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Title: The draft genome of a termite illuminates alternative social organization

Author
item TERRAPON, NICOLAS - Wilhelms University
item LI, CAI - China National Genebank
item ROBERTSON, HUGH - University Of Illinois
item JI, LU - China National Genebank
item MENG, XUEHONG - China National Genebank
item BOOTH, WARREN - North Carolina State University
item CHEN, ZHENSHENG - China National Genebank
item CHILDERS, CHRISTOPHER - Georgetown University
item GLASTAD, KARL - Georgia Institute Of Technology
item GOKHALE, KAUSTUBH - Arizona State University
item GOWIN, JOHANNES - University Of Freiburg
item GRONENBERG, WULFILA - University Of Arizona
item HERMANSEN, RUSSELL - University Of Wyoming
item HU, HAOFU - China National Genebank
item HUNT, BRENDAN - Georgia Institute Of Technology
item HUYLMANS, INA - Wilhelms University
item KHALIL, SAYED - North Carolina State University
item MITCHELL, ROBERT - North Carolina State University
item MUNOZ-TORRES, MONICA - Lawrence Berkeley National Laboratory
item MUSTARD, JULIE - Arizona State University
item PAN, HAILIN - China National Genebank
item REESE, JUSTIN - Georgetown University
item SCHARF, MICHAEL - Purdue University
item SUN, FENGMING - China National Genebank
item VOGEL, HEIKO - Max Planck Society
item XIAO, JIN - China National Genebank
item YANG, WEI - China National Genebank
item YANG, ZHIKAI - China National Genebank
item YANG, ZUOQUAN - China National Genebank
item ZHOU, JIAJIAN - China National Genebank
item ZHU, JIWEI - University Of Illinois
item Brent, Colin
item ELSIK, CHRISTINE - Georgetown University
item GOODISMAN, MICHAEL - Georgia Institute Of Technology
item LIBERLES, DAVID - University Of Wyoming
item ROE, R. - North Carolina State University
item VARGO, EDWARD - North Carolina State University
item VILCINSKAS, ANDREAS - Justus-Liebig University
item WANG, JUN - China National Genebank
item BORNBERG-BAUER, ERICH - Wilhelms University
item KORB, JUDITH - University Of Freiburg
item ZHANG, GUOJIE - China National Genebank
item LIEBIG, JURGEN - Arizona State University

Submitted to: Nature Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/13/2014
Publication Date: 5/20/2014
Citation: 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, I., Khalil, S.M., Mitchell, R., Munoz-Torres, M.C., Mustard, J., Pan, H., Reese, J.T., Scharf, M.E., Sun, F., Vogel, H., Xiao, J., Yang, W., Yang, Z., Yang, Z., Zhou, J., Zhu, J., Brent, C.S., Elsik, C.G., Goodisman, M.A., Liberles, D.A., Roe, R.M., Vargo, E.L., Vilcinskas, A., Wang, J., Bornberg-Bauer, E., Korb, J., Zhang, G., Liebig, J. 2014. The draft genome of a termite illuminates alternative social organization. Nature Communications. 5:3636.

Interpretive Summary: Termites have substantial economic and ecological impact worldwide. They are also the oldest organisms living in complex social colonies in which groups of individuals, or castes, develop different body forms and perform different functions. Termites evolved their social life-style independently of that of other social insects such as ants and honey bees. The mechanism that underlies this complex caste system is regulated by the termite’s genome, the sum of its genetic material (genes) that contains the code directing its growth and development. Decoding, or sequencing, the genome can provide important insights into the evolution of a species and, when compared with the genomes of other species, a relative estimate of relatedness. Here we report the first genome sequence for a termite, Zootermopsis nevadensis. This is the oldest insect lineage for which a genome sequence has been produced. Analyses indicated differences between termite castes (e.g., queens, workers, solders) in the numbers of genes in specific gene families (representing gene duplications) and in the extent to which those genes were used, or expressed. Therefore, these genetic differences appear important in the regulation of termite reproduction, regulation of caste development, and organization of the termite society. Genes typically involved in the production and perception of chemicals used for communication within the colony were reduced in number compared with similar genes in social bees and ants. This suggests a limited role of chemical communication in the early evolution of termite societies. Evidence also suggested the control of termite caste development might be regulated not just by the environment, but also by permanent alterations to the genome that determine which genes are expressed. These results provide insights into the evolution of termite societies and facilitate comparative studies with other insects.

Technical Abstract: Termites have substantial economic and ecological impact worldwide. They are also the oldest organisms living in complex societies, having evolved a caste system independent of that of eusocial Hymenoptera (ants, bees and wasps). Here we provide the first genome sequence for a termite, Zootermopsis nevadensis (Blattodea), representing the phylogenetically deepest rooted insect genome to date. Lineage-specific expansion of several protein families and various gene duplications are associated with differential expression between castes, indicating potential roles in reproduction, caste regulation and social organization. Olfactory genes show patterns of expansion and contraction that contrast with those in social hymenoptera, and suggest a limited role in early termite social evolution. Predicted DNA methylation levels are the highest found in insects to date and their association with alternative splicing events suggests epigenetic regulation of caste differentiation. The results illuminate the impact of social evolution on diverse traits and facilitate comparative studies.