Local adaptation at range edges: comparing elevation and latitudinal gradients

Local adaptation at range edges influences species’ distributions and how they respond to environmental change. However, the factors that affect adaptation, including gene flow and local selection pressures, are likely to vary across different types of range edge. We performed a reciprocal transplant experiment to investigate local adaptation in populations of Plantago lanceolata and P. major from central locations in their European range and from their latitudinal and elevation range edges (in northern Scandinavia and Swiss Alps, respectively). We also characterized patterns of genetic diversity and differentiation in populations using molecular markers. Range‐centre plants of P. major were adapted to conditions at the range centre, but performed similarly to range‐edge plants when grown at the range edges. There was no evidence for local adaptation when comparing central and edge populations of P. lanceolata. However, plants of both species from high elevation were locally adapted when compared with plants from high latitude, although the reverse was not true. This asymmetry was associated with greater genetic diversity and less genetic differentiation over the elevation gradient than over the latitudinal gradient. Our results suggest that adaptation in some range‐edge populations could increase their performance following climate change. However, responses are likely to differ along elevation and latitudinal gradients, with adaptation more likely at high‐elevation. Furthermore, based upon these results, we suggest that gene flow is unlikely to constrain adaptation in range‐edge populations of these species.     

Plant population differentiation and climate change: responses of grassland species along an elevational gradient

Mountain ecosystems are particularly susceptible to climate change. Characterizing intraspecific variation of alpine plants along elevational gradients is crucial for estimating their vulnerability to predicted changes. Environmental conditions vary with elevation, which might influence plastic responses and affect selection pressures that lead to local adaptation. Thus, local adaptation and phenotypic plasticity among low and high elevation plant populations in response to climate, soil and other factors associated with elevational gradients might underlie different responses of these populations to climate warming. Using a transplant experiment along an elevational gradient, we investigated reproductive phenology, growth and reproduction of the nutrient‐poor grassland species Ranunculus bulbosus, Trifolium montanum and Briza media. Seeds were collected from low and high elevation source populations across the Swiss Alps and grown in nine common gardens at three different elevations with two different soil depths. Despite genetic differentiation in some traits, the results revealed no indication of local adaptation to the elevation of population origin. Reproductive phenology was advanced at lower elevation in low and high elevation populations of all three species. Growth and reproduction of T. montanum and B. media were hardly affected by garden elevation and soil depth. In R. bulbosus, however, growth decreased and reproductive investment increased at higher elevation. Furthermore, soil depth influenced growth and reproduction of low elevation R. bulbosus populations. We found no evidence for local adaptation to elevation of origin and hardly any differences in the responses of low and high elevation populations. However, the consistent advanced reproductive phenology observed in all three species shows that they have the potential to plastically respond to environmental variation. We conclude that populations might not be forced to migrate to higher elevations as a consequence of climate warming, as plasticity will buffer the detrimental effects of climate change in the three investigated nutrient‐poor grassland species.     

Trait dimensionality explains widespread variation in local adaptation

All species are locked in a continual struggle to adapt to local ecological conditions. In cases where species fail to locally adapt, they face reduced population growth rates, or even local extinction. Traditional explanations for limited local adaptation focus on maladaptive gene flow or homogeneous environmental conditions. These classical explanations have, however, failed to explain variation in the magnitude of local adaptation observed across taxa. Here we show that variable levels of local adaptation are better explained by trait dimensionality. First, we develop and analyse mathematical models that predict levels of local adaptation will increase with the number of traits experiencing spatially variable selection. Next, we test this prediction by estimating the relationship between dimensionality and local adaptation using data from 35 published reciprocal transplant studies. This analysis reveals a strong correlation between dimensionality and degree of local adaptation, and thus provides empirical support for the predictions of our model.     

Variable effects on growth and defense traits for plant ecotypic differentiation and phenotypic plasticity along elevation gradients

Along ecological gradients, phenotypic differentiation can arise through natural selection on trait diversity and magnitude, and environment‐driven plastic changes. The magnitude of ecotypic differentiation versus phenotypic plasticity can vary depending on the traits under study. Using reciprocal transplant‐common gardens along steep elevation gradients, we evaluated patterns of ecotypic differentiation and phenotypic plasticity of several growth and defense‐related traits for two coexisting but unrelated plant species, Cardamine pratensis and Plantago major. For both species, we observed ecotypic differentiation accompanied by plasticity in growth‐related traits. Plants grew faster and produced more biomass when placed at low elevation. In contrast, we observed fixed ecotypic differentiation for defense and resistance traits. Generally, low‐elevation ecotypes produced higher chemical defenses regardless of the growing elevation. Yet, some plasticity was observed for specific compounds, such as indole glucosinolates. The results of this study may suggest that ecotypic differentiation in defense traits is maintained by costs of chemical defense production, while plasticity in growth traits is regulated by temperature‐driven growth response maximization.     

