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

Abstract

Invasive species have the ability to rapidly adapt in the new regions where they are introduced. Classic evolutionary theory predicts that the accumulation of genetic differences over time in allopatric isolation may lead to reproductive incompatibilities resulting in decreases in reproductive success and, eventually, to speciation. However, experimental evidence for this theoretical prediction in the context of invasive species is lacking. We aimed to test for the potential of allopatry to determine reproductive success of invasive plants, by experimentally admixing genotypes from six different native and non‐native regions of Centaurea solstitialis, an invasive forb for which preliminary studies have detected some degree of reproductive isolation between one native and non‐native region. We grew plants under common garden conditions and outcrossed individuals originating from different source populations in the native and introduced range to evaluate reproductive success in terms of seed to ovule ratio produced. We also assessed geographical and genetic isolation among C. solstitialis regions as a potential driving factor of reproductive success. Experimental admixture generated mixed fitness effects, including significant increases, decreases and no differences in reproductive success as compared to crosses within population (control). Centaurea solstitialis invasive populations in the Americas generated preponderantly negative fitness interactions, regardless of the pollen source, suggesting selection against immigrants and reinforcement. Other non‐native populations (Australia) as well as individuals from the native range of Spain demonstrated an increase in fitness for between‐region crosses, indicating inbreeding. These differences show an asymmetrical response to inter‐regional gene flow, but no evidence of isolation by distance. Synthesis. The speed of adaptation and the accumulation of reproductive incompatibilities among allopatric populations of invasive species might be more rapid than previously assumed. Our data show a global mosaic of reproductive outputs, showcasing an array of evolutionary processes unfolding during colonization at large biogeographical scales.

Fast invasives fastly become faster: Invasive plants align largely with the fast side of the plant economics spectrum

“…Invasive plants have shown a remarkable ability to rapidly adapt to different conditions across the native and non‐native ranges that they occupy (Callaway & Ridenour, 2004; Colautti & Lau, 2015; Hierro et al., 2009, 2020; Maron et al., 2004), frequently presenting distinct genotypes locally adapted to different climatic niches across biogeographic region (Atwater et al., 2018). Local adaptation can occur so frequently and so rapidly that incipient degrees of reproductive isolation have arisen between populations separated for less than 200 generations, which might be seen as the preliminary stages of allopatric speciation (Irimia et al, 2021; Montesinos et al., 2012). Even non‐invasive naturalized exotics have been found to develop the same kind of adaptive trait changes (increased growth, size, etc.)…”

Reduced representation sequencing to understand the evolutionary history of Torrey pine (Pinus torreyana parry) with implications for rare species conservation

“…Rare species often occur in small, fragmented populations across different habitats, and management of such species should consider patterns of neutral and adaptive genetic diversity, historical divergence, and inbreeding. While assessment of parent and advanced‐generation hybrid populations within a common environment is the “gold standard” to empirically test fitness consequences following population admixture (Hamilton et al, 2017; Irimia et al, 2021; Keller et al, 2000; Shi et al, 2018; VanWallendael et al, 2022), the analytical framework described here can provide critical insights into both the risks and benefits of establishing a genetic rescue management strategy.…”

Epigenetics and the success of invasive plants

“…In the context of understanding the importance of hybridization and/or genome duplications in invasions, future studies could follow the lead of previous experiments which have taken advantage of synthetic hybrids ( [20]; e.g. [100,[262][263][264][265]) and synthetic or recent polyploids ( [17,20]; e.g. [266,267]) to examine the effects of these processes on molecular, phenotypic and ecological levels.…”