Intraspecific variation and phenotypic plasticity of olive varieties in response to contrasting environmental conditions

Widespread species often show geographic variation in thermally-sensitive traits, providing insight into how species respond to shifts in temperature through time. Such patterns may arise from phenotypic plasticity, genetic adaptation, or their interaction. In some cases, the effects of genotype and temperature may act together to reduce, or to exacerbate, phenotypic variation in fitness-related traits across varying thermal environments. We find evidence for such interactions in life-history traits of Heteronympha merope, a butterfly distributed across a broad latitudinal gradient in south-eastern Australia. We show that body size in this butterfly is negatively related to developmental temperature in the laboratory, in accordance with the temperature-size rule, but not in the field, despite very strong temperature gradients. A common garden experiment on larval thermal responses, spanning the environmental extremes of H. merope's distribution, revealed that butterflies from low latitude (warmer climate) populations have relatively fast intrinsic growth and development rates compared to those from cooler climates. These synergistic effects of genotype and temperature across the landscape (co-gradient variation) are likely to accentuate phenotypic variation in these traits, and this interaction must be accounted for when predicting how H. merope will respond to temperature change through time. These results highlight the importance of understanding how variation in life-history traits may arise in response to environmental change. Without this knowledge, we may fail to detect whether organisms are tracking environmental change, and if they are, whether it is by plasticity, adaptation or both.

Inter-clonal variation in functional traits in response to drought for a genetically homogeneous Mediterranean conifer

In a rapidly changing climate, alpine plants may persist by adapting to new conditions. However, the rate at which the climate is changing might exceed the rate of adaptation through evolutionary processes in long-lived plants. Persistence may depend on phenotypic plasticity in morphology and physiology. Here we investigated patterns of leaf trait variation including leaf area, leaf thickness, specific leaf area, leaf dry matter content, leaf nutrients (C, N, P) and isotopes (δ13C and δ15N) across an elevation gradient on Gongga Mountain, Sichuan Province, China. We quantified inter- and intra-specific trait variation and the plasticity in leaf traits of selected species to experimental warming and cooling by using a reciprocal transplantation approach. We found substantial phenotypic plasticity in most functional traits where δ15N, leaf area, and leaf P showed greatest plasticity. These traits did not correspond with traits with the largest amount of intraspecific variation. Plasticity in leaf functional traits tended to enable plant populations to shift their trait values toward the mean values of a transplanted plants’ destination community, but only if that population started with very different trait values. These results suggest that leaf trait plasticity is an important mechanism for enabling plants to persist within communities and to better tolerate changing environmental conditions under climate change.

Recent studies of communities have examined phylogenetic signal in species' functional traits to infer drivers of community assembly. Phenotypic variation in traits, arising from “constitutive” genetically based variation and from environmental influences on gene expression, or phenotypic plasticity, could affect inferences about community assembly. We found significant trait plasticity in 12 focal species across four species–interaction treatments grown in four soil environments. Phylogenetic signal in traits was present, but was also dependent on species–interactor treatment, suggesting that phenotypic plasticity and plant neighborhood could affect the ability to detect and interpret community phylogenetic patterns of trait variation. Individuals competing with conspecifics expressed significant divergence in specific leaf area (SLA) relative to when they were grown alone. Combined with the observation that competition is stronger between close relatives than between distant relatives in some soils, these results suggest that trait plasticity may be an adaptive response to competition. To test this hypothesis, we examined total biomass in a pot, relative to the predicted biomass of two individuals grown alone, and related pot biomass to phylogenetic distance of the interactor treatment, as well as to divergence in SLA and root : shoot ratio. Within competition treatments, only plastic divergence in root : shoot ratio in one interactor treatment was correlated with increased productivity, and only in one soil type. We also tested whether, across all treatments, divergence in SLA or root : shoot ratio increased pot productivity. We found that “community” productivity was positively influenced both by phylogenetic distance to competitor, as well as by divergence in root : shoot ratio due to both plasticity and constitutive differences. Phenotypic plasticity resulting in trait divergence may increase the ability of plants to coexist and may also decrease phylogenetic signal in community assembly at small spatial scales.

