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High lifetime inbreeding depression counteracts the reproductive assurance benefit of selfing in a mass-flowering shrub

BACKGROUND: Decreases in mate and/or pollinator availability would be expected to affect the selective pressure on plant mating systems. An increase in self-fertilization may evolve to compensate for the negative effects of pollination failure. However, the benefit of selfing in variable pollination...

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Autores principales: Delmas, Chloé EL, Cheptou, Pierre-Olivier, Escaravage, Nathalie, Pornon, André
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4258271/
https://www.ncbi.nlm.nih.gov/pubmed/25433917
http://dx.doi.org/10.1186/s12862-014-0243-7
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author Delmas, Chloé EL
Cheptou, Pierre-Olivier
Escaravage, Nathalie
Pornon, André
author_facet Delmas, Chloé EL
Cheptou, Pierre-Olivier
Escaravage, Nathalie
Pornon, André
author_sort Delmas, Chloé EL
collection PubMed
description BACKGROUND: Decreases in mate and/or pollinator availability would be expected to affect the selective pressure on plant mating systems. An increase in self-fertilization may evolve to compensate for the negative effects of pollination failure. However, the benefit of selfing in variable pollination environments depends on the relative fitnesses of selfed and outcrossed progeny. We investigated the potential for selfing to provide reproductive assurance over the lifetime of a long-lived perennial species and its variation between plant patches of various sizes. Patch size is likely to affect mate and pollinator availabilities, thereby affecting pollination success and the rate of selfing. We estimated fruit and seed set, reproductive assurance, self-compatibility, the multilocus patch selfing rate and lifetime inbreeding depression in natural patches of Rhododendron ferrugineum (Ericaceae), a mass-flowering species characterized by considerable patch size variation (as estimated by the total number of inflorescences). RESULTS: Open seed set declined linearly with increasing patch size, whereas pollinator-mediated seed set (emasculated flowers) was not significantly affected. Progeny array analysis indicated that the selfing rate declined with increasing patch size, consistent with greater reproductive assurance in small sparse patches than in large, dense patches. However, fruit set and adult fitness decreased with decreasing patch size, with an estimated mean lifetime inbreeding depression of 0.9 (obtained by comparing F values in adults and progenies). CONCLUSIONS: Lifetime inbreeding depression strongly counteracts the advantage of reproductive assurance due to selfing in this long-lived species. The poor fitness of selfed offspring should counteract any evolution towards selfing, despite its potential to alleviate the negative consequences of pollen limitation. This study highlights the need to estimate lifetime inbreeding depression, together with mating system and pollination parameters, if we are to understand the actual benefit of selfing and avoid the overestimation of reproductive assurance. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-014-0243-7) contains supplementary material, which is available to authorized users.
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spelling pubmed-42582712014-12-08 High lifetime inbreeding depression counteracts the reproductive assurance benefit of selfing in a mass-flowering shrub Delmas, Chloé EL Cheptou, Pierre-Olivier Escaravage, Nathalie Pornon, André BMC Evol Biol Research Article BACKGROUND: Decreases in mate and/or pollinator availability would be expected to affect the selective pressure on plant mating systems. An increase in self-fertilization may evolve to compensate for the negative effects of pollination failure. However, the benefit of selfing in variable pollination environments depends on the relative fitnesses of selfed and outcrossed progeny. We investigated the potential for selfing to provide reproductive assurance over the lifetime of a long-lived perennial species and its variation between plant patches of various sizes. Patch size is likely to affect mate and pollinator availabilities, thereby affecting pollination success and the rate of selfing. We estimated fruit and seed set, reproductive assurance, self-compatibility, the multilocus patch selfing rate and lifetime inbreeding depression in natural patches of Rhododendron ferrugineum (Ericaceae), a mass-flowering species characterized by considerable patch size variation (as estimated by the total number of inflorescences). RESULTS: Open seed set declined linearly with increasing patch size, whereas pollinator-mediated seed set (emasculated flowers) was not significantly affected. Progeny array analysis indicated that the selfing rate declined with increasing patch size, consistent with greater reproductive assurance in small sparse patches than in large, dense patches. However, fruit set and adult fitness decreased with decreasing patch size, with an estimated mean lifetime inbreeding depression of 0.9 (obtained by comparing F values in adults and progenies). CONCLUSIONS: Lifetime inbreeding depression strongly counteracts the advantage of reproductive assurance due to selfing in this long-lived species. The poor fitness of selfed offspring should counteract any evolution towards selfing, despite its potential to alleviate the negative consequences of pollen limitation. This study highlights the need to estimate lifetime inbreeding depression, together with mating system and pollination parameters, if we are to understand the actual benefit of selfing and avoid the overestimation of reproductive assurance. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-014-0243-7) contains supplementary material, which is available to authorized users. BioMed Central 2014-11-30 /pmc/articles/PMC4258271/ /pubmed/25433917 http://dx.doi.org/10.1186/s12862-014-0243-7 Text en © Delmas et al.; licensee BioMed Central Ltd. 2014 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Delmas, Chloé EL
Cheptou, Pierre-Olivier
Escaravage, Nathalie
Pornon, André
High lifetime inbreeding depression counteracts the reproductive assurance benefit of selfing in a mass-flowering shrub
title High lifetime inbreeding depression counteracts the reproductive assurance benefit of selfing in a mass-flowering shrub
title_full High lifetime inbreeding depression counteracts the reproductive assurance benefit of selfing in a mass-flowering shrub
title_fullStr High lifetime inbreeding depression counteracts the reproductive assurance benefit of selfing in a mass-flowering shrub
title_full_unstemmed High lifetime inbreeding depression counteracts the reproductive assurance benefit of selfing in a mass-flowering shrub
title_short High lifetime inbreeding depression counteracts the reproductive assurance benefit of selfing in a mass-flowering shrub
title_sort high lifetime inbreeding depression counteracts the reproductive assurance benefit of selfing in a mass-flowering shrub
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4258271/
https://www.ncbi.nlm.nih.gov/pubmed/25433917
http://dx.doi.org/10.1186/s12862-014-0243-7
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