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      Revision of the Japanese species of Epicephala Meyrick with descriptions of seven new species (Lepidoptera, Gracillariidae)

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          Abstract

          Abstract

          Epicephala moths are involved in obligate mutualisms with their Phyllanthaceae hosts, in which the female moths assure pollination and, in return, their progeny develop by consuming the seeds. Ecological, molecular and geographical data suggest that the genus includes several hundred species, but the majority remains to be formally described. Here we revise the Japanese species of Epicephala Meyrick, 1880. In addition to two previously named species, seven species are newly described: Epicephala anthophilia sp. n., Epicephala lanceolatella sp. n., Epicephala perplexa sp. n., Epicephala obovatella sp. n., Epicephala corruptrix sp. n., Epicephala parasitica sp. n. and Epicephala nudilingua sp. n. The first four are species involved in obligate pollination mutualism, while the fifth is a pollinating seed parasite and the last two are derived non-pollinating seed parasites of herbaceous Phyllanthus . Each of the nine Japanese Epicephela species is specialized to a single plant species in the genera Glochidion , Breynia or Phyllanthus , except for Epicephala obovatella and Epicephala corruptrix that each utilizes two closely related Glochidion species. Considerable variations are found in pollination and oviposition behaviors among species, which are reflected in their proboscis and ovipositor morphologies, respectively. Molecular phylogeny indicated that there have been repeated transitions in oviposition mode during the diversification of Epicephala , which were accompanied by changes in ovipositor morphology, as suggested by a correlation analysis. Keys to species are provided.

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          Detecting Correlated Evolution on Phylogenies: A General Method for the Comparative Analysis of Discrete Characters

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            An obligate pollination mutualism and reciprocal diversification in the tree genus Glochidion (Euphorbiaceae).

            Highly coevolved pollination mutualism accompanied by reciprocal diversification has been known in only two plant genera, Ficus (Moraceae) and Yucca (Agavaceae), which are pollinated exclusively by obligate seed-parasitic wasps and moths, respectively. An additional, highly diversified, species-specific pollination mutualism between a monoecious tree genus, Glochidion (Euphorbiaceae), and a moth genus, Epicephala (Gracillariidae), is presented here. At night, the small female moth actively deposits pollen on the cryptic stigma of the female flower by using its proboscis, then oviposits into the style. The moth larva infests only a portion of the developing seeds within fruit. We confirmed that at least three Glochidion species are pollinated only by their respective seed-parasitic moth species, which could be distinguished by genitalic morphology and mitochondrial DNA sequences. These results and widespread evidence of limited seed infestation by the moths associated with Glochidion species suggest that speciation based on the highly specialized Glochidion stylar structure and moth oviposition behavior have promoted species diversification in Glochidion and its pollinators.
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              Repeated independent evolution of obligate pollination mutualism in the Phyllantheae-Epicephala association.

              The well-known fig-fig wasp and yucca-yucca moth mutualisms are classic examples of obligate mutualisms that have been shaped by millions of years of coevolution. Pollination systems involving obligate seed parasites are only expected to evolve under rare circumstances where their positive effects are not swamped by abundant co-pollinators and heavy costs resulting from seed destruction. Here, we show that, in Phyllantheae, specialization to pollination by Epicephala moths evolved at least five times, involving more than 500 Phyllantheae species in this obligate association. Active pollination behaviour evolved once in Epicephala, 10-20 Myr after the initial divergence of their host plants. The pollinating Epicephala moths thus radiated on an already-diverged host lineage and successively colonized new Phyllantheae hosts, thereby giving rise to repeated independent evolution of the specialized pollination system in Phyllantheae. The present evolutionary success of this association rests entirely upon active pollination by Epicephala, making this a distinct example of an evolutionary key innovation. Overall, our findings provide a clear empirical demonstration of how a combination of evolutionary innovation and partner shifts facilitates the spread of mutualism in a coevolving species interaction.
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                Author and article information

                Journal
                Zookeys
                Zookeys
                ZooKeys
                ZooKeys
                Pensoft Publishers
                1313-2989
                1313-2970
                2016
                23 February 2016
                : 568
                : 87-118
                Affiliations
                [1 ]Center for Ecological Research, Kyoto University, 2-509-3 Hirano, Otsu, Shiga 520-2113, Japan
                [2 ]Graduate School of Human and Environmental Studies, Kyoto University, Yoshida-Nihonmatsu-cho, Sakyo 606-8501, Japan
                Author notes
                Corresponding author: Atsushi Kawakita ( kawakita@ 123456ecology.kyoto-u.ac.jp )

                Academic editor: E. van Nieukerken

                Article
                10.3897/zookeys.568.6721
                4829671
                27103875
                c32921e0-b051-4419-ba51-65946a7c70e0
                Atsushi Kawakita, Makoto Kato

                This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 5 October 2015
                : 14 January 2016
                Categories
                Research Article

                Animal science & Zoology
                active pollination behavior,breynia,dna barcode,glochidion,gracillariidae,japan,obligate pollination mutualism,phyllanthus,animalia,lepidoptera

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