Limits to local adaptation in six populations of the annual plant Diodia teres

* Local adaptation is common, but tests for adaptive differentiation frequently compare populations from strongly divergent environments, making it unlikely that any influence of stochastic processes such as drift or mutation on local adaptation will be detected. Here, the hypothesis that local adaptation is more likely to develop when the native environments of populations are more distinct than when they are similar was tested. * A reciprocal transplant experiment including two populations from each of three habitats was conducted to determine the pattern of local adaptation. In addition to testing for local adaptation at the population level, the hypothesis was tested that local adaptation is more common between populations from different habitats than between populations from the same habitat. * Local adaptation was not common, but more evidence was found of local adaptation between populations from different habitats than between populations from the same habitat. Two instances of foreign genotype fitness advantage confirm that stochastic processes such as drift can limit local adaptation. * These results are consistent with the hypothesis that stochastic processes can inhibit local adaptation but are more likely to be overwhelmed by natural selection when populations occur in divergent environments.     

Local adaptation, patterns of selection, and gene flow in the Californian serpentine sunflower (Helianthus exilis)

The traditional view of the species as the fundamental unit of evolution has been challenged by observations that in heterogeneous environments, gene flow may be too restricted to overcome the effects of local selection. Whether a species evolves as a cohesive unit depends critically on the dynamic balance between homogenizing gene flow among populations and potentially disruptive local adaptation. To examine this evolutionary balance between "global" gene flow and local selection, we studied northern Californian populations of Helianthus exilis, the serpentine sunflower, within a mosaic of contrasting serpentine and nonserpentine areas that differ considerably in soil chemistry and water availability. Local adaptation to riparian and serpentine habitats was studied in Helianthus exilis along with an analysis of gene flow patterns among populations within these habitats. Local adaptation was assessed in H. exilis during 2002 and 2003 using reciprocal transplant experiments at multiple locations within serpentine and riparian habitats. Effects of competition and germination date on the expression of local adaptation were also examined within the reciprocal transplant experiments. Local adaptation was detected in both years at the local site level and at the level of habitat. The analysis of the transplanted populations indicated that the patterns of selection differed considerably between riparian and serpentine sites. Differential survivorship occurred in serpentine habitats, whereas selection on reproductive output predominated in riparian habitats. Local adaptation was expressed only in the absence of competition. Local adaptation in terms of survivorship was most strongly expressed in treatments with delayed seed germination. Microsatellite markers were used to quantify population genetic parameters and examine the patterns of gene flow among sampled populations. Analysis of molecular markers revealed a system of population patches that freely exchange genes with each other. Strong selection seems to maintain ecotypic variation within this endemic sunflower species, while extensive gene flow among populations prevents local speciation between serpentine and riparian ecotypes.     

No evidence for local adaptation and an epigenetic underpinning in native and non‐native ruderal plant species in Germany

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Habitat-specific natural selection at a flowering-time QTL is a main driver of local adaptation in two wild barley populations

Understanding the genetic basis of local adaptation requires insight in the fitness effects of individual loci under natural field conditions. While rapid progress is made in the search for genes that control differences between plant populations, it is typically unknown whether the genes under study are in fact key targets of habitat-specific natural selection. Using a quantitative trait loci (QTL) approach, we show that a QTL associated with flowering-time variation between two locally adapted wild barley populations is an important determinant of fitness in one, but not in the other population's native habitat. The QTL mapped to the same position as a habitat-specific QTL for field fitness that affected plant reproductive output in only one of the parental habitats, indicating that the genomic region is under differential selection between the native habitats. Consistent with the QTL results, phenotypic selection of flowering time differed between the two environments, whereas other traits (growth rate and seed weight) were under selection but experienced no habitat-specific differential selection. This implies the flowering-time QTL as a driver of adaptive population divergence. Our results from phenotypic selection and QTL analysis are consistent with local adaptation without genetic trade-offs in performance across environments, i.e. without alleles or traits having opposing fitness effects in contrasting environments.     

