Adaptation to climate in widespread eucalypt species

AbstractThe long term success of revegetation efforts will depend upon the planted species’ resilience to climate change. Many widespread species grow across a range of climatic conditions and, thus, may possess adaptations that could be utilised to improve climate resilience of restored ecosystems. Species can achieve a widespread distribution via two main mechanisms; (1) by diverging into a series of specialised populations, or (2) through high phenotypic plasticity. The extent to which populations are specialised or plastic in response to climate will determine the seed-sourcing strategy required for optimal restoration outcomes under a changing climate. We examined genetic divergence and phenotypic plasticity in two widespread Eucalyptus species (E. tricarpa in southeastern Australia, E. salubris in southwestern Australia), to determine the nature of adaptation to climate in these species, and whether genomic screening might be a useful tool to assess climate adaptation.We examined nine populations of each species across climate gradients and, for E. tricarpa, trees originating from the same populations were also studied in two common garden field trials. We characterised responses in functional traits relevant to climate adaptation, including leaf size, thickness, tissue density, and carbon isotope ratio (δ13C). Genetic variation was assessed with genome scans using DArTseq markers, and ‘outlier markers’ were identified as being linked to regions of the genome that are potentially under selection.Evidence of both plastic response and genetic specialisation for climate was found in both species, indicating that widespread eucalypts utilise a combination of both mechanisms for adaptation to spatial variation in climate. The E. tricarpa common garden data suggested high plasticity in most of the measured functional traits, and the extent of plasticity in some traits (e.g. leaf size and thickness) varied among provenances, suggesting genetic variation for plasticity itself. In E. salubris, most functional traits showed little variation across the gradient. However, water use efficiency appeared highly plastic, as determined from the strong correlation between δ13C and recent precipitation (R2 = 0.83). Both species showed spatial partitioning of genetic variation across the gradient, and data for E. salubris revealed two distinct lineages. The genome scans yielded 16,122 DArTseq markers for “Lineage 1” of E. salubris, of which 0.1% were potentially adaptive ‘outlier loci’, and 6,544 markers for E. tricarpa, of which 2.6% were outliers. Canonical Analysis of Principal Coordinates (CAP) analysis showed that the outlier markers were correlated with climatic variables, and some were also strongly correlated with functional traits. An ‘Aridity Index’ was also developed from the CAP analysis that has potential as a tool for environmental planners to use for matching seed sources to target climates.Widespread eucalypts are likely to possess a capacity to respond plastically to a changing climate to some extent, but selection of seed sources to match projected climate changes may confer even greater climate resilience. Further study of the mechanisms of plasticity in response to climate may improve our ability to assess climate adaptation in other species, and to determine optimal strategies for ecosystem restoration and management under climate change

Performance-based inference of selection on stomatal length and specific leaf area varies with climate-of-origin of the forest tree, Eucalyptus ovata

Understanding how functional traits affect plant performance and fitness is a key step in unravelling the role of natural selection in shaping the evolutionary trajectory of populations. We examined early-age selection acting on leaf traits via their effects on growth performance and fitness, measured in Eucalyptus ovata trees planted in a common-garden field trial embedded in a reforestation planting in Tasmania, Australia. We focused on two important leaf traits - stomatal length and specific leaf area (SLA) - measured two years after planting, and compared interplanted E. ovata groups originating from dry and wet home-site climates, with the trial site having intermediate long-term mean annual rainfall. Two-year height growth was used as the performance attribute, and the time-averaged tree survival over the subsequent six years as the fitness component. There was evidence for performance-based selection on the leaf traits, with the strength and form of selection depending on the trait and climate group being considered. In this sense, selection in the dry group operated mainly on stomatal length where a combination of directional (favouring longer stomata) and stabilizing selection was detected, whereas selection in the wet group acted only on SLA and was purely stabilizing. Estimates of performance-based correlational selection were not statistically significant. For both climate groups, estimates of fitness-based selection gradients provided evidence for significant directional (but not quadratic) selection on height performance, favouring individuals with faster growth, but did not indicate statistical support for direct effects of the leaf traits on tree survival, conditional on measured performance. These results validated qualitative inferences of selection from the performance-based analysis, and suggested that selection on the leaf traits appeared to be mediated by their effects on early-age height performance, which in turn directly influenced later-age survival. We discuss the mechanisms by which the focal traits may have affected height performance, and likely factors contributing to the different patterns of phenotypic selection observed in the two groups experiencing the same environment. We also provide expressions of analytical derivatives that were developed for the estimation of selection gradients based on a logistic regression model relating a binary fitness response to linear and nonlinear covariate terms for the target regressor variables.info:eu-repo/semantics/publishedVersio

Linking leaf economic and hydraulic traits with early-age growth performance and survival of Eucalyptus pauciflora

