Insights into social insects from the genome of the honeybee Apis mellifera

George M. Weinstock; Gene E. Robinson; Richard A. Gibbs; Kim C. Worley; Jay D. Evans; Ryszard Maleszka; Hugh M. Robertson; Daniel B. Weaver; Martin Beye; Peer Bork; Christine G. Elsik; Klaus Hartfelder; Greg J. Hunt; Evgeny M. Zdobnov; Gro V. Amdam; Mrcia M.G. Bitondi; Anita M. Collins; Alexandre S. Cristino; H. Michael G. Lattorff; Carlos H. Lobo; Robin F.A. Moritz; Francis M.F. Nunes; Robert E. Page; Zilá L.P. Simões; Diana Wheeler; Piero Carninci; Shiro Fukuda; Yoshihide Hayashizaki; Chikatoshi Kai; Jun Kawai; Naoko Sakazume; Daisuke Sasaki; Michihira Tagami; Stefan Albert; Geert Baggerman; Kyle T. Beggs; Guy Bloch; Giuseppe Cazzamali; Mira Cohen; Mark David Drapeau; Dorothea Eisenhardt; Christine Emore; Michael A. Ewing; Susan E. Fahrbach; Sylvain Forêt; Cornelis J.P. Grimmelikhuijzen; Frank Hauser; Amanda B. Hummon; Jurgen Huybrechts; Andrew K. Jones; Tatsuhiko Kadowaki; Noam Kaplan; Robert Kucharski; Grard Leboulle; Michal Linial; J. Troy Littleton; Alison R. Mercer; Timothy A. Richmond; Sandra L. Rodriguez-Zas; Elad B. Rubin; David B. Sattelle; David Schlipalius; Liliane Schoofs; Yair Shemesh; Jonathan V. Sweedler; Rodrigo Velarde; Peter Verleyen; Evy Vierstraete; Michael R. Williamson; Seth A. Ament; Susan J. Brown; Miguel Corona; Peter K. Dearden; W. Augustine Dunn; Michelle M. Elekonich; Tomoko Fujiyuki; Irene Gattermeier; Tanja Gempe; Martin Hasselmann; Eriko Kage; Azusa Kamikouchi; Takeo Kubo; Takekazu Kunieda; Marcé Lorenzen; Natalia V. Milshina; Mizue Morioka; Kazuaki Ohashi; Ross Overbeek; Christian A. Ross; Morten Schioett; Teresa Shippy; Hideaki Takeuchi; Amy L. Toth; Judith H. Willis; Megan J. Wilson; Karl H.J. Gordon; Ivica Letunic; Kevin Hackett; Jane Peterson; Adam Felsenfeld; Mark Guyer; Michel Solignac; Richa Agarwala; Jean Marie Cornuet; Monique Monnerot; Florence Mougel; Justin T. Reese; Dominique Vautrin; Joseph J. Gillespie; Jamie J. Cannone; Robin R. Gutell; J. Spencer Johnston; Michael B. Eisen; Venky N. Iyer; Vivek Iyer; Peter Kosarev; Aaron J. Mackey; Victor Solovyev; Alexandre Souvorov; Katherine A. Aronstein; Katarina Bilikova; Yan Ping Chen; Andrew G. Clark; Laura I. Decanini; William M. Gelbart; Charles Hetru; Dan Hultmark; Jean Luc Imler; Haobo Jiang; Michael Kanost; Kiyoshi Kimura; Brian P. Lazzaro; Dawn L. Lopez; Jozef Simuth; Graham J. Thompson; Zhen Zou; Pieter De Jong; Erica Sodergren; Miklós Csurös; Aleksandar Milosavljevic; Kazutoyo Osoegawa; Stephen Richards; Chung Li Shu; Laurent Duret; Eran Elhaik; Dan Graur; Juan M. Anzola; Kathryn S. Campbell; Kevin L. Childs; Derek Collinge; Madeline A. Crosby; C. Michael Dickens; L. Sian Grametes; Christina M. Grozinger; Peter L. Jones; Mireia Jorda; Xu Ling; Beverly B. Matthews; Jonathan Miller; Craig Mizzen; Miguel A. Peinado; Jeffrey G. Reid; Susan M. Russo; Andrew J. Schroeder; Susan E. St. Pierre; Ying Wang; Pinglei Zhou; Huaiyang Jiang; Paul Kitts; Barbara Ruef; Anand Venkatraman; Lan Zhang; Gildardo Aquino-Perez; Charles W. Whitfield; Susanta K. Behura; Stewart H. Berlocher; Walter S. Sheppard; Deborah R. Smith; Andrew V. Suarez; Neil D. Tsutsui; Xuehong Wei; David Wheeler; Paul Havlak; Bingshan Li; Yue Liu; Angela Jovilet; Sandra Lee; Lynne V. Nazareth; Ling Ling Pu; Rachel Thorn; Viktor Stolc; Thomas Newman; Manoj Samanta; Waraporn A. Tongprasit; Charles Claudianos; May R. Berenbaum; Sunita Biswas; Dirk C. De Graaf; Rene Feyereisen; Reed M. Johnson; John G. Oakeshott; Hilary Ranson; Mary A. Schuler; Donna Muzny; Joseph Chacko; Clay Davis; Huyen Dinh; Rachel Gill; Judith Hernandez; Sandra Hines; Jennifer Hume; La Ronda Jackson; Christie Kovar; Lora Lewis; George Miner; Margaret Morgan; Ngoc Nguyen; Geoffrey Okwuonu; Heidi Paul; Jireh Santibanez; Glenford Savery; Amanda Svatek; Donna Villasana; Rita Wright