Phenotypic variation of traits can reflect the ability of plants to adjust to particular environments, but how much of this variation is heritable is not frequently analyzed in natural populations. In the present paper, we investigated the patterns of phenotypic expression in light-related leaf traits of Olea europaea subsp. guanchica, a woody sclerophyllous species endemic to the Canary Islands. We explored phenotypic differentiation and heritable variation across several island populations differing in light environment. A suite of morpho-functional (leaf size, SLA and leaf angle) and physiological (pigment pools: Chl a/b ratio, xantophyll cycle and β-carotene) traits was measured in six populations on three islands. In addition, we estimated heritabilities for these traits following Ritland's method. Variation in morpho-functional, but not in physiological, traits was observed across the islands and was significantly related to the amount of diffuse light experienced by each population. In addition, significant heritabilities were found for morpho-functional traits, whereas expression of similar phenotypes among populations was accompanied by a lack of heritable variation in physiological traits. Most recently established populations did not exhibit lower heritabilities in quantitative traits than older populations, and apparently displayed congruent phenotypes under the local conditions. Our results strongly support the idea that different types of traits show contrasted levels of genetic and phenotypic variation in populations experiencing marked environmental differences.

It is commonly accepted that within-population phenotypic variation is caused by genotypic and environmental heterogeneity. Non-genotypic variation is thought to result from diversity of environmental conditions alone. This however contradicts experimental data showing that even when both genetic and environmental sources of phenotypic variation are neglected, residual variation still exists. This residual phenotypic variation is caused by deviations of developmental trajectories from the target trajectory determined for particular genotype and environment, i.e. by developmental instability. This variation is well-known for morphological traits where it is measured most often by fluctuating asymmetry, i.e. random deviations from perfect symmetry, which can be easily separated from the other type of phenotypic variation. In morphological characters which do not possess symmetry or in non-morphological characters this variation cannot usually be separated from other type of non-genotypic variation, caused by environmental heterogeneity. Most researchers still believe that all non-genotypic variation, even under standardised experimental conditions, is caused by insufficient standardization of environment, rather than by other sources of phenotypic variation. When special efforts are undertaken to analyse variation caused by developmental instability, this variation contributes substantially to non-genotypic variation. To exemplify how variation caused by developmental instability can be separated from phenotypic plasticity we analysed phenotypic variation of resting egg formation in Daphnia pulicaria. The proportion of females carrying resting eggs has been shown to depend on the photoperiod of their mothers, revealing transgeneration effects (Alekseev & Lampert 2001). Developmental instability manifests itself in differences between clonemates within an experimental vessel in a standardized environment. Some females produce resting eggs whereas others do not. Our estimations based on results obtained in experimental conditions and extrapolation to conditions in the wild showed that phenotypic plasticity, i.e. phenotypic response to changes of day duration in maternal environment (phenotypic plasticity) explains only 1-2% of phenotypic variation whereas developmental instability explains approximately 98-99% of phenotypic variance of this trait (i.e. producing or not producing resting eggs), if other factors causing phenotypic plasticity are absent. This example demonstrates a major role of developmental instability in variation of the trait under study. The contribution of developmental instability to phenotypic variation should be considered in studying evolutionary patterns of phenotypic traits.

