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Breeding system of diploid sexuals within the Ranunculus auricomus complex and its role in a geographical parthenogenesis scenario

The larger distribution area of asexuals compared with their sexual relatives in geographical parthenogenesis (GP) scenarios has been widely attributed to the advantages of uniparental reproduction and polyploidy. However, potential disadvantages of sexuals due to their breeding system have received...

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Autores principales: Karbstein, Kevin, Rahmsdorf, Elisabeth, Tomasello, Salvatore, Hodač, Ladislav, Hörandl, Elvira
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7771175/
https://www.ncbi.nlm.nih.gov/pubmed/33391726
http://dx.doi.org/10.1002/ece3.7073
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author Karbstein, Kevin
Rahmsdorf, Elisabeth
Tomasello, Salvatore
Hodač, Ladislav
Hörandl, Elvira
author_facet Karbstein, Kevin
Rahmsdorf, Elisabeth
Tomasello, Salvatore
Hodač, Ladislav
Hörandl, Elvira
author_sort Karbstein, Kevin
collection PubMed
description The larger distribution area of asexuals compared with their sexual relatives in geographical parthenogenesis (GP) scenarios has been widely attributed to the advantages of uniparental reproduction and polyploidy. However, potential disadvantages of sexuals due to their breeding system have received little attention so far. Here, we study the breeding system of five narrowly distributed sexual lineages of Ranunculus notabilis s.l. (R. auricomus complex) and its effects on outcrossing, inbreeding, female fitness, and heterozygosity. We performed selfing and intra‐ and interlineage crossings by bagging 481 flowers (59 garden individuals) followed by germination experiments. We compared seed set and germination rates, and related them to genetic distance and genome‐wide heterozygosity (thousands of RADseq loci). Selfings (2.5%) unveiled a significantly lower seed set compared with intra‐ (69.0%) and interlineage crossings (69.5%). Seed set of intra‐ (65%) compared to interpopulation crossings (78%) was significantly lower. In contrast, all treatments showed comparable germination rates (32%–43%). Generalized linear regressions between seed set and genetic distance revealed positive relationships in general and between lineages, and a negative one within lineages. Seed set was the main decisive factor for female fitness. Germination rates were not related to genetic distance at any level, but were positively associated with heterozygosity in interlineage crossings. Experiments confirmed full crossability and predominant outcrossing among sexual R. notabilis s.l. lineages. However, up to 5% (outliers 15%–31%) of seeds were formed by selfing, probably due to semi‐self‐compatibility in a multi‐locus gametophytic SI system. Less seed set in intrapopulation crossings, and higher seed set and germination rates from crossings of genetically more distant and heterozygous lineages (interlineage) indicate negative inbreeding and positive outbreeding effects. In GP scenarios, sexual species with small and/or isolated populations can suffer from decreased female fitness due to their breeding system. This factor, among others, probably limits range expansion of sexuals.
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spelling pubmed-77711752020-12-31 Breeding system of diploid sexuals within the Ranunculus auricomus complex and its role in a geographical parthenogenesis scenario Karbstein, Kevin Rahmsdorf, Elisabeth Tomasello, Salvatore Hodač, Ladislav Hörandl, Elvira Ecol Evol Original Research The larger distribution area of asexuals compared with their sexual relatives in geographical parthenogenesis (GP) scenarios has been widely attributed to the advantages of uniparental reproduction and polyploidy. However, potential disadvantages of sexuals due to their breeding system have received little attention so far. Here, we study the breeding system of five narrowly distributed sexual lineages of Ranunculus notabilis s.l. (R. auricomus complex) and its effects on outcrossing, inbreeding, female fitness, and heterozygosity. We performed selfing and intra‐ and interlineage crossings by bagging 481 flowers (59 garden individuals) followed by germination experiments. We compared seed set and germination rates, and related them to genetic distance and genome‐wide heterozygosity (thousands of RADseq loci). Selfings (2.5%) unveiled a significantly lower seed set compared with intra‐ (69.0%) and interlineage crossings (69.5%). Seed set of intra‐ (65%) compared to interpopulation crossings (78%) was significantly lower. In contrast, all treatments showed comparable germination rates (32%–43%). Generalized linear regressions between seed set and genetic distance revealed positive relationships in general and between lineages, and a negative one within lineages. Seed set was the main decisive factor for female fitness. Germination rates were not related to genetic distance at any level, but were positively associated with heterozygosity in interlineage crossings. Experiments confirmed full crossability and predominant outcrossing among sexual R. notabilis s.l. lineages. However, up to 5% (outliers 15%–31%) of seeds were formed by selfing, probably due to semi‐self‐compatibility in a multi‐locus gametophytic SI system. Less seed set in intrapopulation crossings, and higher seed set and germination rates from crossings of genetically more distant and heterozygous lineages (interlineage) indicate negative inbreeding and positive outbreeding effects. In GP scenarios, sexual species with small and/or isolated populations can suffer from decreased female fitness due to their breeding system. This factor, among others, probably limits range expansion of sexuals. John Wiley and Sons Inc. 2020-12-03 /pmc/articles/PMC7771175/ /pubmed/33391726 http://dx.doi.org/10.1002/ece3.7073 Text en © 2020 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Research
Karbstein, Kevin
Rahmsdorf, Elisabeth
Tomasello, Salvatore
Hodač, Ladislav
Hörandl, Elvira
Breeding system of diploid sexuals within the Ranunculus auricomus complex and its role in a geographical parthenogenesis scenario
title Breeding system of diploid sexuals within the Ranunculus auricomus complex and its role in a geographical parthenogenesis scenario
title_full Breeding system of diploid sexuals within the Ranunculus auricomus complex and its role in a geographical parthenogenesis scenario
title_fullStr Breeding system of diploid sexuals within the Ranunculus auricomus complex and its role in a geographical parthenogenesis scenario
title_full_unstemmed Breeding system of diploid sexuals within the Ranunculus auricomus complex and its role in a geographical parthenogenesis scenario
title_short Breeding system of diploid sexuals within the Ranunculus auricomus complex and its role in a geographical parthenogenesis scenario
title_sort breeding system of diploid sexuals within the ranunculus auricomus complex and its role in a geographical parthenogenesis scenario
topic Original Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7771175/
https://www.ncbi.nlm.nih.gov/pubmed/33391726
http://dx.doi.org/10.1002/ece3.7073
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