Conclusion
Many of the key questions in invasion genetics highlighted by Bocket al. (2015) remain unanswered, though our ability to obtain and interpret genome sequence data has matured substantially in the past five years. Though WGR data are certainly not a singular solution to outstanding questions about biological invasion, we are increasingly appreciating their potential; of the studies we assessed, over one third were published in the past year and more than two thirds were published within the past two years (Supplementary Table 1). Whilst some research questions have more to gain from WGR than others (e.g. , quantifying hybridization versus spatial inference), appropriately designed population genomics studies can address multiple questions about invasions simultaneously. Indeed, almost without exception, the examples we have highlighted addressed hypotheses from many areas of interest.
Based on existing genomic data, processes that maintain adaptive genetic diversity (i.e. , balancing selection, admixture and adaptive interspecific introgression) are often key to the success of invasive species (e.g. , Calfee et al., 2020; Hessenauer et al., 2020; Stern & Lee, 2020; Valencia-Montoya et al., 2020; Yainna et al., 2020). In other words, standing genetic diversity that has already been shaped by natural selection is often repurposed to rapidly overcome adaptive challenges; invasive species do not have time to re-invent the wheel. This is not a new observation. Several authors have argued that the same ‘combinatorial’ evolutionary processes known to facilitate major ecological transitions and adaptive radiations can also enable biological invasion (Hegarty, 2012; Marques, Meier, & Seehausen, 2019; Prentis et al., 2008; Rieseberg et al., 2003). Genomic data have revealed the frequency of this phenomenon among invasive species. It is now clear that the ‘paradox’ of biological invasion is often explained not only by the fact that many invasive species avoid the negative effects of demographic bottlenecks, but also because they avoid the need for de novo mutation followed by in situ adaptation. This implies a genic view of biological invasion in which the primary aim of management strategies should be to minimise the spread of alleles known to confer invasive success through introduced populations, and potentially through reproductively compatible native populations.
In the studies we surveyed, the most substantial individual contributions to our understanding of invasive species did not come from the largest datasets, but from studies that associated phenotypic or spatial information with genomic data in a hypothesis-driven design that incorporated appropriate modelling (e.g. , Calfee, Agra, Palacio, Ramírez, et al., 2020; Olazcuaga et al., 2020; Stern & Lee, 2020). Future genomic studies will contribute considerably to our understanding of pre- and post-introduction adaptation if they adopt such an approach. Useful inferences will also require development of tailored non-equilibrium models that can incorporate the full complexity of invasive species. In particular, an exciting area is understanding the evolutionary history of loci that contribute to adaptive spread. This will be easiest when studying recent invasions with samples taken over a time series. The second, more challenging step will be to quantify the marginal contribution of positively selected loci to invasive spread. Increasing use of forward-genetic approaches to dissect the genetic basis of invasiveness traits will likely make this task easier. Together, these approaches can be used to test whether the ‘combinatorial’ view of invasion success holds up as a general trend.
Given the pervasive role of hybridization in invasion success, alongside the declining cost of sequencing, we anticipate that whole genome sequence data will become a standardised approach for monitoring the ongoing global redistribution of biodiversity. Comprehensive genomic datasets will eventually allow invasion events to be consistently reconstructed at a resolution that is useful for informing management plans and they will put us in a better position to quantify the contribution of specific mechanisms to overall invasion success.