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Published December 8, 2016 | Published + Supplemental Material
Journal Article Open

Evidence for social parasitism of early insect societies by Cretaceous rove beetles

Abstract

The evolution of eusociality in ants and termites propelled both insect groups to their modern ecological dominance. Yet, eusociality also fostered the evolution of social parasitism—an adverse symbiosis, in which the superorganismal colonies formed by these insects are infiltrated by a profusion of invertebrate species that target nest resources. Predominant among these are the aleocharine rove beetles (Staphylinidae), a vast and ecologically diverse subfamily with numerous morphologically and behaviourally specialized socially parasitic lineages. Here, we report a fossil aleocharine, Mesosymbion compactus gen. et sp. nov., in Burmese amber (∼99 million years old), displaying specialized anatomy that is a hallmark of social parasites. Mesosymbion coexisted in the Burmese palaeofauna with stem-group ants and termites that provide the earliest indications of eusociality in both insect groups. We infer that the advent of eusociality led automatically and unavoidably to selection for social parasitism. The antiquity and adaptive flexibility of aleocharines made them among the first organisms to engage in this type of symbiosis.

Additional Information

© 2016 The Author(s). This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ Received: 10 May 2016. Accepted: 20 October 2016. Published online: 08 December 2016. We thank Yui Takahashi (University of Tsukuba) for preparing the Mesosymbion specimen and David Grimaldi (AMNH) for the providing the accession number of the holotype for deposition. Alfred Newton and Margaret Thayer (Field Museum of Natural History), Taro Eldredge (University of Kansas), Christoph von Beeren (Technische Universität Darmstadt) and Toshiya Hirowatari (Kyushu University) provided important feedback on the manuscript. We are grateful to Takashi Komatsu (Kyushu University), Taisuke Kanao (Kyoto University) and Christoph von Beeren for use of photographs. This study was partially supported by a Grant-in-Aid for JSPS Fellows (14J02669) to S.Y. from the Japan Society for the Promotion of Science, Japan. This is a contribution from the Entomological Laboratory, Faculty of Agriculture, Kyushu University, Fukuoka, Japan (Ser. 7, No. 39). J.P. was funded by a Sir Henry Wellcome Postdoctoral Fellowship and grants from the NIH (RO1 GM113000) and the Ellison Medical Foundation to Gary Struhl, who provided a wonderful environment for this work. Author Contributions: S.Y. and J.P. conceived and designed the project, with input from M.M. J.P. performed confocal and light microscopic imaging of the amber specimen. S.Y. described the specimen, evaluated its systematic placement. S.Y. and J.P. performed phylogenetic analyses. S.Y. and M.M. photographed extant aleocharine specimens. J.P. wrote the paper and produced figures with input from S.Y. and M.M. Nomenclatural acts: This published work and the nomenclatural acts it contains have been registered in ZooBank, the proposed online registration system for the International Code of Zoological Nomenclature. The ZooBank LSIDs (Life Science Identifiers) can be resolved and the associated information viewed through any standard web browser by appending the LSID to the prefix ' http://zoobank.org/'. The LSIDs for this publication are to be found at: urn:lsid:zoobank.org:pub:63EA52A4-765A-4349-A74A-A1032909BA39 Data availability: All data generated or analysed during this study are included in this published article (and its Supplementary Information files). The holotype specimen of Mesosymbion compactus, around which this study is based, is deposited in the American Museum of Natural History, New York (accession number AMNH Bu-SY5). The authors declare no competing financial interests.

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