Adaptive responses to living in stressful habitats: Do invasive and native plant populations use different strategies?

Plants inhabit stressful environments characterized by a variety of stressors, including mine sites, mountains, deserts, and high latitudes. Populations from stressful and reference (non-stressful) sites often have performance differences. However, while invasive and native species may respond differently to stressful environments, there is limited understanding of the patterns in reaction norms of populations from these sites. Here, we use phylogenetically controlled meta-analysis to assess the performance of populations under stress and non-stress conditions. We ask whether stress populations of natives and invasives differ in the magnitude of lowered performance under non-stress conditions and if they vary in the degree of performance advantage under stress. We also assessed whether these distinctions differ with stress intensity. Our findings revealed that natives not only have greater adaptive advantages but also more performance reductions than invasives. Populations from very stressful sites had more efficient adaptations, and performance costs increased with stress intensity in natives only. Overall, the results support the notion that adaptation is frequently costless. Reproductive output was most closely associated with adaptive costs and benefits. Our study characterized the adaptive strategies used by invasive and native plants under stressful conditions, thereby providing important insights into the limitations of adaptation to extreme sites.

The great escape: patterns of enemy release are not explained by time, space or climate.

When a plant is introduced to a new ecosystem it may escape from some of its coevolved herbivores. Reduced herbivore damage, and the ability of introduced plants to allocate resources from defence to growth and reproduction can increase the success of introduced species. This mechanism is known as enemy release and is known to occur in some species and situations, but not in others. Understanding the conditions under which enemy release is most likely to occur is important, as this will help us to identify which species and habitats may be most at risk of invasion. We compared in situ measurements of herbivory on 16 plant species at 12 locations within their native European and introduced Australian ranges to quantify their level of enemy release and understand the relationship between enemy release and time, space and climate. Overall, plants experienced approximately seven times more herbivore damage in their native range than in their introduced range. We found no evidence that enemy release was related to time since introduction, introduced range size, temperature, precipitation, humidity or elevation. From here, we can explore whether traits, such as leaf defences or phylogenetic relatedness to neighbouring plants, are stronger indicators of enemy release across species.

Terrestrial ecosystem restoration increases biodiversity and reduces its variability, but not to reference levels: A global meta-analysis.

Ecological restoration projects often have variable and unpredictable outcomes, and these can limit the overall impact on biodiversity. Previous syntheses have investigated restoration effectiveness by comparing average restored conditions to average conditions in unrestored or reference systems. Here, we provide the first quantification of the extent to which restoration affects both the mean and variability of biodiversity outcomes, through a global meta-analysis of 83 terrestrial restoration studies. We found that, relative to unrestored (degraded) sites, restoration actions increased biodiversity by an average of 20%, while decreasing the variability of biodiversity (quantified by the coefficient of variation) by an average of 14%. As restorations aged, mean biodiversity increased and variability decreased relative to unrestored sites. However, restoration sites remained, on average, 13% below the biodiversity of reference (target) ecosystems, and were characterised by higher (20%) variability. The lower mean and higher variability in biodiversity at restored sites relative to reference sites remained consistent over time, suggesting that sources of variation (e.g. prior land use, restoration practices) have an enduring influence on restoration outcomes. Our results point to the need for new research confronting the causes of variability in restoration outcomes, and close variability and biodiversity gaps between restored and reference conditions.

Advancing the missed mutualist hypothesis, the under-appreciated twin of the enemy release hypothesis.

Introduced species often benefit from escaping their enemies when they are transported to a new range, an idea commonly expressed as the enemy release hypothesis. However, species might shed mutualists as well as enemies when they colonize a new range. Loss of mutualists might reduce the success of introduced populations, or even cause failure to establish. We provide the first quantitative synthesis testing this natural but often overlooked parallel of the enemy release hypothesis, which is known as the missed mutualist hypothesis. Meta-analysis showed that plants interact with 1.9 times more mutualist species, and have 2.3 times more interactions with mutualists per unit time in their native range than in their introduced range. Species may mitigate the negative effects of missed mutualists. For instance, selection arising from missed mutualists could cause introduced species to evolve either to facilitate interactions with a new suite of species or to exist without mutualisms. Just as enemy release can allow introduced populations to redirect energy from defence to growth, potentially evolving increased competitive ability, species that shift to strategies without mutualists may be able to reallocate energy from mutualism toward increased competitive ability or seed production. The missed mutualist hypothesis advances understanding of the selective forces and filters that act on plant species in the early stages of introduction and establishment and thus could inform the management of introduced species.