doi:10.1038/nature05260

Insights into social insects from the genome of the honeybee Apis mellifera

George M. Weinstock^*, Gene E. Robinson, Richard A. Gibbs, Kim C. Worley, Jay D. Evans, Ryszard Maleszka, Hugh M. Robertson, Daniel B. Weaver, Martin Beye, Peer Bork, Christine G. Elsik, Klaus Hartfelder, Greg J. Hunt, Evgeny M. Zdobnov, Gro V. Amdam, Mrcia M.G. Bitondi, Anita M. Collins, Alexandre S. Cristino, H. Michael G. Lattorff, Carlos H. LoboRobin F.A. Moritz, Francis M.F. Nunes, Robert E. Page, Zilá L.P. Simões, Diana Wheeler, Piero Carninci, Shiro Fukuda, Yoshihide Hayashizaki, Chikatoshi Kai, Jun Kawai, Naoko Sakazume, Daisuke Sasaki, Michihira Tagami, Stefan Albert, Geert Baggerman, Kyle T. Beggs, Guy Bloch, Giuseppe Cazzamali, Mira Cohen, Mark David Drapeau, Dorothea Eisenhardt, Christine Emore, Michael A. Ewing, Susan E. Fahrbach, Sylvain Forêt, Cornelis J.P. Grimmelikhuijzen, Frank Hauser, Amanda B. Hummon, Jurgen Huybrechts, Andrew K. Jones, Tatsuhiko Kadowaki, Noam Kaplan, Robert Kucharski, Grard Leboulle, Michal Linial, J. Troy Littleton, Alison R. Mercer, Timothy A. Richmond, Sandra L. Rodriguez-Zas, Elad B. Rubin, David B. Sattelle, David Schlipalius, Liliane Schoofs, Yair Shemesh, Jonathan V. Sweedler, Rodrigo Velarde, Peter Verleyen, Evy Vierstraete, Michael R. Williamson, Seth A. Ament, Susan J. Brown, Miguel Corona, Peter K. Dearden, W. Augustine Dunn, Michelle M. Elekonich, Tomoko Fujiyuki, Irene Gattermeier, Tanja Gempe, Martin Hasselmann, Eriko Kage, Azusa Kamikouchi, Takeo Kubo, Takekazu Kunieda, Marcé Lorenzen, Natalia V. Milshina, Mizue Morioka, Kazuaki Ohashi, Ross Overbeek, Christian A. Ross, Morten Schioett, Teresa Shippy, Hideaki Takeuchi, Amy L. Toth, Judith H. Willis, Megan J. Wilson, Karl H.J. Gordon, Ivica Letunic, Kevin Hackett, Jane Peterson, Adam Felsenfeld, Mark Guyer, Michel Solignac, Richa Agarwala, Jean Marie Cornuet, Monique Monnerot, Florence Mougel, Justin T. Reese, Dominique Vautrin, Joseph J. Gillespie, Jamie J. Cannone, Robin R. Gutell, J. Spencer Johnston, Michael B. Eisen, Venky N. Iyer, Vivek Iyer, Peter Kosarev, Aaron J. Mackey, Victor Solovyev, Alexandre Souvorov, Katherine A. Aronstein, Katarina Bilikova, Yan Ping Chen, Andrew G. Clark, Laura I. Decanini, William M. Gelbart, Charles Hetru, Dan Hultmark, Jean Luc Imler, Haobo Jiang, Michael Kanost, Kiyoshi Kimura, Brian P. Lazzaro, Dawn L. Lopez, Jozef Simuth, Graham J. Thompson, Zhen Zou, Pieter De Jong, Erica Sodergren, Miklós Csurös, Aleksandar Milosavljevic, Kazutoyo Osoegawa, Stephen Richards, Chung Li Shu, Laurent Duret, Eran Elhaik, Dan Graur, Juan M. Anzola, Kathryn S. Campbell, Kevin L. Childs, Derek Collinge, Madeline A. Crosby, C. Michael Dickens, L. Sian Grametes, Christina M. Grozinger, Peter L. Jones, Mireia Jorda, Xu Ling, Beverly B. Matthews, Jonathan Miller, Craig Mizzen, Miguel A. Peinado, Jeffrey G. Reid, Susan M. Russo, Andrew J. Schroeder, Susan E. St. Pierre, Ying Wang, Pinglei Zhou, Huaiyang Jiang, Paul Kitts, Barbara Ruef, Anand Venkatraman, Lan Zhang, Gildardo Aquino-Perez, Charles W. Whitfield, Susanta K. Behura, Stewart H. Berlocher, Walter S. Sheppard, Deborah R. Smith, Andrew V. Suarez, Neil D. Tsutsui, Xuehong Wei, David Wheeler, Paul Havlak, Bingshan Li, Yue Liu, Angela Jovilet, Sandra Lee, Lynne V. Nazareth, Ling Ling Pu, Rachel Thorn, Viktor Stolc, Thomas Newman, Manoj Samanta, Waraporn A. Tongprasit, Charles Claudianos, May R. Berenbaum, Sunita Biswas, Dirk C. De Graaf, Rene Feyereisen, Reed M. Johnson, John G. Oakeshott, Hilary Ranson, Mary A. Schuler, Donna Muzny, Joseph Chacko, Clay Davis, Huyen Dinh, Rachel Gill, Judith Hernandez, Sandra Hines, Jennifer Hume, La Ronda Jackson, Christie Kovar, Lora Lewis, George Miner, Margaret Morgan, Ngoc Nguyen, Geoffrey Okwuonu, Heidi Paul, Jireh Santibanez, Glenford Savery, Amanda Svatek, Donna Villasana, Rita Wright

