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

Irimia, Ramona E., Hierro, José L., Branco, Soraia, Sotes, Gastón, Cavieres, Lohengrin A., Eren, Özkan, Lortie, Christopher J., French, Kristine, Callaway, Ragan M., and Montesinos, Daniel (2021) Experimental admixture among geographically disjunct populations of an invasive plant yields a global mosaic of reproductive incompatibility and heterosis. Journal of Ecology, 109 (5). pp. 2152-2162.

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Abstract

1. 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.

2. 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.

3. 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.

4. 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.

Item ID: 66845
Item Type: Article (Research - C1)
ISSN: 1365-2745
Keywords: Allopatry; Biological invasions; Fecundity; Gene flow; Local adaption; Reproductive isolation; Yellow starthistle
Copyright Information: This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. © 2021 The Authors. Journal of Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society
Funders: Fundação para a Ciência e a Tecnologia (FCT), National Science Foundation (NSF), CONICYT
Projects and Grants: FCT IF00066-2013, FCT PTDC/BIA-PLA/0763/2014, FCT SFRH/BD/110987/2015, FCT UID/BIA/04004/2013, NSF OIA-1757351, CONICYT FONDECYT 1171005
Date Deposited: 07 Mar 2021 23:12
FoR Codes: 31 BIOLOGICAL SCIENCES > 3104 Evolutionary biology > 310403 Biological adaptation @ 40%
31 BIOLOGICAL SCIENCES > 3104 Evolutionary biology > 310405 Evolutionary ecology @ 30%
41 ENVIRONMENTAL SCIENCES > 4102 Ecological applications > 410202 Biosecurity science and invasive species ecology @ 30%
SEO Codes: 18 ENVIRONMENTAL MANAGEMENT > 1806 Terrestrial systems and management > 180602 Control of pests, diseases and exotic species in terrestrial environments @ 100%
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