Demographic history and recent selection in novel environments: an innovative approach to assess benefits and risks of a potential biological control agent

Besides their great relevance for the environment, biological invasions have been recognized as unprecedented bio-geographical experiments to study fundamental ecological and evolutionary processes, such as e.g. local adaptation to the novel conditions in the introduced range. Like no other plant, Ambrosia artemisiifolia, common ragweed, has raised the awareness of invasive plants in Europe, causing great damage to our society due to its highly allergenic pollen, and as an important and hard-to-control crop weed. The recently and accidentally introduced Ophraella communa (Col.: Chrysomelidae) has the potential to reduce the population density and pollen production of ragweed in Europe, and to halt its further spread, but it also bears the risk to attack taxonomically closely-related sunflower and native endangered species. The presently ongoing EU-COST Action FA1203 on “Sustainable management of Ambrosia artemisiifolia in Europe (SMARTER), chaired by the PI, responded to this accidental introduction by launching an Ophraella Task Force, which is currently investigating the risks and potential benefits of using O. communa for biological control of common ragweed in Europe by conducting standard host-range and impact studies. The proposed study capitalizes on these findings and complements it by including genetics and genomics. The goal of this proposal is 1) to illuminate the invasion and spread history of O. communa both in Asia and Europe in order to identify the sources of the introduced populations and the spreading genotypes; 2) to estimate its potential to rapidly adapt to new i) abiotic (temperature) environment to predict its speed and spatial spread into suitable habitats across Europe, and ii) to assess the beetle’s potential for genetically-based changes in preference for and/or performance on non-target plants. More specifically, we propose the following four studies: (A) Identifying spatial genetic patterns and introduction sources using RAD-seq: the genetic diversity of some 36 O. communa populations from both the native (USA) and introduced ranges (China, Japan, CH and Italy) and from different host plants will be compared to reconstruct the global invasion history and to monitor the demographic spread in Europe; (B) Exploring phenotype-environment correlations: in our quarantine facilities, we will study the phenotypic variation in some 10 selected O. communa populations, when exposed to two temperature (abiotic) and three host plants (biotic) conditions. Observed trait variations in larval development and performance will be related to climate variables and host plant use in the source populations in order to test for local adaptation to the abiotic (temperature) or biotic (host plant) environment; (C) Artificial selection experiment with O. communa on sunflower: we will grow sunflower (and ragweed as controls) in large field cages in Italy and transfer several hundred beetles from a wide range as possible and rear them for some 10 generations (three years) to test for the possibility to develop a “sunflower strain”. The outcome will be tested i) in a bioassay in our quarantine facility, and ii) by applying a pooled sequencing approach to follow potential changes in diversity and allele frequencies over time and to identify potential genes involved; (D) Genetics of adaptation by linking (A) and (B): we will perform outlier analyses and genotype-environment associations (using the results from study (A) to test for divergent natural selection among the study populations, and for parallelism along latitudinal clines across continents, and in spreading O. communa populations in Europe. Furthermore, we will associate allele frequencies assessed in study (A) with the phenotypic data form the quarantine phenotyping experiment to investigate trade-offs in abiotic and biotic responses. Our findings will be of great interest not only for basic science through contributing to a better understanding and more accurate predictions of local adaptation, a crucial issue in the light of global environmental change, and especially to render risk-benefit assessments in biological control more predictive. It will also be of high interest to national and European authorities with regard to the prerequisites and regulations of biological control projects in Europe, as well as for the larger audience and society presently suffering from ragweed pollen, as shown by the great interest and good media coverage achieved so far.