^*Corresponding author for this work

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

1566 Scopus citations

Abstract

Here we report the genome sequence of the honeybee Apis mellifera, a key model for social behaviour and essential to global ecology through pollination. Compared with other sequenced insect genomes, the A. mellifera genome has high A+T and CpG contents, lacks major transposon families, evolves more slowly, and is more similar to vertebrates for circadian rhythm, RNA interference and DNA methylation genes, among others. Furthermore, A. mellifera has fewer genes for innate immunity, detoxification enzymes, cuticle-forming proteins and gustatory receptors, more genes for odorant receptors, and novel genes for nectar and pollen utilization, consistent with its ecology and social organization. Compared to Drosophila, genes in early developmental pathways differ in Apis, whereas similarities exist for functions that differ markedly, such as sex determination, brain function and behaviour. Population genetics suggests a novel African origin for the species A. mellifera and insights into whether Africanized bees spread throughout the New World via hybridization or displacement.

Original language	English
Pages (from-to)	931-949
Number of pages	19
Journal	Nature
Volume	443
Issue number	7114
DOIs	https://doi.org/10.1038/nature05260
State	Published - 26 Oct 2006

Bibliographical note

Funding Information:
Acknowledgements Work at the BCM-HGSC was supported by grants from the NHGRI and USDA. BAC and fosmid Library construction was supported by a subcontract from a grant awarded to J.S.J., organized by D.B.W. (President, Bee Weaver Apiaries, Inc.). Fgenesh and Fgenesh11 analysis was donated by Softberry. Other support was received from NIH NIAID (H.M.R.), NRI Functional Genomics (G.E.R.) and Illinois Sociogenomics Initiative (G.E.R.), NSF (M.M.E.; B. Schatz, UIUC), Intramural Research Program NIH NLM (R.A.), USDA-NRI, California Beekeepers Assoc., Texas Beekeepers Assoc., T. W. Burleson and Son, Inc., TAMU, NIH NLM (J.G.R.), RSNZ Marsden Fund (P.K.D.), Danish Research Agency, Carlsberg Foundation, Novo Nordisk Foundation, and DFG. The authors thank the production staff at the HGSC.

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10.1038/nature05260

Cite this

Weinstock, G. M., Robinson, G. E., Gibbs, R. A., Worley, K. C., Evans, J. D., Maleszka, R., Robertson, H. M., Weaver, D. B., Beye, M., Bork, P., Elsik, C. G., Hartfelder, K., Hunt, G. J., Zdobnov, E. M., Amdam, G. V., Bitondi, M. M. G., Collins, A. M., Cristino, A. S., Lattorff, H. M. G., ... Wright, R. (2006). Insights into social insects from the genome of the honeybee Apis mellifera. Nature, 443(7114), 931-949. https://doi.org/10.1038/nature05260

