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Climate change may affect plant-herbivore interactions and their associated ecosystem functions. In an experimental evolution approach, we subjected replicated populations of the invasive Ambrosia artemisiifolia to a combination of simulated warming and herbivory by a potential biocontrol beetle. We tracked genomic and metabolomic changes across generations in field populations and assessed plant offspring phenotypes in a common environment. Using an integrated Bayesian model, we show that increased offspring biomass in response to warming arose through changes in the genetic composition of populations. In contrast, increased resistance to herbivory arose through a shift in plant metabolomic profiles without genetic changes, most likely by transgenerational induction of defences. Importantly, while increased resistance was costly at ambient temperatures, warming removed this constraint and favoured both vigorous and better defended plants under biocontrol. Climate warming may thus decrease biocontrol efficiency and promote Ambrosia invasion, with potentially serious economic and health consequences.

Text S1. Details on methodology. Table S1. Details on provenance of Pilosella rhodopea material used for particular analyses. Table S2. Dataset for 63 plants of Pilosella rhodopea included in the greenhouse experiment. Figure S1. Well-developed and aborted seeds of Pilosella rhodopea. Figure S2. Habitus and vegetative growth characteristics of diploid and autopolyploid plants of Pilosella rhodopea. Figure S3. Percentage of euploid and aneuploid seed progeny produced by diploid, autotriploid and autotetraploid plants of Pilosella rhodopea in natural primary contact zones. Figure S4. Photomicrographs of somatic metaphases in two aneuploid Pilosella rhodopea progeny produced by two triploid (2n = 27) mother plants. Figure S5. Flow cytometric screening analyses of seeds produced by diploid and autopolyploid plants of Pilosella rhodopea.

In the new range, invasive species lack their specialist co-evolved natural enemies, which then might be used as biocontrol agents. Populations of both a plant invader in the introduced range and its potential biocontrol agents in the native range may be genetically differentiated among geographically distinct regions. This, in turn, is expected to affect the outcome of their interaction when brought together, and by this the efficacy of the control. It further raises the question, is the outcome of such interactions mainly driven by the genotype of the plant invader (some plant genotypes being more resistant/tolerant to most of the antagonist genotypes), or by the antagonist genotype (some antagonist genotypes being more effective against most of the plant genotypes)? This is important for biocontrol management, as only the latter is expected to result in more effective control, when introducing the right biocontrol agent genotypes. In a third scenario, where the outcome of the interaction is driven by a specific plant by antagonist genotype interactions, an effective control will need the introduction of carefully selected multiple antagonist genotypes. Here, we challenged in a complete factorial design 11 plant genotypes (mainly half-siblings) of the invasive Ambrosia artemisiifolia with larvae of eight genotypes (full-siblings) of the leaf beetle Ophraella communa, a potential biocontrol insect, and assessed larval and adult performance and leaf consumption as proxies of their expected impact on the efficacy of biological control. Both species were collected from several locations from their native (USA) and introduced ranges (Europe and China). In summary, we found O. communa genotype to be the main driver of this interaction, indicating the potential for at least short-term control efficacy when introducing the best beetle genotypes. Besides the importance of investigating the genetic structure both among and within populations of the plant invader and the biocontrol agent during the pre-release phase of a biocontrol program, we advocate integrating such bioassays, as this will give a first indication of the probability for an – at least – short- to mid-term efficacy when introducing a potential biocontrol agent, and on where to find the most efficient agent genotypes.

Rapid evolution of weed biological control agents (BCAs) to new biotic and abiotic conditions is poorly understood and so far only little considered both in pre-release and post-release studies, despite potential major negative or positive implications for risks of nontargeted attacks or for colonizing yet unsuitable habitats, respectively. Provision of genetic resources, such as assembled and annotated genomes, is essential to assess potential adaptive processes by identifying underlying genetic mechanisms. Here, we provide the first sequenced genome of a phytophagous insect used as a BCA, that is, the leaf beetle Ophraella communa, a promising BCA of common ragweed, recently and accidentally introduced into Europe. A total 33.98 Gb of raw DNA sequences, representing ∼43-fold coverage, were obtained using the PacBio SMRT-Cell sequencing approach. Among the five different assemblers tested, the SMARTdenovo assembly displaying the best scores was then corrected with Illumina short reads. A final genome of 774 Mb containing 7,003 scaffolds was obtained. The reliability of the final assembly was then assessed by benchmarking universal single-copy orthologous genes (>96.0% of the 1,658 expected insect genes) and by remapping tests of Illumina short reads (average of 98.6 ± 0.7% without filtering). The number of protein-coding genes of 75,642, representing 82% of the published antennal transcriptome, and the phylogenetic analyses based on 825 orthologous genes placing O. communa in the monophyletic group of Chrysomelidae, confirm the relevance of our genome assembly. Overall, the genome provides a valuable resource for studying potential risks and benefits of this BCA facing environmental novelties.

