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.     

Temperature effects on forest herbs assessed by warming and transplant experiments along a latitudinal gradient

Slow‐colonizing forest understorey plants are probably not able to rapidly adjust their distribution range following large‐scale climate change. Therefore, the acclimation potential to climate change within their actual occupied habitats will likely be key for their short‐ and long‐term persistence. We combined transplant experiments along a latitudinal gradient with open‐top chambers to assess the effects of temperature on phenology, growth and reproductive performance of multiple populations of slow‐colonizing understorey plants, using the spring flowering geophytic forb Anemone nemorosa and the early summer flowering grass Milium effusum as study species. In both species, emergence time and start of flowering clearly advanced with increasing temperatures. Vegetative growth (plant height, aboveground biomass) and reproductive success (seed mass, seed germination and germinable seed output) of A. nemorosa benefited from higher temperatures. Climate warming may thus increase future competitive ability and colonization rates of this species. Apart from the effects on phenology, growth and reproductive performance of M. effusum generally decreased when transplanted southwards (e.g., plant size and number of individuals decreased towards the south) and was probably more limited by light availability in the south. Specific leaf area of both species increased when transplanted southwards, but decreased with open‐top chamber installation in A. nemorosa. In general, individuals of both species transplanted at the home site performed best, suggesting local adaptation. We conclude that contrasting understorey plants may display divergent plasticity in response to changing temperatures which may alter future understorey community dynamics.     

Plant responses to simulated warming and drought: a comparative study of functional plasticity between congeneric mid and high elevation species

Aims Effects of climate change, especially changes in temperatures and precipitation patterns, are particularly pronounced in alpine regions. In response, plants may exhibit phenotypic plasticity in key functional traits allowing short-term adjustment to novel conditions. However, little is known about the degree of phenotypic plasticity of high elevation species relative to mid elevation congeners.Methods We transplanted 14 herbaceous perennial species from high elevation into two common gardens (1050 and 2000 m.a.s.l.) in the Swiss Alps, and we examined plastic responses in key functional traits to changes in temperature and soil water availability. This design was replicated with 14 congeneric species from mid elevation to assess if the degree of phenotypic plasticity differs between mid and high elevation species. Survival was assessed across two growing seasons, while aboveground biomass and specific leaf area (SLA) were measured after the first growing season, and biomass allocation to belowground and reproductive structures after the second. Moreover, a phenotypic plasticity index was calculated for the functional traits to compare the degree of plasticity between mid and high elevation species.Important findings Aboveground biomass was higher in mid elevation species relative to high elevation congeners in all treatments, yet decreased for both with elevation and drought. Similarly, SLA decreased with elevation and drought. Root mass fraction (RMF) was generally higher in high elevation species, and decreased with drought at the lower site. Drought increased the allocation to reproductive structures, especially when plants were grown at their elevation of origin. Interestingly, no difference was found in the degree of phenotypic plasticity averaged across mid and high elevation species for any of the studied functional traits. These results indicate that phenotypic plasticity in the focal traits did not depend on the elevation of origin of the species. Plasticity was not related to environmental heterogeneity, nor constrained by selective pressures at high elevation. However, both species groups showed a remarkable capacity for short-term acclimation to a prospective climate through rapid adjustments in key functional traits.     

Phenological plasticity is a poor predictor of subalpine plant population performance following experimental climate change