Selection on plant functional traits may occur through their direct effects on fitness (or a fitness component), or may be mediated by attributes of plant performance which have a direct impact on fitness. Understanding this link is particularly challenging for long-lived organisms, such as forest trees, where lifetime fitness assessments are rarely achievable, and performance features and fitness components are usually quantified from early-life history stages. Accordingly, we studied a cohort of trees from multiple populations of Eucalyptus pauciflora grown in a common-garden field trial established at the hot and dry end of the species distribution on the island of Tasmania, Australia. We related the within-population variation in leaf economic (leaf thickness, leaf area and leaf density) and hydraulic (stomatal density, stomatal length and vein density) traits, measured from two-year-old plants, to two-year growth performance (height and stem diameter) and to a fitness component (seven-year survival). When performance-trait relationships were modelled for all traits simultaneously, statistical support for direct effects on growth performance was only observed for leaf thickness and leaf density. Performance-based estimators of directional selection indicated that individuals with reduced leaf thickness and increased leaf density were favoured. Survival-performance relationships were consistent with size- dependent mortality, with fitness-based selection gradients estimated for performance measures providing evidence for directional selection favouring individuals with faster growth. There was no statistical support for an effect associated with the fitness-based quadratic selection gradient estimated for growth performance. Conditional on a performance measure, fitness-based directional selection gradients estimated for the leaf traits did not provide statistical support for direct effects of the focal traits on tree survival. This suggested that, under the environmental conditions of the trial site and time period covered in the current study, early-stage selection on the studied leaf traits may be mediated by their effects on growth performance, which in turn has a positive direct influence on later-age survival. We discuss the potential mechanistic basis of the direct effects of the focal leaf traits on tree growth, and the relevance of a putative causal pathway of trait effects on fitness through mediation by growth performance in the studied hot and dry environmentinfo:eu-repo/semantics/publishedVersio

Directional Selection on Tree Seedling Traits Driven by Experimental Drought Differs Between Mesic and Dry Populations

Original ResearchWe evaluated population differences and drought-induced phenotypic selection on four seedling traits of the Australian forest tree Eucalyptus pauciflora using a glasshouse drydown experiment. We compared dry and mesic populations and tested for directional selection on lamina length (reflecting leaf size), leaf shape, the node of ontogenetic transition to the petiolate leaf (reflecting the loss of vegetative juvenility), and lignotuber size (reflecting a recovery trait). On average, the dry population had smaller and broader leaves, greater retention of the juvenile leaf state and larger lignotubers than the mesic population, but the populations did not differ in seedling survival. While there was statistical support for directional selection acting on the focal traits in one or other population, and for differences between populations in selection gradient estimates for two traits, only one trait—lamina length—exhibited a pattern of directional selection consistent with the observed population differences being a result of past adaptation to reduce seedling susceptibility to acute drought. The observed directional selection for lamina length in the mesic population suggests that future increases in drought risk in the wild will shift the mean of the mesic population toward that of the dry population. Further, we provide evidence suggesting an early age trade-off between drought damage and recovery traits, with phenotypes which develop larger lignotubers early being more susceptible to drought death. Such trade-offs could have contributed to the absence of population mean differences in survival, despite marked differentiation in seedling traitsinfo:eu-repo/semantics/publishedVersio

Recent climate-driven ecological change across a continent as perceived through local ecological knowledge

Documenting effects of climate change is an important step towards designing mitigation and adaptation responses. Impacts of climate change on terrestrial biodiversity and ecosystems have been well-documented in the Northern Hemisphere, but long-term data to detect change in the Southern Hemisphere are limited, and some types of change are generally difficult to measure. Here we present a novel approach using local ecological knowledge to facilitate a continent-scale view of climate change impacts on terrestrial biodiversity and ecosystems that people have perceived in Australia. We sought local knowledge using a national web-based survey, targeting respondents with close links to the environment (e.g. farmers, ecologists), and using a custom-built mapping tool to ask respondents to describe and attribute recent changes they had observed within an area they knew well. Results drawn from 326 respondents showed that people are already perceiving simple and complex climate change impacts on hundreds of species and ecosystems across Australia, significantly extending the detail previously reported for the continent. While most perceived trends and attributions remain unsubstantiated, \u3e35 reported anecdotes concurred with examples in the literature, and \u3e20 were reported more than once. More generally, anecdotes were compatible with expectations from global climate change impact frameworks, including examples across the spectrum from organisms (e.g. increased mortality in \u3e75 species), populations (e.g. changes in recruitment or abundance in \u3e100 species, phenological change in \u3e50 species), and species (e.g. \u3e80 species newly arriving or disappearing), to communities and landscapes (e.g. \u3e50 examples of altered ecological interactions). The overarching pattern indicated by the anecdotes suggests that people are more often noticing climate change losers (typically native species) than winners in their local areas, but with observations of potential ‘adaptation in action’ via compositional and phenological change and through arrivals and range shifts (particularly for native birds and exotic plants). A high proportion of climate change-related anecdotes also involved cumulative or interactive effects of land use. We conclude that targeted elicitation of local ecological knowledge about climate change impacts can provide a valuable complement to data-derived knowledge, substantially extending the volume of explicit examples and offering a foundation for further investigation

