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Molecular Traces of Alternative Social Organization in a Termite Genome

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Molecular Traces of Alternative Social Organization in a Termite Genome Molecular traces of alternative social organization in a termite genome Terrapon, Nicolas; Li, Cai; Robertson, Hugh M.; Ji, Lu; Meng, Xuehong; Booth, Warren; Chen, Zhensheng; Childers, Christopher P.; Glastad, Karl M.; Gokhale, Kaustubh; Gowin, Johannes; Gronenberg, Wulfila; Hermansen, Russell A.; Hu, Haofu; Hunt, Brendan G.; Huylmans, Ann Kathrin; Khalil, Sayed M. S.; Mitchell, Robert D.; Munoz-Torres, Monica C.; Mustard, Julie A.; Pan, Hailin; Reese, Justin T.; Scharf, Michael E.; Sun, Fengming; Vogel, Heiko; Xiao, Jin; Yang, Wei; Yang, Zhikai; Yang, Zuoquan; Zhou, Jiajian; Zhu, Jiwei; Brent, Colin S.; Elsik, Christine G.; Goodisman, Michael A. D.; Liberles, David A.; Roe, R. Michael; Vargo, Edward L.; Vilcinskas, Andreas; Wang, Jun; Bornberg-Bauer, Erich; Korb, Judith; Zhang, Guojie; Liebig, Jurgen Published in: Nature Communications DOI: 10.1038/ncomms4636 Publication date: 2014 Document version Publisher's PDF, also known as Version of record Document license: CC BY-NC-SA Citation for published version (APA): Terrapon, N., Li, C., Robertson, H. M., Ji, L., Meng, X., Booth, W., Chen, Z., Childers, C. P., Glastad, K. M., Gokhale, K., Gowin, J., Gronenberg, W., Hermansen, R. A., Hu, H., Hunt, B. G., Huylmans, A. K., Khalil, S. M. S., Mitchell, R. D., Munoz-Torres, M. C., ... Liebig, J. (2014). Molecular traces of alternative social organization in a termite genome. Nature Communications, 5, [3636]. https://doi.org/10.1038/ncomms4636 Download date: 02. okt.. 2021 ARTICLE Received 17 Jul 2013 | Accepted 13 Mar 2014 | Published 20 May 2014 DOI: 10.1038/ncomms4636 OPEN Molecular traces of alternative social organization in a termite genome Nicolas Terrapon1,*,w, Cai Li2,3,*, Hugh M. Robertson4,LuJi2, Xuehong Meng2, Warren Booth5,w, Zhensheng Chen2, Christopher P. Childers6, Karl M. Glastad7, Kaustubh Gokhale8, Johannes Gowin9,w, Wulfila Gronenberg10, Russell A. Hermansen11, Haofu Hu2, Brendan G. Hunt7,w, Ann Kathrin Huylmans1,w, Sayed M.S. Khalil5,12, Robert D. Mitchell5, Monica C. Munoz-Torres13, Julie A. Mustard8, Hailin Pan2, Justin T. Reese6, Michael E. Scharf14, Fengming Sun2, Heiko Vogel15, Jin Xiao2, Wei Yang2, Zhikai Yang2, Zuoquan Yang2, Jiajian Zhou2, Jiwei Zhu5, Colin S. Brent16, Christine G. Elsik6,17, Michael A. D. Goodisman7, David A. Liberles11, R. Michael Roe5, Edward L. Vargo5, Andreas Vilcinskas18, Jun Wang2,19,20,21,22, Erich Bornberg-Bauer1, Judith Korb9,w, Guojie Zhang2,23 &Ju¨rgen Liebig8 Although eusociality evolved independently within several orders of insects, research into the molecular underpinnings of the transition towards social complexity has been confined primarily to Hymenoptera (for example, ants and bees). Here we sequence the genome and stage-specific transcriptomes of the dampwood termite Zootermopsis nevadensis (Blattodea) and compare them with similar data for eusocial Hymenoptera, to better identify commonalities and differences in achieving this significant transition. We show an expansion of genes related to male fertility, with upregulated gene expression in male reproductive individuals reflecting the profound differences in mating biology relative to the Hymenoptera. For several chemoreceptor families, we show divergent numbers of genes, which may correspond to the more claustral lifestyle of these termites. We also show similarities in the number and expression of genes related to caste determination mechanisms. Finally, patterns of DNA methylation and alternative splicing support a hypothesized epigenetic regulation of caste differentiation. 1 Institute for Evolution and Biodiversity, Westfa¨lische Wilhelms-Universita¨t, Mu¨nster D48149, Germany. 2 China National GeneBank, BGI-Shenzhen, Shenzhen 518083, China. 3 Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Voldgade 5-7, Copenhagen 1350, Denmark. 4 Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, USA. 5 Department of Entomology and W. M Keck Center for Behavioral Biology, North Carolina State University, Raleigh, North Carolina 27695, USA. 6 Division of Animal Sciences, University of Missouri, Columbia, Missouri 65211, USA. 7 School of Biology, Georgia Institute of Technology, Atlanta, Georgia 30332, USA. 8 School of Life Sciences, Arizona State University, Tempe, Arizona 85287, USA. 9 Behavioural Biology, University of Osnabru¨ck, Osnabru¨ck D49076, Germany. 10 Department of Neuroscience, University of Arizona, Tucson, Arizona 85721, USA. 11 Department of Molecular Biology, University of Wyoming, Laramie, Wyoming 82071, USA. 12 Department of Microbial Molecular Biology, Agricultural Genetic Engineering Research Institute, Giza 12619, Egypt. 