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.

Multivariate selection mediated by aridity predicts divergence of drought-resistant traits along natural aridity gradients of an invasive weed.

Geographical variation in the environment underpins selection for local adaptation and evolutionary divergence among populations. Because many environmental conditions vary across species' ranges, identifying the specific environmental variables underlying local adaptation is profoundly challenging. We tested whether natural selection mediated by aridity predicts clinal divergence among invasive populations of capeweed (Arctotheca calendula) that established and spread across southern Australia during the last two centuries. Using common garden experiments with two environmental treatments (wet and dry) that mimic aridity conditions across capeweed's invasive range, we estimated clinal divergence and effects of aridity on fitness and multivariate phenotypic selection in populations sampled along aridity gradients in Australia. We show that: (1) capeweed populations have relatively high fitness in aridity environments similar to their sampling locations; (2) the magnitude and direction of selection strongly differs between wet and dry treatments, with drought stress increasing the strength of selection; and (3) differences in directional selection between wet and dry treatments predict patterns of clinal divergence across the aridity gradient, particularly for traits affecting biomass, flowering phenology and putative antioxidant expression. Our results suggest that aridity-mediated selection contributes to trait diversification among invasive capeweed populations, possibly facilitating the expansion of capeweed across southern Australia.

A lack of genetically compatible mates constrains the spread of an invasive weed.

Introduced populations often experience lag times before invasion, but the mechanisms constraining rapid expansions of introduced populations are unclear. Solidago altissima is a North American native plant with highly invasive Japanese populations and introduced Australian populations that are not invasive despite the climatic and ecological suitability of the region. By contrasting Australian with Japanese populations, we tested the hypothesis that Australian population growth is limited by a lack of long-distance dispersal via seeds owing to a limited number of compatible mates. In the field, Australian populations rarely produced viable seeds. A cross-pollination experiment found that Australian plants are fertile, yet lack compatible mates within Australia. Genetic analysis revealed that Australian individuals descend from a small set of self-incompatible genetic clones, which explains the negligible seed set within Australia. Our results show that low genetic diversity, leading to mate incompatibility, inhibits invasiveness of Australian S.  altissima, and provides compelling evidence for genetic, rather than ecological, factors constraining invasion in Australia.

Evolution of "invasion syndrome" in invasive goldenrod is not constrained by genetic trade-offs.

A suite of plant traits is thought to make weed populations highly invasive, including vigorous growth and reproduction, superior competitive ability, and high dispersal ability. Using a breeding design and a common garden experiment, we tested whether such an "invasion syndrome" has evolved in an invasive range of Solidago altissima, and whether the evolution is likely to be genetically constrained. We found an overall shift in invasive phenotypes between native North American and invasive Japanese populations. The invasive populations were taller and produced more leaves, suggesting a superior ability to exploit limited resources. The populations also produced more allelopathic compounds that can suppress competitor growth. Finally, invasive populations produced more seeds, which are smaller and are released from a greater height, indicating a potential for superior dispersal ability than the native populations. Quantitative genetics analyses found a large amount of additive genetic variation in most focal traits across native and invasive populations, with no systematic differences in its magnitude between the ranges. Genetic covariances among three traits representing invasion strategies (leaf mass, polyacetylene concentration and seed size) were small. The R metric, which measures the effect of genetic covariances on the rate of adaptation, indicated that the covariance neither constrains nor accelerates concerted evolution of these traits. The results suggest that the invasion syndrome in S. altissima has evolved in the novel range due to ample additive genetic variation, and relatively free from genetic trade-offs.

Herbivore exclusion drives the evolution of plant competitiveness via increased allelopathy.