Phenological shifts, changes in the seasonal timing of life cycle events, are among the best documented responses of species to climate change. However, the consequences of these phenological shifts for population dynamics remain unclear. Population growth could be enhanced if species that advance their phenology benefit from longer growing seasons and gain a pre-emptive advantage in resource competition. However, it might also be reduced if phenological advances increase exposure to stresses, such as herbivores and, in colder climates, harsh abiotic conditions early in the growing season. We exposed subalpine grasslands to ~3 K of warming by transplanting intact turfs from 2000 m to 1400 m elevation in the eastern Swiss Alps, with turfs transplanted within the 2000 m site acting as a control. In the first growing season after transplantation, we recorded species’ flowering phenology at both elevations. We also measured species’ cover change for three consecutive years as a measure of plant performance. We used models to estimate species’ phenological plasticity (the response of flowering time to the change in climate) and analysed its relationship with cover changes following climate change. The phenological plasticity of the 18 species in our study varied widely but was unrelated to their changes in cover. Moreover, early- and late-flowering species did not differ in their cover response to warming, nor in the relationship between cover changes and phenological plasticity. These results were replicated in a similar transplant experiment within the same subalpine community, established one year earlier and using larger turfs. We discuss the various ecological processes that can be affected by phenological shifts, and argue why the population-level consequences of these shifts are likely to be species- and context-specific. Our results highlight the importance of testing assumptions about how warming-induced changes in phenotypic traits, like phenology, impact population dynamics.     

Plasticity of functional traits varies clinally along a rainfall gradient in Eucalyptus tricarpa

Widespread species often occur across a range of climatic conditions, through a combination of local genetic adaptations and phenotypic plasticity. Species with greater phenotypic plasticity are likely to be better positioned to cope with rapid anthropogenic climate changes, while those displaying strong local adaptations might benefit from translocations to assist the movement of adaptive genes as the climate changes. Eucalyptus tricarpa occurs across a climatic gradient in south‐eastern Australia, a region of increasing aridity, and we hypothesized that this species would display local adaptation to climate. We measured morphological and physiological traits reflecting climate responses in nine provenances from sites of 460 to 1040 mm annual rainfall, in their natural habitat and in common gardens near each end of the gradient. Local adaptation was evident in functional traits and differential growth rates in the common gardens. Some traits displayed complex combinations of plasticity and genetic divergence among provenances, including clinal variation in plasticity itself. Provenances from drier locations were more plastic in leaf thickness, whereas leaf size was more plastic in provenances from higher rainfall locations. Leaf density and stomatal physiology (as indicated by δ¹³C and δ¹⁸O) were highly and uniformly plastic. In addition to variation in mean trait values, genetic variation in trait plasticity may play a role in climate adaptation.     

Forest tree species adaptation to climate across biomes: Building on the legacy of ecological genetics to anticipate responses to climate change

Intraspecific variation plays a critical role in extant and future forest responses to climate change. Forest tree species with wide climatic niches rely on the intraspecific variation resulting from genetic adaptation and phenotypic plasticity to accommodate spatial and temporal climate variability. A centuries-old legacy of forest ecological genetics and provenance trials has provided a strong foundation upon which to continue building on this knowledge, which is critical to maintain climate-adapted forests. Our overall objective is to understand forest trees intraspecific responses to climate across species and biomes, while our specific objectives are to describe ecological genetics models used to build our foundational knowledge, summarize modeling approaches that have expanded the traditional toolset, and extensively review the literature from 1994 to 2021 to highlight the main contributions of this legacy and the new analyzes of provenance trials. We reviewed 103 studies comprising at least three common gardens, which covered 58 forest tree species, 28 of them with range-wide studies. Although studies using provenance trial data cover mostly commercially important forest tree species from temperate and boreal biomes, this synthesis provides a global overview of forest tree species adaptation to climate. We found that evidence for genetic adaptation to local climate is commonly present in the species studied (79%), being more common in conifers (87.5%) than in broadleaf species (67%). In 57% of the species, clines in fitness-related traits were associated with temperature variables, in 14% of the species with precipitation, and in 25% of the species with both. Evidence of adaptation lags was found in 50% of the species with range-wide studies. We conclude that ecological genetics models and analysis of provenance trial data provide excellent insights on intraspecific genetic variation, whereas the role and limits of phenotypic plasticity, which will likely determine the fate of extant forests, is vastly understudied.     