Strong genetic differentiation but not local adaptation toward the range limit of a coastal dune plant

All species have limited geographic distributions; but the ecological and evolutionary mechanisms causing range limits are largely unknown. That many species’ geographic range limits are coincident with niche limits suggests limited evolutionary potential of marginal populations to adapt to conditions experienced beyond the range. We provide a test of range limit theory by combining population genetic analysis of microsatellite polymorphisms with a transplant experiment within, at the edge of, and 60 km beyond the northern range of a coastal dune plant. Contrary to expectations, lifetime fitness increased toward the range limit with highest fitness achieved by most populations at and beyond the range edge. Genetic differentiation among populations was strong, with very low, nondirectional gene flow suggesting range limitation via constraints to dispersal. In contrast, however, local adaptation was negligible, and a distance‐dependent decline in fitness only occurred for those populations furthest from home when planted beyond the range limit. These results challenge a commonly held assumption that stable range limits match niche limits, but also raise questions about the unique value of peripheral populations in expanding species’ geographical ranges.     

The importance of biotic interactions and local adaptation for plant response to environmental changes: field evidence along an elevational gradient

Predicting the response of species to environmental changes is a great and on‐going challenge for ecologists, and this requires a more in‐depth understanding of the importance of biotic interactions and the population structuration in the landscape. Using a reciprocal transplantation experiment, we tested the response of five species to an elevational gradient. This was combined to a neighbour removal treatment to test the importance of local adaptation and biotic interactions. The trait studied was performance measured as survival and biomass. Species response varied along the elevational gradient, but with no consistent pattern. Performance of species was influenced by environmental conditions occurring locally at each site, as well as by positive or negative effects of the surrounding vegetation. Indeed, we observed a shift from competition for biomass to facilitation for survival as a response to the increase in environmental stress occurring in the different sites. Unlike previous studies pointing out an increase of stress along the elevation gradient, our results supported a stress gradient related to water availability, which was not strictly parallel to the elevational gradient. For three of our species, we observed a greater biomass production for the population coming from the site where the species was dominant (central population) compared to population sampled at the limit of the distribution (marginal population). Nevertheless, we did not observe any pattern of local adaptation that could indicate adaptation of populations to a particular habitat. Altogether, our results highlighted the great ability of plant species to cope with environmental changes, with no local adaptation and great variability in response to local conditions. Our study confirms the importance of taking into account biotic interactions and population structure occurring at local scale in the prediction of communities’ responses to global environmental changes.     

No evidence for adaptation to local rhizobial mutualists in the legume Medicago lupulina

Local adaptation is a common but not ubiquitous feature of species interactions, and understanding the circumstances under which it evolves illuminates the factors that influence adaptive population divergence. Antagonistic species interactions dominate the local adaptation literature relative to mutualistic ones, preventing an overall assessment of adaptation within interspecific interactions. Here, we tested whether the legume Medicago lupulina is adapted to the locally abundant species of mutualistic nitrogen‐fixing rhizobial bacteria that vary in frequency across its eastern North American range. We reciprocally inoculated northern and southern M. lupulina genotypes with the northern (Ensifer medicae) or southern bacterium (E. meliloti) in a greenhouse experiment. Despite producing different numbers of root nodules (the structures in which the plants house the bacteria), neither northern nor southern plants produced more seeds, flowered earlier, or were more likely to flower when inoculated with their local rhizobia. We then used a pre‐existing dataset to perform a genome scan for loci that showed elevated differentiation between field‐collected plants that hosted different bacteria. None of the loci we identified belonged to the well‐characterized suite of legume–rhizobia symbiosis genes, suggesting that the rhizobia do not drive genetic divergence between M. lupulina populations. Our results demonstrate that symbiont local adaptation has not evolved in this mutualism despite large‐scale geographic variation in the identity of the interacting species.     

Spatial scale of local adaptation and population genetic structure in a miniature succulent, Argyroderma pearsonii

Explicit understanding of the spatial scale of evolutionary processes is required in order to set targets for their effective conservation. Here, we explore the spatial context of neutral and adaptive divergence in the species-rich Knersvlakte region of South Africa. Specifically, we aimed to assess the importance of erosional drainage basins as spatial units of evolutionary process. We used amplified fragment length polymorphism (AFLP) and reciprocal transplants to investigate genetic differentiation in Argyroderma pearsonii, sampled from sparse and dense quartz habitats within each of three drainage basins. This design allowed assessment of differentiation at two distinct spatial scales; between habitats within basins, and between basins. We found near-perfect concordance between genetic clusters and basin occupancy, suggesting restricted interbasin gene flow. In addition, transplants reveal adaptive divergence between basins on the dense quartz habitat. We have shown that neutral and adaptive differentiation occurs between basins, but not between habitats within basins, suggesting that conservation plans aimed at conserving multiple interconnected drainage basins will capture an important axis of evolutionary process on the Knersvlakte.     