Allelopathy confers an invasive Wedelia higher resistance to generalist herbivore and pathogen enemies over its native congener.

The Novel Defense Hypothesis predicts that introduced plants may possess novel allelochemicals which act as a defense against native generalist enemies. Here, we aim to test if the chemicals involved in allelopathy in the invasive plant Wedelia trilobata can contribute to higher resistance against generalist herbivore and pathogen enemies by comparing with its native congener W. chinensis in controlled laboratory conditions. The allelopathic effects of the leaf extract from W. trilobata on the generalist enemies were also assessed. We showed that the larvae of two moth species preferred W. chinensis over W. trilobata. The growth rate of larvae feeding on W. trilobata leaves was significantly lower than those feeding on W. chinensis leaves. When detached leaves were inoculated with phytopathogens, the infected leaf area of W. trilobata was significantly smaller than that of W. chinensis. In addition, the leaf extract of W. trilobata also effectively inhibited the growth of the larvae and the mycelial growth of the phytopathogens. Our results indicate that the defenses of invasive W. trilobata against generalist herbivore and pathogen enemies are stronger than that of its native congener, which may be attributed to the allelopathic effects. This study provides novel insights that can comprehensively link the Novel Defense, Behavioral Constraint and Enemy Release hypotheses. These combined hypotheses would explain how invasive plants escape from their natural specialist enemies, where their allelopathic chemicals may deter herbivorous insects and inhibit pathogen infection.

Speciation in the presence of gene flow: population genomics of closely related and diverging Eucalyptus species.

Speciation is a complex process that is fundamental to the origins of biological diversity. While there has been considerable progress in our understanding of speciation, there are still many unanswered questions, especially regarding barriers to gene flow in diverging populations. Eucalyptus is an appropriate system for investigating speciation mechanisms since it comprises species that are rapidly evolving across heterogeneous environments. We examined patterns of genetic variation within and among six closely related Eucalyptus species in subgenus Eucalyptus section Eucalyptus in south-eastern Australia (commonly known as the "green ashes"). We used reduced representation genome sequencing to genotype samples from populations across altitudinal and latitudinal gradients. We found one species, Eucalyptus cunninghamii, to be highly genetically differentiated from the others, and a population of mallees from Mount Banks to be genetically distinct and therefore likely to be a new undescribed species. Only modest levels of differentiation were found between all other species in the study. There was population structure within some species (e.g., E. obstans) corresponding to geographical factors, indicating that vicariance may have played a role in the evolution of the group. Overall, we found that lineages within the green ashes are differentiated to varying extents, from strongly diverged to much earlier stages of the speciation continuum. Furthermore, our results suggest the green ashes represent a group where a range of mechanisms (e.g., reticulate evolution and vicariance) have been operating in concert. These findings not only offer insights into recent speciation mechanisms in Eucalyptus, but also other species complexes.

Seedling response to environmental variability: The relationship between phenotypic plasticity and evolutionary history in closely related Eucalyptus species.