@article{f63be9d863ea4de39273f61b0c994f9d,

title = "Insights into social insects from the genome of the honeybee Apis mellifera",

abstract = "Here we report the genome sequence of the honeybee Apis mellifera, a key model for social behaviour and essential to global ecology through pollination. Compared with other sequenced insect genomes, the A. mellifera genome has high A+T and CpG contents, lacks major transposon families, evolves more slowly, and is more similar to vertebrates for circadian rhythm, RNA interference and DNA methylation genes, among others. Furthermore, A. mellifera has fewer genes for innate immunity, detoxification enzymes, cuticle-forming proteins and gustatory receptors, more genes for odorant receptors, and novel genes for nectar and pollen utilization, consistent with its ecology and social organization. Compared to Drosophila, genes in early developmental pathways differ in Apis, whereas similarities exist for functions that differ markedly, such as sex determination, brain function and behaviour. Population genetics suggests a novel African origin for the species A. mellifera and insights into whether Africanized bees spread throughout the New World via hybridization or displacement.",

author = "Weinstock, {George M.} and Robinson, {Gene E.} and Gibbs, {Richard A.} and Worley, {Kim C.} and Evans, {Jay D.} and Ryszard Maleszka and Robertson, {Hugh M.} and Weaver, {Daniel B.} and Martin Beye and Peer Bork and Elsik, {Christine G.} and Klaus Hartfelder and Hunt, {Greg J.} and Zdobnov, {Evgeny M.} and Amdam, {Gro V.} and Bitondi, {Mrcia M.G.} and Collins, {Anita M.} and Cristino, {Alexandre S.} and Lattorff, {H. Michael G.} and Lobo, {Carlos H.} and Moritz, {Robin F.A.} and Nunes, {Francis M.F.} and Page, {Robert E.} and Sim{\~o}es, {Zil{\'a} L.P.} and Diana Wheeler and Piero Carninci and Shiro Fukuda and Yoshihide Hayashizaki and Chikatoshi Kai and Jun Kawai and Naoko Sakazume and Daisuke Sasaki and Michihira Tagami and Stefan Albert and Geert Baggerman and Beggs, {Kyle T.} and Guy Bloch and Giuseppe Cazzamali and Mira Cohen and Drapeau, {Mark David} and Dorothea Eisenhardt and Christine Emore and Ewing, {Michael A.} and Fahrbach, {Susan E.} and Sylvain For{\^e}t and Grimmelikhuijzen, {Cornelis J.P.} and Frank Hauser and Hummon, {Amanda B.} and Jurgen Huybrechts and Jones, {Andrew K.} and Tatsuhiko Kadowaki and Noam Kaplan and Robert Kucharski and Grard Leboulle and Michal Linial and Littleton, {J. Troy} and Mercer, {Alison R.} and Richmond, {Timothy A.} and Rodriguez-Zas, {Sandra L.} and Rubin, {Elad B.} and Sattelle, {David B.} and David Schlipalius and Liliane Schoofs and Yair Shemesh and Sweedler, {Jonathan V.} and Rodrigo Velarde and Peter Verleyen and Evy Vierstraete and Williamson, {Michael R.} and Ament, {Seth A.} and Brown, {Susan J.} and Miguel Corona and Dearden, {Peter K.} and Dunn, {W. Augustine} and Elekonich, {Michelle M.} and Tomoko Fujiyuki and Irene Gattermeier and Tanja Gempe and Martin Hasselmann and Eriko Kage and Azusa Kamikouchi and Takeo Kubo and Takekazu Kunieda and Marc{\'e} Lorenzen and Milshina, {Natalia V.} and Mizue Morioka and Kazuaki Ohashi and Ross Overbeek and Ross, {Christian A.} and Morten Schioett and Teresa Shippy and Hideaki Takeuchi and Toth, {Amy L.} and Willis, {Judith H.} and Wilson, {Megan J.} and Gordon, {Karl H.J.} and Ivica Letunic and Kevin Hackett and Jane Peterson and Adam Felsenfeld and Mark Guyer and Michel Solignac and Richa Agarwala and Cornuet, {Jean Marie} and Monique Monnerot and Florence Mougel and Reese, {Justin T.} and Dominique Vautrin and Gillespie, {Joseph J.} and Cannone, {Jamie J.} and Gutell, {Robin R.} and Johnston, {J. Spencer} and Eisen, {Michael B.} and Iyer, {Venky N.} and Vivek Iyer and Peter Kosarev and Mackey, {Aaron J.} and Victor Solovyev and Alexandre Souvorov and Aronstein, {Katherine A.} and Katarina Bilikova and Chen, {Yan Ping} and Clark, {Andrew G.} and Decanini, {Laura I.} and Gelbart, {William M.} and Charles Hetru and Dan Hultmark and Imler, {Jean Luc} and Haobo Jiang and Michael Kanost and Kiyoshi Kimura and Lazzaro, {Brian P.} and Lopez, {Dawn L.} and Jozef Simuth and Thompson, {Graham J.} and Zhen Zou and {De Jong}, Pieter and Erica Sodergren and Mikl{\'o}s Csur{\"o}s and Aleksandar Milosavljevic and Kazutoyo Osoegawa and Stephen Richards and Shu, {Chung Li} and Laurent Duret and Eran Elhaik and Dan Graur and Anzola, {Juan M.} and Campbell, {Kathryn S.} and Childs, {Kevin L.} and Derek Collinge and Crosby, {Madeline A.} and Dickens, {C. Michael} and Grametes, {L. Sian} and Grozinger, {Christina M.} and Jones, {Peter L.} and Mireia Jorda and Xu Ling and Matthews, {Beverly B.} and Jonathan Miller and Craig Mizzen and Peinado, {Miguel A.} and Reid, {Jeffrey G.} and Russo, {Susan M.} and Schroeder, {Andrew J.} and {St. Pierre}, {Susan E.} and Ying Wang and Pinglei Zhou and Huaiyang Jiang and Paul Kitts and Barbara Ruef and Anand Venkatraman and Lan Zhang and Gildardo Aquino-Perez and Whitfield, {Charles W.} and Behura, {Susanta K.} and Berlocher, {Stewart H.} and Sheppard, {Walter S.} and Smith, {Deborah R.} and Suarez, {Andrew V.} and Tsutsui, {Neil D.} and Xuehong Wei and David Wheeler and Paul Havlak and Bingshan Li and Yue Liu and Angela Jovilet and Sandra Lee and Nazareth, {Lynne V.} and Pu, {Ling Ling} and Rachel Thorn and Viktor Stolc and Thomas Newman and Manoj Samanta and Tongprasit, {Waraporn A.} and Charles Claudianos and Berenbaum, {May R.} and Sunita Biswas and {De Graaf}, {Dirk C.} and Rene Feyereisen and Johnson, {Reed M.} and Oakeshott, {John G.} and Hilary Ranson and Schuler, {Mary A.} and Donna Muzny and Joseph Chacko and Clay Davis and Huyen Dinh and Rachel Gill and Judith Hernandez and Sandra Hines and Jennifer Hume and Jackson, {La Ronda} and Christie Kovar and Lora Lewis and George Miner and Margaret Morgan and Ngoc Nguyen and Geoffrey Okwuonu and Heidi Paul and Jireh Santibanez and Glenford Savery and Amanda Svatek and Donna Villasana and Rita Wright",

