苇,说明两个地区的芦苇种群之间存在着受遗传决定的表型分化,这可能与两个地区间的降水等气候差异有关。在野外,宁夏芦苇的株高和叶厚显著大于黄河三角洲芦苇,但在同质园中差异消失或相反,说明株高、叶厚受环境影响较大,表型可塑性也是芦苇适应环境变化的重要机制。在同质种植园中,宁夏平原芦苇的叶片氮磷含量较低,但株数却显著多于黄河三角洲芦苇,反映了不同地区芦苇之间存在不同的适应策略,宁夏平原芦苇更偏向于高扩散率的杂草策略,而黄河三角洲芦苇更偏向于竞争策略。此外,宁夏平原芦苇的株高、叶长两个性状以及基径-比叶面积相关性在野外和同质园两个环境中存在一致性,表明了性状变异和权衡策略的遗传稳定性。综上,位于黄河上下游的芦苇种群间存在着适应性分化,这是表型可塑性和遗传变异共同作用的结果,不同来源芦苇对全球变化下的多重环境因子的响应还需要进一步研究。     

Testing the role of phenotypic plasticity for local adaptation: growth and development in time-constrained Rana temporaria populations

Phenotypic plasticity can be important for local adaptation, because it enables individuals to survive in a novel environment until genetic changes have been accumulated by genetic accommodation. By analysing the relationship between development rate and growth rate, it can be determined whether plasticity in life-history traits is caused by changed physiology or behaviour. We extended this to examine whether plasticity had been aiding local adaptation, by investigating whether the plastic response had been fixed in locally adapted populations. Tadpoles from island populations of Rana temporaria, locally adapted to different pool-drying regimes, were monitored in a common garden. Individual differences in development rate were caused by different foraging efficiency. However, developmental plasticity was physiologically mediated by trading off growth against development rate. Surprisingly, plasticity has not aided local adaptation to time-stressed environments, because local adaptation was not caused by genetic assimilation but on selection on the standing genetic variation in development time.     

Evolution of dispersal traits along an invasion route in the wind‐dispersed Senecio inaequidens (Asteraceae)

In introduced organisms, dispersal propensity is expected to increase during range expansion. This prediction is based on the assumption that phenotypic plasticity is low compared to genetic diversity, and an increase in dispersal can be counteracted by the Allee effect. Empirical evidence in support of these hypotheses is however lacking. The present study tested for evidence of differentiation in dispersal‐related traits and the Allee effect in the wind‐dispersed invasive Senecio inaequidens (Asteraceae). We collected capitula from individuals in ten field populations, along an invasion route including the original introduction site in southern France. In addition, we conducted a common garden experiment from field‐collected seeds and obtained capitula from individuals representing the same ten field populations. We analysed phenotypic variation in dispersal traits between field and common garden environments as a function of the distance between populations and the introduction site. Our results revealed low levels of phenotypic differentiation among populations. However, significant clinal variation in dispersal traits was demonstrated in common garden plants representing the invasion route. In field populations, similar trends in dispersal‐related traits and evidence of an Allee effect were not detected. In part, our results supported expectations of increased dispersal capacity with range expansion, and emphasized the contribution of phenotypic plasticity under natural conditions.     

Lessons learned from the dog genome

Extensive genetic resources and a high-quality genome sequence position the dog as an important model species for understanding genome evolution, population genetics and genes underlying complex phenotypic traits. Newly developed genomic resources have expanded our understanding of canine evolutionary history and dog origins. Domestication involved genetic contributions from multiple populations of gray wolves probably through backcrossing. More recently, the advent of controlled breeding practices has segregated genetic variability into distinct dog breeds that possess specific phenotypic traits. Consequently, genome-wide association and selective sweep scans now allow the discovery of genes underlying breed-specific characteristics. The dog is finally emerging as a novel resource for studying the genetic basis of complex traits, including behavior.     

Characterizing the contribution of plasticity and genetic differentiation to community‐level trait responses to environmental change

