Hemimetabolous genomes reveal molecular basis of termite eusociality

Mark C. Harrison; Evelien Jongepier; Hugh M. Robertson; Nicolas Arning; Tristan Bitard-Feildel; Hsu Chao; Christopher P. Childers; Huyen Dinh; Harshavardhan Doddapaneni; Shannon Dugan; Johannes Gowin; Carolin Greiner; Yi Han; Haofu Hu; Daniel S. T. Hughes; Ann-Kathrin Huylmans; Carsten Kemena; Lukas P. M. Kremer; Sandra L. Lee; Alberto Lopez-Ezquerra; Ludovic Mallet; Jose M. Monroy-Kuhn; Annabell Moser; Shwetha C. Murali; Donna M. Muzny; Saria Otani; Maria-Dolors Piulachs; Monica Poelchau; Jiaxin Qu; Florentine Schaub; Ayako Wada-Katsumata; Kim C. Worley; Qiaolin Xie; Guillem Ylla; Michael Poulsen; Richard A. Gibbs; Coby Schal; Stephen Richards; Xavier Belles; Judith Korb; Erich Bornberg-Bauer

doi:10.1038/s41559-017-0459-1

Hemimetabolous genomes reveal molecular basis of termite eusociality

Mark C. Harrison, Evelien Jongepier, Hugh M. Robertson, Nicolas Arning, Tristan Bitard-Feildel, Hsu Chao, Christopher P. Childers, Huyen Dinh, Harshavardhan Doddapaneni, Shannon Dugan, Johannes Gowin, Carolin Greiner, Yi Han, Haofu Hu, Daniel S. T. Hughes, Ann-Kathrin Huylmans, Carsten Kemena, Lukas P. M. Kremer, Sandra L. Lee, Alberto Lopez-EzquerraLudovic Mallet, Jose M. Monroy-Kuhn, Annabell Moser, Shwetha C. Murali, Donna M. Muzny, Saria Otani, Maria-Dolors Piulachs, Monica Poelchau, Jiaxin Qu, Florentine Schaub, Ayako Wada-Katsumata, Kim C. Worley, Qiaolin Xie, Guillem Ylla, Michael Poulsen, Richard A. Gibbs, Coby Schal, Stephen Richards, Xavier Belles, Judith Korb, Erich Bornberg-Bauer

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Abstract

Around 150 million years ago, eusocial termites evolved from within the cockroaches, 50 million years before eusocial Hymenoptera, such as bees and ants, appeared. Here, we report the 2-Gb genome of the German cockroach, Blattella germanica, and the 1.3-Gb genome of the drywood termite Cryptotermes secundus. We show evolutionary signatures of termite eusociality by comparing the genomes and transcriptomes of three termites and the cockroach against the background of 16 other eusocial and non-eusocial insects. Dramatic adaptive changes in genes underlying the production and perception of pheromones confirm the importance of chemical communication in the termites. These are accompanied by major changes in gene regulation and the molecular evolution of caste determination. Many of these results parallel molecular mechanisms of eusocial evolution in Hymenoptera. However, the specific solutions are remarkably different, thus revealing a striking case of convergence in one of the major evolutionary transitions in biological complexity.

Original language	English
Pages (from-to)	557–566
Number of pages	10
Journal	Nature Ecology & Evolution
Volume	2
Early online date	5 Feb 2018
DOIs	https://doi.org/10.1038/s41559-017-0459-1
Publication status	Published - Mar 2018
Externally published	Yes

Bibliographical note

This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

Funder

M.C.H. and E.J. are supported by DFG grant BO2544/11-1 to E.B.-B. J.K. is supported by University of Osnabrück and DFG grant KO1895/16-1. X.B. and M.-D.P. are supported by Spanish Ministerio de Economía y Competitividad (CGL2012-36251 and CGL2015-64727-P to X.B., and CGL2016-76011-R to M.-D.P.), including FEDER funds, and by Catalan Government (2014 SGR 619). C.S. is supported by grants from the US Department of Housing and Urban Development (NCHHU-0017-13), the National Science Foundation (IOS-1557864), the Alfred P. Sloan Foundation (2013-5-35 MBE), the National Institute of Environmental Health Sciences (P30ES025128) to the Center for Human Health and the Environment, and the Blanton J. Whitmire Endowment. M.P. is supported by a Villum Kann Rasmussen Young Investigator Fellowship (VKR10101).

