Genetic adaptation and phenotypic plasticity influence trait expression under heatwave and water deficit conditions in the foundation tree, Corymbia calophylla

Climate change presents a major threat to forests globally, and is currently impacting forest carbon sequestration and contributing to increased tree mortality. Rising temperature, greater heatwave intensity and rainfall reductions associated with climate change are projected throughout many forested regions. Trees must respond to climate change through genetic adaptation, phenotypic plasticity or a combination of these processes, if not risk local extinction. Identifying the capacity for trees to respond through adaptive capacity to high temperature and water deficit conditions may help us better understand and predict forest resilience and function under climate change. Genetic adaptation is a shift in the genotypic composition of a population caused by environmental change typically over multiple generations. Phenotypic plasticity is the differential expression of a phenotype in response to variable environments by a genotype potentially providing a rapid response from minutes, hours, days to years. A genotype-by-environment interaction is the differential expression of plant traits by multiple genotypes across contrasting environments. These processes can be identified by measuring traits indicative of plant performance and survival for multiple genotypes in common garden experiments with contrasting environments and reciprocal plantings. The main aim of this thesis was to identify genetic adaptation, phenotypic plasticity and genotype-by-environment interactions influencing important temperature and drought-associated traits in the south west Australian foundation tree species, Corymbia calophylla (R. Br.) K.D. Hill & L.A.S. Johnson (Eucalyptus sensu lato; family Myrtaceae) under mild temperature and water availability conditions, and also stress-inducing heatwave and water deficit conditions. This was achieved using three common garden experiments involving water or temperature manipulation with multiple populations grown reciprocally across contrasting environments. This study contributes to the understanding of forest responses to climate change-associated shifts in temperature and rainfall, and critically, it provides important information on adaptive capacity to climate change provided through genetic adaptation and phenotypic plasticity

Plant functional traits differ in adaptability and are predicted to be differentially affected by climate change

1. Climate change is testing the resilience of forests worldwide pushing physiological tolerance to climatic extremes. Plant functional traits have been shown to be adapted to climate and have evolved patterns of trait correlations (similar patterns of distribution) and coordinations (mechanistic trade-off). We predicted that traits would differentiate between populations associated with climatic gradients, suggestive of adaptive variation, and correlated traits would adapt to future climate scenarios in similar ways. 2. We measured genetically determined trait variation and described patterns of correlation for seven traits: photochemical reflectance index (PRI), normalized difference vegetation index (NDVI), leaf size (LS), specific leaf area (SLA), δ13C (integrated water-use efficiency, WUE), nitrogen concentration (NCONC), and wood density (WD). All measures were conducted in an experimental plantation on 960 trees sourced from 12 populations of a key forest canopy species in southwestern Australia. 3. Significant differences were found between populations for all traits. Narrow sense heritability was significant for five traits (0.15–0.21), indicating that natural selection can drive differentiation; however, SLA (0.08) and PRI (0.11) were not significantly heritable. Generalized additive models predicted trait values across the landscape for current and future climatic conditions (>90% variance). The percent change differed markedly among traits between current and future predictions (differing as little as 1.5% (δ13C) or as much as 30% (PRI)). Some trait correlations were predicted to break down in the future (SLA:NCONC, δ13C:PRI, and NCONC:WD). 4. Synthesis: Our results suggest that traits have contrasting genotypic patterns and will be subjected to different climate selection pressures, which may lower the working optimum for functional traits. Further, traits are independently associated with different climate factors, indicating that some trait correlations may be disrupted in the future. Genetic constraints and trait correlations may limit the ability for functional traits to adapt to climate change

Ahrens et al. 2019 Evol App raw data

Raw data for the plantation from years 2015 and 2016. Height (HT), Diameter (D), and Blight (BT) with the year of collection after the trait abbreviation. Here blight is the blight damage score, so to calculate blight resistance subtract 5 from the score (i.e. blight resistence = BL16 - 5). Unique identifier, row, column, and block (Rep) are provided. For Trial, CAL02 is Margaret River and CAL03 is Mount Barker

Adaptive plasticity in plant traits increases time to hydraulic failure under drought in a foundation tree

