Hemimetabolous genomes reveal molecular basis of termite eusociality

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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.

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Most cited references 57

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Profile hidden Markov models.

S. Eddy (1998)

The recent literature on profile hidden Markov model (profile HMM) methods and software is reviewed. Profile HMMs turn a multiple sequence alignment into a position-specific scoring system suitable for searching databases for remotely homologous sequences. Profile HMM analyses complement standard pairwise comparison methods for large-scale sequence analysis. Several software implementations and two large libraries of profile HMMs of common protein domains are available. HMM methods performed comparably to threading methods in the CASP2 structure prediction exercise.

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LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons

David Ellinghaus, Stefan Kurtz, Ute Willhoeft (2008)

Background Transposable elements are abundant in eukaryotic genomes and it is believed that they have a significant impact on the evolution of gene and chromosome structure. While there are several completed eukaryotic genome projects, there are only few high quality genome wide annotations of transposable elements. Therefore, there is a considerable demand for computational identification of transposable elements. LTR retrotransposons, an important subclass of transposable elements, are well suited for computational identification, as they contain long terminal repeats (LTRs). Results We have developed a software tool LTRharvest for the de novo detection of full length LTR retrotransposons in large sequence sets. LTRharvest efficiently delivers high quality annotations based on known LTR transposon features like length, distance, and sequence motifs. A quality validation of LTRharvest against a gold standard annotation for Saccharomyces cerevisae and Drosophila melanogaster shows a sensitivity of up to 90% and 97% and specificity of 100% and 72%, respectively. This is comparable or slightly better than annotations for previous software tools. The main advantage of LTRharvest over previous tools is (a) its ability to efficiently handle large datasets from finished or unfinished genome projects, (b) its flexibility in incorporating known sequence features into the prediction, and (c) its availability as an open source software. Conclusion LTRharvest is an efficient software tool delivering high quality annotation of LTR retrotransposons. It can, for example, process the largest human chromosome in approx. 8 minutes on a Linux PC with 4 GB of memory. Its flexibility and small space and run-time requirements makes LTRharvest a very competitive candidate for future LTR retrotransposon annotation projects. Moreover, the structured design and implementation and the availability as open source provides an excellent base for incorporating novel concepts to further improve prediction of LTR retrotransposons.

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Mobile elements: drivers of genome evolution.

Haig H. Kazazian (2004)

Mobile elements within genomes have driven genome evolution in diverse ways. Particularly in plants and mammals, retrotransposons have accumulated to constitute a large fraction of the genome and have shaped both genes and the entire genome. Although the host can often control their numbers, massive expansions of retrotransposons have been tolerated during evolution. Now mobile elements are becoming useful tools for learning more about genome evolution and gene function.

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Author and article information

Journal

Journal ID (nlm-journal-id): 101698577

Journal ID (pubmed-jr-id): 46074

Journal ID (nlm-ta): Nat Ecol Evol

Journal ID (iso-abbrev): Nat Ecol Evol

Title: Nature ecology & evolution

ISSN (Electronic): 2397-334X

Publication date Nihms-submitted: 16 April 2019

Publication date (Electronic): 05 February 2018

Publication date (Print): March 2018

Publication date PMC-release: 25 April 2019

Volume: 2

Issue: 3

Pages: 557-566

Affiliations

[1 ]Institute for Evolution and Biodiversity, University of Münster, Münster, Germany.

[2 ]Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, IL, USA.

[3 ]Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, Houston, TX, USA.

[4 ]USDA-ARS, National Agricultural Library, Beltsville, MD, USA.

[5 ]Evolutionary Biology & Ecology, University of Freiburg, Freiburg, Germany.

[6 ]Behavioral Biology, University of Osnabrück, Osnabrück, Germany.

[7 ]Ecology and Evolution, University of Copenhagen, Copenhagen, Denmark.

[8 ]Institute of Science and Technology Austria, Klosterneuburg, Austria.

[9 ]Institut de Biologia Evolutiva, CSIC-University Pompeu Fabra, Barcelona, Spain.

[10 ]Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, USA.

