Adaptation to pollination by fungus gnats underlies the evolution of pollination syndrome in the genus Euonymus.

IF 3.6 2区 生物学 Q1 PLANT SCIENCES Annals of botany Pub Date : 2023-10-18 DOI:10.1093/aob/mcad081
Ko Mochizuki, Tomoko Okamoto, Kai-Hsiu Chen, Chun-Neng Wang, Matthew Evans, Andrea T Kramer, Atsushi Kawakita
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Abstract

Background and aims: Dipteran insects are known pollinators of many angiosperms, but knowledge on how flies affect floral evolution is relatively scarce. Some plants pollinated by fungus gnats share a unique set of floral characters (dark red display, flat shape and short stamens), which differs from any known pollination syndromes. We tested whether this set of floral characters is a pollination syndrome associated with pollination by fungus gnats, using the genus Euonymus as a model.

Methods: The pollinator and floral colour, morphology and scent profile were investigated for ten Euonymus species and Tripterygium regelii as an outgroup. The flower colour was evaluated using bee and fly colour vision models. The evolutionary association between fungus gnat pollination and each plant character was tested using a phylogenetically independent contrast. The ancestral state reconstruction was performed on flower colour, which is associated with fungus gnat pollination, to infer the evolution of pollination in the genus Euonymus.

Key results: The red-flowered Euonymus species were pollinated predominantly by fungus gnats, whereas the white-flowered species were pollinated by bees, beetles and brachyceran flies. The colour vision analysis suggested that red and white flowers are perceived as different colours by both bees and flies. The floral scents of the fungus gnat-pollinated species were characterized by acetoin, which made up >90 % of the total scent in three species. Phylogenetically independent contrast showed that the evolution of fungus gnat pollination is associated with acquisition of red flowers, short stamens and acetoin emission.

Conclusions: Our results suggest that the observed combination of floral characters is a pollination syndrome associated with the parallel evolution of pollination by fungus gnats. Although the role of the red floral display and acetoin in pollinator attraction remains to be elucidated, our finding underscores the importance of fungus gnats as potential contributors to floral diversification.

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对真菌昆虫授粉的适应是卫矛属授粉综合征进化的基础。
背景和目的:已知Dipteran昆虫是许多被子植物的传粉昆虫,但关于苍蝇如何影响花的进化的知识相对较少。一些由真菌昆虫授粉的植物有一套独特的花特征(暗红色、扁平形状和短雄蕊),这与任何已知的授粉综合征都不同。我们以卫矛属为模型,测试了这组花特征是否是与真菌昆虫授粉相关的授粉综合征。方法:以10种卫矛和雷公藤为外类群,对其花粉和花的颜色、形态和气味特征进行了研究。使用蜜蜂和苍蝇的颜色视觉模型来评估花朵的颜色。利用系统发育独立的对比测试了真菌-昆虫授粉与每种植物特征之间的进化联系。对与真菌-昆虫授粉有关的花的颜色进行了祖先状态重建,以推断卫矛属授粉的进化。关键结果:红花卫矛主要由真菌-昆虫传粉,而白花卫矛则由蜜蜂、甲虫和短头苍蝇授粉。色觉分析表明,蜜蜂和苍蝇都认为红色和白色的花朵是不同的颜色。真菌昆虫授粉种的花香以乙偶姻为特征,占三种昆虫花香总量的90%以上。系统发育独立性对比表明,真菌-昆虫授粉的进化与红花、短雄蕊的获得和乙偶姻的释放有关。结论:我们的研究结果表明,观察到的花性状组合是一种授粉综合征,与真菌昆虫授粉的平行进化有关。尽管红色花朵展示和乙偶姻在吸引传粉昆虫中的作用仍有待阐明,但我们的发现强调了真菌昆虫作为花朵多样化潜在贡献者的重要性。
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来源期刊
Annals of botany
Annals of botany 生物-植物科学
CiteScore
7.90
自引率
4.80%
发文量
138
审稿时长
3 months
期刊介绍: Annals of Botany is an international plant science journal publishing novel and rigorous research in all areas of plant science. It is published monthly in both electronic and printed forms with at least two extra issues each year that focus on a particular theme in plant biology. The Journal is managed by the Annals of Botany Company, a not-for-profit educational charity established to promote plant science worldwide. The Journal publishes original research papers, invited and submitted review articles, ''Research in Context'' expanding on original work, ''Botanical Briefings'' as short overviews of important topics, and ''Viewpoints'' giving opinions. All papers in each issue are summarized briefly in Content Snapshots , there are topical news items in the Plant Cuttings section and Book Reviews . A rigorous review process ensures that readers are exposed to genuine and novel advances across a wide spectrum of botanical knowledge. All papers aim to advance knowledge and make a difference to our understanding of plant science.
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