The viability of forest trees, in response to climate change-associated drought, will depend on their capacity to survive through genetic adaptation and phenotypic plasticity in drought tolerance traits. Genotypes with enhanced plasticity for drought tolerance (adaptive plasticity) will have a greater ability to persist and delay the onset of hydraulic failure. By examining populations from different climate-origins grown under contrasting soil water availability, we tested for genotype (G), environment (E) and genotype-by-environment (G × E) effects on traits that determine the time it takes for saplings to desiccate from stomatal closure to 88% loss of stem hydraulic conductance (time to hydraulic failure, THF). Specifically, we hypothesized that: (i) THF is dependent on a G × E interaction, with longer THF for warm, dry climate populations in response to chronic water deficit treatment compared with cool, wet populations, and (ii) hydraulic and allometric traits explain the observed patterns in THF. Corymbia calophylla saplings from two populations originating from contrasting climates (warm-dry or cool-wet) were grown under well-watered and chronic soil water deficit treatments in large containers. Hydraulic and allometric traits were measured and then saplings were dried-down to critical levels of drought stress to estimate THF. Significant plasticity was detected in the warm-dry population in response to water deficit, with enhanced drought tolerance compared with the cool-wet population. Projected leaf area and total plant water storage showed treatment variation, and minimum conductance showed significant population differences driving longer THF in trees from warm-dry origins grown in water-limited conditions. Our findings contribute information on intraspecific variation in key drought traits, including hydraulic and allometric determinants of THF. It highlights the need to quantify adaptive capacity in populations of forest trees in climate change-type drought to improve predictions of forest die-back

Functional adaptations and trait plasticity of urban trees along a climatic gradient

In urban environments, long-term tree survival and performance requires physiological tolerance or phenotypic plasticity in plant functional traits. Knowledge of these traits can inform the likely persistence of urban forests under future, more severe climates. We assessed the plasticity of morphological and physiological traits of tree species planted along an urban climatic gradient in the Greater Sydney region during a severe, multi-year drought in eastern Australia. We selected four sites along a ∼55 km east-west transect, ranging from the cool/ wet coast to the warm/dry inland. We assessed five tree species (four natives, one exotic) with different predicted climatic vulnerability based on climate-origins, estimating functional traits indicative of drought tolerance: carbon isotope composition (δ13C), Huber value (HV), specific leaf area (SLA), wood density (WD), and leaf turgor loss point (πtlp). Broadly, trees planted in warm/dry sites had more negative πtlp, higher WD, δ13C and HV, and lower SLA than cool/wet sites, indicating phenotypic plasticity to drought. The leaf-level traits πtlp, δ13C and SLA were more strongly correlated with temperature and precipitation, compared to HV and WD. Species differed in the extent of their trait shifts along the transect, with greater plasticity evident in the exotic Celtis australis and the more temperate cool-climate Tristaniopsis laurina, compared to the more tropical, warm-climate Cupaniopsis anacardioides, which showed limited plasticity and lower drought tolerance. Our findings reveal adaptive capacity of urban trees to climate via plasticity in drought tolerance traits, which can direct species selection to improve urban forests resistance to climate change

[In Press] Repeated extreme heatwaves result in higher leaf thermal tolerances and greater safety margins

The frequency and severity of heatwave events are increasing, exposing species to conditions beyond their physiological limits. Species respond to heatwaves in different ways, however it remains unclear if plants have the adaptive capacity to successfully respond to hotter and more frequent heatwaves. We exposed eight tree populations from two climate regions grown under cool and warm temperatures to repeated heatwave events of moderate (40°C) and extreme (46°C) severity to assess adaptive capacity to heatwaves. Leaf damage and maximum quantum efficiency of photosystem II (Fv/Fm) were significantly impacted by heatwave severity and growth temperatures, respectively; populations from a warm-origin avoided damage under moderate heatwaves compared to those from a cool-origin, indicating a degree of local adaptation. We found that plasticity to heatwave severity and repeated heatwaves contributed to enhanced thermal tolerance and lower leaf temperatures, leading to greater thermal safety margins (thermal tolerance minus leaf temperature) in a second heatwave. Notably, while we show that adaptation and physiological plasticity are important factors affecting plant adaptive capacity to thermal stress, plasticity of thermal tolerances and thermal safety margins provides the opportunity for trees to persist among fluctuating heatwave exposures

Data from: Adaptive variation for growth and resistance to a novel pathogen along climatic gradients in a foundation tree

Natural ecosystems are under pressure from increasing abiotic and biotic stressors, including climate change and novel pathogens, which are putting species at risk of local extinction, and altering community structure, composition, and function. Here, we aim to assess adaptive variation in growth and fungal disease resistance within a foundation tree, Corymbia calophylla to determine local adaptation, trait heritability, and genetic constraints in adapting to future environments. Two experimental planting sites were established in regions of contrasting rainfall with seed families from 18 populations capturing a wide range of climate origins (~4000 individuals at each site). Every individual was measured in 2015 and 2016 for growth (height, basal diameter) and disease resistance to a recently introduced leaf blight pathogen (Quambalaria pitereka). Narrow-sense heritability was estimated along with trait covariation. Trait variation was regressed against climate-of-origin and multivariate models were used to develop predictive maps of growth and disease resistance. Growth and blight resistance traits differed significantly among populations, and these differences were consistent between experimental sites and sampling years. Growth and blight resistance were heritable, and comparisons between trait differentiation (QST) and genetic differentiation (FST) revealed that population differences in height and blight resistance traits are due to divergent natural selection. Traits were significantly correlated with climate-of-origin, with cool and wet populations showing the highest levels of growth and blight resistance. These results provide evidence that plants have adaptive growth strategies and pathogen defense strategies. Indeed, the presence of standing genetic variation and trait heritability of growth and blight resistance provide capacity to respond to novel, external pressures. The integration of genetic variation into adaptive management strategies, such as assisted gene migration and seed sourcing, may be used to provide greater resilience for natural ecosystems to both biotic and abiotic stressors

