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Termite evolution: mutualistic associations, key innovations, and the rise of Termitidae

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Abstract

Termites are a clade of eusocial wood-feeding roaches with > 3000 described species. Eusociality emerged ~ 150 million years ago in the ancestor of modern termites, which, since then, have acquired and sometimes lost a series of adaptive traits defining of their evolution. Termites primarily feed on wood, and digest cellulose in association with their obligatory nutritional mutualistic gut microbes. Recent advances in our understanding of termite phylogenetic relationships have served to provide a tentative timeline for the emergence of innovative traits and their consequences on the ecological success of termites. While all “lower” termites rely on cellulolytic protists to digest wood, “higher” termites (Termitidae), which comprise ~ 70% of termite species, do not rely on protists for digestion. The loss of protists in Termitidae was a critical evolutionary step that fostered the emergence of novel traits, resulting in a diversification of morphology, diets, and niches to an extent unattained by “lower” termites. However, the mechanisms that led to the initial loss of protists and the succession of events that took place in the termite gut remain speculative. In this review, we provide an overview of the key innovative traits acquired by termites during their evolution, which ultimately set the stage for the emergence of “higher” termites. We then discuss two hypotheses concerning the loss of protists in Termitidae, either through an externalization of the digestion or a dietary transition. Finally, we argue that many aspects of termite evolution remain speculative, as most termite biological diversity and evolutionary trajectories have yet to be explored.

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Acknowledgements

TC thanks Nan-Yao Su, Paul Bardunias, Aaron Mullins for the many discussions over the years about the various aspects of evolutionary trajectories in termites. MSE is grateful to the late Kumar Krishna for his many stimulating discussions regarding termites and their evolution. All authors are thankful to all the participants of the ‘2019 termite course’ (Ft Lauderdale, FL), the event that nurtured this collaboration.

Funding

This study was supported in part by, a grant from USDA National Institute of Food and Agriculture Hatch projects number FLA-FLT 005660 (TC), by a NSF-DEB grant, under the agreement no. 1754083 (TC), by the project IGA 20205014 realized at Faculty of Tropical AgriSciences, Czech University of Life Sciences Prague (JŠ and TB), and by the subsidiary funding to OIST (TB).

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Authors and Affiliations

  1. Entomology and Nematology Department, Institute of Food and Agricultural Science, Ft Lauderdale Research and Education Center, University of Florida, Davie, FL, USA

    Thomas Chouvenc

  2. Faculty of Tropical AgriSciences, Czech University of Life Sciences, Prague, Czech Republic

    Jan Šobotník & Thomas Bourguignon

  3. Division of Entomology, Natural History Museum, and Department of Ecology and Evolutionary Biology, University of Kansas, 1501 Crestline Drive, Suite 140, Lawrence, KS, 66045, USA

    Michael S. Engel

  4. Okinawa Institute of Science and Technology Graduate University, Onna-son, Okinawa, Japan

    Thomas Bourguignon

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  4. Thomas Bourguignon
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TC and TB jointly prepared the initial draft, and JŠ and MSE contributed additional information. All authors were actively involved with the development of the main narrative of this review.

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Correspondence to Thomas Chouvenc or Thomas Bourguignon.

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Chouvenc, T., Šobotník, J., Engel, M.S. et al. Termite evolution: mutualistic associations, key innovations, and the rise of Termitidae. Cell. Mol. Life Sci. 78, 2749–2769 (2021). https://doi.org/10.1007/s00018-020-03728-z

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