Hemimetabolous genomes reveal molecular basis of termite eusociality

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 Thomas-Poulsen; Richard A. Gibbs; Coby Schal; Stephen Richards; Xavier Belles; Judith Korb; Erich Bornberg-Bauer

doi:10.1038/s41559-017-0459-1

Hemimetabolous genomes reveal molecular basis of termite eusociality

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-EzquerraLudovic 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 Thomas-Poulsen, Richard A. Gibbs, Coby Schal, Stephen Richards, Xavier Belles^*, Judith Korb, Erich Bornberg-Bauer

^*Corresponding author af dette arbejde

82 Citationer (Scopus)

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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.

Originalsprog	Engelsk
Tidsskrift	Nature Ecology and Evolution
Vol/bind	2
Udgave nummer	3
Sider (fra-til)	557-566
Antal sider	10
ISSN	2397-334X
DOI	https://doi.org/10.1038/s41559-017-0459-1
Status	Udgivet - 2018

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10.1038/s41559-017-0459-1

Hemimetabolous genomes reveal molecular basis of termite eusocialityForlagets udgivne version, 3,47 MB

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Harrison, M. C., Jongepier, E., Robertson, H. M., Arning, N., Bitard-Feildel, T., Chao, H., Childers, C. P., Dinh, H., Doddapaneni, H., Dugan, S., Gowin, J., Greiner, C., Han, Y., Hu, H., Hughes, D. S. T., Huylmans, A. K., Kemena, C., Kremer, L. P. M., Lee, S. L., ... Bornberg-Bauer, E. (2018). Hemimetabolous genomes reveal molecular basis of termite eusociality. Nature Ecology and Evolution, 2(3), 557-566. https://doi.org/10.1038/s41559-017-0459-1

Harrison, MC, Jongepier, E, Robertson, HM, Arning, N, Bitard-Feildel, T, Chao, H, Childers, CP, Dinh, H, Doddapaneni, H, Dugan, S, Gowin, J, Greiner, C, Han, Y, Hu, H, Hughes, DST, Huylmans, AK, Kemena, C, Kremer, LPM, Lee, SL, Lopez-Ezquerra, A, Mallet, L, Monroy-Kuhn, JM, Moser, A, Murali, SC, Muzny, DM, Otani, S, Piulachs, MD, Poelchau, M, Qu, J, Schaub, F, Wada-Katsumata, A, Worley, KC, Xie, Q, Ylla, G, Thomas-Poulsen, M, Gibbs, RA, Schal, C, Richards, S, Belles, X, Korb, J & Bornberg-Bauer, E 2018, 'Hemimetabolous genomes reveal molecular basis of termite eusociality', Nature Ecology and Evolution, bind 2, nr. 3, s. 557-566. https://doi.org/10.1038/s41559-017-0459-1

@article{029024f83ba9489ea175c2390c8d54d3,

title = "Hemimetabolous genomes reveal molecular basis of termite eusociality",

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.",

author = "Harrison, {Mark C.} and Evelien Jongepier and Robertson, {Hugh M.} and Nicolas Arning and Tristan Bitard-Feildel and Hsu Chao and Childers, {Christopher P.} and Huyen Dinh and Harshavardhan Doddapaneni and Shannon Dugan and Johannes Gowin and Carolin Greiner and Yi Han and Haofu Hu and Hughes, {Daniel S.T.} and Huylmans, {Ann Kathrin} and Carsten Kemena and Kremer, {Lukas P.M.} and Lee, {Sandra L.} and Alberto Lopez-Ezquerra and Ludovic Mallet and Monroy-Kuhn, {Jose M.} and Annabell Moser and Murali, {Shwetha C.} and Muzny, {Donna M.} and Saria Otani and Piulachs, {Maria Dolors} and Monica Poelchau and Jiaxin Qu and Florentine Schaub and Ayako Wada-Katsumata and Worley, {Kim C.} and Qiaolin Xie and Guillem Ylla and Michael Thomas-Poulsen and Gibbs, {Richard A.} and Coby Schal and Stephen Richards and Xavier Belles and Judith Korb and Erich Bornberg-Bauer",

year = "2018",

doi = "10.1038/s41559-017-0459-1",

language = "English",

volume = "2",

pages = "557--566",

journal = "Nature Ecology and Evolution",

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T1 - Hemimetabolous genomes reveal molecular basis of termite eusociality

AU - Harrison, Mark C.

AU - Jongepier, Evelien

AU - Robertson, Hugh M.

AU - Arning, Nicolas

AU - Bitard-Feildel, Tristan

AU - Chao, Hsu

AU - Childers, Christopher P.

AU - Dinh, Huyen

AU - Doddapaneni, Harshavardhan

AU - Dugan, Shannon

AU - Gowin, Johannes

AU - Greiner, Carolin

AU - Han, Yi

AU - Hu, Haofu

AU - Hughes, Daniel S.T.

AU - Huylmans, Ann Kathrin

AU - Kemena, Carsten

AU - Kremer, Lukas P.M.

AU - Lee, Sandra L.

AU - Lopez-Ezquerra, Alberto

AU - Mallet, Ludovic

AU - Monroy-Kuhn, Jose M.

AU - Moser, Annabell

AU - Murali, Shwetha C.

AU - Muzny, Donna M.

AU - Otani, Saria

AU - Piulachs, Maria Dolors

AU - Poelchau, Monica

AU - Qu, Jiaxin

AU - Schaub, Florentine

AU - Wada-Katsumata, Ayako

AU - Worley, Kim C.

AU - Xie, Qiaolin

AU - Ylla, Guillem

AU - Thomas-Poulsen, Michael

AU - Gibbs, Richard A.

AU - Schal, Coby

AU - Richards, Stephen

AU - Belles, Xavier

AU - Korb, Judith

AU - Bornberg-Bauer, Erich

PY - 2018

Y1 - 2018

N2 - 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.

AB - 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.

U2 - 10.1038/s41559-017-0459-1

DO - 10.1038/s41559-017-0459-1

M3 - Journal article

C2 - 29403074

AN - SCOPUS:85041598541

SN - 2397-334X

VL - 2

SP - 557

EP - 566

JO - Nature Ecology and Evolution

JF - Nature Ecology and Evolution

IS - 3

ER -

Hemimetabolous genomes reveal molecular basis of termite eusociality

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