Hemimetabolous genomes reveal molecular basis of termite eusociality
Harrison M, Jongepier E, Robertson H, Arning N, Bitard Feildel T, Chao H, Childers C, Dinh H, Doddapaneni H, Dugan S, Gowin J, Greiner C, Han Y, Hu H, Hughes D, Huylmans AK, Kemena K, Kremer L, Lee S, López Ezquerra A, Mallet L, Monroy Kuhn J, Moser A, Murali S, Muzny D, Otani S, Piulachs M, Poelchau M, Qu J, Schaub F, Wada Katsumata A, Worley K, Xie Q, Ylla G, Poulsen M, Gibbs R, Schal C, Richards S, Belles X, Korb J, Bornberg Bauer E. 2018. Hemimetabolous genomes reveal molecular basis of termite eusociality. Nature Ecology and Evolution. 2(3), 557–566.
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Author
Harrison, Mark;
Jongepier, Evelien;
Robertson, Hugh;
Arning, Nicolas;
Bitard Feildel, Tristan;
Chao, Hsu;
Childers, Christopher;
Dinh, Huyen;
Doddapaneni, Harshavardhan;
Dugan, Shannon;
Gowin, Johannes;
Greiner, Carolin
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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.
Publishing Year
Date Published
2018-02-05
Journal Title
Nature Ecology and Evolution
Acknowledgement
We thank O. Niehuis for allowing use of the unpublished E. danica genome, J. Gadau and C. Smith for comments and advice on the manuscript, and J. Schmitz for assistance with analyses and proofreading the manuscript. J.K. thanks Charles Darwin University (Australia), especially S. Garnett and the Horticulture and Aquaculture team, for providing logistic support to collect C. secundus. The Parks and Wildlife Commission, Northern Territory, the Department of the Environment, Water, Heritage and the Arts gave permission to collect (Permit number 36401) and export (Permit WT2010-6997) the termites. USDA is an equal opportunity provider and employer. 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).
Volume
2
Issue
3
Page
557-566
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Cite this
Harrison M, Jongepier E, Robertson H, et al. Hemimetabolous genomes reveal molecular basis of termite eusociality. Nature Ecology and Evolution. 2018;2(3):557-566. doi:10.1038/s41559-017-0459-1
Harrison, M., Jongepier, E., Robertson, H., Arning, N., Bitard Feildel, T., Chao, H., … Bornberg Bauer, E. (2018). Hemimetabolous genomes reveal molecular basis of termite eusociality. Nature Ecology and Evolution. Springer Nature. https://doi.org/10.1038/s41559-017-0459-1
Harrison, Mark, Evelien Jongepier, Hugh Robertson, Nicolas Arning, Tristan Bitard Feildel, Hsu Chao, Christopher Childers, et al. “Hemimetabolous Genomes Reveal Molecular Basis of Termite Eusociality.” Nature Ecology and Evolution. Springer Nature, 2018. https://doi.org/10.1038/s41559-017-0459-1.
M. Harrison et al., “Hemimetabolous genomes reveal molecular basis of termite eusociality,” Nature Ecology and Evolution, vol. 2, no. 3. Springer Nature, pp. 557–566, 2018.
Harrison M, Jongepier E, Robertson H, Arning N, Bitard Feildel T, Chao H, Childers C, Dinh H, Doddapaneni H, Dugan S, Gowin J, Greiner C, Han Y, Hu H, Hughes D, Huylmans AK, Kemena K, Kremer L, Lee S, López Ezquerra A, Mallet L, Monroy Kuhn J, Moser A, Murali S, Muzny D, Otani S, Piulachs M, Poelchau M, Qu J, Schaub F, Wada Katsumata A, Worley K, Xie Q, Ylla G, Poulsen M, Gibbs R, Schal C, Richards S, Belles X, Korb J, Bornberg Bauer E. 2018. Hemimetabolous genomes reveal molecular basis of termite eusociality. Nature Ecology and Evolution. 2(3), 557–566.
Harrison, Mark, et al. “Hemimetabolous Genomes Reveal Molecular Basis of Termite Eusociality.” Nature Ecology and Evolution, vol. 2, no. 3, Springer Nature, 2018, pp. 557–66, doi:10.1038/s41559-017-0459-1.
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