Introduction
As an unintended consequence of global commerce and climate change, biodiversity is being redistributed at an unprecedented rate (Ding, Mack, Lu, Ren, & Huang, 2008; Muirhead, Minton, Miller, & Ruiz, 2015; Ricciardi, 2007; Sardain, Sardain, & Leung, 2019; Seebens et al., 2015). Many introductions fail to form viable populations on foreign soil, but those that go on to establish and spread — invasive species — are a dominant cause of biodiversity declines and a major threat to global food security (Clavero, Brotons, Pons, & Sol, 2009; Clavero & García-Berthou, 2005; Maxwell, Fuller, Brooks, & Watson, 2016; Oerke, 2006). Invasion biology is an interdisciplinary field that aims to understand the transport, establishment and spread of invasive species and inform management strategies that mitigate their impact. Invasion genetics has proven to be an essential part of this effort (Barrett, 2015). From a purely biological perspective, many invasive species are ideal natural experiments that enable the observation of rapid adaptation, parallel evolution, inter- and intra-specific hybridization and speciation in the wild (C. E. Lee, 2002; Prentis, Wilson, Dormontt, Richardson, & Lowe, 2008; Vallejo-Marin & Hiscock, 2016). Quantifying such phenomena in invasive species will inevitably shed light on the factors that facilitate their transport, establishment and spread. A cursory examination of past issues of Molecular Ecology will attest to the long history of invasion geneticists working on pure and applied aspects of invasion biology in equal measure.
High-throughput sequencing is now broadly recognised as an important tool for monitoring, managing and mitigating the impact of invasive species (Chown et al., 2015; Hamelin & Roe, 2020; Rius, Bourne, Hornsby, & Chapman, 2015; Tay & Gordon, 2019). As a result, there has been a recent increase in the availability of reference genomes for invasive species, laying the groundwork for population resequencing projects (McCartney, Mallez, & Gohl, 2019). With the ease of transferable skills between study systems in molecular population genetics, the cost of sequencing continuing to decline, general bioinformatics literacy continuing to increase, and a greater recognition of the value of DNA sequence data in invasion science, we anticipate that whole-genome resequencing (WGR) will become a crucial tool in invasion genetics.
[ BOX 1 ]
What can population genomics add to the field of invasion genetics? The decision to sequence multiple whole genomes is not straightforward. This is primarily because progress in the field of invasion genetics is limited by a lack of manipulative experiments at least as much as it is limited by a lack of genome sequence data (Bock et al., 2015). Additionally, WGR is still a non-trivial cost in many systems and reduced-representation sequencing is in some cases sufficient to address key questions in invasion genetics (see Box 1). Here, we review the extent to which WGR has been adopted in the field of invasion genetics, assessing its existing and potential impact beyond other sequencing technologies (e.g. , transcriptomics, reduced-representation sequencing or comparative genomics of single reference genomes). To achieve this, we assessed 1,614 publications that appeared in a Web of Science search using the term “invasive species” ⋅ “genom*” ¬ “cancer”. By combining the results of this search with recent pre-prints at the time of writing, a total of 31 studies that used WGR to study invasive species were identified (Supplementary Table 1, examples shown in Figure 1). We highlight key case studies form this list, summarise theoretical considerations relevant to the population genomics of invasive species, and highlight newly developed technologies and analyses that enable novel insights though the use of WGR. Population genomic studies of native species evolving in response to invasive species, and studies of pathogens, are outside the scope of this review.
[ FIGURE 1 ]
We discuss five broad themes in invasion biology research that have involved, or could benefit from, high-throughput sequencing. These are 1) the role of pre-invasion adaptation in enabling subsequent spread; 2) tools to reconstruct invasion routes in space; 3) demographic inference to reconstruct the timing of invasion events, which also sheds light on the role of population bottlenecks during invasion; 4) post-introduction adaptation as a driver of spread in novel bioregions; and finally 5) the role of hybridization and introgression during invasion, which brings together all four of the preceding themes. These key themes reflect the focus of existing WGR papers in invasion biology and span the temporal range of the invasion sequence (Figure 2).
[ FIGURE 2 ]