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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Main Authors: Kenta Watanabe, Akira Shimizu, Takashi Sugawara
Format: Article
Language:English
Published: PeerJ Inc. 2021-11-01
Series:PeerJ
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Online Access:https://peerj.com/articles/12318.pdf
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author Kenta Watanabe
Akira Shimizu
Takashi Sugawara
author_facet Kenta Watanabe
Akira Shimizu
Takashi Sugawara
author_sort Kenta Watanabe
collection DOAJ
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 doaj.art-7879faf9963d4cbd97882269f2d7338b2023-12-02T22:01:42ZengPeerJ Inc.PeerJ2167-83592021-11-019e1231810.7717/peerj.12318Polygamous breeding system identified in the distylous genus Psychotria: P. manillensis in the Ryukyu archipelago, JapanKenta Watanabe0Akira Shimizu1Takashi Sugawara2National Institute of Technology, Okinawa College, Henoko, Nago, Okinawa, JapanDepartment of Biological Sciences, School of Science, Tokyo Metropolitan University, Minami-Ohsawa, Hachioji, Tokyo, JapanDepartment of Botany, National Museum of Nature and Science, Amakubo, Tsukuba, Ibaraki, JapanDistyly 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.https://peerj.com/articles/12318.pdfBreeding systemDistylyMonoecismPolygamousPsychotria manillensisRubiaceae
spellingShingle Kenta Watanabe
Akira Shimizu
Takashi Sugawara
Polygamous breeding system identified in the distylous genus Psychotria: P. manillensis in the Ryukyu archipelago, Japan
PeerJ
Breeding system
Distyly
Monoecism
Polygamous
Psychotria manillensis
Rubiaceae
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 Breeding system
Distyly
Monoecism
Polygamous
Psychotria manillensis
Rubiaceae
url https://peerj.com/articles/12318.pdf
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AT akirashimizu polygamousbreedingsystemidentifiedinthedistylousgenuspsychotriapmanillensisintheryukyuarchipelagojapan
AT takashisugawara polygamousbreedingsystemidentifiedinthedistylousgenuspsychotriapmanillensisintheryukyuarchipelagojapan