Aim
Many studies use differences among plant populations to infer future plant responses, but these predictions will provide meaningful insights only if patterns of plasticity among populations are ...similar (i.e., in the absence of population‐by‐environment interaction, P × E). In this study, we tested whether P × E is considered in climate change studies. Specifically, we evaluated whether population differentiation varies across environments and whether P × E is determined by aspects of the study system and experimental design.
Location
Global.
Methods
We conducted a literature search in the Thomson Reuters Web of Science database to identify studies assessing population differentiation in a climate change context. We quantified the occurrence of P × E and performed a meta‐analysis to calculate the percentage of traits showing P × E in the study cases.
Results
We identified 309 study cases (from 237 published articles) assessing population differentiation in 172 plant species, of which 64% included more than one test environment and tested P × E. In 77% of these studies, P × E was significant for at least one functional trait. The overall proportion of traits showing P × E was 33.4% (95% confidence interval 27.7–39.3). These results were generally consistent across life‐forms, ecoregions and type of experiment. Furthermore, population differentiation varied across test environments in 76% of cases. The overall proportion of traits showing environment‐dependent population differentiation was 53.7% (95% confidence interval 37.9–69.3).
Conclusions
Our findings revealed that differences in phenotypic plasticity among populations are common but are usually neglected in order to forecast population responses to climate change. Future studies should assess population differentiation in many test environments (accounting for P × E) that realistically reflect future environmental conditions, assessing climate change drivers that are rarely considered (e.g., multifactor experiments incorporating higher CO2 levels). Our review also revealed the predominant focus of population studies on trees from temperate climates, identifying underexplored life‐forms (shrubs, annuals), phylogenetic groups (ferns, ancient gymnosperms) and ecoregions (tropical, arctic) that should receive more attention in future.
• It is hypothesised that tree distributions in Europe are largely limited by their ability to cope with the summer drought imposed by the Mediterranean climate in the southern areas and by their ...competitive potential in central regions with more mesic conditions.
• We investigated the extent to which leaf and plant morphology, gas exchange, leaf and stem hydraulics and growth rates have evolved in a coordinated way in oaks (Quercus) as a result of adaptation to contrasting environmental conditions in this region. We implemented an experiment in which seedlings of 12 European/North African oaks were grown under two watering treatments, a well-watered treatment and a drought treatment in which plants were subjected to three cycles of drought.
• Consistent with our hypothesis, species from drier summers had traits conferring more tolerance to drought such as small sclerophyllous leaves and lower percent loss of hydraulic conductivity. However, these species did not have lower growth rates as expected by a trade-off with drought tolerance.
• Overall, our results revealed that climate is an important driver of functional strategies in oaks and that traits have evolved along two coordinated functional axes to adapt to different precipitation and temperature regimes.
Summary
Resource‐use strategies are hypothesized to evolve along climatic gradients. However, our understanding of the environmental factors driving divergent evolution of resource‐use strategies and ...the relationship between trait genetic variation and phenotypic plasticity is far from complete. Using the Mediterranean tree Quercus faginea as study system, we tested the hypothesis that a conservative resource‐use strategy with increased drought tolerance and reduced phenotypic plasticity has evolved in areas with longer and more severe dry seasons.
We conducted a glasshouse experiment in which we measured leaf morphological, physiological, growth and allocation traits in seedlings from 10 range‐wide climatically contrasting populations, grown under two different watering treatments.
Both univariate and multivariate analyses revealed a genetic gradient of resource‐use strategies and phenotypic plasticity associated with provenance climate. In particular, populations from harsher (drier and colder) environments had more sclerophyllous leaves, lower growth rates, better physiological performance under dry conditions and reduced multi‐trait phenotypic plasticity compared to populations from more mesic and milder environments.
Our results suggest that contrasting precipitation and temperature regimes play an important role in the adaptive intraspecific evolution of multivariate phenotypes and their plasticity, resulting in coordinated morphology, physiology, growth and allometry according to alternative resource‐use strategies.
This article comments on:
Georgia L. Vasey, Alexandra K. Urza, Jeanne C. Chambers, Elizabeth G. Pringle and Peter J. Weisberg. Clinal variations in seedling traits and responses to water availability ...correspond to seed-source environmental gradients in a foundational dryland tree species, Annals of Botany, Volume 132, Issue 2, 25 July 2023, Pages 203–216, https://doi.org/10.1093/aob/mcad041
Summary
Future increases in drought severity and frequency are predicted to have substantial impacts on plant function and survival. However, there is considerable uncertainty concerning what drought ...adjustment is and whether plants can adjust to sustained drought. This review focuses on woody plants and synthesises the evidence for drought adjustment in a selection of key above‐ground and below‐ground plant traits. We assess whether evaluating the drought adjustment of single traits, or selections of traits that operate on the same plant functional axis (e.g. photosynthetic traits) is sufficient, or whether a multi‐trait approach, integrating across multiple axes, is required. We conclude that studies on drought adjustments in woody plants might overestimate the capacity for adjustment to drier environments if spatial studies along gradients are used, without complementary experimental approaches. We provide evidence that drought adjustment is common in above‐ground and below‐ground traits; however, whether this is adaptive and sufficient to respond to future droughts remains uncertain for most species. To address this uncertainty, we must move towards studying trait integration within and across multiple axes of plant function (e.g. above‐ground and below‐ground) to gain a holistic view of drought adjustments at the whole‐plant scale and how these influence plant survival.