The 'Evolution of Increased Competitive Ability (EICA)' hypothesis predicts the evolution of plant invasiveness in introduced ranges when plants escape from their natural enemies. So far, the EICA hypothesis has been tested by comparing plant vigor from native and invasive populations, but these studies are confounded by among-population differences in additional environmental factors and/or founder effects. We tested the major prediction of EICA by comparing the competitive ability (CA) of Solidago altissima plants originating from artificial selection plots in which we manipulated directly the exposure to above-ground herbivores. In a common garden experiment, we found an increase in inter-specific, but not intra-specific, CA in clones from herbivore exclusion plots relative to control plots. The evolutionary increase in inter-specific CA coincided with the increased production of polyacetylenes, whose major constituent was allelopathic against a heterospecific competitor, Poa pratensis, but not against conspecifics. Our results provide direct evidence that release from herbivory alone can lead to an evolutionary increase in inter-specific CA, which is likely to be mediated by the increased production of allelopathic compounds in S. altissima.

A test of genotypic variation in specificity of herbivore-induced responses in Solidago altissima L. (Asteraceae).

Plant-induced responses to multiple herbivores can mediate ecological interactions among herbivore species, thereby influencing herbivore community composition in nature. Several studies have indicated high specificity of induced responses to different herbivore species. In addition, there may be genetic variation for plant response specificity that can have significant ecological implications, by altering the competitive strength and hierarchical relationships among interacting herbivore species. However, few studies have examined whether plant populations harbor genetic variation for induction specificity. Using three distinct genotypes of Solidago altissima plants, we examined whether specialist herbivore species Dichomeris leuconotella, Microrhopala vittata, and Trirhabda virgata elicit specific induction responses from plants (specificity of elicitation), and whether induction differentially affects these herbivore species (specificity of effect). Results from bioassays and secondary metabolite analyses suggest that there is specificity of both elicitation and effect in the induced responses: D. leuconotella and M. vittata preferred and performed better on leaves damaged by conspecifics than heterospecifics, and induced qualitatively different secondary metabolite profiles. In contrast, T. virgata equally avoided but physiologically tolerated all types of damage. These patterns of specificity suggest that plant-induced responses mediate asymmetric competitive interactions between herbivore species, which potentially intensifies inter-specific relative to intra-specific competition. Plant genotypes widely differed in overall susceptibility to the herbivores and secondary metabolite production, yet we found no genotype-by-treatment interactions in insect performance, preference and plant secondary metabolite production. This lack of genetic variation for induction specificity suggests that competitive interactions between herbivore species on S. altissima are homogeneous across plant genotypes.

Effects of Salinity on the Growth and Nutrition of Taro (Colocasia esculenta): Implications for Food Security.

Taro (Colocasia esculenta (L.) Schott) is a staple food crop in the Asia-Pacific region in areas where rising sea levels are threatening agricultural production. However, little is known about its response to salinity. In this study, we investigated the effects of salinity on the growth, morphology, physiology, and chemical traits of taro to predict the impacts of rising sea levels on taro production and nutritional value in the Pacific. We grew taro (approximately 4 months old) with a range of NaCl treatments (0-200 mM) for 12 weeks. Full nutrient, micronutrient, and secondary metabolite analyses were conducted, including measures of calcium oxalate (CaOx), an irritant that reduces palatability. Significant reductions in growth and biomass were observed at and above 100 mM NaCl. Concentrations of macro- and micronutrients, including sodium, were higher on a per mass basis in corms of plants experiencing salt stress. Foliar sodium concentrations remained stable, indicating that taro may utilize a salt exclusion mechanism. There was a large amount of individual variation in the concentrations of oxalate and phenolics, but overall, the concentrations were similar in the plants grown with different levels of salt. The total contents of CaOx and phenolics decreased in plants experiencing salt stress. Taro's ability to survive and produce corms when watered with a 200 mM NaCl solution places it among the salt-tolerant non-halophytes. The nutritional quality of the crop is only marginally affected by salt stress. Taro is, therefore, likely to remain a useful staple in the Pacific region in the future.

Insect Herbivory Selects for Volatile-Mediated Plant-Plant Communication.