PREMISE OF THE STUDY: Phenotypic plasticity is an important means through which organisms cope with environmental variability. We investigated seedling plasticity in the green ash eucalypts within a phylogenetic framework to examine the relationship between plasticity and evolutionary history. The green ashes are a diverse group, which include the tallest flowering plant in the world (Eucalyptus regnans) and a rare mallee less than 1 m tall (E. cunninghamii). METHODS: Seedlings of 12 species were exposed to high and low nutrient and water availability in a factorial experiment. Leaf trait and total plant plasticity were evaluated using the phenotypic plasticity index. A phylogeny of the species was estimated using genome-wide scans. KEY RESULTS: We found significant differences in functional traits across species, growth forms, and substrates in response to changes in resource availability. Many traits (e.g., leaf width) were highly plastic for most species. Interspecific differences in leaf-level plasticity was significant, however plasticity was not correlated with phylogeny. Species with broader environmental niches had higher leaf-level plasticity than species with narrower environmental ranges. CONCLUSIONS: Plastic responses to environmental variability can differ widely among closely related species, and plasticity is therefore likely to be associated with many factors, including habitat and range size, as well as evolutionary history. Our results provided insights for species delimitation in Eucalyptus, which have management implications. Because of the high number of rare species and that other species are commercially important, a more comprehensive understanding of plasticity is essential for predicting their response to changing climates.

Plasticity and the adaptive evolution of switchlike reaction norms under environmental change.

Phenotypic plasticity is often posited as an avenue for adaptation to environmental change, whereby environmental influences on phenotypes could shift trait expression toward new optimal values. Conversely, plastic trait expression may inhibit adaptation to environmental change by reducing selective pressure on ill-adapted traits. While plastic responses are often assumed to be linear, nonlinear phenotype-environment relationships are common, especially in thermally sensitive traits. Here we examine nonlinear plasticity in a trait with great ecological and evolutionary significance: sexual phenotype in species with environmental sex determination (ESD). In species with ESD, development switches between male and female at an environmental threshold (the inflection point). The inflection point is a key trait for adaptive responses to changing environments and should evolve toward the new optimum in order to maintain evolutionarily stable sex ratios. We used an individual-based theoretical model to investigate how two forms of plasticity in the ESD reaction norm-the nonlinear slope of the reaction norm and a linear shift in the inflection point-influence the evolution of the inflection point under climate warming. We found that steeper reaction norm slopes (high nonlinear plasticity) promoted evolution toward new optimal phenotypes (higher inflection points). In contrast, increased linear plasticity in the inflection point (shift) hindered adaptive evolution. Additionally, populations in moderate warming scenarios showed greater adaptive evolution of the inflection point compared with populations in extreme warming scenarios, suggesting that the proximity of existing phenotypes to new optimal phenotypes influences evolutionary outcomes. Unexpectedly, we found greater population persistence under high climate variability, due to the increased production of rare-sex individuals in unusually cold years. Our results demonstrate that different forms of phenotypic plasticity have crucially different effects on adaptive evolution. Plasticity that prevented sex ratio bias hindered the evolution of the inflection point, while plasticity that exacerbated sex ratio bias promoted adaptation to environmental change.

Introduced species shed friends as well as enemies.

Many studies seeking to understand the success of biological invasions focus on species' escape from negative interactions, such as damage from herbivores, pathogens, or predators in their introduced range (enemy release). However, much less work has been done to assess the possibility that introduced species might shed mutualists such as pollinators, seed dispersers, and mycorrhizae when they are transported to a new range. We ran a cross-continental field study and found that plants were being visited by 2.6 times more potential pollinators with 1.8 times greater richness in their native range than in their introduced range. Understanding both the positive and negative consequences of introduction to a new range can help us predict, monitor, and manage future invasion events.

Is sex advantageous in adverse environments? A test of the abandon-ship hypothesis.

Understanding the evolution and maintenance of sexual reproduction remains a long-standing challenge in evolutionary biology. Stress often induces sexual reproduction in facultatively sexual species (those species capable of both sexual and asexual reproduction). The abandon-ship hypothesis predicts higher allocation to sex under stress to allow low-fitness individuals to recombine their genotype, potentially increasing offspring fitness. However, effective tests of the abandon-ship hypothesis, particularly in multicellular organisms, are lacking. Here we test the abandon-ship hypothesis, using cyanogenic and acyanogenic defense phenotypes of the short-lived perennial herb Trifolium repens. Cyanogenesis provides an effective defense against herbivores and is under relatively simple genetic control (plants dominant for cyanogenesis at two alleles express the defended phenotype). Thus, maladapted individuals can acquire adaptive defense alleles for their offspring in a single episode of sexual reproduction. Plants were grown under high- and low-herbivory treatments (plants were exposed to herbivorous snails) and a control treatment (no herbivory). Herbivores reduced growth and fitness in all treated plants, but herbivory induced higher sexual allocation only in maladapted (acyanogenic) individuals. Overall, our results support the abandon-ship hypothesis.