Genomic and chemical evidence for local adaptation in resistance to different herbivores in Datura stramonium

Because most species are collections of genetically variable populations distributed to habitats differing in their abiotic/biotic environmental factors and community composition, the pattern and strength of natural selection imposed by species on each other's traits are also expected to be highly spatially variable. Here, we used genomic and quantitative genetic approaches to understand how spatially variable selection operates on the genetic basis of plant defenses to herbivores. To this end, an F₂ progeny was generated by crossing Datura stramonium (Solanaceae) parents from two populations differing in their level of chemical defense. This F₂ progeny was reciprocally transplanted into the parental plants’ habitats and by measuring the identity by descent (IBD) relationship of each F₂ plant to each parent, we were able to elucidate how spatially variable selection imposed by herbivores operated on the genetic background (IBD) of resistance to herbivory, promoting local adaptation. The results highlight that plants possessing the highest total alkaloid concentrations (sum of all alkaloid classes) were not the most well-defended or fit. Instead, specific alkaloids and their linked loci/alleles were favored by selection imposed by different herbivores. This has led to population differentiation in plant defenses and thus, to local adaptation driven by plant-herbivore interactions.     

Strong patterns of intraspecific variation and local adaptation in Great Basin plants revealed through a review of 75 years of experiments

Variation in natural selection across heterogeneous landscapes often produces (a) among‐population differences in phenotypic traits, (b) trait‐by‐environment associations, and (c) higher fitness of local populations. Using a broad literature review of common garden studies published between 1941 and 2017, we documented the commonness of these three signatures in plants native to North America's Great Basin, an area of extensive restoration and revegetation efforts, and asked which traits and environmental variables were involved. We also asked, independent of geographic distance, whether populations from more similar environments had more similar traits. From 327 experiments testing 121 taxa in 170 studies, we found 95.1% of 305 experiments reported among‐population differences, and 81.4% of 161 experiments reported trait‐by‐environment associations. Locals showed greater survival in 67% of 24 reciprocal experiments that reported survival, and higher fitness in 90% of 10 reciprocal experiments that reported reproductive output. A meta‐analysis on a subset of studies found that variation in eight commonly measured traits was associated with mean annual precipitation and mean annual temperature at the source location, with notably strong relationships for flowering phenology, leaf size, and survival, among others. Although the Great Basin is sometimes perceived as a region of homogeneous ecosystems, our results demonstrate widespread habitat‐related population differentiation and local adaptation. Locally sourced plants likely harbor adaptations at rates and magnitudes that are immediately relevant to restoration success, and our results suggest that certain key traits and environmental variables should be prioritized in future assessments of plants in this region.     

No evidence for local adaptation in an invasive alien plant: field and greenhouse experiments tracing a colonization sequence

Background and Aims

Local adaptation enables plant species to persist under different environmental conditions. Evolutionary change can occur rapidly in invasive annual species and has been shown to lead to local adaptation. However, the patterns and mechanisms of local adaptation in invasive species along colonization sequences are not yet understood. Thus, in this study the alien annual Impatiens glandulifera was used to investigate local adaptation to distinct habitats that have been consecutively invaded in central Europe.

Methods

A reciprocal transplant experiment was performed using 15 populations from alluvial deciduous forests, fallow meadows and coniferous upland forests, and a greenhouse experiment was performed in which plants from these habitats were grown under treatments reflecting the main habitat differentiators (shade, soil acidity, competition).

Key Results

Biomass production, specific leaf area, plant height and relative growth rate differed between habitats in the field experiment and between treatments in the greenhouse, but not between seed origins. Overall, there was no indication of local adaptation in either experiment.

Conclusions

Since I. glandulifera is a successful invader in many habitats without showing local adaptation, it is suggested that the species is coping with environmental variation by means of high phenotypic plasticity. The species seems to follow a ‘jack-and-master’ strategy, i.e. it is able to maintain high fitness under a wide range of environmental conditions, but performs particularly well in favourable habitats. Therefore, the proposed colonization sequence is likely to be based primarily on changes in propagule pressure. It is concluded that invasive alien plants can become dominant in distinct habitats without local adaptation.     