Key message
Local adaptation largely segregates between traits affecting light responses and water relations, but population-level differences in stomatal conductance when growth is unconstrained ...converge among populations under water stress.
Warming temperatures and altered precipitation patterns threaten plant populations worldwide. European beech (
Fagus sylvatica
) is a species that expresses both high phenotypic plasticity and local adaptation among populations. Beech seedlings’ susceptibility to prolonged drought may be dictated by their immediate light environment. We tested whether seedlings of four beech provenances, from contrasting edaphoclimatic environments, expressed differences in trait responses to imposed water stress under sun and shade treatments. Populations from the southern range margin were expected to display greater water-stress tolerance and core populations’ faster growth rates in the absence of abiotic limitations. Both high light and water stress induced differences in trait responses among provenances, but traits that failed to respond to our experimental treatments likewise did not segregate at the provenance level. Hence, those traits responding to light, e.g., increasing leaf flavonol index and leaf mass area, also tended to differ among provenances. Similarly, there was evidence of local adaptation among provenances in traits, like midday leaf water potential, responding to water stress. Exceptionally, there was a three way interaction water- × -light- × -provenance for stomatal conductance which converged among provenances under water stress. Leaf chlorophyll content also varied both with light and water in a provenance-specific manner. We found core provenances’ growth traits to outperform others under favourable conditions, whereas southern and high-elevation populations displayed traits adapted to tolerate high irradiance. Only stomatal conductance produced a complementary interactive response between light- × -water across provenances, whereas other traits responded less to combined water stress and high irradiance than to either treatment alone.
Abstract
In Mediterranean-type ecosystems, drought is considered the main ecological filter for seedling establishment. The evergreen oaks Quercus ilex L. and Quercus suber L. are two of the most ...abundant tree species in the Mediterranean Basin. Despite their shared evergreen leaf habit and ability to resist low soil water potentials, traditionally it has been suggested that Q. ilex is better suited to resist dry conditions than Q. suber. In this study, we examined how seedlings of Q. ilex and Q. suber grown in sandy soils responded to different levels of water availability using natural dry conditions and supplemental watering. Specifically, we estimated survival and water status of seedlings and explored the role of acorn mass and belowground biomass in seedling performance. To our surprise, Q. suber was better able to survive the summer drought in our experiment than Q. ilex. Nearly 55% of the Q. suber seedlings remained alive after a 2-month period without rain or supplemental water, which represents almost 20% higher survival than Q. ilex over the same period. At the end of the dry period, the surviving seedlings of Q. suber had strikingly higher water potential, potential maximum quantum yield of photosystem II (Fv/Fm) and stomatal conductance (gs) than those of Q. ilex. Acorn mass was associated with the probability of survival under dry conditions; however, it did not explain the differences in survival or water status between the species. In contrast, Q. suber had a higher root ratio and root:shoot ratio than Q. ilex and these traits were positively associated with predawn leaf water potential, Fv/Fm, gs and survival. Taken together, our results suggest that the higher relative investment in roots by Q. suber when growing in a sandy acidic substrate allowed this species to maintain better physiological status and overall condition than Q. ilex, increasing its probability of survival in dry conditions.
Phenotypic differences among populations stem from the interaction between neutral and adaptive processes, and phenotypic plasticity. Although clinal trait variation along climatic gradients often ...evolves in widely distributed species, it is unknown whether substrate specialization, such as that of Mediterranean gypsum plants, has constrained adaptation to climate.
Using a common garden experiment with two contrasting watering treatments, we quantified phenotypic plasticity, assessed evidence for footprints of selection using FST – QST comparisons, and evaluated the ecological factors driving genetically based phenotypic differentiation of 11 populations encompassing the full environmental range of the gypsum shrub Lepidium subulatum.
We found evidence for genetic differentiation among populations related to climatic differences, with populations from warmer and drier sites showing lower specific leaf area and leaf N, earlier phenology, greater water use efficiency and greater fitness. Multiple lines of evidence suggest that this differentiation was driven by past divergent selection rather than neutral processes. All populations showed high phenotypic plasticity, indicating that plasticity has not been selected against, even in populations from sites with harsher climatic conditions.