Trait differentiation and adaptation of plants along elevation gradients

Studies of genetic adaptation in plant populations along elevation gradients in mountains have a long history, but there has until now been neither a synthesis of how frequently plant populations exhibit adaptation to elevation nor an evaluation of how consistent underlying trait differences across species are. We reviewed studies of adaptation along elevation gradients (i) from a meta‐analysis of phenotypic differentiation of three traits (height, biomass and phenology) from plants growing in 70 common garden experiments; (ii) by testing elevation adaptation using three fitness proxies (survival, reproductive output and biomass) from 14 reciprocal transplant experiments; (iii) by qualitatively assessing information at the molecular level, from 10 genomewide surveys and candidate gene approaches. We found that plants originating from high elevations were generally shorter and produced less biomass, but phenology did not vary consistently. We found significant evidence for elevation adaptation in terms of survival and biomass, but not for reproductive output. Variation in phenotypic and fitness responses to elevation across species was not related to life history traits or to environmental conditions. Molecular studies, which have focussed mainly on loci related to plant physiology and phenology, also provide evidence for adaptation along elevation gradients. Together, these studies indicate that genetically based trait differentiation and adaptation to elevation are widespread in plants. We conclude that a better understanding of the mechanisms underlying adaptation, not only to elevation but also to environmental change, will require more studies combining the ecological and molecular approaches.     

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.     

Phenotypic differentiation of the Solidago virgaurea complex along an elevational gradient: Insights from a common garden experiment and population genetics

Plant species distributed along wide elevational or latitudinal gradients show phenotypic variation due to their heterogeneous habitats. This study investigated whether phenotypic variation in populations of the Solidago virgaurea complex along an elevational gradient is caused by genetic differentiation. A common garden experiment was based on seeds collected from nine populations of the S. virgaurea complex growing at elevations from 1,597 m to 2,779 m a.s.l. on Mt. Norikura in central Japan. Population genetic analyses with microsatellite markers were used to infer the genetic structure and levels of gene flow between populations. Leaf mass per area was lower, while leaf nitrogen and chlorophyll concentrations were greater for higher elevations at which seeds were originally collected. For reproductive traits, plants derived from higher elevations had larger flower heads on shorter stems and flowering started earlier. These elevational changes in morphology were consistent with the clines in the field, indicating that phenotypic variation along the elevational gradient would have been caused by genetic differentiation. However, population genetic analysis using 16 microsatellite loci suggested an extremely low level of genetic differentiation of neutral genes among the nine populations. Analysis of molecular variance also indicated that most genetic variation was partitioned into individuals within a population, and the genetic differentiation among the populations was not significant. This study suggests that genome regions responsible for adaptive traits may differ among the populations despite the existence of gene flow and that phenotypic variation of the S. virgaurea complex along the elevational gradient is maintained by strong selection pressure.     

Adaptive responses for seed and leaf phenology in natural populations of sessile oak along an altitudinal gradient

We assessed the adaptive potential of seed and leaf phenology in 10 natural populations of sessile oak (Quercus petraea) sampled along two altitudinal transects using common garden experiments. Population differentiation for both phenological traits was observed with high-altitude populations germinating and flushing later than low altitude ones. However, high genetic variation and heritability values were also maintained within populations, despite slightly decreasing for dates of leaf unfolding with increasing altitude. We suggest that biotic and abiotic fluctuating selection pressures within populations and high gene flow are the main mechanisms maintaining high genetic variation for these fitness related traits. Moreover, changes in selection intensity and/or selection pressures along the altitudinal gradient can explain the reduction in genetic variation observed for leaf phenology. We anticipate that the maintenance of high genetic variation will be a valuable resource for future adaptation of sessile oak populations undergoing an upslope shift caused by climate change.     