note = "Funding Information: Acknowledgements Work at the BCM-HGSC was supported by grants from the NHGRI and USDA. BAC and fosmid Library construction was supported by a subcontract from a grant awarded to J.S.J., organized by D.B.W. (President, Bee Weaver Apiaries, Inc.). Fgenesh and Fgenesh11 analysis was donated by Softberry. Other support was received from NIH NIAID (H.M.R.), NRI Functional Genomics (G.E.R.) and Illinois Sociogenomics Initiative (G.E.R.), NSF (M.M.E.; B. Schatz, UIUC), Intramural Research Program NIH NLM (R.A.), USDA-NRI, California Beekeepers Assoc., Texas Beekeepers Assoc., T. W. Burleson and Son, Inc., TAMU, NIH NLM (J.G.R.), RSNZ Marsden Fund (P.K.D.), Danish Research Agency, Carlsberg Foundation, Novo Nordisk Foundation, and DFG. The authors thank the production staff at the HGSC.",

year = "2006",

month = oct,

day = "26",

doi = "10.1038/nature05260",

language = "אנגלית",

volume = "443",

pages = "931--949",

journal = "Nature",

issn = "0028-0836",

publisher = "Nature Research",

number = "7114",

}

Weinstock, GM, Robinson, GE, Gibbs, RA, Worley, KC, Evans, JD, Maleszka, R, Robertson, HM, Weaver, DB, Beye, M, Bork, P, Elsik, CG, Hartfelder, K, Hunt, GJ, Zdobnov, EM, Amdam, GV, Bitondi, MMG, Collins, AM, Cristino, AS, Lattorff, HMG, Lobo, CH, Moritz, RFA, Nunes, FMF, Page, RE, Simões, ZLP, Wheeler, D, Carninci, P, Fukuda, S, Hayashizaki, Y, Kai, C, Kawai, J, Sakazume, N, Sasaki, D, Tagami, M, Albert, S, Baggerman, G, Beggs, KT, Bloch, G, Cazzamali, G, Cohen, M, Drapeau, MD, Eisenhardt, D, Emore, C, Ewing, MA, Fahrbach, SE, Forêt, S, Grimmelikhuijzen, CJP, Hauser, F, Hummon, AB, Huybrechts, J, Jones, AK, Kadowaki, T, Kaplan, N, Kucharski, R, Leboulle, G, Linial, M, Littleton, JT, Mercer, AR, Richmond, TA, Rodriguez-Zas, SL, Rubin, EB, Sattelle, DB, Schlipalius, D, Schoofs, L, Shemesh, Y, Sweedler, JV, Velarde, R, Verleyen, P, Vierstraete, E, Williamson, MR, Ament, SA, Brown, SJ, Corona, M, Dearden, PK, Dunn, WA, Elekonich, MM, Fujiyuki, T, Gattermeier, I, Gempe, T, Hasselmann, M, Kage, E, Kamikouchi, A, Kubo, T, Kunieda, T, Lorenzen, M, Milshina, NV, Morioka, M, Ohashi, K, Overbeek, R, Ross, CA, Schioett, M, Shippy, T, Takeuchi, H, Toth, AL, Willis, JH, Wilson, MJ, Gordon, KHJ, Letunic, I, Hackett, K, Peterson, J, Felsenfeld, A, Guyer, M, Solignac, M, Agarwala, R, Cornuet, JM, Monnerot, M, Mougel, F, Reese, JT, Vautrin, D, Gillespie, JJ, Cannone, JJ, Gutell, RR, Johnston, JS, Eisen, MB, Iyer, VN, Iyer, V, Kosarev, P, Mackey, AJ, Solovyev, V, Souvorov, A, Aronstein, KA, Bilikova, K, Chen, YP, Clark, AG, Decanini, LI, Gelbart, WM, Hetru, C, Hultmark, D, Imler, JL, Jiang, H, Kanost, M, Kimura, K, Lazzaro, BP, Lopez, DL, Simuth, J, Thompson, GJ, Zou, Z, De