Synthesis. Our results indicate that despite strong substrate specialization, adaptive differentiation related to climatic gradients occurs in this species. However, we also found that populations from mesic sites may be particularly vulnerable to future climate change given their relatively lower fitness under both wet and dry conditions.
Resumen
Las diferencias fenotípicas entre poblaciones son fruto de la interacción entre los procesos evolutivos neutrales y adaptativos, y la plasticidad fenotípica. Las poblaciones de especies ampliamente distribuidas a menudo muestran diferencias fenotípicas asociadas a un determinado gradiente ambiental. Sin embargo, se desconoce si la especialización a substratos específicos, como la ocurrida en las plantas mediterráneas restringidas a suelos de yeso, ha podido limitar su adaptación al clima.
Usando un experimento de jardín común con dos tratamientos contrastados de disponibilidad hídrica, hemos evaluado los patrones de plasticidad fenotípica, la evidencia de huellas de selección pasada mediante comparaciones FST ‐ QST, y los factores ecológicos involucrados en la diferenciación fenotípica de base genética de 11 poblaciones a lo largo de todo el gradiente ambiental del arbusto gipsófito Lepidium subulatum.
Encontramos diferenciación genética ligada a diferencias climáticas. Las poblaciones de sitios más cálidos y secos mostraron menor área foliar específica y nitrógeno foliar, fenologías adelantadas, mayor eficiencia del uso del agua y mayor éxito reproductivo. Múltiples evidencias sugieren que dicha diferenciación ha sido causada por selección divergente pasada en vez de por procesos neutrales. Todas las poblaciones mostraron una elevada plasticidad fenotípica, lo que indica que la selección natural no ha actuado en contra de la plasticidad, incluso en las poblaciones con condiciones ambientales más duras.
Síntesis. Nuestros resultados muestran que, a pesar de la fuerte especialización al sustrato, existe diferenciación fenotípica adaptativa asociada a un gradiente climático en esta especie. No obstante, las poblaciones de sitios más fríos y húmedos podrían mostrar una mayor vulnerabilidad al cambio climático, debido a su menor éxito reproductivo tanto en condiciones de sequía como de alta disponibilidad hídrica.
Despite strong specialization to gypsum soils, past divergent selection related to climatic gradients has driven adaptive population differentiation in Lepidium subulatum. All populations showed high but similar plasticity to drought, indicating that selection did not act against plasticity in harsh environmental conditions. Populations from mesic sites may be particularly vulnerable to climate change, given their lower fitness under both wet and dry conditions.
Improving our knowledge of how past climate‐driven selection has acted on present‐day trait population divergence is essential to understand local adaptation processes and improve our predictions of ...evolutionary trajectories in the face of altered selection pressures resulting from climate change. In this study, we investigated signals of selection on traits related to drought tolerance and growth rates in two Mediterranean oak species (Quercus faginea and Q. lusitanica) with contrasting distribution ranges and climatic niches. We genotyped 182 individuals from 24 natural populations of the two species using restriction‐site‐associated DNA sequencing and conducted a thorough functional characterization in 1602 seedlings from 21 populations cultivated in common garden experiments under contrasting watering treatments. Our genomic data revealed that both Q. faginea and Q. lusitanica have very weak population genetic structure, probably as a result of high rates of pollen‐mediated gene flow among populations and large effective population sizes. In contrast, common garden experiments showed evidence of climate‐driven divergent selection among populations on traits related to leaf morphology, physiology and growth in both species. Overall, our study suggests that climate is an important selective factor for Mediterranean oaks and that ecophysiological traits have evolved in drought‐prone environments even in a context of very high rates of gene flow among populations.
Summary
Early‐stage fitness variation has been seldom evaluated at broad scales in forest tree species, despite the long tradition of studying climate‐driven intraspecific genetic variation. In this ...study, we evaluated the role of climate in driving patterns of population differentiation at early‐life stages in Pinus sylvestris and explored the fitness and growth consequences of seed transfer within the species range.
We monitored seedling emergence, survival and growth over a 2‐yr period in a multi‐site common garden experiment which included 18 European populations and spanned 25° in latitude and 1700 m in elevation.
Climate–fitness functions showed that populations exhibited higher seedling survival and growth at temperatures similar to their home environment, which is consistent with local adaptation. Northern populations experienced lower survival and growth at warmer sites, contrary to previous studies on later life stages. Seed mass was higher in populations from warmer areas and was positively associated with survival and growth at more southern sites. Finally, we did not detect a survival–growth trade‐off; on the contrary, bigger seedlings exhibited higher survival probabilities under most climatic conditions.
In conclusion, our results reveal that contrasting temperature regimes have played an important role in driving the divergent evolution of P. sylvestris populations at early‐life stages.
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