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The genomes of two key bumblebee species with primitive eusocial organization

BACKGROUND: The shift from solitary to social behavior is one of the major evolutionary transitions. Primitively eusocial bumblebees are uniquely placed to illuminate the evolution of highly eusocial insect societies. Bumblebees are also invaluable natural and agricultural pollinators, and there is...

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Autores principales: Sadd, Ben M, Barribeau, Seth M, Bloch, Guy, de Graaf, Dirk C, Dearden, Peter, Elsik, Christine G, Gadau, Jürgen, Grimmelikhuijzen, Cornelis JP, Hasselmann, Martin, Lozier, Jeffrey D, Robertson, Hugh M, Smagghe, Guy, Stolle, Eckart, Van Vaerenbergh, Matthias, Waterhouse, Robert M, Bornberg-Bauer, Erich, Klasberg, Steffen, Bennett, Anna K, Câmara, Francisco, Guigó, Roderic, Hoff, Katharina, Mariotti, Marco, Munoz-Torres, Monica, Murphy, Terence, Santesmasses, Didac, Amdam, Gro V, Beckers, Matthew, Beye, Martin, Biewer, Matthias, Bitondi, Márcia MG, Blaxter, Mark L, Bourke, Andrew FG, Brown, Mark JF, Buechel, Severine D, Cameron, Rossanah, Cappelle, Kaat, Carolan, James C, Christiaens, Olivier, Ciborowski, Kate L, Clarke, David F, Colgan, Thomas J, Collins, David H, Cridge, Andrew G, Dalmay, Tamas, Dreier, Stephanie, du Plessis, Louis, Duncan, Elizabeth, Erler, Silvio, Evans, Jay, Falcon, Tiago, Flores, Kevin, Freitas, Flávia CP, Fuchikawa, Taro, Gempe, Tanja, Hartfelder, Klaus, Hauser, Frank, Helbing, Sophie, Humann, Fernanda C, Irvine, Frano, Jermiin, Lars S, Johnson, Claire E, Johnson, Reed M, Jones, Andrew K, Kadowaki, Tatsuhiko, Kidner, Jonathan H, Koch, Vasco, Köhler, Arian, Kraus, F Bernhard, Lattorff, H Michael G, Leask, Megan, Lockett, Gabrielle A, Mallon, Eamonn B, Antonio, David S Marco, Marxer, Monika, Meeus, Ivan, Moritz, Robin FA, Nair, Ajay, Näpflin, Kathrin, Nissen, Inga, Niu, Jinzhi, Nunes, Francis MF, Oakeshott, John G, Osborne, Amy, Otte, Marianne, Pinheiro, Daniel G, Rossié, Nina, Rueppell, Olav, Santos, Carolina G, Schmid-Hempel, Regula, Schmitt, Björn D, Schulte, Christina, Simões, Zilá LP, Soares, Michelle PM, Swevers, Luc, Winnebeck, Eva C, Wolschin, Florian, Yu, Na, Zdobnov, Evgeny M, Aqrawi, Peshtewani K, Blankenburg, Kerstin P, Coyle, Marcus, Francisco, Liezl, Hernandez, Alvaro G, Holder, Michael, Hudson, Matthew E, Jackson, LaRonda, Jayaseelan, Joy, Joshi, Vandita, Kovar, Christie, Lee, Sandra L, Mata, Robert, Mathew, Tittu, Newsham, Irene F, Ngo, Robin, Okwuonu, Geoffrey, Pham, Christopher, Pu, Ling-Ling, Saada, Nehad, Santibanez, Jireh, Simmons, DeNard, Thornton, Rebecca, Venkat, Aarti, Walden, Kimberly KO, Wu, Yuan-Qing, Debyser, Griet, Devreese, Bart, Asher, Claire, Blommaert, Julie, Chipman, Ariel D, Chittka, Lars, Fouks, Bertrand, Liu, Jisheng, O’Neill, Meaghan P, Sumner, Seirian, Puiu, Daniela, Qu, Jiaxin, Salzberg, Steven L, Scherer, Steven E, Muzny, Donna M, Richards, Stephen, Robinson, Gene E, Gibbs, Richard A, Schmid-Hempel, Paul, Worley, Kim C