Jong, P, Sodergren, E, Csurös, M, Milosavljevic, A, Osoegawa, K, Richards, S, Shu, CL, Duret, L, Elhaik, E, Graur, D, Anzola, JM, Campbell, KS, Childs, KL, Collinge, D, Crosby, MA, Dickens, CM, Grametes, LS, Grozinger, CM, Jones, PL, Jorda, M, Ling, X, Matthews, BB, Miller, J, Mizzen, C, Peinado, MA, Reid, JG, Russo, SM, Schroeder, AJ, St. Pierre, SE, Wang, Y, Zhou, P, Jiang, H, Kitts, P, Ruef, B, Venkatraman, A, Zhang, L, Aquino-Perez, G, Whitfield, CW, Behura, SK, Berlocher, SH, Sheppard, WS, Smith, DR, Suarez, AV, Tsutsui, ND, Wei, X, Wheeler, D, Havlak, P, Li, B, Liu, Y, Jovilet, A, Lee, S, Nazareth, LV, Pu, LL, Thorn, R, Stolc, V, Newman, T, Samanta, M, Tongprasit, WA, Claudianos, C, Berenbaum, MR, Biswas, S, De Graaf, DC, Feyereisen, R, Johnson, RM, Oakeshott, JG, Ranson, H, Schuler, MA, Muzny, D, Chacko, J, Davis, C, Dinh, H, Gill, R, Hernandez, J, Hines, S, Hume, J, Jackson, LR, Kovar, C, Lewis, L, Miner, G, Morgan, M, Nguyen, N, Okwuonu, G, Paul, H, Santibanez, J, Savery, G, Svatek, A, Villasana, D & Wright, R 2006, 'Insights into social insects from the genome of the honeybee Apis mellifera', Nature, vol. 443, no. 7114, pp. 931-949. https://doi.org/10.1038/nature05260

TY - JOUR

T1 - Insights into social insects from the genome of the honeybee Apis mellifera

AU - Weinstock, George M.

AU - Robinson, Gene E.

AU - Gibbs, Richard A.

AU - Worley, Kim C.

AU - Evans, Jay D.

AU - Maleszka, Ryszard

AU - Robertson, Hugh M.

AU - Weaver, Daniel B.

AU - Beye, Martin

AU - Bork, Peer

AU - Elsik, Christine G.

AU - Hartfelder, Klaus

AU - Hunt, Greg J.

AU - Zdobnov, Evgeny M.

AU - Amdam, Gro V.

AU - Bitondi, Mrcia M.G.

AU - Collins, Anita M.

AU - Cristino, Alexandre S.

AU - Lattorff, H. Michael G.

AU - Lobo, Carlos H.

AU - Moritz, Robin F.A.

AU - Nunes, Francis M.F.

AU - Page, Robert E.

AU - Simões, Zilá L.P.

AU - Wheeler, Diana

AU - Carninci, Piero

AU - Fukuda, Shiro

AU - Hayashizaki, Yoshihide

AU - Kai, Chikatoshi

AU - Kawai, Jun

AU - Sakazume, Naoko

AU - Sasaki, Daisuke

AU - Tagami, Michihira

AU - Albert, Stefan

AU - Baggerman, Geert

AU - Beggs, Kyle T.

AU - Bloch, Guy

AU - Cazzamali, Giuseppe

AU - Cohen, Mira

AU - Drapeau, Mark David

AU - Eisenhardt, Dorothea

AU - Emore, Christine

AU - Ewing, Michael A.

