What makes some species highly invasive? An experimental study in the major crop pest Arionid slugs

Invasive species significantly impact ecosystem services and food security. Molluscs are now considered a major threat to food security, with banning of molluscicides, and their resilience to control measures and high intrinsic rates of increase. These omnivorous vectors of important plant pathogens hybridise with and drive out endemic species. Arrival of invasive slugs associates with declines in local biodiversity, with profound implications for food security and ecosystem stability. The extent to which invasive traits are species-specific, a consequence of hybridization/introgression or carriage/introduction of native-range microbiota remains unknown.

To gain new insights on the underlying cause(s) of invasions UK invasive arionid slugs, the pests Arion vulgaris and A. flagellus1 will be used as an experimental system to quantify phenotypic, genotypic and microbial consequences of interactions with native species. Few taxonomists specialize in this group of sibling species, whose frequent hybridization1 and facultative self-fertile breeding system confound identification. Taxonomic confusion and lack of high resolution molecular tools means colonization history, distributions and genetic interaction of invasive forms with endemics and succeeding invasion waves remain poorly known1. Hybridization with sibling taxa has been proposed to favour invasiveness (i) through the acquisition and exploitation of plant pathogenic bacteria as gut commensals, aiding digestion of plant material, and/or (ii) through the recurrent introgression of mitochondrial genes that could serve as source of adaptations to their new environment2. Hence, there is a need to assess the differential potential of invasive and endemic arionids to gain selective advantage from carriage and admixture of microbiota, and their ability to act as vectors of plant pathogenic bacteria, such that invasive hybrids may pose novel ecological and agricultural threats. The importance of mitochondrial by nuclear genome interactions in facilitating and promoting adaption to the environment in invasive species also remains elusive.
You will integrate taxon-specific anatomical, morphometric and colormetric traits with cutting edge markers (SNPs) from 'genotyping-by-sequencing' approaches and mitochondrial sequencing to make the first objective definition of each large arionid taxon, using individuals from native-range centres. This will provide markers to assess introgression, quantifying assimilation of endemic genomes and hence their contribution to invasion. You will quantify traits contributing to invasive potential (e.g. fecundity, longevity, survival during development, temperature, pathogen tolerance and markers of microbiome diversity). You will assess the contributions of heterosis (extreme genetic variability), microbiota, and mito-nuclear interactions to invasions, using contemporary and historic material from samples spanning 35 years from first contact. You will study consequences of mito-nuclear interaction from the level of the mitochondria to whole organism using a wide range of state-of-the-art physiological tools including high resolution respirometry. Finally, you will determine association of plant pathogens with taxa and level of introgression by qPCR3 and investigate plant pathogen spread by assessing the contribution of selected pathogens to invasive traits using a backcross population. All findings will be incorporated into ecological theory-based models to compare actual and predicted spread of invasive forms under different climate scenarios and to model slug-plant-pathogen interactions and epidemiology.