Invasive species are predicted to suffer from reductions in genetic diversity during founding events, reducing adaptive potential. Integrating evidence from two literature reviews and two case studies, we address the following questions: How much genetic diversity is lost in invasions? Do multiple introductions ameliorate this loss? Is there evidence for loss of diversity in quantitative traits? Do invaders that have experienced strong bottlenecks show adaptive evolution? How do multiple introductions influence adaptation on a landscape scale? We reviewed studies of 80 species of animals, plants, and fungi that quantified nuclear molecular diversity within introduced and source populations. Overall, there were significant losses of both allelic richness and heterozygosity in introduced populations, and large gains in diversity were rare. Evidence for multiple introductions was associated with increased diversity, and allelic variation appeared to increase over long timescales (~100 years), suggesting a role for gene flow in augmenting diversity over the long-term. We then reviewed the literature on quantitative trait diversity and found that broad-sense variation rarely declines in introductions, but direct comparisons of additive variance were lacking. Our studies of Hypericum canariense invasions illustrate how populations with diminished diversity may still evolve rapidly. Given the prevalence of genetic bottlenecks in successful invading populations and the potential for adaptive evolution in quantitative traits, we suggest that the disadvantages associated with founding events may have been overstated. However, our work on the successful invader Verbascum thapsus illustrates how multiple introductions may take time to commingle, instead persisting as a 'mosaic of maladaptation' where traits are not distributed in a pattern consistent with adaptation. We conclude that management limiting gene flow among introduced populations may reduce adaptive potential but is unlikely to prevent expansion or the evolution of novel invasive behaviour.

The influence of genetic variation on invasion success has captivated researchers since the start of the field of invasion genetics 50 years ago. We review the history of work on this question and conclude that genetic variation-as surveyed with molecular markers-appears to shape invasion rarely. Instead, there is a significant disconnect between marker assays and ecologically relevant genetic variation in introductions. We argue that the potential for adaptation to facilitate invasion will be shaped by the details of genotypes affecting phenotypes, and we highlight three areas in which we see opportunities to make powerful new insights. (i) The genetic architecture of adaptive variation. Traits shaped by large-effect alleles may be strongly impacted by founder events yet more likely to respond to selection when genetic drift is strong. Large-effect loci may be especially relevant for traits involved in biotic interactions. (ii) Cryptic genetic variation exposed during invasion. Introductions have strong potential to uncover masked variation due to alterations in genetic and ecological environments. (iii) Genetic interactions during admixture of multiple source populations. As divergence among sources increases, positive followed by increasingly negative effects of admixture should be expected. Although generally hypothesized to be beneficial during invasion, admixture is most often reported among sources of intermediate divergence, supporting the possibility that incompatibilities among divergent source populations might be limiting their introgression. Finally, we note that these details of invasion genetics can be coupled with comparative demographic analyses to link genetic changes to the evolution of invasiveness itself.

Human-mediated species introductions offer opportunities to investigate when and how non-native species to adapt to novel environments, and whether evolution has the potential to contribute to colonization success. Many long-established introductions harbour high genetic diversity, raising the possibility that multiple introductions of genetic material catalyze adaptation and/or the evolution of invasiveness. Studies of nascent invasions are rare but crucial for understanding whether genetic diversity facilitates population expansion. We explore variation and evolution in founder populations of the invasive shrub Hypericum canariense. We find that these introductions have experienced large reductions in genetic diversity, but that increased growth and a latitudinal cline in flowering phenology have nevertheless evolved. These life history changes are consistent with predictions for invasive plants. Our results highlight the potential for even genetically depauperate founding populations to adapt and evolve invasive patters of spread.

Identifying sources of genetic variation and reconstructing invasion routes for non-native introduced species is central to understanding the circumstances under which they may evolve increased invasiveness. In this study, we used genome-wide single nucleotide polymorphisms to study the colonization history of Centaurea solstitialis in its native range in Eurasia and invasions into the Americas. We leveraged this information to pinpoint key evolutionary shifts in plant size, a focal trait associated with invasiveness in this species. Our analyses revealed clear population genomic structure of potential source populations in Eurasia, including deep differentiation of a lineage found in the southern Apennine and Balkan Peninsulas and divergence among populations in Asia, eastern Europe, and western Europe. We found strongest support for an evolutionary scenario in which western European populations were derived from an ancient admixture event between populations from eastern Europe and Asia, and subsequently served as the main genetic ‘bridgehead’ for introductions to the Americas. Introductions to California appear to be from a single source region, and multiple, independent introductions of divergent genotypes likely occurred into the Pacific Northwest. Plant size has evolved significantly at three points during range expansion, including a large size increase in the lineage responsible for the aggressive invasion of California’s interior. These results reveal a long history of colonization, admixture, and trait evolution in C. solstitialis, and suggest routes for improving evidence-based management decisions for one of the most ecologically and economically damaging invasive species in the western United States.

Non-native plants are now a pervasive feature of ecosystems across the globe1. One hypothesis for this pattern is that introduced species occupy open niches in recipient communities2,3. If true, then non-native plants should often benefit from low competition for limiting resources that define niches. Many plants have evolved larger size after introduction, consistent with increased access to limiting resources4–9. It has been difficult to test whether larger size reflects adaptation to exploit open resources, however, because vacant niches are generally challenging to identify in plants. Here we take advantage of a situation in which a highly invasive non-native plant, Centaurea solstitialis L. (yellow starthistle, hereafter ‘YST’), occupies a well-described environmental niche, wherein water is a known limiting resource10,11. We use a glasshouse common environment and climatic niche modeling to reveal that invading YST has evolved a higher-fitness life history at the expense of increased dependence on water. Critically, historical declines in resident competitors have made water more available for introduced plants11,12, demonstrating how native biodiversity declines can open niches and create opportunities for introduced species to evolve increased resource use, a potentially widespread basis for introduction success and the evolution of invasive life histories.