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Evolution of selfing syndrome and its influence on genetic diversity and inbreeding: A range‐wide study in Oenothera primiveris

PREMISE: To avoid inbreeding depression, plants have evolved diverse breeding systems to favor outcrossing, such as self‐incompatibility. However, changes in biotic and abiotic conditions can result in selective pressures that lead to a breakdown in self‐incompatibility. The shift to increased selfi...

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Autores principales: Cisternas‐Fuentes, Anita, Jogesh, Tania, Broadhead, Geoffrey T., Raguso, Robert A., Skogen, Krissa A., Fant, Jeremie B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9320852/
https://www.ncbi.nlm.nih.gov/pubmed/35596689
http://dx.doi.org/10.1002/ajb2.1861
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author Cisternas‐Fuentes, Anita
Jogesh, Tania
Broadhead, Geoffrey T.
Raguso, Robert A.
Skogen, Krissa A.
Fant, Jeremie B.
author_facet Cisternas‐Fuentes, Anita
Jogesh, Tania
Broadhead, Geoffrey T.
Raguso, Robert A.
Skogen, Krissa A.
Fant, Jeremie B.
author_sort Cisternas‐Fuentes, Anita
collection PubMed
description PREMISE: To avoid inbreeding depression, plants have evolved diverse breeding systems to favor outcrossing, such as self‐incompatibility. However, changes in biotic and abiotic conditions can result in selective pressures that lead to a breakdown in self‐incompatibility. The shift to increased selfing is commonly associated with reduced floral features, lower attractiveness to pollinators, and increased inbreeding. We tested the hypothesis that the loss of self‐incompatibility, a shift to self‐fertilization (autogamy), and concomitant evolution of the selfing syndrome (reduction in floral traits associated with cross‐fertilization) will lead to increased inbreeding and population differentiation in Oenothera primiveris. Across its range, this species exhibits a shift in its breeding system and floral traits from a self‐incompatible population with large flowers to self‐compatible populations with smaller flowers. METHODS: We conducted a breeding system assessment, evaluated floral traits in the field and under controlled conditions, and measured population genetic parameters using RADseq data. RESULTS: Our results reveal a bimodal transition to the selfing syndrome from the west to the east of the range of O. primiveris. This shift includes variation in the breeding system and the mating system, a reduction in floral traits (flower diameter, herkogamy, and scent production), a shift to greater autogamy, reduced genetic diversity, and increased inbreeding. CONCLUSIONS: The observed variation highlights the importance of range‐wide studies to understand breeding system variation and the evolution of the selfing syndrome within populations and species.
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spelling pubmed-93208522022-07-30 Evolution of selfing syndrome and its influence on genetic diversity and inbreeding: A range‐wide study in Oenothera primiveris Cisternas‐Fuentes, Anita Jogesh, Tania Broadhead, Geoffrey T. Raguso, Robert A. Skogen, Krissa A. Fant, Jeremie B. Am J Bot Research Articles PREMISE: To avoid inbreeding depression, plants have evolved diverse breeding systems to favor outcrossing, such as self‐incompatibility. However, changes in biotic and abiotic conditions can result in selective pressures that lead to a breakdown in self‐incompatibility. The shift to increased selfing is commonly associated with reduced floral features, lower attractiveness to pollinators, and increased inbreeding. We tested the hypothesis that the loss of self‐incompatibility, a shift to self‐fertilization (autogamy), and concomitant evolution of the selfing syndrome (reduction in floral traits associated with cross‐fertilization) will lead to increased inbreeding and population differentiation in Oenothera primiveris. Across its range, this species exhibits a shift in its breeding system and floral traits from a self‐incompatible population with large flowers to self‐compatible populations with smaller flowers. METHODS: We conducted a breeding system assessment, evaluated floral traits in the field and under controlled conditions, and measured population genetic parameters using RADseq data. RESULTS: Our results reveal a bimodal transition to the selfing syndrome from the west to the east of the range of O. primiveris. This shift includes variation in the breeding system and the mating system, a reduction in floral traits (flower diameter, herkogamy, and scent production), a shift to greater autogamy, reduced genetic diversity, and increased inbreeding. CONCLUSIONS: The observed variation highlights the importance of range‐wide studies to understand breeding system variation and the evolution of the selfing syndrome within populations and species. John Wiley and Sons Inc. 2022-05-21 2022-05 /pmc/articles/PMC9320852/ /pubmed/35596689 http://dx.doi.org/10.1002/ajb2.1861 Text en © 2022 The Authors. American Journal of Botany published by Wiley Periodicals LLC on behalf of Botanical Society of America. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Cisternas‐Fuentes, Anita
Jogesh, Tania
Broadhead, Geoffrey T.
Raguso, Robert A.
Skogen, Krissa A.
Fant, Jeremie B.
Evolution of selfing syndrome and its influence on genetic diversity and inbreeding: A range‐wide study in Oenothera primiveris
title Evolution of selfing syndrome and its influence on genetic diversity and inbreeding: A range‐wide study in Oenothera primiveris
title_full Evolution of selfing syndrome and its influence on genetic diversity and inbreeding: A range‐wide study in Oenothera primiveris
title_fullStr Evolution of selfing syndrome and its influence on genetic diversity and inbreeding: A range‐wide study in Oenothera primiveris
title_full_unstemmed Evolution of selfing syndrome and its influence on genetic diversity and inbreeding: A range‐wide study in Oenothera primiveris
title_short Evolution of selfing syndrome and its influence on genetic diversity and inbreeding: A range‐wide study in Oenothera primiveris
title_sort evolution of selfing syndrome and its influence on genetic diversity and inbreeding: a range‐wide study in oenothera primiveris
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9320852/
https://www.ncbi.nlm.nih.gov/pubmed/35596689
http://dx.doi.org/10.1002/ajb2.1861
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