Plant volatile organic compounds (VOCs) are major vehicles of information transfer between organisms and mediate many ecological interactions [1-3]. Altering VOC emission in response to herbivore damage has been hypothesized to be adaptive, as it can deter subsequent herbivores [4], attract natural enemies of herbivores [5], or transmit information about attacks between distant parts of the same plant [6-9]. Neighboring plants may also respond to these VOC cues by priming their own defenses against oncoming herbivory, thereby reducing future damage [10-12]. However, under which conditions such information sharing provides fitness benefits to emitter plants, and, therefore, whether selection by herbivores affects the evolution of such VOC signaling, is still unclear [13]. Here, we test the predictions of two alternative hypotheses, the kin selection and mutual benefits hypotheses [14], to uncover the selective environment that may favor information sharing in plants. Measuring the response to natural selection in Solidago altissima, we found strong effects of herbivory on the way plants communicated with neighbors. Plants from populations that experienced selection by insect herbivory induced resistance in all neighboring conspecifics by airborne cues, whereas those from populations experiencing herbivore exclusion induced resistance only in neighbors of the same genotype. Furthermore, the information-sharing plants converged on a common, airborne VOC signal upon damage. We demonstrate that herbivory can drive the evolution of plant-plant communication via induction of airborne cues and suggest plants as a model system for understanding information sharing and communication among organisms in general.

Rapid growth and defence evolution following multiple introductions.

Rapid adaptation can aid invasive populations in their competitive success. Resource allocation trade-off hypotheses predict higher resource availability or the lack of natural enemies in introduced ranges allow for increased growth and reproduction, thus contributing to invasive success. Evidence for such hypotheses is however equivocal and tests among multiple ranges over productivity gradients are required to provide a better understanding of the general applicability of these theories.Using common gardens, we investigated the adaptive divergence of various constitutive and inducible defence-related traits between the native North American and introduced European and Australian ranges, while controlling for divergence due to latitudinal trait clines, individual resource budgets, and population differentiation, using >11,000 SNPs.Rapid, repeated clinal adaptation in defence-related traits was apparent despite distinct demographic histories. We also identified divergence among ranges in some defence-related traits, although differences in energy budgets among ranges may explain some, but not all, defence-related trait divergence. We do not identify a general reduction in defence in concert with an increase in growth among the multiple introduced ranges as predicted trade-off hypotheses. Synthesis: The rapid spread of invasive species is affected by a multitude of factors, likely including adaptation to climate and escape from natural enemies. Unravelling the mechanisms underlying invasives' success enhances understanding of eco-evolutionary theory and is essential to inform management strategies in the face of ongoing climate change. OPEN RESEARCH BADGES: This article has been awarded Open Materials, Open Data, Preregistered Research Designs Badges. All materials and data are publicly accessible via the Open Science Framework at https://doi.org/10.6084/m9.figshare.8028875.v1, https://github.com/lotteanna/defence_adaptation,https://doi.org/10.1101/435271.

Relaxation of herbivore-mediated selection drives the evolution of genetic covariances between plant competitive and defense traits.

Insect herbivores are important mediators of selection on traits that impact plant defense against herbivory and competitive ability. Although recent experiments demonstrate a central role for herbivory in driving rapid evolution of defense and competition-mediating traits, whether and how herbivory shapes heritable variation in these traits remains poorly understood. Here, we evaluate the structure and evolutionary stability of the G matrix for plant metabolites that are involved in defense and allelopathy in the tall goldenrod, Solidago altissima. We show that G has evolutionarily diverged between experimentally replicated populations that evolved in the presence versus the absence of ambient herbivory, providing direct evidence for the evolution of G by natural selection. Specifically, evolution in an herbivore-free habitat altered the orientation of G, revealing a negative genetic covariation between defense- and competition-related metabolites that is typically masked in herbivore-exposed populations. Our results may be explained by predictions of classical quantitative genetic theory, as well as the theory of acquisition-allocation trade-offs. The study provides compelling evidence that herbivory drives the evolution of plant genetic architecture.