Widespread phenotypic and genetic divergence along altitudinal gradients in animals

Altitudinal gradients offer valuable study systems to investigate how adaptive genetic diversity is distributed within and between natural populations and which factors promote or prevent adaptive differentiation. The environmental clines along altitudinal gradients tend to be steep relative to the dispersal distance of many organisms, providing an opportunity to study the joint effects of divergent natural selection and gene flow. Temperature is one variable showing consistent altitudinal changes, and altitudinal gradients can therefore provide spatial surrogates for some of the changes anticipated under climate change. Here, we investigate the extent and patterns of adaptive divergence in animal populations along altitudinal gradients by surveying the literature for (i) studies on phenotypic variation assessed under common garden or reciprocal transplant designs and (ii) studies looking for signatures of divergent selection at the molecular level. Phenotypic data show that significant between‐population differences are common and taxonomically widespread, involving traits such as mass, wing size, tolerance to thermal extremes and melanization. Several lines of evidence suggest that some of the observed differences are adaptively relevant, but rigorous tests of local adaptation or the link between specific phenotypes and fitness are sorely lacking. Evidence for a role of altitudinal adaptation also exists for a number of candidate genes, most prominently haemoglobin, and for anonymous molecular markers. Novel genomic approaches may provide valuable tools for studying adaptive diversity, also in species that are not amenable to experimentation.     

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.     

Microbial composition affects the functioning of estuarine sediments

Although microorganisms largely drive many ecosystem processes, the relationship between microbial composition and their functioning remains unclear. To tease apart the effects of composition and the environment directly, microbial composition must be manipulated and maintained, ideally in a natural ecosystem. In this study, we aimed to test whether variability in microbial composition affects functional processes in a field setting, by reciprocally transplanting riverbed sediments between low- and high-salinity locations along the Nonesuch River (Maine, USA). We placed the sediments into microbial ‘cages'' to prevent the migration of microorganisms, while allowing the sediments to experience the abiotic conditions of the surroundings. We performed two experiments, short- (1 week) and long-term (7 weeks) reciprocal transplants, after which we assayed a variety of functional processes in the cages. In both experiments, we examined the composition of bacteria generally (targeting the 16S rDNA gene) and sulfate-reducing bacteria (SRB) specifically (targeting the dsrAB gene) using terminal restriction fragment length polymorphism (T-RFLP). In the short-term experiment, sediment processes (CO₂ production, CH₄ flux, nitrification and enzyme activities) depended on both the sediment''s origin (reflecting differences in microbial composition between salt and freshwater sediments) and the surrounding environment. In the long-term experiment, general bacterial composition (but not SRB composition) shifted in response to their new environment, and this composition was significantly correlated with sediment functioning. Further, sediment origin had a diminished effect, relative to the short-term experiment, on sediment processes. Overall, this study provides direct evidence that microbial composition directly affects functional processes in these sediments.     

Rapid evolution of photoperiodic response in a recently introduced insect Ophraella communa along geographic gradients

The introduced beetle Ophraella communa was first found in 1996 in Japan and has rapidly expanded its distribution to include regions that encompass a wide range of latitude and altitude and are dominated by different host‐plants. In this study, we investigated geographic variation in its photoperiodic response for the induction of reproductive diapause, with which the beetle adjusts its life cycle to local climate and host‐plant phenology. The beetle lines were collected from 18 sites in Japan. The diapause incidence under a photoperiodic condition of 13 h light : 11 h dark (LD 13:11) and the critical day length differed among the beetle lines. Analysis with the generalized linear model showed that latitude, altitude and host‐plant species (Ambrosia artemisiifolia vs. Ambrosia trifida) had significant effects on diapause incidence under LD 13:11. These results suggest that the O. communa populations have rapidly adapted to local environmental conditions after their colonization. However, the photoperiodic response of the O. communa population in Tomakomai, the northernmost part of its distribution range in Japan, deviated significantly from the general trend. We suggest that this deviation is attributed to either: (i) that this beetle has colonized Tomakomai more recently compared to the other sites; or (ii) that the Tomakomai population has adapted to local environments in a different way from other populations.     

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.     

