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Polygamous breeding system identified in the distylous genus Psychotria: P. manillensis in the Ryukyu archipelago, Japan

Distyly is a genetic polymorphism composed of long-and short-styled flowers in a population. The evolutionary breakdown of distyly has been reported in many taxa, and mainly involves a shift toward monomorphism or dioecism. However, a shift toward monoecism has not been reported in distylous species...

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Autores principales: Watanabe, Kenta, Shimizu, Akira, Sugawara, Takashi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: PeerJ Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8590391/
https://www.ncbi.nlm.nih.gov/pubmed/34824905
http://dx.doi.org/10.7717/peerj.12318
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author Watanabe, Kenta
Shimizu, Akira
Sugawara, Takashi
author_facet Watanabe, Kenta
Shimizu, Akira
Sugawara, Takashi
author_sort Watanabe, Kenta
collection PubMed
description Distyly is a genetic polymorphism composed of long-and short-styled flowers in a population. The evolutionary breakdown of distyly has been reported in many taxa, and mainly involves a shift toward monomorphism or dioecism. However, a shift toward monoecism has not been reported in distylous species. Psychotria (Rubiaceae), one of the world largest genera, consists of distylous species and their derivatives. In our preliminary study, however, we identified some monoecious individuals in a population of Psychotria manillensis. To understand the breeding system and reproductive biology of P. manillensis, we investigated floral traits, open fruit set, and flower visitors, and performed hand pollination and bagging experiments in five populations of Okinawa and Iriomote islands, Ryukyu Islands, Japan. The populations of P. manillensis were composed mainly of monoecious individuals (54%), followed by female (30%), male (14%), and hermaphroditic (2%) individuals at the time of flower collection. Of the collected flowers, 93% were functionally unisexual (male or female), whereas only 6.5% were perfect (hermaphroditic). However, some individuals changed sex mainly towards increasing femaleness during the flowering period. Moreover, 35% of the studied plants changed their sexual expression over the years. P. manillensis showed self-compatibility and no agamospermy. The fruit set under open pollination varied among populations and years (1.8–21.9%), but it was significantly higher than that of auto-selfing (0.68–1.56%). Wasps and flies were the main flower visitors and probably the main pollinators of the species. In conclusion, P. manillensis was revealed to be polygamous, involving monoecious, female, male, and hermaphroditic individuals. This is the first report of the polygamous breeding system not only in the genus Psychotria, but also in all heterostylous taxa.
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spelling pubmed-85903912021-11-24 Polygamous breeding system identified in the distylous genus Psychotria: P. manillensis in the Ryukyu archipelago, Japan Watanabe, Kenta Shimizu, Akira Sugawara, Takashi PeerJ Biodiversity Distyly is a genetic polymorphism composed of long-and short-styled flowers in a population. The evolutionary breakdown of distyly has been reported in many taxa, and mainly involves a shift toward monomorphism or dioecism. However, a shift toward monoecism has not been reported in distylous species. Psychotria (Rubiaceae), one of the world largest genera, consists of distylous species and their derivatives. In our preliminary study, however, we identified some monoecious individuals in a population of Psychotria manillensis. To understand the breeding system and reproductive biology of P. manillensis, we investigated floral traits, open fruit set, and flower visitors, and performed hand pollination and bagging experiments in five populations of Okinawa and Iriomote islands, Ryukyu Islands, Japan. The populations of P. manillensis were composed mainly of monoecious individuals (54%), followed by female (30%), male (14%), and hermaphroditic (2%) individuals at the time of flower collection. Of the collected flowers, 93% were functionally unisexual (male or female), whereas only 6.5% were perfect (hermaphroditic). However, some individuals changed sex mainly towards increasing femaleness during the flowering period. Moreover, 35% of the studied plants changed their sexual expression over the years. P. manillensis showed self-compatibility and no agamospermy. The fruit set under open pollination varied among populations and years (1.8–21.9%), but it was significantly higher than that of auto-selfing (0.68–1.56%). Wasps and flies were the main flower visitors and probably the main pollinators of the species. In conclusion, P. manillensis was revealed to be polygamous, involving monoecious, female, male, and hermaphroditic individuals. This is the first report of the polygamous breeding system not only in the genus Psychotria, but also in all heterostylous taxa. PeerJ Inc. 2021-11-10 /pmc/articles/PMC8590391/ /pubmed/34824905 http://dx.doi.org/10.7717/peerj.12318 Text en © 2021 Watanabe et al. https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.
spellingShingle Biodiversity
Watanabe, Kenta
Shimizu, Akira
Sugawara, Takashi
Polygamous breeding system identified in the distylous genus Psychotria: P. manillensis in the Ryukyu archipelago, Japan
title Polygamous breeding system identified in the distylous genus Psychotria: P. manillensis in the Ryukyu archipelago, Japan
title_full Polygamous breeding system identified in the distylous genus Psychotria: P. manillensis in the Ryukyu archipelago, Japan
title_fullStr Polygamous breeding system identified in the distylous genus Psychotria: P. manillensis in the Ryukyu archipelago, Japan
title_full_unstemmed Polygamous breeding system identified in the distylous genus Psychotria: P. manillensis in the Ryukyu archipelago, Japan
title_short Polygamous breeding system identified in the distylous genus Psychotria: P. manillensis in the Ryukyu archipelago, Japan
title_sort polygamous breeding system identified in the distylous genus psychotria: p. manillensis in the ryukyu archipelago, japan
topic Biodiversity
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8590391/
https://www.ncbi.nlm.nih.gov/pubmed/34824905
http://dx.doi.org/10.7717/peerj.12318
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