Genomic investigations of successful invasions: the picture emerging from recent studies

Abstract

Invasion biology aims to identify traits and mechanisms that contribute to successful invasions, while also providing general insights into the mechanisms underlying population expansion and adaptation to rapid climate and habitat changes. Certain phenotypic attributes have been linked to successful invasions, and the role of genetics has been critical in understanding adaptation of invasive species. Nevertheless, a comprehensive summary evaluating the most common evolutionary mechanisms associated with successful invasions across species and environments is still lacking. Here we present a systematic review of studies since 2015 that have applied genomic tools to investigate mechanisms of successful invasions across different organisms. We examine demographic patterns such as changes in genomic diversity at the population level, the presence of genetic bottlenecks and gene flow in the invasive range. We review mechanisms of adaptation such as selection from standing genetic variation and de novo mutations, hybridisation and introgression, all of which can have an impact on invasion success. This comprehensive review of recent articles on the genomic diversity of invasive species led to the creation of a searchable database to provide researchers with an accessible resource. Analysis of this database allowed quantitative assessment of demographic and adaptive mechanisms acting in invasive species. A predominant role of admixture in increasing levels of genetic diversity enabling molecular adaptation in novel habitats is the most important finding of our study. The "genetic paradox" of invasive species was not validated in genomic data across species and ecosystems. Even though the presence of genetic drift and bottlenecks is commonly reported upon invasion, a large reduction in genomic diversity is rarely observed. Any decrease in genetic diversity is often relatively mild and almost always restored via gene flow between different invasive populations. The fact that loci under selection are frequently detected suggests that adaptation to novel habitats on a molecular level is not hindered. The above findings are confirmed herein for the first time in a semi-quantitative manner by molecular data. We also point to gaps and potential improvements in the design of studies of mechanisms driving rapid molecular adaptation in invasive populations. These include the scarcity of comprehensive studies that include sampling from multiple native and invasive populations, identification of invasion sources, longitudinal population sampling, and the integration of fitness measures into genomic analyses. We also note that the potential of whole genome studies is often not exploited fully in predicting invasive potential. Comparative genomic studies identifying genome features promoting invasions are underrepresented despite their potential for use as a tool in invasive species control.

Keywords: adaptation; admixture; biological invasions; genomic diversity; invasive species; next‐generation sequencing; selection.

Fig. 1

(A) Number of publications identified by our search terms according to kingdom. (B) Number of publications in different kingdoms in terrestrial versus aquatic habitats. (C) Publications studying selection occurring pre‐ and post‐introduction into the invasive range. (D) Publications studying admixture and hybridisation. (E) Publications studying source of invasion and the number of invasions. (F) Publications measuring genetic bottlenecks and/or genetic drift. (G) Publications assessing the change in genomic diversity between native and invasive ranges and/or quantifying the level of genomic diversity. Genomic diversity is categorised as: maintained = moderate decrease, no change, or increase in comparison with native populations; or decreased = marked decrease in comparison with native populations. Genomic diversity in the invasive range is categorised as: high = reported as high in the invasive range; or low = reported as low in the invasive range. Classification as high or low and maintained or decreased is based solely on the interpretation of the authors of each study.

Fig. 2

Genomic methods applied in the studies included in our database for the period 2015–2022. CGH, comparative genetic hybridisation; DE, differential gene expression; MSAP, methylation sensitive amplified polymorphisms; RRS, reduced representation sequencing; SNP, single nucleotide polymorphism; WGS, whole genome sequencing.

Fig. 3

Demographic factors shaping genetic diversity in invasive populations: (A) the percentage of articles detecting the presence of genetic bottleneck and/or genetic drift (both or one of the mechanisms was assessed in the article) or their absence (none of the mechanisms was confirmed in the article), and the percentage of articles where genetic diversity of invasive populations was assessed by the authors of each article as high or low; (B) the percentage of articles where admixture was reported or not, the percentage of articles detecting the presence of genetic bottleneck and/or genetic drift or not and the percentage of articles where genetic diversity of invasive populations was assessed by the article authors as high or low. Empty regions reflect a lack of information in the analysed articles. ADM, presence of admixture; B/D, presence of genetic bottleneck and/or genetic drift; HD, high level of genetic diversity in invasive populations; LD, low level of genetic diversity in invasive populations; NO ADM, absence of admixture; NO B/D, absence of genetic bottleneck and genetic drift.

Fig. 4

Demographic factors shaping genetic diversity in invasive populations. Percentage of articles detecting the presence of genetic bottleneck and/or genetic drift (both or one of the mechanisms was assessed in the article) or its absence (none of the mechanisms was confirmed in the article), the percentage of articles where either single or multiple introductions were detected and the percentage of articles where genetic diversity of invasive populations was assessed by the authors of each article as high or low. Empty regions reflect a lack of information in the analysed articles. B/D, presence of genetic bottleneck and/or genetic drift; HD, high level of genetic diversity in invasive populations; LD, low level of genetic diversity in invasive populations; MULTIPLE, detection of more than one event of introduction; NO B/D, absence of genetic bottleneck and genetic drift; SINGLE, detection of one introduction.

Fig. 5

Sunburst charts displaying the frequency of demographic factors affecting genomic diversity in articles where selection was detected: (A) the percentage of articles where selection was detected, the percentage of articles detecting the presence of genetic bottleneck and/or genetic drift (both or one of the mechanisms was assessed in the article) or absence (none of the mechanisms was confirmed in the article), and the percentage of articles where genetic diversity of invasive populations was assessed by the authors of each article as high or low; and (B) the percentage of articles where selection was detected, the percentage of articles where admixture was reported or not and the percentage of articles where genetic diversity of invasive populations was assessed as high or low. Empty regions reflect the lack of information in the analysed articles. ADM, presence of admixture; B/D, presence of genetic bottleneck and/or genetic drift; HD, high level of genetic diversity in invasive populations; LD, low level of genetic diversity in invasive populations; NO ADM, absence of admixture; NO B/D, absence of genetic bottleneck and genetic drift; SEL, presence of selection in invasive range.