The match between functional trait variation in communities and environmental gradients is maintained by three processes: phenotypic plasticity and genetic differentiation (intraspecific processes), and species turnover (interspecific). Recently, evidence has emerged suggesting that intraspecific variation might have a potentially large role in driving functional community composition and response to environmental change. However, empirical evidence quantifying the respective importance of phenotypic plasticity and genetic differentiation relative to species turnover is still lacking. We performed a reciprocal transplant experiment using a common herbaceous plant species (Oxalis montana) among low‐, mid‐, and high‐elevation sites to first quantify the contributions of plasticity and genetic differentiation in driving intraspecific variation in three traits: height, specific leaf area, and leaf area. We next compared the contributions of these intraspecific drivers of community trait–environment matching to that of species turnover, which had been previously assessed along the same elevational gradient. Plasticity was the dominant driver of intraspecific trait variation across elevation in all traits, with only a small contribution of genetic differentiation among populations. Local adaptation was not detected to a major extent along the gradient. Fitness components were greatest in O. montana plants with trait values closest to the local community‐weighted means, thus supporting the common assumption that community‐weighted mean trait values represent selective optima. Our results suggest that community‐level trait responses to ongoing climate change should be mostly mediated by species turnover, even at the small spatial scale of our study, with an especially small contribution of evolutionary adaptation within species.     

Glacial History Affected Phenotypic Differentiation in the Alpine Plant,Campanula thyrsoides

Numerous widespread Alpine plant species show molecular differentiation among populations from distinct regions. This has been explained as the result of genetic drift during glacial survival in isolated refugia along the border of the European Alps. Since genetic drift may affect molecular markers and phenotypic traits alike, we asked whether phenotypic differentiation mirrors molecular patterns among Alpine plant populations from different regions. Phenotypic traits can be under selection, so we additionally investigated whether part of the phenotypic differentiation can be explained by past selection and/or current adaptation. Using the monocarpic Campanula thyrsoides as our study species, a common garden experiment with plants from 21 populations from four phylogeographic groups located in regions across the Alps and the Jura Mountains was performed to test for differentiation in morphological and phenological traits. Past selection was investigated by comparing phenotypic differentiation among and within regions with molecular differentiation among and within regions. The common garden results indicated regional differentiation among populations for all investigated phenotypic traits, particularly in phenology. Delayed flowering in plants from the South-eastern Alps suggested adaptation to long sub-mediterranean summers and contrasted with earlier flowering of plants experiencing shorter growing seasons in regions with higher elevation to the West. Comparisons between molecular and phenotypic differentiation revealed diversifying selection among regions in height and biomass, which is consistent with adaptation to environmental conditions in glacial refugia. Within regions, past selection acted against strong diversification for most phenotypic traits, causing restricted postglacial adaptation. Evidence consistent with post-glacial adaptation was also given by negative correlation coefficients between several phenotypic traits and elevation of the population''s origin. In conclusion, our study suggests that, irrespective of adaptation of plants to their current environment, glacial history can have a strong and long-lasting influence on the phenotypic evolution of Alpine plants.     

Evidence of Adaptive Evolutionary Divergence during Biological Invasion

Rapid phenotypic diversification during biological invasions can either arise by adaptation to alternative environments or by adaptive phenotypic plasticity. Where experimental evidence for adaptive plasticity is common, support for evolutionary diversification is rare. Here, we performed a controlled laboratory experiment using full-sib crosses between ecologically divergent threespine stickleback populations to test for a genetic basis of adaptation. Our populations are from two very different habitats, lake and stream, of a recently invaded range in Switzerland and differ in ecologically relevant morphological traits. We found that in a lake-like food treatment lake fish grow faster than stream fish, resembling the difference among wild type individuals. In contrast, in a stream-like food treatment individuals from both populations grow similarly. Our experimental data suggest that genetically determined diversification has occurred within less than 140 years after the arrival of stickleback in our studied region.     

Rapid evolution of dispersal‐related traits during range expansion of an invasive vine Mikania micrantha

Rapid range expansion of invasive plants provides a unique opportunity to explore evolutionary changes of dispersal‐related traits during the invasion process. Increasing evidence now suggests that a higher dispersal rate is favored at the invasion front. However, little is known about the role of genetic differentiation and phenotypic plasticity on patterns of dispersal ability during the invasion process. In this study, we combined a field survey and a common garden transplant experiment to test for evidence of genetically based dispersal ability in Mikania micrantha, a highly invasive vine, across its invaded range in southern China. Three dispersal‐related traits, plume loading, seed mass and pappus radius, were measured in both natural and common garden populations. We found that in natural conditions, plume loading and seed mass significantly decreased with expanding distance from the source population, but in controlled conditions, these two traits exhibited a significant humped trend against percent field cover, indicating that dispersal ability of M. micrantha was selected for during range expansion and that the related traits were likely to be under genetic control. Furthermore, rebounding dispersal ability was detected in highly competitive sites in the range core, which suggested that this evolutionary process was likely partially driven by intraspecific competition. Because more and more plant species are under spatial nonequilibirum due to climate change, this study can serve to provide hints at the fate of spatially fluctuant populations.