Differences in forest plant functional trait distributions across land-use and productivity gradients.

PREMISE OF STUDY: Plant functional traits are commonly used as proxies for plant responses to environmental challenges, yet few studies have explored how functional trait distributions differ across gradients of land-use change. By comparing trait distributions in intact forests with those across land-use change gradients, we can improve our understanding of the ways land-use change alters the diversity and functioning of plant communities. METHODS: We examined how the variation and distribution of trait values for seven plant functional traits differ between reference natural forest and three types of land-use conversion (pasture, old-field, or "legacy" sites-regrowth following logging), landscape productivity (NPP) and vegetation strata (tree or non-tree "understory"), in a meta-analysis of studies from 15 landscapes across five continents. KEY RESULTS: Although trait variation often differed between land-uses within a landscape, these patterns were rarely consistent across landscapes. The variance and distribution of traits were more likely to differ consistently between natural forest and land-use conversion categories for understory (non-tree) plants than for trees. Landscape productivity did not significantly alter the difference in trait variance between natural forest and land-use conversion categories for any trait except dispersal. CONCLUSIONS: Our results suggest that even for traits well linked to plant environmental response strategies, broad classes of land-use change and landscape productivity are not generally useful indicators of the mechanisms driving compositional changes in human-modified forest systems.

Island biogeography, competition, and abiotic filtering together control species richness in habitat islands formed by nurse tree canopies in an arid environment.

The theory of island biogeography predicts that island size is a key predictor of community species richness. Islands can include any habitat surrounded environments that are inhospitable to the resident species. In arid environments, nurse trees act as islands in an environment uninhabitable to many plant species, and the size of the canopy controls the size of the understory plant community. We predicted that plant species richness will be affected by the area of the habitat and decrease with habitat isolation. We sampled the adult and seedling plant communities at canopy center, canopy edge, and outside canopy microhabitats. We found that species richness in both adult and seedling communities increases with increasing island area. However, richness in seedling communities was greater than in adult communities, and this effect was greatest at the canopy center microhabitat. Competition has been demonstrated to be more important in controlling species distributions near the canopy center, and stress is more important near the canopy edge. Thus, our results suggest that neutral forces, biotic interactions, and abiotic filtering act together to control species richness in these island communities.

Arbuscular Mycorrhizal Fungi Contribute to Phosphorous Uptake and Allocation Strategies of Solidago canadensis in a Phosphorous-Deficient Environment.

Arbuscular mycorrhizal fungi (AMF) can facilitate the uptake of limiting or inaccessible nutrients by plants. However, the importance of AMF for invasive plants under phosphorus (P) limitation is poorly well understood because of the presence of non-focal microorganisms, such as endophytes or rhizosphere bacteria. In this study, we investigated how an invasive clonal plant Solidago canadensis benefits from the AMF Glomus intraradices by using a completely sterile culturing system, which is composed of aseptic seedlings, a pure AMF strain, and a sterile growth environment. We found that the colonization rate, abundance, and spore production of AMF in the insoluble P treatment was more than twice as much as in the available P treatment. Plant above-ground growth was enhanced almost 50% by AMF in the insoluble P treatment. Importantly, AMF were able to facilitate P acquisition by the plant in insoluble P conditions, allowing plants to have lower investment into below-ground biomass and higher benefit/return for above-ground biomass. This study demonstrated the important contribution that AMF make to plants in phosphate-deficient environments eliminating interference from non-focal microorganisms. Our results also suggest that interaction with AMF could contribute to the invasiveness of clonal plant S. canadensis in a resource-deficient environment.

