Ecological trade-offs drive phenotypic and genetic differentiation of Arabidopsis thaliana in Europe.

Plant diversity is shaped by trade-offs between traits related to competitive ability, propagule dispersal, and stress resistance. However, we still lack a clear understanding of how these trade-offs influence species distribution and population dynamics. In Arabidopsis thaliana, recent genetic analyses revealed a group of cosmopolitan genotypes that successfully recolonized Europe from its center after the last glaciation, excluding older (relict) lineages from the distribution except for their north and south margins. Here, we tested the hypothesis that cosmopolitans expanded due to higher colonization ability, while relicts persisted at the margins due to higher tolerance to competition and/or stress. We compared the phenotypic and genetic differentiation between 71 European genotypes originating from the center, and the south and north margins. We showed that a trade-off between plant fecundity and seed mass shapes the differentiation of A. thaliana in Europe, suggesting that the success of the cosmopolitan groups could be explained by their high dispersal ability. However, at both north and south margins, we found evidence of selection for alleles conferring low dispersal but highly competitive and stress-resistance abilities. This study sheds light on the role of ecological trade-offs as evolutionary drivers of the distribution and dynamics of plant populations.

Into the range: a latitudinal gradient or a center-margins differentiation of ecological strategies in Arabidopsis thaliana?

BACKGROUND AND AIMS: Determining within-species large-scale variation in phenotypic traits is central to elucidate the drivers of species' ranges. Intraspecific comparisons offer the opportunity to understand how trade-offs and biogeographical history constrain adaptation to contrasted environmental conditions. Here we test whether functional traits, ecological strategies from the CSR scheme and phenotypic plasticity in response to abiotic stress vary along a latitudinal or a center- margins gradient within the native range of Arabidopsis thaliana. METHODS: We experimentally examined the phenotypic outcomes of plant adaptation at the center and margins of its geographic range using 30 accessions from southern, central and northern Europe. We characterized the variation of traits related to stress tolerance, resource use, colonization ability, CSR strategy scores, survival and fecundity in response to high temperature (34 °C) or frost (- 6 °C), combined with a water deficit treatment. KEY RESULTS: We found evidence for both a latitudinal and a center-margins differentiation for the traits under scrutiny. Age at maturity, leaf dry matter content, specific leaf area and leaf nitrogen content varied along a latitudinal gradient. Northern accessions presented a greater survival to stress than central and southern accessions. Leaf area, C-scores, R-scores and fruit number followed a center-margins differentiation. Central accessions displayed a higher phenotypic plasticity than northern and southern accessions for most studied traits. CONCLUSIONS: Traits related to an acquisitive/conservative resource-use trade-off followed a latitudinal gradient. Traits associated with a competition/colonization trade-off differentiated along the historic colonization of the distribution range and then followed a center-margins differentiation. Our findings pinpoint the need to consider the joint effect of evolutionary history and environmental factors when examining phenotypic variation across the distribution range of a species.

Linking functional traits with tree growth and forest productivity in Quercus ilex forests along a climatic gradient.

Plant functional traits are highly plastic to changes in climatic factors and nutrient availability. However, the intraspecific plant response to abiotic factors and the overall effect on tree growth and productivity is still under debate. We studied forest productivity for 30 Quercus ilex subsp. ballota forests in Spain along a broad climatic gradient of aridity (mean annual precipitation from 321 to 858 mm). We used linear mixed models to quantify the effect of climatic and edaphic (soil nutrients, topography, and texture) factors on tree functional traits (leaf and branch traits), and subsequently, the effect of such functional traits and abiotic factors on the relative growth rate (RGR) of adult trees. We used piecewise structural equation models (SEMs) to determine the causal effect of intrinsic and extrinsic factors on forest productivity. Our results showed that tree functional traits were mainly explained by climatic and edaphic factors. Functional traits and tree biomass explained forest biomass and RGR, respectively, which ultimately explained forest productivity. In conclusion, intraspecific variability of functional traits has a significant effect on plant biomass and growth, which ultimately may explain forest productivity in Quercus ilex forests.

The GenTree Platform: growth traits and tree-level environmental data in 12 European forest tree species.