Symbiosis limits establishment of legumes outside their native range at a global scale

Microbial symbiosis is integral to plant growth and reproduction, but its contribution to global patterns of plant distribution is unknown. Legumes (Fabaceae) are a diverse and widely distributed plant family largely dependent on symbiosis with nitrogen-fixing rhizobia, which are acquired from soil after germination. This dependency is predicted to limit establishment in new geographic areas, owing to a disruption of compatible host-symbiont associations. Here we compare non-native establishment patterns of symbiotic and non-symbiotic legumes across over 3,500 species, covering multiple independent gains and losses of rhizobial symbiosis. We find that symbiotic legume species have spread to fewer non-native regions compared to non-symbiotic legumes, providing strong support for the hypothesis that lack of suitable symbionts or environmental conditions required for effective nitrogen-fixation are driving these global introduction patterns. These results highlight the importance of mutualisms in predicting non-native species establishment and the potential impacts of microbial biogeography on global plant distribution

Genomic Scans across Three Eucalypts Suggest that Adaptation to Aridity is a Genome-Wide Phenomenon

Widespread species spanning strong environmental (e.g., climatic) gradients frequently display morphological and physiological adaptations to local conditions. Some adaptations are common to different species that occupy similar environments. However, the genomic architecture underlying such convergent traits may not be the same between species. Using genomic data from previous studies of three widespread eucalypt species that grow along rainfall gradients in southern Australia, our probabilistic approach provides evidence that adaptation to aridity is a genome-wide phenomenon, likely to involve multiple and diverse genes, gene families and regulatory regions that affect a multitude of complex genetic and biochemical processes

Climate-adjusted provenancing: A strategy for climate-resilient ecological restoration

Investments in ecological restoration are estimated at $US 2 trillion per annum worldwide and are increasing rapidly (Cunningham, 2008; Williams et al., 2014). These investments are occurring in an environment of accelerated climate change that is projected to continue into the next century, yet they currently take little account of such change. This has significant implications for the long-term success of restoration plantings across millions of hectares, with germplasm used in current restoration efforts potentially poorly-adapted to future climates. New approaches that optimize the climate-resilience of these restoration efforts are thus essential (Breed et al., 2013; Williams et al., 2014; Havens et al., 2015)..

Thermal acclimation of leaf photosynthetic traits in an evergreen woodland, consistent with the coordination hypothesis

Ecosystem models commonly assume that key photosynthetic traits, such as carboxylation capacity measured at a standard temperature, are constant in time. The temperature responses of modelled photosynthetic or respiratory rates then depend entirely on enzyme kinetics. Optimality considerations, however, suggest this assumption may be incorrect. The coordination hypothesis (that Rubisco- and electron-transport-limited rates of photosynthesis are co-limiting under typical daytime conditions) predicts, instead, that carboxylation (Vcmax) capacity should acclimate so that it increases somewhat with growth temperature but less steeply than its instantaneous response, implying that Vcmax when normalized to a standard temperature (e.g. 25 °C) should decline with growth temperature. With additional assumptions, similar predictions can be made for electron-transport capacity (Jmax) and mitochondrial respiration in the dark (Rdark). To explore these hypotheses, photosynthetic measurements were carried out on woody species during the warm and the cool seasons in the semi-arid Great Western Woodlands, Australia, under broadly similar light environments. A consistent proportionality between Vcmax and Jmax was found across species. Vcmax, Jmax and Rdark increased with temperature in most species, but their values standardized to 25 °C declined. The ci : ca ratio increased slightly with temperature. The leaf N  :  P ratio was lower in the warm season. The slopes of the relationships between log-transformed Vcmax and Jmax and temperature were close to values predicted by the coordination hypothesis but shallower than those predicted by enzyme kinetics.This research was funded by the Terrestrial Ecosystem Research Network (TERN), Macquarie University and the Australian National University. Henrique Fürstenau Togashi was supported by an international Macquarie University International Research Scholarship (iMQRES). Iain Colin Prentice, Bradley John Evans, and Henrique Fürstenau Togashi were funded by the Ecosystem Modelling and Scaling Infrastructure (eMAST, part of TERN). TERN and eMAST have been supported by the Australian Government through the National Collaborative Research Infrastructure Strategy (NCRIS). Owen Atkin acknowledges the support of the Australian Research Council (DP130101252 and CE140100008)