The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change

Species are the unit of analysis in many global change and conservation biology studies; however, species are not uniform entities but are composed of different, sometimes locally adapted, populations differing in plasticity. We examined how intraspecific variation in thermal niches and phenotypic plasticity will affect species distributions in a warming climate. We first developed a conceptual model linking plasticity and niche breadth, providing five alternative intraspecific scenarios that are consistent with existing literature. Secondly, we used ecological niche‐modeling techniques to quantify the impact of each intraspecific scenario on the distribution of a virtual species across a geographically realistic setting. Finally, we performed an analogous modeling exercise using real data on the climatic niches of different tree provenances. We show that when population differentiation is accounted for and dispersal is restricted, forecasts of species range shifts under climate change are even more pessimistic than those using the conventional assumption of homogeneously high plasticity across a species' range. Suitable population‐level data are not available for most species so identifying general patterns of population differentiation could fill this gap. However, the literature review revealed contrasting patterns among species, urging greater levels of integration among empirical, modeling and theoretical research on intraspecific phenotypic variation.     

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.     

Clinal adaptation and adaptive plasticity in Artemisia californica: implications for the response of a foundation species to predicted climate change

Local adaptation and plasticity pose significant obstacles to predicting plant responses to future climates. Although local adaptation and plasticity in plant functional traits have been documented for many species, less is known about population‐level variation in plasticity and whether such variation is driven by adaptation to environmental variation. We examined clinal variation in traits and performance – and plastic responses to environmental change – for the shrub Artemisia californica along a 700 km gradient characterized (from south to north) by a fourfold increase in precipitation and a 61% decrease in interannual precipitation variation. Plants cloned from five populations along this gradient were grown for 3 years in treatments approximating the precipitation regimes of the north and south range margins. Most traits varying among populations did so clinally; northern populations (vs. southern) had higher water‐use efficiencies and lower growth rates, C : N ratios and terpene concentrations. Notably, there was variation in plasticity for plant performance that was strongly correlated with source site interannual precipitation variability. The high‐precipitation treatment (vs. low) increased growth and flower production more for plants from southern populations (181% and 279%, respectively) than northern populations (47% and 20%, respectively). Overall, precipitation variability at population source sites predicted 86% and 99% of variation in plasticity in growth and flowering, respectively. These striking, clinal patterns in plant traits and plasticity are indicative of adaptation to both the mean and variability of environmental conditions. Furthermore, our analysis of long‐term coastal climate data in turn indicates an increase in interannual precipitation variation consistent with most global change models and, unexpectedly, this increased variation is especially pronounced at historically stable, northern sites. Our findings demonstrate the critical need to integrate fundamental evolutionary processes into global change models, as contemporary patterns of adaptation to environmental clines will mediate future plant responses to projected climate change.     

Transgenerational plasticity as an important mechanism affecting response of clonal species to changing climate

In spite of the increasing number of studies on the importance of transgenerational plasticity for species response to novel environments, its effects on species ability to respond to climate change are still largely unexplored. We study the importance of transgenerational plasticity for response of a clonal species Festuca rubra. Individuals from four natural populations representing two levels of temperature and two levels of precipitation were cultivated in four growth chambers that simulate the temperature and precipitation of origin of the populations (maternal phase). Each population was represented in each growth chamber. After 6 months, single young ramets of these plants were reshuffled among the growth chambers and let to grow for additional 2 months (offspring phase). The results show that transgenerational effects (i.e., maternal phase conditions) significantly modify species response to novel climates, and the direction and intensity of the response depend on the climate of origin of the plants. For traits related to recourse acquisition, the conditions of maternal phase, either alone or in interaction mainly with climate of origin, had stronger effect than the conditions of cultivation. Overall, the maternal climate interacted more intensively with the climate of origin than with the offspring climate. The direction of the effect of the maternal climate was of different directions and intensities depending on plant origin and trait studied. The data demonstrated strong significant effects of conditions during maternal phase on species response to novel climates. These transgenerational affects were, however, not adaptive. Still, transgenerational plasticity may be an important driver of species response to novel conditions across clonal generations. These effects thus need to be carefully considered in future studies exploring species response to novel climates. This will also have strong effects on species performance under increasingly variable climates expected to occur with the climate change.     