In 2013, the North American oligophagous leaf beetle, Ophraella communa LeSage (Coleoptera: Chrysomelidae), was found in Europe for the first time. Recent studies in Northern Italy and Southern Switzerland record extensive defoliation by O. communa on its preferred host, common ragweed, Ambrosia artemisiifolia L. (Asteraceae, Tribe Heliantheae), and reductions in its flowering and seeding. In some regions in Northern Italy, this has reportedly led to a > 80% depletion in airborne A. artemisiifolia pollen concentrations. The potential for non-target damage by O. communa to closely related native European plant species was previously unknown. During extensive field surveys covering 18 populations of nine potential non-target species, we found adult O. communa on a single plant individual. In a common garden field experiment in Northern Italy in an area with high O. communa densities, leaf damage was highest on two other Asteraceae species, Dittrichia graveolens (L.) Greuter and Pentanema helveticum (Weber) D.Gut.Larr. (both in the Tribe Inuleae). While adult feeding was observed on most of the test plant species, only D. graveolens, which has recently extended its range and is now an invasive species in Western Europe, sustained all life stages of O. communa in the common garden and in laboratory experiments. We found no evidence of substantial non-target effects by O. communa that could potentially threaten populations of European native plant species that are taxonomically closely related to ragweed.

Predicting plant distributions under climate change is constrained by our limited understanding of potential rapid adaptive evolution. In an experimental evolution study with the invasive common ragweed (Ambrosia artemisiifolia L.) we subjected replicated populations of the same initial genetic composition to simulated climate warming. Pooled DNA sequencing of parental and offspring populations showed that warming populations experienced greater genetic divergence from their parents, than control populations. In a common environment, offspring from warming populations showed more convergent phenotypes in seven out of nine plant traits, with later flowering and larger biomass, than plants from control populations. For both traits, we also found a significantly higher ratio of phenotypic to genetic differentiation across generations for warming than for control populations, indicating stronger response to selection under warming conditions. As a measure for evolutionary rate, the phenotypic and sequence divergence between generations were assessed using the Haldane metric. Our approach combining comparisons between generations (allochronic) and between treatments (synchronic) in an experimental evolutionary field study, and linking population genomic data with phenotyping analyses provided a powerful test to detect rapid responses to selection. Our findings demonstrate that ragweed populations can rapidly evolve in response to climate change within a single generation. Short‐term evolutionary responses to climate change may aggravate the impact of some plant invaders in the future and should be considered when making predictions about future distributions and impacts of plant invaders.

Highly biodiversity communities have been shown to better resist plant invasions through complementarity effects. Species richness (SR) is a widely used biodiversity metric but lacks explanatory power when there are only a few species. Communities with low SR can have a wide variety of phylogenetic diversities (PD), which might allow for a better prediction of invasibility. We assessed the effect of diversity reduction of a wetland community assemblage typical of the Beijing area on biotic resistance to invasion of the exotic weed Alternanthera philoxeroides and compared the reduction in SR and PD in predicting community invasibility. The eight studied resident species performed similarly when grown alone and when grown in eight-species communities together with the invasive A. philoxeroides. Variation partitioning showed that PD contributed more to variation in both A. philoxeroides traits and community indicators than SR. All A. philoxeroides traits and community indicators, except for evenness index, showed a linear relationship with PD. However, only stem length of A. philoxeroides differed between the one- and two-species treatments, and the diversity index of the communities differed between the one- and two-species treatments and between the one- and four-species treatments. Our results showed that in natural or semi-natural wetlands with relatively low SR, PD may be a better predictor of invasibility than SR. When designing management strategies for mitigating A. philoxeroides invasion, deliberately raising PD is expected to be more efficient than simply increasing species number.