The evolutionary dynamics of biological invasions: A multi-approach perspective

Abstract

Biological invasions, the establishment and spread of non-native species in new regions, can have extensive economic and environmental consequences. Increased global connectivity accelerates introduction rates, while climate and land-cover changes may decrease the barriers to invasive populations spread. A detailed knowledge of the invasion history, including assessing source populations, routes of spread, number of independent introductions, and the effects of genetic bottlenecks and admixture on the establishment success, adaptive potential, and further spread, is crucial from an applied perspective to mitigate socioeconomic impacts of invasive species, as well as for addressing fundamental questions on the evolutionary dynamics of the invasion process. Recent advances in genomics together with the development of geographic information systems provide unprecedented large genetic and environmental datasets at global and local scales to link population genomics, landscape ecology, and species distribution modeling into a common framework to study the invasion process. Although the factors underlying population invasiveness have been extensively reviewed, analytical methods currently available to optimally combine molecular and environmental data for inferring invasive population demographic parameters and predicting further spreading are still under development. In this review, we focus on the few recent insect invasion studies that combine different datasets and approaches to show how integrating genetic, observational, ecological, and environmental data pave the way to a more integrative biological invasion science. We provide guidelines to study the evolutionary dynamics of invasions at each step of the invasion process, and conclude on the benefits of including all types of information and up-to-date analytical tools from different research areas into a single framework.

Keywords: biological invasion; demo‐genomics; dispersal; genetic diversity; insect; integrative approach; local adaptation; occurrence time series; species distribution modeling.

FIGURE 1

Types of information needed to identify the potential source populations: genetic, historical, and ecological. Blue: genetic variability, orange: dated introductions, green: observational and environmental data. For the illustration, the native range of the species is North America. There are five invaded ranges: Africa, Asia, South America, Australia, and Europe, and the studied invaded area is Europe. ABC scenario topologies are designed based on genetic hypotheses only: genetic similarities among populations (blue) from a representative sampling of the whole distribution range or a reduced sampling based on the likelihood of introduction (orange, no sampling in South America due to low proportion of interceptions) and/or establishment (green, sampling restricted to North America and Asia because predicted invaded ranges from these populations include Europe)

FIGURE 2

Types of information needed to reconstruct and test the role of introduction modalities in the invasion success using studies in H. axyridis. Blue: genetic variability, orange: historical data, gray: phenotypic data, and light red: simulated data. Photo from https://commons.wikimedia.org/wiki/File:Harmonia_axyridis_(Pallas_1773).png (CC BY‐SA 4.0). Figures adapted from cited literature. References [1] Lombaert et al. (2010); [2] Blekhman et al. (2020); [3] Lombaert, Guillemaud, et al. (2014)); [4] Facon, Hufbauer, et al. (2011)); [5] Facon, Crespin, et al. (2011)); [6] Turgeon et al. (2011); [7] Tayeh et al. (2013); [8] Laugier, (2013).

FIGURE 3

Types of information needed to test the preadaptation and post‐introduction adaptation hypotheses using studies in A. albopictus. Blue: genetic variability, green: environmental and occurrence data, orange: historical data, gray: phenotypic data. Photo of A. albopictus from https://commons.wikimedia.org/wiki/ File:CDC‐Gathany‐Aedes‐albopictus‐1.jpg (CC0, James Gathany). Figures adapted from cited literature

FIGURE 4

Types of information needed to assess the spread dynamics of invasive species and to reconstruct the expansion history. Blue: genetic variability, orange: dated introductions, green: observational and environmental data, violet: biological data, gray: phenotypic data. For the illustration, the studied invasion process is the northward expansion (CORE vs. FRONT 1). SI: stage of invasion; ESI: early stage of invasion