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 ]