Potential limits to the benefits of admixture during biological invasion

Abstract

Species introductions often bring together genetically divergent source populations, resulting in genetic admixture. This geographic reshuffling of diversity has the potential to generate favorable new genetic combinations, facilitating the establishment and invasive spread of introduced populations. Observational support for the superior performance of admixed introductions has been mixed, however, and the broad importance of admixture to invasion questioned. Under most underlying mechanisms, admixture’s benefits should be expected to increase with greater divergence among and lower genetic diversity within source populations, though these effects have not been quantified in invaders. We experimentally crossed source populations differing in divergence in the invasive plant Centaurea solstitialis. Crosses resulted in many positive (heterotic) interactions, but fitness benefits declined and were ultimately negative at high source divergence, with patterns suggesting cyto-nuclear epistasis. We explored the literature to assess whether such negative epistatic interactions might be impeding admixture at high source population divergence. Admixed introductions reported for plants came from sources with a wide range of genetic variation, but were disproportionately absent where there was high genetic divergence among native populations. We conclude that while admixture is common in species introductions and often happens under conditions expected to be beneficial to invaders, these conditions may be constrained by predictable negative genetic interactions, potentially explaining conflicting evidence for admixture’s benefits to invasion.

Experimental admixture among geographically disjunct populations of an invasive plant yields a global mosaic of reproductive incompatibility and heterosis

“…Interestingly, an F 1 generation of progenies of C . solstitialis derived from crosses among geographically distant populations in the native range, most commonly exhibited increased growth rates, consistent with heterosis (Barker et al., 2019). Admixture experiments are thus a powerful tool to enhance our understanding of invasive species dynamics, such as underlying mechanisms of reproductive isolation and the rate at which they occur.…”

“…Documenting the rates at which reproductive isolation develops in allopatry as well as its effects on different fitness components can be done by means of experimental crosses between previously isolated lineages (Sapir & Mazzucco, 2015; Verrell & Arnold, 1989; Waser & Price, 1989). Relatively, few studies have evaluated the potential consequences of admixture across invasive species ranges (Barker et al., 2019; Dlugosch, Anderson, et al., 2015; Montesinos et al., 2012; Shi et al., 2018; van Kleunen et al., 2015; Wolfe et al., 2007). For example, van Kleunen et al., (2015) observed an increase in biomass and seed production in F 1 hybrids of Mimulus guttatus , when outcrossing plants from native and invasive populations, with fitness benefits partially maintained in the F 2 generation (Li et al., 2017).…”

“…Moreover, there is evidence for incipient reproductive incompatibilities between populations in some neo‐allopatric and native regions (Montesinos et al., 2012). In spite of such phenotypic differences, native and non‐native populations do not display notable differentiation in genetic makeup (Barker et al., 2017; Eriksen et al., 2014), and successful crosses between some geographically distant populations have been generated (Barker et al., 2019; Montesinos et al., 2012). In this study, we addressed the following predictions: (a) experimental admixture within the native range will lead to increased fecundity indicating inbreeding depression; (b) admixture will result in decreased fecundity in the introduced range, because populations in those regions are already the product of several past admixture events and (c) reproductive output will decrease with increasing the crossing distance, as a result of isolation by distance.…”

Population genomic and historical analysis suggests a global invasion by bridgehead processes in Mimulus guttatus

“…Bridgehead populations may have already been selected for their ability to colonise beyond their native range, making them particularly good candidates for additional range expansions. Multiple introductions and admixture can, in principle, both increase or decrease the performance and adaptive potential of invasive populations [48][49][50] . Multiple introductions from genetically distinct sources introduce variation and alleviate the negative effects of demographic bottlenecks associated with colonisation.…”

“…Multiple introductions and admixture can, in principle, both increase or decrease the performance and adaptive potential of invasive populations 48 – 50 . Multiple introductions from genetically distinct sources introduce variation and alleviate the negative effects of demographic bottlenecks associated with colonisation.…”