Stress avoidance in a common annual: reproductive timing is important for local adaptation and geographic distribution

Adaptation to local environments may be an important determinant of species' geographic range. However, little is known about which traits contribute to adaptation or whether their further evolution would facilitate range expansion. In this study, we assessed the adaptive value of stress avoidance traits in the common annual Cocklebur (Xanthium strumarium) by performing a reciprocal transplant across a broad latitudinal gradient extending to the species' northern border. Populations were locally adapted and stress avoidance traits accounted for most fitness differences between populations. At the northern border where growing seasons are cooler and shorter, native populations had evolved to reproduce earlier than native populations in the lower latitude gardens. This clinal pattern in reproductive timing corresponded to a shift in selection from favouring later to earlier reproduction. Thus, earlier reproduction is an important adaptation to northern latitudes and constraint on the further evolution of this trait in marginal populations could potentially limit distribution.     

Using archaeogenomic and computational approaches to unravel the history of local adaptation in crops

Our understanding of the evolution of domestication has changed radically in the past 10 years, from a relatively simplistic rapid origin scenario to a protracted complex process in which plants adapted to the human environment. The adaptation of plants continued as the human environment changed with the expansion of agriculture from its centres of origin. Using archaeogenomics and computational models, we can observe genome evolution directly and understand how plants adapted to the human environment and the regional conditions to which agriculture expanded. We have applied various archaeogenomics approaches as exemplars to study local adaptation of barley to drought resistance at Qasr Ibrim, Egypt. We show the utility of DNA capture, ancient RNA, methylation patterns and DNA from charred remains of archaeobotanical samples from low latitudes where preservation conditions restrict ancient DNA research to within a Holocene timescale. The genomic level of analyses that is now possible, and the complexity of the evolutionary process of local adaptation means that plant studies are set to move to the genome level, and account for the interaction of genes under selection in systems-level approaches. This way we can understand how plants adapted during the expansion of agriculture across many latitudes with rapidity.     

Clinal variation in MHC diversity with temperature: evidence for the role of host-pathogen interaction on local adaptation in Atlantic salmon

In vertebrates, variability at genes of the Major Histocompatibility Complex (MHC) represents an important adaptation for pathogen resistance, whereby high allelic diversity confers resistance to a greater number of pathogens. Pathogens can maintain diversifying selection pressure on their host's immune system that can vary in intensity based on pathogen richness, pathogen virulence, and length of the cohabitation period, which tend to increase with temperature. In this study, we tested the hypothesis that genetic diversity of MHC increases with temperature along a latitudinal gradient in response to pathogen selective pressure in the wild. A total of 1549 Atlantic salmon from 34 rivers were sampled between 46 degrees N and 58 degrees N in Eastern Canada. The results supported our working hypothesis. In contrast to the overall pattern observed at microsatellites, MHC class II allelic diversity increased with temperature, thus creating a latitudinal gradient. The observed temperature gradient was more pronounced for MHC amino acids of the peptide-binding region (PBR), a region that specifically binds to pathogens, than for the non-PBR. For the subset of rivers analyzed for bacterial diversity, MHC amino acid diversity of the PBR also increased significantly with bacterial diversity in each river. A comparison of the relative influence of temperature and bacterial diversity revealed that the latter could have a predominant role on MHC PBR variability. However, temperature was also identified as an important selective agent maintaining MHC diversity in the wild. Based on the bacteria results and given the putative role of temperature in shaping large-scale patterns of pathogen diversity and virulence, bacterial diversity is a plausible selection mechanism explaining the observed association between temperature and MHC variability. Therefore, we propose that genetic diversity at MHC class II represents local adaptation to cope with pathogen diversity in rivers associated with different thermal regimes. This study illuminates the link between selection pressure from the environment, host immune adaptation, and the large-scale genetic population structure for a nonmodel vertebrate in the wild.     