Evidence of neutral and adaptive genetic divergence between European trout populations sampled along altitudinal gradients

Species with a wide geographical distribution are often composed of distinct subgroups which may be adapted to their local environment. European trout (Salmo trutta species complex) provide an example of such a complex consisting of several genetically and ecologically distinct forms. However, trout populations are strongly influenced by human activities, and it is unclear to what extent neutral and adaptive genetic differences have persisted. We sampled 30 Swiss trout populations from heterogeneous environments along replicated altitudinal gradients in three major European drainages. More than 850 individuals were genotyped at 18 microsatellite loci which included loci diagnostic for evolutionary lineages and candidate markers associated with temperature tolerance, reproductive timing and immune defence. We find that the phylogeographic structure of Swiss trout populations has not been completely erased by stocking. Distinct genetic clusters corresponding to the different drainages could be identified, although nonindigenous alleles were clearly present, especially in the two Mediterranean drainages. We also still detected neutral genetic differentiation within rivers which was often associated with the geographical distance between populations. Five loci showed evidence of divergent selection between populations with several drainage-specific patterns. Lineage-diagnostic markers, a marker linked to a quantitative trait locus for upper temperature tolerance in other salmonids and a marker linked to the major histocompatibility class I gene were implicated in local adaptation and some patterns were associated with altitude. In contrast, tentative evidence suggests a signal of balancing selection at a second immune relevant gene (TAP2). Our results confirm the persistence of both neutral and potentially adaptive genetic differences between trout populations in the face of massive human-mediated dispersal.     

Response of dark respiration to temperature in Eriophorum vaginatum from a 30-year-old transplant experiment in Alaska

Background: In the Arctic region, temperature increases are expected to be greater under anticipated climate change than the global average. Understanding how dark respiration (R_d) of common Arctic plant species acclimates to changes in the environment is therefore important for predicting changes to the Arctic carbon balance.

Aims: The aim of this study is to investigate the influence of genotype and growing environment on R_d, the temperature response (Q₁₀) of R_d, and foliar N (N_leaf) of the Arctic sedge Eriophorum vaginatum.

Methods: We measured R_d, and determined its Q₁₀ and N_leaf of E. vaginatum populations that were reciprocally transplanted 30 years previously along a latitudinal transect of 370 km in northern Alaska.

Results: R_d and Q₁₀ did not differ among populations (ecotypes) of E. vaginatum, but the local environment had a significant effect on both variables. R_d as well as N_leaf was higher in northern, colder sites, while Q₁₀ was lower there.

Conclusions: R_d in the different populations of E. vaginatum is a very plastic trait and controlled by growing environment, as is N_leaf. The lower Q₁₀ values in the northern sites were most likely a consequence of substrate inhibition of R_d at higher temperatures.     

Testing the functional significance of microbial composition in natural communities

Ecologists have long studied the relationship between biotic composition and ecosystem functioning in larger organisms; however, only recently has this relationship been investigated widely in microorganisms. Recent studies are reviewed within a framework of three experimental approaches that are often used to study larger organisms: environmental treatment, common garden, and reciprocal transplant experiments. Although the composition of microorganisms cannot be easily manipulated in the field, applying these approaches to intact microbial communities can begin to tease apart the effects of microbial composition from environmental parameters on ecosystem functioning. The challenges in applying these approaches to microorganisms are highlighted and it is discussed how the experimental approach and duration affects a study's interpretation. In general, long-term environmental treatment experiments identify correlative relationships between microbial composition and ecosystem functioning, whereas short-term common garden experiments demonstrate that microbial composition influences ecosystem functioning. Finally, reciprocal transplants simultaneously test for interactive effects of the environment and composition on functioning. The studies reviewed provide evidence that, at least in some cases, microbial composition influences ecosystem functioning. It is concluded that whole-community experiments offer a way to test whether information about microbial composition will help predict ecosystem responses to global change.     

Climate change disrupts local adaptation and favours upslope migration

Contemporary climate change is proceeding at an unprecedented rate. The question remains whether populations adapted to historical conditions can persist under rapid environmental change. We tested whether climate change will disrupt local adaptation and reduce population growth rates using the perennial plant Boechera stricta (Brassicaceae). In a large‐scale field experiment conducted over five years, we exposed > 106 000 transplants to historical, current, or future climates and quantified fitness components. Low‐elevation populations outperformed local populations under simulated climate change (snow removal) across all five experimental gardens. Local maladaptation also emerged in control treatments, but it was less pronounced than under snow removal. We recovered local adaptation under snow addition treatments, which reflect historical conditions. Our results revealed that low elevation populations risk rapid decline, whereas upslope migration could enable population persistence and expansion at higher elevation locales. Local adaptation to historical conditions could increase vulnerability to climate change, even for geographically widespread species.     