BACKGROUND: Progress in the field of evolutionary forest ecology has been hampered by the huge challenge of phenotyping trees across their ranges in their natural environments, and the limitation in high-resolution environmental information. FINDINGS: The GenTree Platform contains phenotypic and environmental data from 4,959 trees from 12 ecologically and economically important European forest tree species: Abies alba Mill. (silver fir), Betula pendula Roth. (silver birch), Fagus sylvatica L. (European beech), Picea abies (L.) H. Karst (Norway spruce), Pinus cembra L. (Swiss stone pine), Pinus halepensis Mill. (Aleppo pine), Pinus nigra Arnold (European black pine), Pinus pinaster Aiton (maritime pine), Pinus sylvestris L. (Scots pine), Populus nigra L. (European black poplar), Taxus baccata L. (English yew), and Quercus petraea (Matt.) Liebl. (sessile oak). Phenotypic (height, diameter at breast height, crown size, bark thickness, biomass, straightness, forking, branch angle, fructification), regeneration, environmental in situ measurements (soil depth, vegetation cover, competition indices), and environmental modeling data extracted by using bilinear interpolation accounting for surrounding conditions of each tree (precipitation, temperature, insolation, drought indices) were obtained from trees in 194 sites covering the species' geographic ranges and reflecting local environmental gradients. CONCLUSION: The GenTree Platform is a new resource for investigating ecological and evolutionary processes in forest trees. The coherent phenotyping and environmental characterization across 12 species in their European ranges allow for a wide range of analyses from forest ecologists, conservationists, and macro-ecologists. Also, the data here presented can be linked to the GenTree Dendroecological collection, the GenTree Leaf Trait collection, and the GenTree Genomic collection presented elsewhere, which together build the largest evolutionary forest ecology data collection available.

Importance of overstorey attributes for understorey litter production and nutrient cycling in European forests.

BACKGROUND: In contrast with the negligible contribution of the forest understorey to the total aboveground phytobiomass of a forest, its share in annual litter production and nutrient cycling may be more important. Whether and how this functional role of the understorey differs across forest types and depends upon overstorey characteristics remains to be investigated. METHODS: We sampled 209 plots of the FunDivEUROPE Exploratory Platform, a network of study plots covering local gradients of tree diversity spread over six contrasting forest types in Europe. To estimate the relative contribution of the understorey to carbon and nutrient cycling, we sampled non-lignified aboveground understorey biomass and overstorey leaf litterfall in all plots. Understorey samples were analysed for C, N and P concentrations, overstorey leaf litterfall for C and N concentrations. We additionally quantified a set of overstorey attributes, including species richness, proportion of evergreen species, light availability (representing crown density) and litter quality, and investigated whether they drive the understorey's contribution to carbon and nutrient cycling. RESULTS AND CONCLUSIONS: Overstorey litter production and nutrient stocks in litterfall clearly exceeded the contribution of the understorey for all forest types, and the share of the understorey was higher in forests at the extremes of the climatic gradient. In most of the investigated forest types, it was mainly light availability that determined the contribution of the understorey to yearly carbon and nutrient cycling. Overstorey species richness did not affect the contribution of the understorey to carbon and nutrient cycling in any of the investigated forest types.

Author Correction: The GenTree Dendroecological Collection, tree-ring and wood density data from seven tree species across Europe.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Intraspecific perspective of phenotypic coordination of functional traits in Scots pine.

Functional traits have emerged as a key to understand species responses to environmental conditions. The concerted expression of multiple traits gives rise to the phenotype of each individual, which is the one interacting with the environment and evolving. However, patterns of trait covariation and how they vary in response to environmental conditions remain poorly understood, particularly at the intraspecific scale. Here, we have measured traits at different scales and in different organs, and analysed their covariation in a large number of conspecifics distributed in two contrasting environments. We expected significant correlations among traits, not only within clusters of traits as found in global, multispecies studies, but also among clusters, with more relationships within clusters, due to genetic constraints, and among clusters due to more coordinated phenotypes than community level, multispecies studies. We surveyed 100 Pinus sylvestris trees in a Mediterranean mountainous area distributed in two contrasting elevations. We measured 13 functional traits, in three clusters (leaf, stem and whole-plant traits), and analysed their variation and coordination. We found significant coordination among traits belonging to different clusters that reveals coordinated phenotypes. However, we found fewer correlations within trait clusters than initially expected. Trait correlation structures (number, intensity and type of correlations among traits) differed among individuals at different elevations. We observed more correlations within trait clusters at low elevation compared to those at high elevation. Moreover, the higher number of correlations among different trait clusters and the lower trait variation at the higher elevation suggests that variability decreases under more stressful conditions. Altogether, our results reveal that traits at intraspecific scale are coordinated in a broad network and not only within clusters of traits but also that this trait covariation is significantly affected by environmental conditions.