Global urban environmental change drives adaptation in white clover.

Urbanization transforms environments in ways that alter biological evolution. We examined whether urban environmental change drives parallel evolution by sampling 110,019 white clover plants from 6169 populations in 160 cities globally. Plants were assayed for a Mendelian antiherbivore defense that also affects tolerance to abiotic stressors. Urban-rural gradients were associated with the evolution of clines in defense in 47% of cities throughout the world. Variation in the strength of clines was explained by environmental changes in drought stress and vegetation cover that varied among cities. Sequencing 2074 genomes from 26 cities revealed that the evolution of urban-rural clines was best explained by adaptive evolution, but the degree of parallel adaptation varied among cities. Our results demonstrate that urbanization leads to adaptation at a global scale.

Optimal allocation of resources in response to shading and neighbours in the heteroblastic species, Acacia implexa.

BACKGROUND AND AIMS: Heteroblasty is an encompassing term referring to ontogenetic changes in the plant shoot. A shaded environment is known to affect the process of heteroblastic development; however, it is not known whether crowded or high density growing conditions can also alter heteroblasty. Compound leaves of the shade-intolerant Acacia implexa allocate less biomass per unit photosynthetic area than transitional leaves or phyllodes and it is hypothesized that this trait will convey an advantage in a crowded environment. Compound leaves also have larger photosynthetic capture area - a trait known to be advantageous in shade. This studied tested the hypothesis that more compound leaves will be developed under shade and crowded environments. Furthermore, this species should undergo optimal allocation of biomass to shoots and roots given shaded and crowded environments. METHODS: A full factorial design of irradiance (high and low) and density levels (high, medium and low) on three populations sourced from varying rainfall regions (high, medium and low) was established under controlled glasshouse conditions. Traits measured include the number of nodes expressing a compound leaf, biomass allocation to shoots and roots, and growth traits. Key Results A higher number of nodes expressed a compound leaf under low irradiance and in high density treatments; however, there were no significant interactions across treatments. Phenotypes strongly associated with the shade avoidance syndrome were developed under low irradiance; however, this was not observed under high density. There was no significant difference in relative growth rates across light treatments, but growth was significantly slower in a crowded environment. Conclusions Heteroblastic development in Acacia can be altered by shade and crowded environments. In this experiment, light was clearly the most limiting factor to growth in a shaded environment; however, in a crowded environment there were additional limiting resources to growth.

Habitat Quality Differentiation and Consequences for Ecosystem Service Provision of an Amazonian Hyperdominant Tree Species.

Ecosystem services of Amazonian forests are disproportionally produced by a limited set of hyperdominant tree species. Yet the spatial variation in the delivery of ecosystem services by individual hyperdominant species across their distribution ranges and corresponding environmental gradients is poorly understood. Here, we use the concept of habitat quality to unravel the effect of environmental gradients on seed production and aboveground biomass (AGB) of the Brazil nut, one of Amazonia's largest and most long-lived hyperdominants. We find that a range of climate and soil gradients create trade-offs between density and fitness of Brazil nut trees. Density responses to environmental gradients were in line with predictions under the Janzen-Connell and Herms-Mattson hypotheses, whereas tree fitness responses were in line with resource requirements of trees over their life cycle. These trade-offs resulted in divergent responses in area-based seed production and AGB. While seed production and AGB of individual trees (i.e., fitness) responded similarly to most environmental gradients, they showed opposite tendencies to tree density for almost half of the gradients. However, for gradients creating opposite fitness-density responses, area-based seed production was invariable, while trends in area-based AGB tended to mirror the response of tree density. We conclude that while the relation between environmental gradients and tree density is generally indicative of the response of AGB accumulation in a given area of forest, this is not necessarily the case for fruit production.

Land-use intensification reduces functional redundancy and response diversity in plant communities.