Variation in soil aluminium tolerance genes is associated with local adaptation to soils at the Park Grass Experiment

Studies of the wild grass Anthoxanthum odoratum at the long‐term Park Grass Experiment (PGE, Harpenden, UK) document a well‐known example of rapid plant evolution in response to environmental change. Repeated fertilizer applications have acidified the soil in some experimental plots over the past 150+ years, and Anthoxanthum subpopulations have quickly become locally adapted. Early reciprocal transplants showed subpopulation differentiation specifically in response to soil aluminium (Al) toxicity across the experiment, even at small (30 m) spatial scales. Almost 40 years after its original measurement, we reassessed the degree of local adaptation to soil Al at the PGE using updated phenotyping methods and identified genes with variation linked to the tolerance trait. Root growth assays show that plants are locally adapted to soil Al at both the seedling and adult growth stages, but to a smaller extent than previously inferred. Among a large suite of candidate loci that were previously shown to have Al‐sensitive expression differences between sensitive and tolerant plants, three loci contained SNPs that are associated with both Al tolerance and soil acidity: an Al‐sensitive malate transporter (ALMT), a tonoplast intrinsic protein (TIP) and the putative homolog of the rice cell‐wall modification gene STAR1. Natural genetic variation at these loci is likely to have contributed to the recent rapid evolution at PGE. Continued study of Al tolerance variants in Anthoxanthum will allow us to test hypotheses about the nature and source of genetic variation that enables some species to adapt to soil acidification and other types of rapid environmental change.     

The genomic basis of adaptation to high‐altitude habitats in the eastern honey bee (Apis cerana)

The eastern honey bee (Apis cerana) is of central importance for agriculture in Asia. It has adapted to a wide variety of environmental conditions across its native range in southern and eastern Asia, which includes high‐altitude regions. eastern honey bees inhabiting mountains differ morphologically from neighbouring lowland populations and may also exhibit differences in physiology and behaviour. We compared the genomes of 60 eastern honey bees collected from high and low altitudes in Yunnan and Gansu provinces, China, to infer their evolutionary history and to identify candidate genes that may underlie adaptation to high altitude. Using a combination of F_ST‐based statistics, long‐range haplotype tests and population branch statistics, we identified several regions of the genome that appear to have been under positive selection. These candidate regions were strongly enriched for coding sequences and had high haplotype homozygosity and increased divergence specifically in highland bee populations, suggesting they have been subjected to recent selection in high‐altitude habitats. Candidate loci in these genomic regions included genes related to reproduction and feeding behaviour in honey bees. Functional investigation of these candidate loci is necessary to fully understand the mechanisms of adaptation to high‐altitude habitats in the eastern honey bee.     

Landscape genomics reveals genetic evidence of local adaptation in a widespread tree,the Chinese wingnut (Pterocarya stenoptera)

Understanding the genetic basis underpinning local adaptation is one of the fundamental issues in ecological and evolutionary biology. In this study, we investigated the genomic basis underlying local adaptation of the Chinese wingnut (Pterocarya stenoptera C. DC). Our population genomic analyses revealed nine spatial genetic clusters across the current distribution range of this species. Based on the assessment of genetic–environment association, we found that adaptive divergence of the P. stenoptera populations were mainly shaped by solar radiation during fruit development, temperature seasonality, annual temperature, precipitation, and air humidity. In particular, our genome-wide scanning identified a total of 801 candidate single nucleotide polymorphisms (SNPs) that are highly correlated with diverse environmental factors. Further functional annotation of the SNPs identified some candidate genes that are involved into temperature, water, and light adaptation. Taken together, our results suggest that natural selection during local adaptation has contributed to the success of survival to diverse heterogenous environmental conditions. Our study provides important insights into the fundamental knowledge of the genetic basis underlying the local adaptation of non-model species.     

Lack of evidence for local adaptation to individual plant clones or site by a mobile specialist herbivore

Several studies have documented local adaptation by sedentary insects to individual phenotypes of their host plants. Here, I examined whether a similar phenomenon could be found in a mobile, specialized insect, the sumac flea beetle. Previous work has shown that sumac individuals differ in their suitability as hosts for these beetles and that differences have both an environmental and a genetic basis. Using beetle populations collected as eggs from eight different sumac clones along an east-west transect, a reciprocal transfer experiment was conducted to determine whether there was any evidence for local adaptation by beetles to individual plant clones or to site. Variables examined were larval survivorship past first instar, development time, weight at pupation and patterns of predation by enemies. While no evidence for local adaptation was found, there were significant effects of plant clone on which larvae developed, origin of the larval population and the interaction of these effects on larval performance. For larval weight at pupation, there was also some indication that trade-offs may exist in ability of larvae to use different host plant clones. In addition, there were significant environmental effects on several measures of larval performance. Predation rates differed by plant clone, but not by site or with respect to origin of larvae. While no evidence for local adaptation was found in this study, prerequisites for finding such patterns may exist in this system. Received: 23 May 1996 / Accepted: 26 September 1996