The GenTree Dendroecological Collection, tree-ring and wood density data from seven tree species across Europe.

The dataset presented here was collected by the GenTree project (EU-Horizon 2020), which aims to improve the use of forest genetic resources across Europe by better understanding how trees adapt to their local environment. This dataset of individual tree-core characteristics including ring-width series and whole-core wood density was collected for seven ecologically and economically important European tree species: silver birch (Betula pendula), European beech (Fagus sylvatica), Norway spruce (Picea abies), European black poplar (Populus nigra), maritime pine (Pinus pinaster), Scots pine (Pinus sylvestris), and sessile oak (Quercus petraea). Tree-ring width measurements were obtained from 3600 trees in 142 populations and whole-core wood density was measured for 3098 trees in 125 populations. This dataset covers most of the geographical and climatic range occupied by the selected species. The potential use of it will be highly valuable for assessing ecological and evolutionary responses to environmental conditions as well as for model development and parameterization, to predict adaptability under climate change scenarios.

Selfing and Drought-Stress Strategies Under Water Deficit for Two Herbaceous Species in the South American Andes.

Angiosperms are highly diverse in their reproductive systems, including predominantly selfing, exclusive outcrossing, and mixed mating systems. Even though selfing can have negative consequences on natural populations, it has been proposed that plants having a predominantly selfing strategy are also associated with fast development strategies through time limitation mechanisms that allow them to complete their life cycle before the onset of severe drought. This relationship might be affected by the challenges imposed by global change, such as a decrease in pollinator availability and the earlier and more severe onset of droughts. In this work, our aim was to investigate whether selfing is correlated with a dehydration avoidance strategy, and how this could affect drought resistance and survival in two species with different types of selfing: pollinator-independent delayed selfing (Schizanthus grahamii) and pollinator-dependent selfing (Schizanthus hookeri), representing a gradient in selfing rates. We hypothesize that delayed selfing species and highly selfing populations will show "fast" plant traits whereas we will find no pattern in more outcrossed populations of the pollinator-dependent species. However, we predicted that high selfing populations would have lower survival rates when exposed to chronic drought early in their development since fast traits imply physiological compromises that will affect their drought survival. To evaluate these hypotheses, we characterized different physiological and morphological traits in response to two contrasting treatments (moist and dry) in a total of six populations of the two species. We found a relationship between the delayed selfing species and a dehydration avoidance strategy and also with low drought survival. Our work offers evidence to support the importance of abiotic factors, such as drought, on the possible variation in selfing rates on natural populations, and the effect that this mating system could have in their ability to face new environmental conditions such as those imposed by climate change.

Continental mapping of forest ecosystem functions reveals a high but unrealised potential for forest multifunctionality.

Humans require multiple services from ecosystems, but it is largely unknown whether trade-offs between ecosystem functions prevent the realisation of high ecosystem multifunctionality across spatial scales. Here, we combined a comprehensive dataset (28 ecosystem functions measured on 209 forest plots) with a forest inventory dataset (105,316 plots) to extrapolate and map relationships between various ecosystem multifunctionality measures across Europe. These multifunctionality measures reflected different management objectives, related to timber production, climate regulation and biodiversity conservation/recreation. We found that trade-offs among them were rare across Europe, at both local and continental scales. This suggests a high potential for 'win-win' forest management strategies, where overall multifunctionality is maximised. However, across sites, multifunctionality was on average 45.8-49.8% below maximum levels and not necessarily highest in protected areas. Therefore, using one of the most comprehensive assessments so far, our study suggests a high but largely unrealised potential for management to promote multifunctional forests.

Biodiversity and ecosystem functioning relations in European forests depend on environmental context.

The importance of biodiversity in supporting ecosystem functioning is generally well accepted. However, most evidence comes from small-scale studies, and scaling-up patterns of biodiversity-ecosystem functioning (B-EF) remains challenging, in part because the importance of environmental factors in shaping B-EF relations is poorly understood. Using a forest research platform in which 26 ecosystem functions were measured along gradients of tree species richness in six regions across Europe, we investigated the extent and the potential drivers of context dependency of B-EF relations. Despite considerable variation in species richness effects across the continent, we found a tendency for stronger B-EF relations in drier climates as well as in areas with longer growing seasons and more functionally diverse tree species. The importance of water availability in driving context dependency suggests that as water limitation increases under climate change, biodiversity may become even more important to support high levels of functioning in European forests.

