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Rapid elimination of symbiotic intestinal protists during the neotenic differentiation in a subterranean termite, Reticulitermes speratus

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Abstract

The symbiosis between lower termites and their intestinal microorganisms, essential for wood digestion, is well characterized. Termites exhibit a reproductive division of labor—kings and queens specialize in reproduction, and workers are responsible for foraging and feeding the colony members. Therefore, the gut microbial community in royals is expected to be down-regulated because it is less important than that in workers. Indeed, we recently reported that, in the termite species Reticulitermes speratus, workers have symbiotic protists; kings, and neotenic queens in mature field colonies completely lose protists in their guts. However, the dynamics of the protist community during caste differentiation remain unclear. In this study, we investigated the relationship between the abundance of intestinal protists and the neotenic differentiation of R. speratus. First, we confirmed that both sexes of late instar nymphs possessed intestinal protist communities like those of workers. Nevertheless, after molting for neotenic differentiation, they lost most of their intestinal protists and did not regain them. Based on our behavioral observation, workers, nymphs, and neotenics received proctodeal food from surrounding workers. This suggests protists can enter neotenics’ guts, while they cannot establish after the neotenic differentiation. Our study highlights that the interaction between termites and gut microbes changes dynamically during caste differentiation.

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Data availability

The dataset is available in Supplementary Information (Table S1, S2, S3 and S4).

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Acknowledgements

We thank the members of the Laboratory of Insect Ecology in Kyoto University for helpful discussions and Kazuki Takahashi for the valuable comments on the manuscript. We would also like to thank Editage for English language editing.

Funding

This study was supported by funding from the Japan Society for the Promotion of Science to TI (Research Fellowship for Young Scientists No. 18J13513 and No. 20J00986) and KM (Kiban Kenkyu S No. 25221206 and No. 18H05268).

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Authors and Affiliations

  1. Laboratory of Insect Ecology, Graduate School of Agriculture, Kyoto University, Kyoto, Japan

    T. Inagaki, T. Nozaki & K. Matsuura

  2. School of Life Science and Technology, Tokyo Institute of Technology, Tokyo, Japan

    T. Inagaki

  3. Laboratory of Evolutionary Genomics, National Institute for Basic Biology, Aichi, Japan

    T. Nozaki

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  1. T. Inagaki
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  2. T. Nozaki
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  3. K. Matsuura
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TI designed experiments. TI and TN performed experiments. TI, TN, and KM wrote the manuscript, and all authors are accountable for the content and approve the final version of the manuscript.

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Correspondence to T. Inagaki.

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Inagaki, T., Nozaki, T. & Matsuura, K. Rapid elimination of symbiotic intestinal protists during the neotenic differentiation in a subterranean termite, Reticulitermes speratus. Insect. Soc. 69, 335–343 (2022). https://doi.org/10.1007/s00040-022-00877-1

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