The study of intraspecific genetic variation in plant traits for use in tropical forest restoration has broad potential for increasing our ability to achieve multi-functional objectives during this era of climate change. Developing seed-sourcing guidelines that optimize phenotypic characteristics best suited to a particular planting site as well as to future conditions imposed by environmental change could be useful for effective reforestation. Because evolution operates differently across tree species, this is an especially cumbersome task in tropical forests that contain thousands of species. Partially due to this high plant diversity, research and application of intraspecific variation in genetics, plant traits, and plant function in tropical forests wane far behind less diverse forest biomes. To examine the potential for improving reforestation efforts in tropical forests by considering intraspecific variation in plant traits and functions, we review the state of knowledge on intraspecific variation in South-east Asia as a case study. We focus on the dipterocarp family ( Dipterocarpaceae ), a highly diverse family of 16 genera with approximately 695 known species that often dominate lowland tropical rainforests of South-east Asia with many of these forests in a degraded state and in need of restoration. We found that there is research accumulating to understand genetic variation in approximately 10% of these 695 species. Intraspecific molecular variation exists at different spatial scales among species with 74% of species having moderate to high population differentiation (Fst > 0.10) and 92% of species with evidence of fine-scale genetic structure. Although this suggests a high potential for trait variation, few studies associated molecular with phenotypic variation. Seventeen tree species across 11 studies revealed intraspecific variation in traits or functions. Research indicates that intraspecific variation in growth may vary two-fold and drought tolerance four-fold among genotypes highlighting the possibility to pre-adapt trees to climate change during reforestation and to use intraspecific variation to promote the use of native species in commercial forestry. Our review presents opportunities and ideas for developing seed-sourcing guidelines to take advantage of intraspecific variation in traits and function by identifying how to locate this variation, which species would benefit, and how to test for trait variation. We also highlight an emerging area of research on local adaptation, common garden studies, and adaptive drought conditioning to improve reforestation during climate change.

Preface: Functional biogeography in Japanese cedar

Global change is widely altering environmental conditions which makes accurately predicting species range limits across natural landscapes critical for conservation and management decisions. If climate pressures along elevation gradients influence the distribution of phenotypic and genetic variation of plant functional traits, then such trait variation may be informative of the selective mechanisms and adaptations that help define climatic niche limits. Using extensive field surveys along 16 elevation transects and a large common garden experiment, we tested whether functional trait variation could predict the climatic niche of a widespread tree species (Populus angustifolia) with a double quantile regression approach. We show that intraspecific variation in plant size, growth, and leaf morphology corresponds with the species' total climate range and certain climatic limits related to temperature and moisture extremes. Moreover, we find evidence of genetic clines and phenotypic plasticity at environmental boundaries, which we use to create geographic predictions of trait variation and maximum values due to climatic constraints across the western US. Overall, our findings show the utility of double quantile regressions for connecting species distributions and climate gradients through trait‐based mechanisms. We highlight how new approaches like ours that incorporate genetic variation in functional traits and their response to climate gradients will lead to a better understanding of plant distributions as well as identifying populations anticipated to be maladapted to future environments.

The study of variation at different levels is a constant topic of research. In the field of genetics, it is necessary to know the causes and the effects of variation in traits that influence traits of individuals in their natural habitats. Genetic variation is considered the most basic level of biological diversity and a prerequisite for the variability of species, populations, and ecosystems. Populations that lose genetic variation cannot evolve since evolution cannot proceed without genetic variation and populations that are unable to adapt to changing conditions will go extinct. Forest genetics studies have shown that environmental heterogeneity influences the genetic differentiation among tree populations, creating geographic genetic patterns that are consistent with phenotypic traits. One can look at this association to detect climate variables that are shaping the genetic structure of populations or even identify which genes are under pronounced natural selection. Genetic conservation aims to protect and preserve genetic variation, vital for the maintenance of adaptive potential within populations and species. Conserving forest genetic resources (FGR) constitute a unique and irreplaceable resource for the future, including for sustainable economic growth and progress and environmental adaption. The aim of this thesis is to investigate the phenotypic variation among natural population of pines at local and regional scales, and define its implications in the use and conservation of genetic resources. At first step, we analyzed the relationship between within-population variance in fitness-related phenotypic traits (survival, height and diameter), phenotypic plasticity of these traits, and environmental (climatic) heterogeneity in the region surrounding provenances of Pinus sylvestris, P. pinaster and P. halepensis. We used multi-site tree provenance tests of Iberian pine species and a model selection approach to infer the relationship between them. It was found that climatic heterogeneity at different spatial scale can explain a significant part of the intrapopulation phenotypic variation in different traits, but the relationships depend on the species and traits considered. Second, we assessed the inter- and intraspecific genetic variation in seedling drought tolerance in Pinus oocarpa, P. patula and P. pseudostrobus from the Trans-Mexican Volcanic Belt, a relevant genetic resource management scale. It was evaluated the growth and biomass fractions of pine seedlings in a greenhouse with two highly contrasted watering regimes. We found that even at reduced geographical scales, Mexican pines present differences in the response to water stress. The responses differed among species, including the allometric phenotypic changes in biomass allocation (plasticity), the genetic differences among populations, and the differences in phenotypic plasticity among populations. 10 Third, we identified areas for gene conservation and proposing measures for the conservation and sustainable use of forest genetic resources for four pines species: P. greggii, P. oocarpa, P. patula and P. pseudostrobus. It was obtained the most relevant information related to the identification and characterization of forest genetic resources of these species. We used the distribution range of the species, and information for conservation of forest genetic resources and for the sustainable use of forest genetic resources. It was checked gaps considering the distribution area and the genetic zones of the species. We propose recommendations to improve the status of conservation and sustainable use of forest genetic resources in the evaluated species.