Adaptive variation for growth and resistance to a novel pathogen along climatic gradients in a foundation tree

Natural ecosystems are under pressure from increasing abiotic and biotic stressors, including climate change and novel pathogens, which are putting species at risk of local extinction, and altering community structure, composition and function. Here, we aim to assess adaptive variation in growth and fungal disease resistance within a foundation tree, Corymbia calophylla to determine local adaptation, trait heritability and genetic constraints in adapting to future environments. Two experimental planting sites were established in regions of contrasting rainfall with seed families from 18 populations capturing a wide range of climate origins (~4,000 individuals at each site). Every individual was measured in 2015 and 2016 for growth (height, basal diameter) and disease resistance to a recently introduced leaf blight pathogen (Quambalaria pitereka). Narrow‐sense heritability was estimated along with trait covariation. Trait variation was regressed against climate‐of‐origin, and multivariate models were used to develop predictive maps of growth and disease resistance. Growth and blight resistance traits differed significantly among populations, and these differences were consistent between experimental sites and sampling years. Growth and blight resistance were heritable, and comparisons between trait differentiation (QST) and genetic differentiation (FST) revealed that population differences in height and blight resistance traits are due to divergent natural selection. Traits were significantly correlated with climate‐of‐origin, with cool and wet populations showing the highest levels of growth and blight resistance. These results provide evidence that plants have adaptive growth strategies and pathogen defence strategies. Indeed, the presence of standing genetic variation and trait heritability of growth and blight resistance provide capacity to respond to novel, external pressures. The integration of genetic variation into adaptive management strategies, such as assisted gene migration and seed sourcing, may be used to provide greater resilience for natural ecosystems to both biotic and abiotic stressors

Canopy dieback and recovery in Australian native forests following extreme drought

In 2019, south-eastern Australia experienced its driest and hottest year on record, resulting in massive canopy dieback events in eucalypt dominated forests. A subsequent period of high precipitation in 2020 provided a rare opportunity to quantify the impacts of extreme drought and consequent recovery. We quantified canopy health and hydraulic impairment (native percent loss of hydraulic conductivity, PLC) of 18 native tree species growing at 15 sites that were heavily impacted by the drought both during and 8-10 months after the drought. Most species exhibited high PLC during drought (PLC:65.1 +/- 3.3%), with no clear patterns across sites or species. Heavily impaired trees (PLC > 70%) showed extensive canopy browning. In the post-drought period, most surviving trees exhibited hydraulic recovery (PLC:26.1 +/- 5.1%), although PLC remained high in some trees (50-70%). Regained hydraulic function (PLC < 50%) corresponded to decreased canopy browning indicating improved tree health. Similar drought (37.1 +/- 4.2%) and post-drought (35.1 +/- 4.4%) percentages of basal area with dead canopy suggested that trees with severely compromised canopies immediately after drought were not able to recover. This dataset provides insights into the impacts of severe natural drought on the health of mature trees, where hydraulic failure is a major contributor in canopy dieback and tree mortality during extreme drought events

Trait selection and community weighting are key to understanding ecosystem responses to changing precipitation regimes

Plant traits can be used to predict ecosystem responses to environmental change using a response\u2013effect trait framework. To do this, appropriate traits must be identified that explain a species' influence on ecosystem function (\u201ceffect traits\u201d) and the response of those species to environmental change (\u201cresponse traits\u201d). Response traits are often identified and measured along gradients in plant resources, such as water availability; however, precipitation explains very little variation in most plant traits globally. Given the strong relationship between plant traits and ecosystem functions, such as net primary productivity (NPP), and between NPP and precipitation, the lack of correlation between precipitation and plant traits is surprising. We address this issue through a systematic review of >500 published studies that describe plant trait responses to altered water availability. The overarching goal of this review was to identify potential causes for the weak relationship between commonly measured plant traits and water availability so that we may identify more appropriate \u201cresponse traits.\u201d We attribute weak trait\u2013precipitation relationships to an improper selection of traits (e.g., nonhydraulic traits) and a lack of trait-based approaches that adjust for trait variation within communities (only 4% of studies measure community-weighted traits). We then highlight the mechanistic value of hydraulic traits as more appropriate \u201cresponse traits\u201d with regard to precipitation, which should be included in future community-scale trait surveys. Trait-based ecology has the potential to improve predictions of ecosystem responses to predicted changes in precipitation; however, this predictive power depends heavily on the identification of reliable response and effect traits. To this end, trait surveys could be improved by a selection of traits that reflect physiological functions directly related to water availability with traits weighted by species relative abundance. A plain language summary is available for this article