Molecular traces of alternative social organization in a termite genome

Nicolas Terrapon; Cai Li; Hugh M. Robertson; Lu Ji; Xuehong Meng; Warren Booth; Zhensheng Chen; Christopher P. Childers; Karl M. Glastad; Kaustubh Gokhale; Johannes Gowin; Wulfila Gronenberg; Russell A. Hermansen; Haofu Hu; Brendan G. Hunt; Ann Kathrin Huylmans; Sayed M S Khalil; Robert D. Mitchell; Monica C. Munoz-Torres; Julie A. Mustard; Hailin Pan; Justin T. Reese; Michael E. Scharf; Fengming Sun; Heiko Vogel; Jin Xiao; Wei Yang; Zhikai Yang; Zuoquan Yang; Jiajian Zhou; Jiwei Zhu; Colin S. Brent; Christine G. Elsik; Michael A D Goodisman; David A. Liberles; R. Michael Roe; Edward L. Vargo; Andreas Vilcinskas; Jun Wang; Erich Bornberg-Bauer; Judith Korb; Guojie Zhang; Juergen Liebig

doi:10.1038/ncomms4636

Molecular traces of alternative social organization in a termite genome

Nicolas Terrapon, Cai Li, Hugh M. Robertson, Lu Ji, Xuehong Meng, Warren Booth, Zhensheng Chen, Christopher P. Childers, Karl M. Glastad, Kaustubh Gokhale, Johannes Gowin, Wulfila Gronenberg, Russell A. Hermansen, Haofu Hu, Brendan G. Hunt, Ann Kathrin Huylmans, Sayed M S Khalil, Robert D. Mitchell, Monica C. Munoz-Torres, Julie A. MustardHailin Pan, Justin T. Reese, Michael E. Scharf, Fengming Sun, Heiko Vogel, Jin Xiao, Wei Yang, Zhikai Yang, Zuoquan Yang, Jiajian Zhou, Jiwei Zhu, Colin S. Brent, Christine G. Elsik, Michael A D Goodisman, David A. Liberles, R. Michael Roe, Edward L. Vargo, Andreas Vilcinskas, Jun Wang, Erich Bornberg-Bauer, Judith Korb, Guojie Zhang, Juergen Liebig

Life Sciences, School of (SOLS)

Research output: Contribution to journal › Article › peer-review

290 Scopus citations

Abstract

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.

Original language	English (US)
Article number	3636
Journal	Nature communications
Volume	5
DOIs	https://doi.org/10.1038/ncomms4636
State	Published - May 20 2014

ASJC Scopus subject areas

General Physics and Astronomy
General Chemistry
General Biochemistry, Genetics and Molecular Biology

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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, Article 3636. https://doi.org/10.1038/ncomms4636

Terrapon, N, Li, C, Robertson, HM, Ji, L, Meng, X, Booth, W, Chen, Z, Childers, CP, Glastad, KM, Gokhale, K, Gowin, J, Gronenberg, W, Hermansen, RA, Hu, H, Hunt, BG, Huylmans, AK, Khalil, SMS, Mitchell, RD, Munoz-Torres, MC, Mustard, JA, Pan, H, Reese, JT, Scharf, ME, Sun, F, Vogel, H, Xiao, J, Yang, W, Yang, Z, Yang, Z, Zhou, J, Zhu, J, Brent, CS, Elsik, CG, Goodisman, MAD, Liberles, DA, Roe, RM, Vargo, EL, Vilcinskas, A, Wang, J, Bornberg-Bauer, E, Korb, J, Zhang, G & Liebig, J 2014, 'Molecular traces of alternative social organization in a termite genome', Nature communications, vol. 5, 3636. https://doi.org/10.1038/ncomms4636