Adaptive Phenotypic Plasticity: Target or By-Product of Selection in a Variable Environment?

BackgroundPlant functional traits co-vary along strategy spectra, thereby defining trade-offs for resource acquisition and utilization amongst other processes. A main objective of plant ecology is to quantify the correlations among traits and ask why some of them are sufficiently closely coordinated to form a single axis of functional specialization. However, due to trait co-variations in nature, it is difficult to propose a mechanistic and causal explanation for the origin of trade-offs among traits observed at both intra- and inter-specific level.Methodology/Principal FindingsUsing the Gemini individual-centered model which coordinates physiological and morphological processes, we investigated with 12 grass species the consequences of deliberately decoupling variation of leaf traits (specific leaf area, leaf lifespan) and plant stature (height and tiller number) on plant growth and phenotypic variability. For all species under both high and low N supplies, simulated trait values maximizing plant growth in monocultures matched observed trait values. Moreover, at the intraspecific level, plastic trait responses to N addition predicted by the model were in close agreement with observed trait responses. In a 4D trait space, our modeling approach highlighted that the unique trait combination maximizing plant growth under a given environmental condition was determined by a coordination of leaf, root and whole plant processes that tended to co-limit the acquisition and use of carbon and of nitrogen.Conclusion/SignificanceOur study provides a mechanistic explanation for the origin of trade-offs between plant functional traits and further predicts plasticity in plant traits in response to environmental changes. In a multidimensional trait space, regions occupied by current plant species can therefore be viewed as adaptive corridors where trait combinations minimize allometric and physiological constraints from the organ to the whole plant levels. The regions outside this corridor are empty because of inferior plant performance.

Widespread plant species generally have high intraspecific variation in functional traits, which is reflected in their great variety of phenotypes. This variety can result from both genetic differences due to local adaptation and phenotypic plasticity. With high intraspecific variation and nearly global distribution, the common reed Phragmites australis is a suitable model species for studying the underlying mechanisms of intraspecific trait variation. In this study, 71 genotypes of P. australis from seven phylogeographic groups were transplanted into two replicate common gardens located in very different climates: northern Europe and mid‐east Asia. We measured seven functional traits of all these genotypes over the growing season, including shoot height, maximum biomass per shoot, shoot density, node number per stem, leaf life span, flowering occurrence and flowering date. Our aim was to assess the relative effects of genetic (phylogeographic origin) and environmental (common garden) status, and interactions between them, on intraspecific variation in functional traits of P. australis. We found common garden having the strongest influence on most functional traits studied. All traits except flowering occurrence varied significantly across gardens, revealing the important role of phenotypic plasticity on trait variation in P. australis. We also found significant differences in trait variation among the different phylogeographic groups of P. australis and, thus, evidence for genetically determined intraspecific variation in the morphological and life‐history traits addressed in this study. All functional traits showed significant (p ≤ 0.0054), albeit minor to moderately explained (R2 ≤ 0.57), latitudinal patterns in both gardens. Covariation of multiple traits was similar in the two gardens. Phenotypic plasticity was trait‐ specific, and the plasticity of shoot height and maximum biomass per shoot increased towards higher latitude of genotypic origin. Our results indicate that the latitude of origin affects the evolution of functional traits, as well as their phenotypic plasticity. Since phenotypic plasticity is a crucial mechanism for acclimation and evolution, our findings support the role of gene‐based adaptive phenotypic plasticity in plant evolution. The intraspecific spatial variation in functional traits and their phenotypic plasticity can help predict species distribution, persistence and invasion under global climate change.