AU - Fahrbach, Susan E.

AU - Forêt, Sylvain

AU - Grimmelikhuijzen, Cornelis J.P.

AU - Hauser, Frank

AU - Hummon, Amanda B.

AU - Huybrechts, Jurgen

AU - Jones, Andrew K.

AU - Kadowaki, Tatsuhiko

AU - Kaplan, Noam

AU - Kucharski, Robert

AU - Leboulle, Grard

AU - Linial, Michal

AU - Littleton, J. Troy

AU - Mercer, Alison R.

AU - Richmond, Timothy A.

AU - Rodriguez-Zas, Sandra L.

AU - Rubin, Elad B.

AU - Sattelle, David B.

AU - Schlipalius, David

AU - Schoofs, Liliane

AU - Shemesh, Yair

AU - Sweedler, Jonathan V.

AU - Velarde, Rodrigo

AU - Verleyen, Peter

AU - Vierstraete, Evy

AU - Williamson, Michael R.

AU - Ament, Seth A.

AU - Brown, Susan J.

AU - Corona, Miguel

AU - Dearden, Peter K.

AU - Dunn, W. Augustine

AU - Elekonich, Michelle M.

AU - Fujiyuki, Tomoko

AU - Gattermeier, Irene

AU - Gempe, Tanja

AU - Hasselmann, Martin

AU - Kage, Eriko

AU - Kamikouchi, Azusa

AU - Kubo, Takeo

AU - Kunieda, Takekazu

AU - Lorenzen, Marcé

AU - Milshina, Natalia V.

AU - Morioka, Mizue

AU - Ohashi, Kazuaki

AU - Overbeek, Ross

AU - Ross, Christian A.

AU - Schioett, Morten

AU - Shippy, Teresa

AU - Takeuchi, Hideaki

AU - Toth, Amy L.

AU - Willis, Judith H.

AU - Wilson, Megan J.

AU - Gordon, Karl H.J.

AU - Letunic, Ivica

AU - Hackett, Kevin

AU - Peterson, Jane

AU - Felsenfeld, Adam

AU - Guyer, Mark

AU - Solignac, Michel

AU - Agarwala, Richa

AU - Cornuet, Jean Marie

AU - Monnerot, Monique

AU - Mougel, Florence

AU - Reese, Justin T.

AU - Vautrin, Dominique

AU - Gillespie, Joseph J.

AU - Cannone, Jamie J.

AU - Gutell, Robin R.

AU - Johnston, J. Spencer

AU - Eisen, Michael B.

AU - Iyer, Venky N.

AU - Iyer, Vivek

AU - Kosarev, Peter

AU - Mackey, Aaron J.

AU - Solovyev, Victor

AU - Souvorov, Alexandre

AU - Aronstein, Katherine A.

AU - Bilikova, Katarina

AU - Chen, Yan Ping

AU - Clark, Andrew G.

AU - Decanini, Laura I.

AU - Gelbart, William M.

AU - Hetru, Charles

AU - Hultmark, Dan

AU - Imler, Jean Luc

AU - Jiang, Haobo

AU - Kanost, Michael

AU - Kimura, Kiyoshi

AU - Lazzaro, Brian P.

AU - Lopez, Dawn L.

AU - Simuth, Jozef

AU - Thompson, Graham J.

AU - Zou, Zhen

AU - De Jong, Pieter

AU - Sodergren, Erica

AU - Csurös, Miklós

AU - Milosavljevic, Aleksandar

AU - Osoegawa, Kazutoyo

AU - Richards, Stephen

AU - Shu, Chung Li

AU - Duret, Laurent

AU - Elhaik, Eran

AU - Graur, Dan

AU - Anzola, Juan M.

AU - Campbell, Kathryn S.

AU - Childs, Kevin L.

AU - Collinge, Derek

AU - Crosby, Madeline A.

AU - Dickens, C. Michael

AU - Grametes, L. Sian

AU - Grozinger, Christina M.

AU - Jones, Peter L.

AU - Jorda, Mireia

AU - Ling, Xu

AU - Matthews, Beverly B.

AU - Miller, Jonathan

AU - Mizzen, Craig

AU - Peinado, Miguel A.

AU - Reid, Jeffrey G.

AU - Russo, Susan M.

AU - Schroeder, Andrew J.

AU - St. Pierre, Susan E.

AU - Wang, Ying

AU - Zhou, Pinglei

AU - Jiang, Huaiyang

AU - Kitts, Paul

AU - Ruef, Barbara

AU - Venkatraman, Anand

AU - Zhang, Lan

AU - Aquino-Perez, Gildardo

AU - Whitfield, Charles W.

AU - Behura, Susanta K.

AU - Berlocher, Stewart H.

AU - Sheppard, Walter S.

AU - Smith, Deborah R.