Funding

M.C.H. and E.J. are supported by DFG grant BO2544/11-1 to E.B.-B. J.K. is supported by University of Osnabrück and DFG grant KO1895/16-1. X.B. and M.-D.P. are supported by Spanish Ministerio de Economía y Competitividad (CGL2012-36251 and CGL2015-64727-P to X.B., and CGL2016-76011-R to M.-D.P.), including FEDER funds, and by Catalan Government (2014 SGR 619). C.S. is supported by grants from the US Department of Housing and Urban Development (NCHHU-0017-13), the National Science Foundation (IOS-1557864), the Alfred P. Sloan Foundation (2013-5-35 MBE), the National Institute of Environmental Health Sciences (P30ES025128) to the Center for Human Health and the Environment, and the Blanton J. Whitmire Endowment. M.P. is supported by a Villum Kann Rasmussen Young Investigator Fellowship (VKR10101).

Funders	Funder number
Deutsche Forschungsgemeinschaft	BO2544/11-1, KO1895/16-1
University of Osnabruck	KO1895/16-1
Ministerio de Economía y Competitividad	CGL2012-36251, CGL2015-64727-P, CGL2016-76011-R
Generalitat de Catalunya	2014 SGR 619
US Department of Housing and Urban Development	NCHHU-0017-13
National Science Foundation	IOS-1557864
Alfred P. Sloan Foundation	2013-5-35 MBE
National Institute of Environmental Health Sciences	P30ES025128
Villum Foundation	VKR10101

Keywords

Comparative genomics
Molecular evolution
Social evolution

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10.1038/s41559-017-0459-1Licence: CC BY

Harrison2018VoRFinal published version, 3.69 MBLicence: CC BY

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Harrison, M. C., Jongepier, E., Robertson, H. M., Arning, N., Bitard-Feildel, T., Chao, H., Childers, C. P., Dinh, H., Doddapaneni, H., Dugan, S., Gowin, J., Greiner, C., Han, Y., Hu, H., Hughes, D. S. T., Huylmans, A.-K., Kemena, C., Kremer, L. P. M., Lee, S. L., ... Bornberg-Bauer, E. (2018). Hemimetabolous genomes reveal molecular basis of termite eusociality. Nature Ecology & Evolution, 2, 557–566. https://doi.org/10.1038/s41559-017-0459-1

Harrison, MC, Jongepier, E, Robertson, HM, Arning, N, Bitard-Feildel, T, Chao, H, Childers, CP, Dinh, H, Doddapaneni, H, Dugan, S, Gowin, J, Greiner, C, Han, Y, Hu, H, Hughes, DST, Huylmans, A-K, Kemena, C, Kremer, LPM, Lee, SL, Lopez-Ezquerra, A, Mallet, L, Monroy-Kuhn, JM, Moser, A, Murali, SC, Muzny, DM, Otani, S, Piulachs, M-D, Poelchau, M, Qu, J, Schaub, F, Wada-Katsumata, A, Worley, KC, Xie, Q, Ylla, G, Poulsen, M, Gibbs, RA, Schal, C, Richards, S, Belles, X, Korb, J & Bornberg-Bauer, E 2018, 'Hemimetabolous genomes reveal molecular basis of termite eusociality', Nature Ecology & Evolution, vol. 2, pp. 557–566. https://doi.org/10.1038/s41559-017-0459-1

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AU - Chao, Hsu

AU - Childers, Christopher P.

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AU - Doddapaneni, Harshavardhan

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N2 - Around 150 million years ago, eusocial termites evolved from within the cockroaches, 50 million years before eusocial Hymenoptera, such as bees and ants, appeared. Here, we report the 2-Gb genome of the German cockroach, Blattella germanica, and the 1.3-Gb genome of the drywood termite Cryptotermes secundus. We show evolutionary signatures of termite eusociality by comparing the genomes and transcriptomes of three termites and the cockroach against the background of 16 other eusocial and non-eusocial insects. Dramatic adaptive changes in genes underlying the production and perception of pheromones confirm the importance of chemical communication in the termites. These are accompanied by major changes in gene regulation and the molecular evolution of caste determination. Many of these results parallel molecular mechanisms of eusocial evolution in Hymenoptera. However, the specific solutions are remarkably different, thus revealing a striking case of convergence in one of the major evolutionary transitions in biological complexity.

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KW - Molecular evolution

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JO - Nature Ecology & Evolution

JF - Nature Ecology & Evolution

ER -

Hemimetabolous genomes reveal molecular basis of termite eusociality

Abstract

Bibliographical note

Funder

Funding

Keywords

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