Ecosystem resilience depends on functional redundancy (the number of species contributing similarly to an ecosystem function) and response diversity (how functionally similar species respond differently to disturbance). Here, we explore how land-use change impacts these attributes in plant communities, using data from 18 land-use intensity gradients that represent five biomes and > 2800 species. We identify functional groups using multivariate analysis of plant traits which influence ecosystem processes. Functional redundancy is calculated as the species richness within each group, and response diversity as the multivariate within-group dispersion in response trait space, using traits that influence responses to disturbances. Meta-analysis across all datasets showed that land-use intensification significantly reduced both functional redundancy and response diversity, although specific relationships varied considerably among the different land-use gradients. These results indicate that intensified management of ecosystems for resource extraction can increase their vulnerability to future disturbances.

The adaptive value of functional and life-history traits across fertility treatments in an annual plant.

BACKGROUND AND AIMS: Plant functional traits are assumed to be adaptive. As selection acts on individuals and not on traits, interpreting the adaptive value of a trait not may be straightforward. For example, productive leaves are associated with fertile environments. However, it is not clear if productive leaves confer an advantage in these habitats, or if they are an advantage as part of a suite of coordinated traits. METHODS: Genotypes of Arabidopsis thaliana were grown in high and low nutrient treatments and low, neutral and high pH treatments. Nutrient availability is reduced in acidic or basic soils relative to neutral pH soils. pH treatments were used to alter the availability of resources rather than the amount of resources. KEY RESULTS: Leaf function (specific leaf area, SLA) and life history (size at reproduction, age at reproduction) were variable across genotypes and were plastic. High nutrient availability induced higher SLA and larger size at reproduction. Genotypes that reproduced at large size in high nutrient conditions at neutral pH had the greatest fruit production. SLA was only indirectly related to fruit production through a causal relationship with rosette size; in high nutrient conditions, plants with high SLA were large at reproduction and had higher fruit production. In high nutrient and high pH treatments, plants were large at reproduction, but large size at reproduction was associated with low fecundity. This suggests that large size is adaptive under high nutrient availability. CONCLUSIONS: Interpreting the adaptive value of functional traits will sometimes only be possible when these traits are considered as a suite of correlated and coordinated traits. Leaf functional traits may be important in defining adaptive strategies in A. thaliana but only through how they affect plant life history. Finally, manipulating soil pH can be a valuable tool in assessing adaptive plasticity on nutrient gradients.

Heteroblastic development and the optimal partitioning of traits among contrasting environments in Acacia implexa.

BACKGROUND AND AIMS: Optimal partitioning theory (OPT) predicts plants will allocate biomass to organs where resources are limiting. Studies of OPT focus on root, stem and leaf mass ratios where roots and stems are often further sub-divided into organs such as fine roots/tap roots or branches/main stem. Leaves, however, are rarely sub-divided into different organs. Heteroblastic species develop juvenile and adult foliage and provide an opportunity of sub-dividing leaf mass ratio into distinct organs. Acacia implexa (Mimosaceae) is a heteroblastic species that develops compound (juvenile), transitional and phyllode (adult) leaves that differ dramatically in form and function. The aims of the present study were to grow A. implexa to examine patterns of plastic development of whole-plant and leaf traits under the OPT framework. METHODS: Plants were grown in a glasshouse under contrasting nutrient, light and water environments in a full factorial design. Allocation to whole-plant and leaf-level traits was measured and analysed with multivariate statistics. KEY RESULTS: Whole-plant traits strongly followed patterns predicted by OPT. Leaf-level traits showed a more complex pattern in response to experimental treatments. Compound leaves on low nutrient plants had significantly lower specific leaf area (SLA) and were retained for longer as quantified by a significantly greater compound leaf mass ratio after 120 d. There was no significant difference in SLA of compound leaves in the light treatment, yet transitional SLA was significantly higher under the low light treatment. The timing of heteroblastic shift from compound to transitional leaves was significantly delayed only in the low light treatment. Therefore, plants in the light treatment responded at the whole-plant level by adjusting allocation to productive compound leaves and at the leaf-level by adjusting SLA. There were no significant SLA differences in the water treatment despite strong trends at the whole-plant level. CONCLUSION: Explicitly sub-dividing leaves into different types provided greater insights into OPT.