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title = "Molecular traces of alternative social organization in a termite genome",

abstract = "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.",

author = "Nicolas Terrapon and Cai Li and Robertson, {Hugh M.} and Lu Ji and Xuehong Meng and Warren Booth and Zhensheng Chen and Childers, {Christopher P.} and Glastad, {Karl M.} and Kaustubh Gokhale and Johannes Gowin and Wulfila Gronenberg and Hermansen, {Russell A.} and Haofu Hu and Hunt, {Brendan G.} and Huylmans, {Ann Kathrin} and Khalil, {Sayed M S} and Mitchell, {Robert D.} and Munoz-Torres, {Monica C.} and Mustard, {Julie A.} and Hailin Pan and Reese, {Justin T.} and Scharf, {Michael E.} and Fengming Sun and Heiko Vogel and Jin Xiao and Wei Yang and Zhikai Yang and Zuoquan Yang and Jiajian Zhou and Jiwei Zhu and Brent, {Colin S.} and Elsik, {Christine G.} and Goodisman, {Michael A D} and Liberles, {David A.} and Roe, {R. Michael} and Vargo, {Edward L.} and Andreas Vilcinskas and Jun Wang and Erich Bornberg-Bauer and Judith Korb and Guojie Zhang and Juergen Liebig",

note = "Funding Information: We thank the administrators of the Pebble Beach Company for permission to collect termites and Navdeep Mutti for initial help in RNA and DNA sampling. This work was supported by the Agriculture and Food Research Initiative Competitive Grant number 2007-35302-18172 from the USDA National Institute of Food and Agriculture to J.L. and C.S.B.; and a research grant from the Deutschen Forschungsgemeinschaft (DFG) to J.K. (KO1895/6) and LOEWE Research Focus {\textquoteleft}Insect Biotechnology{\textquoteright} to A.V. Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture. USDA is an equal opportunity provider and employer.",

year = "2014",

month = may,

day = "20",

doi = "10.1038/ncomms4636",

language = "English (US)",

volume = "5",

journal = "Nature communications",

issn = "2041-1723",

publisher = "Nature Publishing Group",

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TY - JOUR

T1 - Molecular traces of alternative social organization in a termite genome

AU - Terrapon, Nicolas

AU - Li, Cai

AU - Robertson, Hugh M.

AU - Ji, Lu

AU - Meng, Xuehong

AU - Booth, Warren

AU - Chen, Zhensheng

AU - Childers, Christopher P.

AU - Glastad, Karl M.

AU - Gokhale, Kaustubh

AU - Gowin, Johannes

AU - Gronenberg, Wulfila

AU - Hermansen, Russell A.

AU - Hu, Haofu

AU - Hunt, Brendan G.

AU - Huylmans, Ann Kathrin

AU - Khalil, Sayed M S

AU - Mitchell, Robert D.

AU - Munoz-Torres, Monica C.

AU - Mustard, Julie A.

AU - Pan, Hailin

AU - Reese, Justin T.

AU - Scharf, Michael E.

AU - Sun, Fengming

AU - Vogel, Heiko

AU - Xiao, Jin

AU - Yang, Wei

AU - Yang, Zhikai

AU - Yang, Zuoquan

AU - Zhou, Jiajian

AU - Zhu, Jiwei

AU - Brent, Colin S.

AU - Elsik, Christine G.

AU - Goodisman, Michael A D

AU - Liberles, David A.

AU - Roe, R. Michael

AU - Vargo, Edward L.

AU - Vilcinskas, Andreas

AU - Wang, Jun

AU - Bornberg-Bauer, Erich

AU - Korb, Judith

AU - Zhang, Guojie

AU - Liebig, Juergen

N1 - Funding Information: We thank the administrators of the Pebble Beach Company for permission to collect termites and Navdeep Mutti for initial help in RNA and DNA sampling. This work was supported by the Agriculture and Food Research Initiative Competitive Grant number 2007-35302-18172 from the USDA National Institute of Food and Agriculture to J.L. and C.S.B.; and a research grant from the Deutschen Forschungsgemeinschaft (DFG) to J.K. (KO1895/6) and LOEWE Research Focus ‘Insect Biotechnology’ to A.V. Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture. USDA is an equal opportunity provider and employer.

PY - 2014/5/20

Y1 - 2014/5/20

N2 - 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.

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Molecular traces of alternative social organization in a termite genome

Abstract

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