AU - Suarez, Andrew V.

AU - Tsutsui, Neil D.

AU - Wei, Xuehong

AU - Wheeler, David

AU - Havlak, Paul

AU - Li, Bingshan

AU - Liu, Yue

AU - Jovilet, Angela

AU - Lee, Sandra

AU - Nazareth, Lynne V.

AU - Pu, Ling Ling

AU - Thorn, Rachel

AU - Stolc, Viktor

AU - Newman, Thomas

AU - Samanta, Manoj

AU - Tongprasit, Waraporn A.

AU - Claudianos, Charles

AU - Berenbaum, May R.

AU - Biswas, Sunita

AU - De Graaf, Dirk C.

AU - Feyereisen, Rene

AU - Johnson, Reed M.

AU - Oakeshott, John G.

AU - Ranson, Hilary

AU - Schuler, Mary A.

AU - Muzny, Donna

AU - Chacko, Joseph

AU - Davis, Clay

AU - Dinh, Huyen

AU - Gill, Rachel

AU - Hernandez, Judith

AU - Hines, Sandra

AU - Hume, Jennifer

AU - Jackson, La Ronda

AU - Kovar, Christie

AU - Lewis, Lora

AU - Miner, George

AU - Morgan, Margaret

AU - Nguyen, Ngoc

AU - Okwuonu, Geoffrey

AU - Paul, Heidi

AU - Santibanez, Jireh

AU - Savery, Glenford

AU - Svatek, Amanda

AU - Villasana, Donna

AU - Wright, Rita

N1 - Funding Information: Acknowledgements Work at the BCM-HGSC was supported by grants from the NHGRI and USDA. BAC and fosmid Library construction was supported by a subcontract from a grant awarded to J.S.J., organized by D.B.W. (President, Bee Weaver Apiaries, Inc.). Fgenesh and Fgenesh11 analysis was donated by Softberry. Other support was received from NIH NIAID (H.M.R.), NRI Functional Genomics (G.E.R.) and Illinois Sociogenomics Initiative (G.E.R.), NSF (M.M.E.; B. Schatz, UIUC), Intramural Research Program NIH NLM (R.A.), USDA-NRI, California Beekeepers Assoc., Texas Beekeepers Assoc., T. W. Burleson and Son, Inc., TAMU, NIH NLM (J.G.R.), RSNZ Marsden Fund (P.K.D.), Danish Research Agency, Carlsberg Foundation, Novo Nordisk Foundation, and DFG. The authors thank the production staff at the HGSC.

PY - 2006/10/26

Y1 - 2006/10/26

N2 - Here we report the genome sequence of the honeybee Apis mellifera, a key model for social behaviour and essential to global ecology through pollination. Compared with other sequenced insect genomes, the A. mellifera genome has high A+T and CpG contents, lacks major transposon families, evolves more slowly, and is more similar to vertebrates for circadian rhythm, RNA interference and DNA methylation genes, among others. Furthermore, A. mellifera has fewer genes for innate immunity, detoxification enzymes, cuticle-forming proteins and gustatory receptors, more genes for odorant receptors, and novel genes for nectar and pollen utilization, consistent with its ecology and social organization. Compared to Drosophila, genes in early developmental pathways differ in Apis, whereas similarities exist for functions that differ markedly, such as sex determination, brain function and behaviour. Population genetics suggests a novel African origin for the species A. mellifera and insights into whether Africanized bees spread throughout the New World via hybridization or displacement.

AB - Here we report the genome sequence of the honeybee Apis mellifera, a key model for social behaviour and essential to global ecology through pollination. Compared with other sequenced insect genomes, the A. mellifera genome has high A+T and CpG contents, lacks major transposon families, evolves more slowly, and is more similar to vertebrates for circadian rhythm, RNA interference and DNA methylation genes, among others. Furthermore, A. mellifera has fewer genes for innate immunity, detoxification enzymes, cuticle-forming proteins and gustatory receptors, more genes for odorant receptors, and novel genes for nectar and pollen utilization, consistent with its ecology and social organization. Compared to Drosophila, genes in early developmental pathways differ in Apis, whereas similarities exist for functions that differ markedly, such as sex determination, brain function and behaviour. Population genetics suggests a novel African origin for the species A. mellifera and insights into whether Africanized bees spread throughout the New World via hybridization or displacement.

UR - http://www.scopus.com/inward/record.url?scp=33750460281&partnerID=8YFLogxK

U2 - 10.1038/nature05260

DO - 10.1038/nature05260

M3 - ???researchoutput.researchoutputtypes.contributiontojournal.article???

C2 - 17073008

AN - SCOPUS:33750460281

SN - 0028-0836

VL - 443

SP - 931

EP - 949

JO - Nature

JF - Nature

IS - 7114

ER -

Insights into social insects from the genome of the honeybee Apis mellifera

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