13 Genomics Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA. 14 Department of Entomology, Purdue University, West Lafayette, Indiana 47907, USA. 15 Department of Entomology, Max Planck Institute for Chemical Ecology, Jena D-07745, Germany. 16 Arid Land Agricultural Research Center, United States Department of Agriculture, Maricopa, Arizona 85138, USA. 17 Division of Plant Sciences, University of Missouri, Columbia, Missouri 65211, USA. 18 Institut fu¨r Phytopathologie und Angewandte Zoologie, Justus-Liebig-Universita¨t Giessen, Giessen D35390, Germany. 19 Department of Biology, University of Copenhagen, Copenhagen DK-1165, Denmark. 20 Princess Al Jawhara Center of Excellence in the Research of Hereditary Disorders, King Abdulaziz University, 21589 Jeddah, Saudi Arabia. 21 Macau University of Science and Technology, Avenida Wai long, Taipa, Macau 999078, China. 22 Department of Medicine, University of Hong Kong, Hong Kong. 23 Centre for Social Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark. * These authors contributed equally to this work. w Present addresses: Architecture et Fonction des Macromole´cules Biologiques, Aix-Marseille Universite´, 13288 Marseille, France (N.T.); Department of Biological Sciences, The University of Tulsa, Tulsa, Oklahoma 74104, USA (W.B.); Evolutionary Biology & Ecology, University of Freiburg, D 79117 Freiburg, Germany (J.G. or J.K.); Department of Entomology, University of Georgia, Griffin Campus, Griffin, Georgia 30223 USA (B.G.H.); Department Biology II, Ludwig-Maximilians-University Munich, Planegg-Martinsried D-82152, Germany (A.K.H.). Correspondence and requests for materials should be addressed to J.K. (email: [email protected]) or to G.Z. (email: [email protected]) or to J.L. (email: [email protected]). NATURE COMMUNICATIONS | 5:3636 | DOI: 10.1038/ncomms4636 | www.nature.com/naturecommunications 1 & 2014 Macmillan Publishers Limited. All rights reserved. ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms4636 ermites are major pests of human structures, with an length of 740 kb and a coverage of 493.5 Mb, or 88% of the annual worldwide cost in damage and control estimated at genome (Methods; Supplementary Table 3). TUS$40 B1. However, in tropical habitats termites are Expression analysis of 25 transcriptomes of different sex, pivotal for ecosystem function and maintaining biodiversity2. developmental stage and caste (Fig. 1; Table 1; Supplementary Their complex societies have enhanced their environmental Note 2; Supplementary Tables 4 and 5) was used to highlight the adaptability, contributing to their success. Similar to eusocial molecular basis of caste and life stage evolution of Z. nevadensis. Hymenoptera (ants, some bees and wasps), termites are We identified gene families that are specifically overexpressed in characterized by a caste system in which a few individuals some castes or life stages (Fig. 2; Methods and Supplementary reproduce (queens and, in termites, kings) while the large Note 2.6; Supplementary Tables 6 and 7). Five of these families majority (workers and soldiers) perform tasks such as foraging, were significantly expanded in the termite lineage (see below). brood care or defence3. Despite these similarities to eusocial Finally, we observed caste-specific expression of orphan genes, Hymenoptera, termite societies have a phylogenetically distinct that is, genes without any identifiable orthologues, supporting the origin and divergent biological traits. They form a monophyletic recently predicted lineage-specific function of orphans15. clade nested within the Blattodea4, indicating a single origin of A total of 15,876 protein-coding genes are reported in OGSv2.2 termite eusociality, whereas eusociality independently evolved (Methods; Supplementary Figs 2 and 3; Supplementary Table 8) multiple times within the Hymenoptera3. Termites are with most (95.9%) of them supported by expression data from hemimetabolous, having several immature stages that become subsequent transcriptomes. We performed the annotation of the more adult like with each transition, while Hymenoptera have a non-coding RNA (ncRNA) and repeated elements (Methods; holometabolous development in which the final larval stage Supplementary Tables 9–12) and predicted protein sequences develops via a pupa into adulthood. Despite having distinct were functionally annotated using Interpro domains, gene lineages with different phylogenetic constraints, termites and ontology (GO) terms and the Kyoto Encyclopedia of Genes and eusocial Hymenoptera have evolved similar social and Genomes (KEGG) database (Methods). Pfam annotation yielded physiological traits. Understanding the selective pressures and 17,505 predicted domains (3,460 distinct families found in 52% of specific adaptations
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