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Diversity and evolution of pollinator rewards and protection by Macaranga (Euphorbiaceae) bracteoles

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Abstract

Flowering plants have modified their floral organs in remarkably diverse ways to optimize their interaction with pollinators. Although floral organs represent a major source of floral diversity, many plants also use extrafloral organs, such as bracts and bracteoles, in interacting with pollinators; however, the evolutionary dynamics of non-floral organs involved in pollination are poorly studied. The genus Macaranga is characterized by protective mutualisms with ants that potentially interfere with pollinators on flowers. Macaranga flowers lack perianths and, notably, bracteoles serve the dual function of rewarding pollinators and protecting them from guarding ants; in one group of species, bracteoles provide a nectar reward to generalist pollinators, while in another group, bracteole “chambers” protect thrips or hemipteran pollinators that use these structures as feeding and breeding sites. We examined the diversity and evolutionary dynamics of inflorescence morphology in Macaranga, focusing on bracteoles. We recognized three inflorescence types based on examination of herbarium materials: Discoid-gland, which possess disc-shaped glands on the bracteole surfaces (including all the generalist-pollinated species); Enclosing, in which bracteoles cover flowers (including all the thrips- and hemipteran-pollinated species); and Inconspicuous, in which bracteoles are small, narrow or absent. Ancestral state reconstruction indicated that inflorescence morphologies have changed multiple times in the genus. These findings suggest that morphological changes in non-floral characters (bracteoles) of Macaranga species have occurred as frequently as in the floral structures of many flowering plants. The multiple evolutions of the Enclosing bracteoles, which protect pollinators, might have been facilitated by pollination interference from mutualistic ants.

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Acknowledgments

We are grateful to herbaria of Royal Botanic Gardens, Kew (K), Leiden Naturalis Biodiversity Center (L), Kyoto University (KYO) and Department of Forestry, Sarawak (SAR) for providing Macaranga specimens. This study was financially supported by the Research Institute for Humanity and Nature (Project D-04), Grants-in-Aid No. 21570028 from the Ministry of Education, Culture, Sports, Science and Technology, Japan, to S.S., Grants-in-Aid for JSPS Fellows from the Japan Society for the Promotion of Science (No. 24-1464 to E.Y.), and Kyoto University Global COE program “Formation of a strategic base for biodiversity and evolutionary research: from genome to ecosystem”.

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Correspondence to Eri Yamasaki.

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Yamasaki, E., Kawakita, A. & Sakai, S. Diversity and evolution of pollinator rewards and protection by Macaranga (Euphorbiaceae) bracteoles. Evol Ecol 29, 379–390 (2015). https://doi.org/10.1007/s10682-014-9750-7

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