Several studies on individual physiological traits assume that past records may predict future performance. Marine mollusks, as other animals, show a wide range of between- and within-individual variation of physiological traits. However, in this group, almost nothing is known about the relative influence of genetic factors on that variation. Repeatability (R) is a measure of the consistency of the variation of a trait, which includes its genetic variance and represents the maximum potential value of its heritability (h 2). Traits that show high inter-individual variation and high repeatability levels could potentially evolve through selection (natural or artificial). We estimated the repeatability [using intra-class (τ) and Pearson-moment (r) correlation coefficients] of several physiological traits related to energy acquisition and allocation in juvenile Pacific abalone Haliotis discus hannai, maintained under controlled environment growing systems. In order to estimate the range of the R values and the effect of the time elapsed between measurements on these estimates, we measured these traits monthly during 6 months for each individual. Among the physiological traits, those related to energy allocation like oxygen consumption (standard metabolic rate, SMR) and ammonium excretion rates, and oxygen/nitrogen ratio (O/N), showed intermediate levels of repeatability (0.48, 0.55 and 0.39, respectively), when this was estimated by τ coefficient. However, the r estimation showed that SMR and O/N repeatability were significant and high (0.6–0.7 and 0.5–0.7, respectively) during the first 5 consecutive measurements, decreasing strongly (0.3 and 0.2, respectively) during the last measurement. For ammonia excretion, although repeatability (r) decreased from 0.8 to 0.5 during the 6 consecutive measurements, they remain significant during the experimental period. Therefore, our results indicate that for H. discus hannai juveniles, physiological traits like SMR, ammonia excretion and O/N are significantly repeatable (i.e. good predictors of future measurements) during a period of 4–5 months. These significant repeatability values suggest an important genetic control upon the phenotypic variation of these physiological traits, and could potentially respond to natural or artificial selection, and be used in genetic improvement programs. By contrast, those traits related to energy acquisition (i.e. ingestion, absorption and assimilation) and physiological efficiencies (i.e. net growth and scope for growth) showed very low levels of repeatability (0–0.07). This indicates that the phenotypic variation of these traits would be more influenced by environment rather than by genetic factors.

Intraspecific trait variability has a fundamental contribution to the overall trait variability. However, little is known concerning the relative role of local (e.g. disturbances and species interaction) and regional (biogeographical) processes in generating this intraspecific trait variability. While biogeographical processes enhance plant trait variability between distant populations, in fire-prone ecosystems, recurrent fires may have a preponderant role in generating variability at a local scale. We hypothesize that plants respond to the local spatio-temporal heterogeneity generated by fire by having a relatively large local variability in regeneration traits in such a way that overrides the variability at a broader biogeographical scale. We test this hypothesis by assessing the intraspecific variability in fire-related regeneration traits of two species (Cistus salviifolius and Lavandula stoechas) growing in fire-prone ecosystems of the Mediterranean Basin. For each species, we selected six populations in two distant regions, three in the east (Anatolian Peninsula) and three in the west (Iberian Peninsula). For each species and population, we analysed the following regeneration traits: seed size, seed dormancy and stimulated germination by fire-related cues (heat and smoke). To evaluate the distribution of the variability in these traits, we decomposed the variability of trait values at each level, between regions (regional) and between population within region (local), using linear mixed-effect models. Despite the biogeographical and climatic differences between regions, for the two species, intraspecific variability in regeneration traits was higher at a local (within regions) than at a regional scale (between regions). Our results suggest that, in Mediterranean ecosystems, fire is an important source of intraspecific variability in regeneration traits. This supports the prominent role of fire as an ecological and evolutionary process, producing trait variability and shaping biodiversity in fire-prone ecosystems.