Temperature adaptation of soil bacterial communities along an Antarctic climate gradient: predicting responses to climate warming

Soil microorganisms, the central drivers of terrestrial Antarctic ecosystems, are being confronted with increasing temperatures as parts of the continent experience considerable warming. Here we determined short‐term temperature dependencies of Antarctic soil bacterial community growth rates, using the leucine incorporation technique, in order to predict future changes in temperature sensitivity of resident soil bacterial communities. Soil samples were collected along a climate gradient consisting of locations on the Antarctic Peninsula (Anchorage Island, 67 °34′S, 68 °08′W), Signy Island (60 °43′S, 45 °38′W) and the Falkland Islands (51 °76′S 59 °03′W). At each location, experimental plots were subjected to warming by open top chambers (OTCs) and paired with control plots on vegetated and fell‐field habitats. The bacterial communities were adapted to the mean annual temperature of their environment, as shown by a significant correlation between the mean annual soil temperature and the minimum temperature for bacterial growth (T_min). Every 1 °C rise in soil temperature was estimated to increase T_min by 0.24–0.38 °C. The optimum temperature for bacterial growth varied less and did not have as clear a relationship with soil temperature. Temperature sensitivity, indicated by Q₁₀ values, increased with mean annual soil temperature, suggesting that bacterial communities from colder regions were less temperature sensitive than those from the warmer regions. The OTC warming (generally <1 °C temperature increases) over 3 years had no effects on temperature relationship of the soil bacterial community. We estimate that the predicted temperature increase of 2.6 °C for the Antarctic Peninsula would increase T_min by 0.6–1 °C and Q₁₀ (0–10 °C) by 0.5 units.     

Local adaptation and cogradient selection in the alpine plant, Poa hiemata, along a narrow altitudinal gradient

Alpine environments are particularly susceptible to environmental changes associated with global warming but there is potential for alpine plants to adapt to warming if local adaptation occurs and gene flow allows genotypes adapted to low altitudes to colonize higher altitude sites. Here we examine the adaptive potential of a common alpine grass, Poa hiemata, within the restricted alpine habitat of Australian mountains, across a narrow altitudinal gradient replicated in three areas. Grasses at high altitude sites had shorter leaf lengths and larger circumferences than those at lower sites. Transplant experiments with clonal material and plants grown from seed indicated that these differences were partly genetic, with environmental and genetic factors both contributing to the differences between altitudes. Differences in altitudinal forms were also evident in a common garden experiment. Plants showed a home-site advantage in terms of survival. A fitness analysis indicated that at high altitude sites, selection favored plants with short leaves and larger circumferences, whereas these traits were selected in the opposite direction at the low altitude sites. These findings indicate cogradient selection and potential for both plastic and genotypic shifts in response to climate change in P. hiemata.     

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.     

Distinct responses and range shifts of lizard populations across an elevational gradient under climate change

Ongoing climate change has profoundly affected global biodiversity, but its impacts on populations across elevations remain understudied. Using mechanistic niche models incorporating species traits, we predicted ecophysiological responses (activity times, oxygen consumption and evaporative water loss) for lizard populations at high-elevation (<3600 m asl) and extra-high-elevation (≥3600 m asl) under recent (1970–2000) and future (2081–2100) climates. Compared with their high-elevation counterparts, lizards from extra-high-elevation are predicted to experience a greater increase in activity time and oxygen consumption. By integrating these ecophysiological responses into hybrid species distribution models (HSDMs), we were able to make the following predictions under two warming scenarios (SSP1-2.6, SSP5-8.5). By 2081–2100, we predict that lizards at both high- and extra-high-elevation will shift upslope; lizards at extra-high-elevation will gain more and lose less habitat than will their high-elevation congeners. We therefore advocate the conservation of high-elevation species in the context of climate change, especially for those populations living close to their lower elevational range limits. In addition, by comparing the results from HSDMs and traditional species distribution models, we highlight the importance of considering intraspecific variation and local adaptation in physiological traits along elevational gradients when forecasting species' future distributions under climate change.