Is heterostyly rare on oceanic islands?

Watanabe, Kenta; Sugawara, Takashi

doi:10.1093/aobpla/plv087

Cited by 23 publications

(14 citation statements)

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“…Since distyly is the ancestral breeding system in the genus Psychotria (Hamilton 1989; Watanabe and Sugawara 2015), it is interesting to know how this polygamous breeding system evolved in P. manillensis . It is possible that P. manillensis is derived from an autopolyploid P. asiatica or an allopolyploid P. asiatica and another species (polyploid hybrid).…”

Section: Discussionmentioning

confidence: 99%

“…Of these, monomorphism (homostyly or pin/thrum monomorphy), which is the most frequently reported evolutionary transition (Vuilleumier 1967;Naiki and Nagamasu 2004;Nakamura et al 2007;Naiki 2012), has been identified in Psychotria (Hamilton 1990;Sakai and Wright 2008;Consolaro et al 2011). The evolution of dioecy from distyly has also been reported for several species (Watanabe and Sugawara 2015), including the Hawaiian Psychotria (Beach and Bawa 1980;Muenchow and Grebus 1989;Sakai et al 1995;Wagner et al 1999) and Psychotria asiatica in Japan (Watanabe et al 2014b). However, there is no report of the evolution of monoecism in any distylous taxa.…”

Section: Introductionmentioning

confidence: 99%

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Polygamous breeding system identified in the distylous genusPsychotria:P. manillensisin the Ryukyu archipelago, Japan

Watanabe

Shimizu

Sugawara

2020

Preprint

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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 (44%), followed by female (38%), male (14%), and hermaphroditic (3%) individuals at the time of flower collection. Of the collected flowers, 94% were functionally unisexual (male or female), whereas only 6% were perfect (hermaphrodic). 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, composed of 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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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Polygamous breeding system identified in the distylous genusPsychotria:P. manillensisin the Ryukyu archipelago, Japan

Watanabe

Shimizu

Sugawara

2020

Preprint

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“…Distyly is usually rare or absent in species thriving on oceanic islands (Pailler et al ; Kondo et al ; Watanabe & Sugawara ; Watanabe et al ). This rarity is probably attributable to the fact that the simultaneous colonization of both morphs is difficult and pollinators are scarce on islands (Watanabe & Sugawara ). Nevertheless, some distylous species do exist on oceanic islands, but their reproduction dynamics have not been studied sufficiently.…”

Section: Introductionmentioning

confidence: 99%

Pollination and reproduction of Psychotria homalosperma, an endangered distylous tree endemic to the oceanic Bonin (Ogasawara) Islands, Japan

Watanabe

Kato

Kuraya

et al. 2017

Plant Species Biology

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Distyly is usually rare or not observed in species thriving on oceanic islands. The rarity of this breeding system is probably because of the difficulty of colonization for distylous plants and the paucity of pollinators on oceanic islands. However, the endemic and endangered tree Psychotria homalosperma has maintained its distylous nature in the oceanic Bonin Islands, Japan. To understand how the distylous breeding system of P. homalosperma has been maintained on these islands and to characterize the reproduction systems, we studied the pollination and reproductive biology of this species. Specifically, we observed current flower visitors and estimated their effects on plant reproduction. We also examined the floral traits and floral volatiles of P. homalosperma to infer its original pollinators, because plant-pollinator relationships in the Bonin Islands have recently been disrupted by anthropological activities. Finally, we examined the fruit set and pollen tube growth in the stigmas under hand and open pollination. Although original pollinators were presumed to be moths with long proboscises, the introduced honeybee, Apis mellifera, was the most common flower visitor. The honeybee carried pollen grains only unidirectionally, from the short-to long-styled morphs, because it could not reach the hidden stigmas of the short-styled flowers, and long-styled flowers set fruits 1.7-38 times more than short-styled ones. This case study indicates that the instability of pollinator fauna can cause distylous species to be rare on oceanic islands.

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“…The evolution of heterostyly on oceanic islands is compounded by the complexity of the genetic system involved in maintaining it and, as such, is thought to be a rarity on remote island systems. Watanabe and Sugawara (2015) investigated the frequency of heterostyly among oceanic island lineages and then explore the evolution of this trait within Psychotria (Rubiaceae), a genus of ∼2000 species, widespread throughout the tropics and exhibiting variation for the heterostylous habit. Their study sheds light on the rarity of heterostyly on islands.…”

Section: Introductionmentioning

confidence: 99%

Introduction to the Special Issue: Advances in island plant biology since Sherwin Carlquist's Island Biology

Traveset¹,

Fernández‐Palacios²,

Kueffer³

et al. 2015

AoB PLANTS

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This is the introductory paper of the special issue emerging from the First Island Biology Symposium hosted in Honolulu on July 2014. The 18 papers compiled present data from multiple archipelagos across the world and from different disciplines within plant sciences, showing us how much island biology has advanced since Carlquist's inspiring contribution Island Biology. Such advance has been possible mostly thanks to the increasing availability and richness of island data, new information from the geosciences, phylogenetics, and palaeoecology, and new methodological advances in analyzing data at large spatial scales. A group of papers deal with issues to which Carlquist contributed most: long-distance dispersal, adaptive radiation, and plant reproductive biology, whereas others cover a range of topics related to plant conservation on islands.

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Is heterostyly rare on oceanic islands?

Cited by 23 publications

References 123 publications

Polygamous breeding system identified in the distylous genusPsychotria:P. manillensisin the Ryukyu archipelago, Japan

Polygamous breeding system identified in the distylous genusPsychotria:P. manillensisin the Ryukyu archipelago, Japan

Pollination and reproduction of Psychotria homalosperma, an endangered distylous tree endemic to the oceanic Bonin (Ogasawara) Islands, Japan

Introduction to the Special Issue: Advances in island plant biology since Sherwin Carlquist's Island Biology

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