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

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

Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe

Soil microorganisms are critical to ecosystem functioning and the maintenance of soil fertility. However, despite global increases in the inputs of nitrogen (N) and phosphorus (P) to ecosystems due to human activities, we lack a predictive understanding of how microbial communities respond to elevated nutrient inputs across environmental gradients. Here we used high-throughput sequencing of marker genes to elucidate the responses of soil fungal, archaeal, and bacterial communities using an N and P addition experiment replicated at 25 globally distributed grassland sites. We also sequenced metagenomes from a subset of the sites to determine how the functional attributes of bacterial communities change in response to elevated nutrients. Despite strong compositional differences across sites, microbial communities shifted in a consistent manner with N or P additions, and the magnitude of these shifts was related to the magnitude of plant community responses to nutrient inputs. Mycorrhizal fungi and methanogenic archaea decreased in relative abundance with nutrient additions, as did the relative abundances of oligotrophic bacterial taxa. The metagenomic data provided additional evidence for this shift in bacterial life history strategies because nutrient additions decreased the average genome sizes of the bacterial community members and elicited changes in the relative abundances of representative functional genes. Our results suggest that elevated N and P inputs lead to predictable shifts in the taxonomic and functional traits of soil microbial communities, including increases in the relative abundances of faster-growing, copiotrophic bacterial taxa, with these shifts likely to impact belowground ecosystems worldwide

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

Grassland productivity limited by multiple nutrients

Terrestrial ecosystem productivity is widely accepted to be nutrient limited1. Although nitrogen (N) is deemed a key determinant of aboveground net primary production (ANPP)2,3, the prevalence of co-limitation by N and phosphorus (P) is increasingly recognized4,​5,​6,​7,​8. However, the extent to which terrestrial productivity is co-limited by nutrients other than N and P has remained unclear. Here, we report results from a standardized factorial nutrient addition experiment, in which we added N, P and potassium (K) combined with a selection of micronutrients (K+μ), alone or in concert, to 42 grassland sites spanning five continents, and monitored ANPP. Nutrient availability limited productivity at 31 of the 42 grassland sites. And pairwise combinations of N, P, and K+μ co-limited ANPP at 29 of the sites. Nitrogen limitation peaked in cool, high latitude sites. Our findings highlight the importance of less studied nutrients, such as K and micronutrients, for grassland productivity, and point to significant variations in the type and degree of nutrient limitation. We suggest that multiple-nutrient constraints must be considered when assessing the ecosystem-scale consequences of nutrient enrichment

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

Arbuscular mycorrhizal communities respond to nutrient enrichment and plant invasion in phosphorus‐limited eucalypt woodlands

Arbuscular mycorrhizal fungi (AMF) facilitate ecosystem functioning through provision of plant hosts with phosphorus (P), especially where soil P is limiting. Changes in soil nutrient regimes are expected to impact AMF, but the direction of the impact may depend on context. We predicted that nitrogen (N)-only enrichment promotes plant invasions and exacerbates their P limitation, increasing the utility of AMF and promoting AMF diversity. We expected that enrichment with N, P and other nutrients similarly promotes plant invasions, but decreases the benefit and diversity of AMF because P is readily available for both native and exotic plants. We tested these hypotheses in eucalypt woodlands of south-western Australia, that occur on soils naturally low in P. We evaluated AMF communities within three modified ground-layer states representing different types of nutrient enrichment and associated plant invasions. We compared these modified states to near-natural reference woodlands. AMF richness varied across ground-layer states. The moderately invaded/N-enriched state showed the highest AMF richness, while the highly invaded/NP-enriched state showed the lowest AMF richness. The reference state and the weakly invaded/enriched state were intermediate. AMF richness and colonisation were higher in roots of exotic than native plant species. AMF community composition differed among ground-layer states, with the highly invaded/NP-enriched state being most distinct. Distinctions among states were often driven by family-level patterns. Reference and moderately invaded/N-enriched states each supported distinct groups of zero-radius operational taxonomic units (zOTUs) in Acaulosporaceae, Gigasporaceae and Glomeraceae, whereas Gigasporaceae and Glomeraceae were nearly absent from the highly invaded/NP-enriched state. Further, Diversisporaceae and Glomeraceae were most diverse in the moderately invaded/N-enriched state. Synthesis. Both the nature of soil nutrient enrichment and plant provenance matter for AMF. N-only enrichment of low-P soils increased AMF richness, likely due to the introduction of AMF-dependent exotic plant species and exacerbation of their P limitation. In contrast, multi-nutrient enrichment, decreased AMF richness potentially due to a decrease in host dependence on AMF, regardless of host provenance. The changes in AMF community composition with nutrient enrichment and plant invasion warrant further research into predicting the functional implications of these changes