Reproductive modes in populations of late-acting self-incompatible and self-compatible polyploid Ludwigia grandiflora subsp. hexapetala in western Europe

Reproductive mode, i.e., the proportion of individuals produced by clonality, selfing and outcrossing in populations, determines how hereditary material is transmitted through generations. It shapes genetic diversity and its structure over time and space, which can be used to infer reproductive mode...

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Main Authors: Stoeckel, Solenn, Becheler, Ronan, Portillo-Lemus, Luis, Harang, Marilyne, Besnard, Anne-Laure, Lassalle, Gilles, Causse-Védrines, Romain, Michon-Coudouel, Sophie, Park, Daniel J., Pope, Bernard J., Petit, Eric J., Barloy, Dominique
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Language:English
Published: Peer Community In 2024-09-01
Series:Peer Community Journal
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Online Access:https://peercommunityjournal.org/articles/10.24072/pcjournal.458/
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author Stoeckel, Solenn
Becheler, Ronan
Portillo-Lemus, Luis
Harang, Marilyne
Besnard, Anne-Laure
Lassalle, Gilles
Causse-Védrines, Romain
Michon-Coudouel, Sophie
Park, Daniel J.
Pope, Bernard J.
Petit, Eric J.
Barloy, Dominique
author_facet Stoeckel, Solenn
Becheler, Ronan
Portillo-Lemus, Luis
Harang, Marilyne
Besnard, Anne-Laure
Lassalle, Gilles
Causse-Védrines, Romain
Michon-Coudouel, Sophie
Park, Daniel J.
Pope, Bernard J.
Petit, Eric J.
Barloy, Dominique
author_sort Stoeckel, Solenn
collection DOAJ
description Reproductive mode, i.e., the proportion of individuals produced by clonality, selfing and outcrossing in populations, determines how hereditary material is transmitted through generations. It shapes genetic diversity and its structure over time and space, which can be used to infer reproductive modes. Ludwigia grandiflora subsp. hexapetala (Lgh) is a partially clonal, polyploid, hermaphroditic, and heteromorphic plant that recently colonized multiple countries worldwide. In western Europe, individuals are either self-incompatible caused by a late-acting self-incompatibility (LSI) system developing long-styled flowers, or self-compatible (SC), with short-styled flowers. In this study, we genotyped 53 long- and short-styled populations newly colonizing France and northern Spain using SNPs to estimate rates of clonality, selfing and outcrossing. We found that populations reproduced mainly clonally but with a high diversity of genotypes along with rates of sexuality ranging from 10% up to 40%. We also found evidence for local admixture between long- and short-styled populations in a background of genetic structure between floral morphs that was twice the level found within morphs. Long- and short-styled populations showed similar rates of clonality, but short-styled populations presented significantly higher rates of selfing, as expected considering their breeding system and despite the small rates of failure of the LSI system. Within the 53 studied populations, the 13 short-styled populations had fewer effective alleles, lower observed heterozygosity, and higher inbreeding coefficients, linkage disequilibrium and estimates of selfing than what was found in long-styled populations. These results emphasize the necessity to consider the variation of reproductive modes when managing invasive plant species. The overall maintenance of higher genetic diversity with the possibility of maintaining populations clonally in the absence of compatible partners may explain why long-styled individuals seem to be more prevalent in all newly expanding populations worldwide. Beyond Lgh, our methodological approach may inspire future studies to assess the reproductive modes in other autopolyploid populations.
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spelling doaj-art-4b2fa09f49de4aea9cca6e1d84f532a22025-02-07T10:17:17ZengPeer Community InPeer Community Journal2804-38712024-09-01410.24072/pcjournal.45810.24072/pcjournal.458Reproductive modes in populations of late-acting self-incompatible and self-compatible polyploid Ludwigia grandiflora subsp. hexapetala in western Europe Stoeckel, Solenn0https://orcid.org/0000-0001-6064-5941Becheler, Ronan1https://orcid.org/0000-0001-9322-0771Portillo-Lemus, Luis2https://orcid.org/0000-0003-2123-4714Harang, Marilyne3Besnard, Anne-Laure4https://orcid.org/0000-0002-5221-3855Lassalle, Gilles5https://orcid.org/0000-0002-3264-1449Causse-Védrines, Romain6Michon-Coudouel, Sophie7Park, Daniel J.8Pope, Bernard J.9https://orcid.org/0000-0002-4840-1095Petit, Eric J.10https://orcid.org/0000-0001-5058-5826Barloy, Dominique11https://orcid.org/0000-0001-5810-4871DECOD (Ecosystem Dynamics and Sustainability), Institut Agro, IFREMER, INRAE, Rennes, France; IGEPP, INRAE, Institut Agro, Université de Rennes, Le Rheu, FranceDECOD (Ecosystem Dynamics and Sustainability), Institut Agro, IFREMER, INRAE, Rennes, France; IGEPP, INRAE, Institut Agro, Université de Rennes, Le Rheu, FranceDECOD (Ecosystem Dynamics and Sustainability), Institut Agro, IFREMER, INRAE, Rennes, FranceDECOD (Ecosystem Dynamics and Sustainability), Institut Agro, IFREMER, INRAE, Rennes, FranceDECOD (Ecosystem Dynamics and Sustainability), Institut Agro, IFREMER, INRAE, Rennes, FranceDECOD (Ecosystem Dynamics and Sustainability), Institut Agro, IFREMER, INRAE, Rennes, FrancePlateforme EcogenO, UAR3343 OSUR, Université de Rennes, CNRS, Rennes, FrancePlateforme EcogenO, UAR3343 OSUR, Université de Rennes, CNRS, Rennes, FranceMelbourne Bioinformatics, The University of Melbourne, Parkville, AustraliaMelbourne Bioinformatics, The University of Melbourne, Parkville, AustraliaDECOD (Ecosystem Dynamics and Sustainability), Institut Agro, IFREMER, INRAE, Rennes, FranceDECOD (Ecosystem Dynamics and Sustainability), Institut Agro, IFREMER, INRAE, Rennes, FranceReproductive mode, i.e., the proportion of individuals produced by clonality, selfing and outcrossing in populations, determines how hereditary material is transmitted through generations. It shapes genetic diversity and its structure over time and space, which can be used to infer reproductive modes. Ludwigia grandiflora subsp. hexapetala (Lgh) is a partially clonal, polyploid, hermaphroditic, and heteromorphic plant that recently colonized multiple countries worldwide. In western Europe, individuals are either self-incompatible caused by a late-acting self-incompatibility (LSI) system developing long-styled flowers, or self-compatible (SC), with short-styled flowers. In this study, we genotyped 53 long- and short-styled populations newly colonizing France and northern Spain using SNPs to estimate rates of clonality, selfing and outcrossing. We found that populations reproduced mainly clonally but with a high diversity of genotypes along with rates of sexuality ranging from 10% up to 40%. We also found evidence for local admixture between long- and short-styled populations in a background of genetic structure between floral morphs that was twice the level found within morphs. Long- and short-styled populations showed similar rates of clonality, but short-styled populations presented significantly higher rates of selfing, as expected considering their breeding system and despite the small rates of failure of the LSI system. Within the 53 studied populations, the 13 short-styled populations had fewer effective alleles, lower observed heterozygosity, and higher inbreeding coefficients, linkage disequilibrium and estimates of selfing than what was found in long-styled populations. These results emphasize the necessity to consider the variation of reproductive modes when managing invasive plant species. The overall maintenance of higher genetic diversity with the possibility of maintaining populations clonally in the absence of compatible partners may explain why long-styled individuals seem to be more prevalent in all newly expanding populations worldwide. Beyond Lgh, our methodological approach may inspire future studies to assess the reproductive modes in other autopolyploid populations.https://peercommunityjournal.org/articles/10.24072/pcjournal.458/Partial clonality, Mating system, Late-acting self-incompatibility system, Selfing, Outcrossing, Autopolyploidy, Water primrose
spellingShingle Stoeckel, Solenn
Becheler, Ronan
Portillo-Lemus, Luis
Harang, Marilyne
Besnard, Anne-Laure
Lassalle, Gilles
Causse-Védrines, Romain
Michon-Coudouel, Sophie
Park, Daniel J.
Pope, Bernard J.
Petit, Eric J.
Barloy, Dominique
Reproductive modes in populations of late-acting self-incompatible and self-compatible polyploid Ludwigia grandiflora subsp. hexapetala in western Europe
Peer Community Journal
Partial clonality, Mating system, Late-acting self-incompatibility system, Selfing, Outcrossing, Autopolyploidy, Water primrose
title Reproductive modes in populations of late-acting self-incompatible and self-compatible polyploid Ludwigia grandiflora subsp. hexapetala in western Europe
title_full Reproductive modes in populations of late-acting self-incompatible and self-compatible polyploid Ludwigia grandiflora subsp. hexapetala in western Europe
title_fullStr Reproductive modes in populations of late-acting self-incompatible and self-compatible polyploid Ludwigia grandiflora subsp. hexapetala in western Europe
title_full_unstemmed Reproductive modes in populations of late-acting self-incompatible and self-compatible polyploid Ludwigia grandiflora subsp. hexapetala in western Europe
title_short Reproductive modes in populations of late-acting self-incompatible and self-compatible polyploid Ludwigia grandiflora subsp. hexapetala in western Europe
title_sort reproductive modes in populations of late acting self incompatible and self compatible polyploid ludwigia grandiflora subsp hexapetala in western europe
topic Partial clonality, Mating system, Late-acting self-incompatibility system, Selfing, Outcrossing, Autopolyploidy, Water primrose
url https://peercommunityjournal.org/articles/10.24072/pcjournal.458/
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