Hemimetabolous Genomes Reveal Molecular Basis of Termite Eusociality

Overview

Journal Nat Ecol Evol

Publisher Springer Nature

Specialty Biology

Date 2018 Feb 7

PMID 29403074

Citations 101

Authors

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

Affiliations

Soon will be listed here.

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.

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References

Dallerac R, Labeur C, Jallon J, Knipple D, Roelofs W, Wicker-Thomas C . A delta 9 desaturase gene with a different substrate specificity is responsible for the cuticular diene hydrocarbon polymorphism in Drosophila melanogaster. Proc Natl Acad Sci U S A. 2000; 97(17):9449-54. PMC: 16884. DOI: 10.1073/pnas.150243997. View

Dietemann V, Peeters C, Liebig J, Thivet V, Holldobler B . Cuticular hydrocarbons mediate discrimination of reproductives and nonreproductives in the ant Myrmecia gulosa. Proc Natl Acad Sci U S A. 2003; 100(18):10341-6. PMC: 193563. DOI: 10.1073/pnas.1834281100. View

Li L, Stoeckert Jr C, Roos D . OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 2003; 13(9):2178-89. PMC: 403725. DOI: 10.1101/gr.1224503. View

Kazazian Jr H . Mobile elements: drivers of genome evolution. Science. 2004; 303(5664):1626-32. DOI: 10.1126/science.1089670. View

Birney E, Clamp M, Durbin R . GeneWise and Genomewise. Genome Res. 2004; 14(5):988-95. PMC: 479130. DOI: 10.1101/gr.1865504. View

Korf I . Gene finding in novel genomes. BMC Bioinformatics. 2004; 5:59. PMC: 421630. DOI: 10.1186/1471-2105-5-59. View

Min X, Butler G, Storms R, Tsang A . OrfPredictor: predicting protein-coding regions in EST-derived sequences. Nucleic Acids Res. 2005; 33(Web Server issue):W677-80. PMC: 1160155. DOI: 10.1093/nar/gki394. View

Lomsadze A, Ter-Hovhannisyan V, Chernoff Y, Borodovsky M . Gene identification in novel eukaryotic genomes by self-training algorithm. Nucleic Acids Res. 2005; 33(20):6494-506. PMC: 1298918. DOI: 10.1093/nar/gki937. View

Stanke M, Keller O, Gunduz I, Hayes A, Waack S, Morgenstern B . AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res. 2006; 34(Web Server issue):W435-9. PMC: 1538822. DOI: 10.1093/nar/gkl200. View

10.

Suyama M, Torrents D, Bork P . PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 2006; 34(Web Server issue):W609-12. PMC: 1538804. DOI: 10.1093/nar/gkl315. View

11.

Sonobe H, Ohira T, Ieki K, Maeda S, Ito Y, Ajimura M . Purification, kinetic characterization, and molecular cloning of a novel enzyme, ecdysteroid 22-kinase. J Biol Chem. 2006; 281(40):29513-24. DOI: 10.1074/jbc.M604035200. View

12.

. Insights into social insects from the genome of the honeybee Apis mellifera. Nature. 2006; 443(7114):931-49. PMC: 2048586. DOI: 10.1038/nature05260. View

13.

Rewitz K, Rybczynski R, Warren J, Gilbert L . The Halloween genes code for cytochrome P450 enzymes mediating synthesis of the insect moulting hormone. Biochem Soc Trans. 2006; 34(Pt 6):1256-60. DOI: 10.1042/BST0341256. View

14.

Campbell M, Haas B, Hamilton J, Mount S, Buell C . Comprehensive analysis of alternative splicing in rice and comparative analyses with Arabidopsis. BMC Genomics. 2006; 7:327. PMC: 1769492. DOI: 10.1186/1471-2164-7-327. View

15.

Elsik C, Mackey A, Reese J, Milshina N, Roos D, Weinstock G . Creating a honey bee consensus gene set. Genome Biol. 2007; 8(1):R13. PMC: 1839126. DOI: 10.1186/gb-2007-8-1-r13. View

16.

Nene V, Wortman J, Lawson D, Haas B, Kodira C, Tu Z . Genome sequence of Aedes aegypti, a major arbovirus vector. Science. 2007; 316(5832):1718-23. PMC: 2868357. DOI: 10.1126/science.1138878. View

17.

Kong L, Zhang Y, Ye Z, Liu X, Zhao S, Wei L . CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res. 2007; 35(Web Server issue):W345-9. PMC: 1933232. DOI: 10.1093/nar/gkm391. View

18.

Ellinghaus D, Kurtz S, Willhoeft U . LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinformatics. 2008; 9:18. PMC: 2253517. DOI: 10.1186/1471-2105-9-18. View

19.

Fan Y, Eliyahu D, Schal C . Cuticular hydrocarbons as maternal provisions in embryos and nymphs of the cockroach Blattella germanica. J Exp Biol. 2008; 211(Pt 4):548-54. DOI: 10.1242/jeb.009233. View

20.

Kolodziejczyk R, Bujacz G, Jakob M, Ozyhar A, Jaskolski M, Kochman M . Insect juvenile hormone binding protein shows ancestral fold present in human lipid-binding proteins. J Mol Biol. 2008; 377(3):870-81. DOI: 10.1016/j.jmb.2008.01.026. View