Intraspecific leaf trait variability along a boreal-to-tropical community diversity gradient.

Disentangling the mechanisms that shape community assembly across diversity gradients is a central matter in ecology. While many studies have explored community assembly through species average trait values, there is a growing understanding that intraspecific trait variation (ITV) can also play a critical role in species coexistence. Classic biodiversity theory hypothesizes that higher diversity at species-rich sites can arise from narrower niches relative to species-poor sites, which would be reflected in reduced ITV as species richness increases. To explore how ITV in woody plant communities changes with species richness, we compiled leaf trait data (leaf size and specific leaf area) in a total of 521 woody plant species from 21 forest communities that differed dramatically in species richness, ranging from boreal to tropical rainforests. At each forest, we assessed ITV as an estimate of species niche breadth and we quantified the degree of trait overlap among co-occurring species as a measure of species functional similarity. We found ITV was relatively invariant across the species richness gradient. In addition, we found that species functional similarity increased with diversity. Contrary to the expectation from classic biodiversity theory, our results rather suggest that neutral processes or equalizing mechanisms can be acting as potential drivers shaping community assembly in hyperdiverse forests.

Jack-of-all-trades effects drive biodiversity-ecosystem multifunctionality relationships in European forests.

There is considerable evidence that biodiversity promotes multiple ecosystem functions (multifunctionality), thus ensuring the delivery of ecosystem services important for human well-being. However, the mechanisms underlying this relationship are poorly understood, especially in natural ecosystems. We develop a novel approach to partition biodiversity effects on multifunctionality into three mechanisms and apply this to European forest data. We show that throughout Europe, tree diversity is positively related with multifunctionality when moderate levels of functioning are required, but negatively when very high function levels are desired. For two well-known mechanisms, 'complementarity' and 'selection', we detect only minor effects on multifunctionality. Instead a third, so far overlooked mechanism, the 'jack-of-all-trades' effect, caused by the averaging of individual species effects on function, drives observed patterns. Simulations demonstrate that jack-of-all-trades effects occur whenever species effects on different functions are not perfectly correlated, meaning they may contribute to diversity-multifunctionality relationships in many of the world's ecosystems.

Biotic homogenization can decrease landscape-scale forest multifunctionality.

Many experiments have shown that local biodiversity loss impairs the ability of ecosystems to maintain multiple ecosystem functions at high levels (multifunctionality). In contrast, the role of biodiversity in driving ecosystem multifunctionality at landscape scales remains unresolved. We used a comprehensive pan-European dataset, including 16 ecosystem functions measured in 209 forest plots across six European countries, and performed simulations to investigate how local plot-scale richness of tree species (α-diversity) and their turnover between plots (ß-diversity) are related to landscape-scale multifunctionality. After accounting for variation in environmental conditions, we found that relationships between α-diversity and landscape-scale multifunctionality varied from positive to negative depending on the multifunctionality metric used. In contrast, when significant, relationships between ß-diversity and landscape-scale multifunctionality were always positive, because a high spatial turnover in species composition was closely related to a high spatial turnover in functions that were supported at high levels. Our findings have major implications for forest management and indicate that biotic homogenization can have previously unrecognized and negative consequences for large-scale ecosystem multifunctionality.

Species coexistence in a changing world.

The consequences of global change for the maintenance of species diversity will depend on the sum of each species responses to the environment and on the interactions among them. A wide ecological literature supports that these species-specific responses can arise from factors related to life strategies, evolutionary history and intraspecific variation, and also from environmental variation in space and time. In the light of recent advances from coexistence theory combined with mechanistic explanations of diversity maintenance, we discuss how global change drivers can influence species coexistence. We revise the importance of both competition and facilitation for understanding coexistence in different ecosystems, address the influence of phylogenetic relatedness, functional traits, phenotypic plasticity and intraspecific variability, and discuss lessons learnt from invasion ecology. While most previous studies have focused their efforts on disentangling the mechanisms that maintain the biological diversity in species-rich ecosystems such as tropical forests, grasslands and coral reefs, we argue that much can be learnt from pauci-specific communities where functional variability within each species, together with demographic and stochastic processes becomes key to understand species interactions and eventually community responses to global change.