Climate adaptation is not enough: warming does not facilitate success of southern tundra plant populations in the high Arctic

Rapidly rising temperatures are expected to cause latitudinal and elevational range shifts as species track their optimal climate north and upward. However, a lack of adaptation to environmental conditions other than climate – for example photoperiod, biotic interactions, or edaphic conditions – might limit the success of immigrants in a new location despite hospitable climatic conditions. Here, we present one of the first direct experimental tests of the hypothesis that warmer temperatures at northern latitudes will confer a fitness advantage to southern immigrants relative to native populations. As rates of warming in the Arctic are more than double the global average, understanding the impacts of warming in Arctic ecosystems is especially urgent. We established experimentally warmed and nonwarmed common garden plots at Alexandra Fiord, Ellesmere Island in the Canadian High Arctic with seeds of two forb species (Oxyria digyna and Papaver radicatum) originating from three to five populations at different latitudes across the Arctic. We found that plants from the local populations generally had higher survival and obtained a greater maximum size than foreign individuals, regardless of warming treatment. Phenological traits varied with latitude of the source population, such that southern populations demonstrated substantially delayed leaf‐out and senescence relative to northern populations. Our results suggest that environmental conditions other than temperature may influence the ability of foreign populations and species to establish at more northerly latitudes as the climate warms, potentially leading to lags in northward range shifts for some species.     

Differentiation in populations of Hordeum spontaneum along a gradient of environmental productivity and predictability: life history and local adaptation

Reciprocal introduction of seeds and seedlings of wild barley, Hordeum spontaneum , originating in four different environments of Israel was used to: (1) test for local adaptation, (2) make inferences about environmental effects on life‐history and reproductive traits, and (3) identify trait combinations with recognizable ‘strategies’. The four populations examined represented the following environments: (1) desert ? low productivity and predictability, drought stress; (2) semi‐steppe batha ? moderate productivity and predictability; (3) grassland ? high productivity and predictability; and (4) mountain ? high productivity and predictability but with severe frost stress. Significant genotype‐by‐environment interactions were observed for yield and reproductive biomass, seedling biomass and percentage germinated and survived seeds, suggesting local ecotype adaptation. Increasing productivity and predictability of environment in respect to rainfall, without concomitant frost stress, was found to select for high reproductive biomass and large seeds, a high fraction of germinating seeds and high vigour of seedlings. The optimal strategy changes with increasing productivity and predictability and involves a trade‐off between seed size and number, with reduced yield but increased seed mass, consistent with competition selection (or K‐selection sensu MacArthur & Wilson (1967 )) type. No specific life‐history adaptations to predictable frost stress were detected for the mountain ecotype, but there was higher survival of seedlings in their indigenous (mountain) environment compared with other ecotypes. The latter appears to be a physiological adaptation to frost, which is consistent with selection for stress tolerance (or S‐selection sensu Grime (1977 )) type. The other stress factor, drought, which is very unpredictable in deserts, was associated with high seed dormancy, small seed size and low vigour of seedlings, but relatively high yield, which is consistent with a stress‐escape bet‐hedging strategy. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77 , 479–490.     

Local adaptation and ecological differentiation under selection,migration, and drift in Arabidopsis lyrata*

How the balance between selection, migration, and drift influences the evolution of local adaptation has been under intense theoretical scrutiny. Yet, empirical studies that relate estimates of local adaptation to quantification of gene flow and effective population sizes have been rare. Here, we conducted a reciprocal transplant trial, a common garden trial, and a whole‐genome‐based demography analysis to examine these effects among Arabidopsis lyrata populations from two altitudinal gradients in Norway. Demography simulations indicated that populations within the two gradients are connected by gene flow (0.1 < 4N_em < 11) and have small effective population sizes (N_e < 6000), suggesting that both migration and drift can counteract local selection. However, the three‐year field experiments showed evidence of local adaptation at the level of hierarchical multiyear fitness, attesting to the strength of differential selection. In the lowland habitat, local superiority was associated with greater fecundity, while viability accounted for fitness differences in the alpine habitat. We also demonstrate that flowering time differentiation has contributed to adaptive divergence between these locally adapted populations. Our results show that despite the estimated potential of gene flow and drift to hinder differentiation, selection among these A. lyrata populations has resulted in local adaptation.