Evidence for reduced immune gene diversity and activity during the evolution of termites

Shulin He; Thorben Sieksmeyer; Yanli Che; M Alejandra Esparza Mora; Petr Stiblik; Ronald Banasiak; Mark C Harrison; Jan Šobotnik; Zongqing Wang; Paul R Johnston; Dino P. McMahon

doi:10.1098/rspb.2020.3168

Evidence for reduced immune gene diversity and activity during the evolution of termites

Shulin He, Thorben Sieksmeyer, Yanli Che, M Alejandra Esparza Mora, Petr Stiblik, Ronald Banasiak, Mark C Harrison, Jan Šobotnik, Zongqing Wang, Paul R Johnston, Dino P. McMahon

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Abstract

The evolution of biological complexity is associated with the emergence of bespoke immune systems that maintain and protect organism integrity. Unlike the well-studied immune systems of cells and individuals, little is known about the origins of immunity during the transition to eusociality, a major evolutionary transition comparable to the evolution of multicellular organisms from single-celled ancestors. We aimed to tackle this by characterizing the immune gene repertoire of 18 cockroach and termite species, spanning the spectrum of solitary, subsocial and eusocial lifestyles. We find that key transitions in termite sociality are correlated with immune gene family contractions. In cross-species comparisons of immune gene expression, we find evidence for a caste-specific social defence system in termites, which appears to operate at the expense of individual immune protection. Our study indicates that a major transition in organismal complexity may have entailed a fundamental reshaping of the immune system optimized for group over individual defence.

Original language	English
Article number	20203168
Number of pages	10
Journal	Proceedings of the Royal Society B: Biological Sciences
Volume	288
Issue number	1945
Early online date	17 Feb 2021
DOIs	https://doi.org/10.1098/rspb.2020.3168
Publication status	Published - 24 Feb 2021
Externally published	Yes

Bibliographical note

Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

Funder

This study was supported by Freie Universität Internal Research Funding and Devtsche Forschungsgemeinschaft (DFG, grant no. MC 436/5-1) to D.P.M. S.H., P.S. and J.S. are supported by ‘EVA4.0’ (no. CZ.02.1.01/0.0/0.0/16_019/0000803), and P.S. and J.S. are supported by CIGA no. 20184306. Y.C. and Z.W. are supported by the National Natural Science Foundation of China (grant no. 31672329).

Funding

This study was supported by Freie Universität Internal Research Funding and Deutsche Forschungsgemeinschaft (DFG, grant no. MC 436/5-1) to D.P.M. S.H., P.S. and J.S. are supported by ‘EVA4.0’ (no. CZ.02.1.01/0.0/0.0/16_019/0000803), and P.S. and J.S. are supported by CIGA no. 20184306. Y.C. and Z.W. are supported by the National Natural Science Foundation of China (grant no. 31672329).

Funders	Funder number
Freie Universität Berlin
Deutsche Forschungsgemeinschaft	MC 436/5-1
Czech University of Life Sciences Prague	CZ.02.1.01/0.0/0.0/16_019/0000803
National Natural Science Foundation of China	31672329

Keywords

social insect
subsocial
cockroach
major transition
contraction
expansion

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10.1098/rspb.2020.3168Licence: CC BY

Harrison2021VoRFinal published version, 1.63 MBLicence: CC BY

Cite this

He, S., Sieksmeyer, T., Che, Y., Mora, M. A. E., Stiblik, P., Banasiak, R., Harrison, M. C., Šobotnik, J., Wang, Z., Johnston, P. R., & McMahon, D. P. (2021). Evidence for reduced immune gene diversity and activity during the evolution of termites. Proceedings of the Royal Society B: Biological Sciences, 288(1945), Article 20203168. https://doi.org/10.1098/rspb.2020.3168

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Evidence for reduced immune gene diversity and activity during the evolution of termites

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