[11 ]China National GeneBank, Beijing Genomics Institute (BGI)-Shenzhen, Shenzhen, China.

[12 ]These authors contributed equally: Mark C. Harrison, Evelien Jongepier and Hugh M. Robertson.

Author notes

Author contributions

E.B.-B. conceived, managed and coordinated the project; M.C.H., E.J. and H.M.R. are joint first authors. J.K. conceived and managed the C. secundus sequencing project, and coordinated termite-related analyses; S.R. conceived and managed the B. germanica sequencing project; S.R., S.D., S.L.L., H.C., H.V.D., H.D., Y.H., J.Q., S.C.M., D.S.T.H., K.C.W., D.M.M. and R.A.G. carried out B. germanica library construction, genome sequencing and assembly; C.S. and A.W-.K. provided biological material through full-sib mating for B. germanica; X.B. and C.S. co-managed the B. germanica analysis; M.P. and C.P.C. implemented Web Apollo data traces; S.O. and M.P. provided biological material for M. natalensis; C.G., J.G., J.M.M.-K., A.M., F.S., H.H. and J.K. coordinated and carried out DNA and RNA sequencing for C. secundus; M-D.P., X.B. and G.Y. coordinated transcriptome sequencing of B. germanica; L.M. performed automated gene prediction on C. secundus; E.J. and N.A. improved assembly and annotation for B. germanica & C. secundus, and compared and analysed genome sizes and quality. E.J., N.A. and L.P.M.K. analysed TEs; M.C.H. analysed CpG patterns and signatures of selection; T.B-F., E.J., C.K., L.P.M.K. and A.L-E. performed orthology and phylogenetic analyses; L.P.M.K., E.J., H.M.R. and M.C.H. analysed gene family evolution; A.L-E., E.J. and M.C.H. analysed transcriptomes and performed differential expression analyses; T.B.-F. and A.L-E. carried out orthoMCL clustering; H.M.R. corrected gene models for chemoreceptors; C.K. and E.J. corrected gene models for desaturases and elongases; A-K.H. and M.C.H. corrected gene models for cytochrome P450s; E.B.-B. and M.C.H drafted and wrote the manuscript; X.B., M.-D.P. and J.K. contributed to sections of the manuscript; E.J., L.P.M.K., A.L-E., C.K. and M.C.H. wrote and organized the Supplementary Information; L.P.M.K., N.A., A.L-E., M.C.H. and E.B.-B. prepared figures for the manuscript. All authors read, corrected and commented on the manuscript.

[* ] Correspondence and requests for materials should be addressed to X.B. or J.K. or E.B.-B. xavier.belles@ 123456ibe.upf-csic.es ; judith.korb@ 123456biologie.uni-freiburg.de ; ebb@ 123456uni-muenster.de

Author information

Mark C. Harrison https://orcid.org/0000-0003-3095-019X

Christopher P. Childers https://orcid.org/0000-0002-1253-5550

Ann-Kathrin Huylmans https://orcid.org/0000-0001-8871-4961

Lukas P. M. Kremer https://orcid.org/0000-0003-3170-6295

Ludovic Mallet https://orcid.org/0000-0002-3246-389X

Ayako Wada-Katsumata https://orcid.org/0000-0002-2895-1102

Guillem Ylla https://orcid.org/0000-0003-4540-0131

Michael Poulsen https://orcid.org/0000-0002-2839-1715

Xavier Belles https://orcid.org/0000-0002-1566-303X

Judith Korb https://orcid.org/0000-0001-9577-9376

Erich Bornberg-Bauer https://orcid.org/0000-0002-1826-3576

Article

Manuscript ID: NIHMS1022840

DOI: 10.1038/s41559-017-0459-1

PMC ID: 6482461

PubMed ID: 29403074

SO-VID: 161745d9-bae9-4f8d-aedc-51e5ce659078

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Hemimetabolous genomes reveal molecular basis of termite eusociality

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Abstract

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Hymenoptera

Most cited references 57

Profile hidden Markov models.

LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons

Mobile elements: drivers of genome evolution.

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