The Genetic Paradox of Invasions revisited: the potential role of inbreeding × environment interactions in invasion success

Abstract

Invasive species that successfully establish, persist, and expand within an area of introduction, in spite of demographic bottlenecks that reduce their genetic diversity, represent a paradox. Bottlenecks should inhibit population growth and invasive expansion, as a decrease in genetic diversity should result in inbreeding depression, increased fixation of deleterious mutations by genetic drift (drift load), and reduced evolutionary potential to respond to novel selection pressures. Here, we focus on the problems of inbreeding depression and drift load in introduced populations as key components of the Genetic Paradox of Invasions (GPI). We briefly review published explanations for the GPI, which are based on various mechanisms (invasion history events, reproductive traits, genetic characteristics) that mediate the avoidance of inbreeding depression and drift load. We find that there is still a substantial lack of explanation and empirical evidence for explaining the GPI for strongly bottlenecked invasions, or for during critical invasion phases (e.g. initial colonization, leading edges of range expansion) where strong genetic depletion, inbreeding depression and drift load occurs. Accordingly, we suggest that discussion of the GPI should be revived to find additional mechanisms applicable to explaining invasion success for such species and invasion phases. Based on a synthesis of the literature on the population genetics of invaders and the ecology of invaded habitats, we propose that inbreeding × environment (I × E) interactions are one such mechanism that may have strong explanatory power to address the GPI. Specifically, we suggest that a temporary or permanent release from stress in invaded habitats may alleviate the negative effects of genetic depletion on fitness via I × E interactions, and present published empirical evidence supporting this hypothesis. We additionally discuss that I × E interactions can result in rapid evolutionary changes, and may even contribute to adaptation of invaders in the absence of high genetic variation. With a view to encouraging further empirical research, we propose an experimental approach to investigate the occurrence of I × E interactions in ongoing invasions. Revived research on the GPI should provide new fundamental insights into eco-evolutionary invasion biology, and more generally into the evolutionary consequences of the interactions between inbreeding and environment.

Host‐targeted RAD‐Seq reveals genetic changes in the coral Oculina patagonica associated with range expansion along the Spanish Mediterranean coast

“…Population bottlenecks associated with colonization may lead to reduced genetic diversity, potentially limiting the ability of newly founded populations to adapt and persist (Frankham & Ralls, ; Lee, ). This genetic paradox in invasive species (i.e., how bottlenecked populations can still become successful) has intrigued researchers, who continue to explore possible mechanisms underlining this mystery (Frankham, ; Schrieber & Lachmuth, ).…”

Invasion success in polyploids: the role of inbreeding in the contrasting colonization abilities of diploid versus tetraploid populations of Centaurea stoebe s.l.

“…Murren & Dudash ; Mullarkey, Byers & Anderson ; Szűcs et al . ; Schrieber & Lachmuth ). During initial colonization and subsequent range expansion at the leading edges (Slatkin & Excoffier ; Hufbauer et al .…”

Non-native populations of an invasive tree outperform their native conspecifics

“…It has been found that non-native populations are often characterized by reduced genetic diversity compared with native populations due to bottlenecks during introduction (Sakai et al 2001, Hirsch et al 2011). Despite this, rapid evolution of non-native species may occur even when experiencing bottleneck events (Dlugosch and Parker 2008; Schrieber and Lachmuth 2016; Zenni et al 2016a, b, this issue). Some studies, however, provide evidence that reduced genetic diversity is not always the rule for non-native populations, and that genetic diversity can be maintained by different mechanisms dependent on introduction history (multiple vs. single introductions), native range genetic structure and propagule pressure (Petit et al 2004; Prentis et al 2008; Le Roux et al 2011; Mandák et al 2013).…”