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4414376/
https://www.ncbi.nlm.nih.gov/pubmed/25908251
http://dx.doi.org/10.1186/s13059-015-0623-3
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author Sadd, Ben M
Barribeau, Seth M
Bloch, Guy
de Graaf, Dirk C
Dearden, Peter
Elsik, Christine G
Gadau, Jürgen
Grimmelikhuijzen, Cornelis JP
Hasselmann, Martin
Lozier, Jeffrey D
Robertson, Hugh M
Smagghe, Guy
Stolle, Eckart
Van Vaerenbergh, Matthias
Waterhouse, Robert M
Bornberg-Bauer, Erich
Klasberg, Steffen
Bennett, Anna K
Câmara, Francisco
Guigó, Roderic
Hoff, Katharina
Mariotti, Marco
Munoz-Torres, Monica
Murphy, Terence
Santesmasses, Didac
Amdam, Gro V
Beckers, Matthew
Beye, Martin
Biewer, Matthias
Bitondi, Márcia MG
Blaxter, Mark L
Bourke, Andrew FG
Brown, Mark JF
Buechel, Severine D
Cameron, Rossanah
Cappelle, Kaat
Carolan, James C
Christiaens, Olivier
Ciborowski, Kate L
Clarke, David F
Colgan, Thomas J
Collins, David H
Cridge, Andrew G
Dalmay, Tamas
Dreier, Stephanie
du Plessis, Louis
Duncan, Elizabeth
Erler, Silvio
Evans, Jay
Falcon, Tiago
Flores, Kevin
Freitas, Flávia CP
Fuchikawa, Taro
Gempe, Tanja
Hartfelder, Klaus
Hauser, Frank
Helbing, Sophie
Humann, Fernanda C
Irvine, Frano
Jermiin, Lars S
Johnson, Claire E
Johnson, Reed M
Jones, Andrew K
Kadowaki, Tatsuhiko
Kidner, Jonathan H
Koch, Vasco
Köhler, Arian
Kraus, F Bernhard
Lattorff, H Michael G
Leask, Megan
Lockett, Gabrielle A
Mallon, Eamonn B
Antonio, David S Marco
Marxer, Monika
Meeus, Ivan
Moritz, Robin FA
Nair, Ajay
Näpflin, Kathrin
Nissen, Inga
Niu, Jinzhi
Nunes, Francis MF
Oakeshott, John G
Osborne, Amy
Otte, Marianne
Pinheiro, Daniel G
Rossié, Nina
Rueppell, Olav
Santos, Carolina G
Schmid-Hempel, Regula
Schmitt, Björn D
Schulte, Christina
Simões, Zilá LP
Soares, Michelle PM
Swevers, Luc
Winnebeck, Eva C
Wolschin, Florian
Yu, Na
Zdobnov, Evgeny M
Aqrawi, Peshtewani K
Blankenburg, Kerstin P
Coyle, Marcus
Francisco, Liezl
Hernandez, Alvaro G
Holder, Michael
Hudson, Matthew E
Jackson, LaRonda
Jayaseelan, Joy
Joshi, Vandita
Kovar, Christie
Lee, Sandra L
Mata, Robert
Mathew, Tittu
Newsham, Irene F
Ngo, Robin
Okwuonu, Geoffrey
Pham, Christopher
Pu, Ling-Ling
Saada, Nehad
Santibanez, Jireh
Simmons, DeNard
Thornton, Rebecca
Venkat, Aarti
Walden, Kimberly KO
Wu, Yuan-Qing
Debyser, Griet
Devreese, Bart
Asher, Claire
Blommaert, Julie
Chipman, Ariel D
Chittka, Lars
Fouks, Bertrand
Liu, Jisheng
O’Neill, Meaghan P
Sumner, Seirian
Puiu, Daniela
Qu, Jiaxin
Salzberg, Steven L
Scherer, Steven E
Muzny, Donna M
Richards, Stephen
Robinson, Gene E
Gibbs, Richard A
Schmid-Hempel, Paul
Worley, Kim C
author_facet Sadd, Ben M
Barribeau, Seth M
Bloch, Guy
de Graaf, Dirk C
Dearden, Peter
Elsik, Christine G
Gadau, Jürgen
Grimmelikhuijzen, Cornelis JP
Hasselmann, Martin
Lozier, Jeffrey D
Robertson, Hugh M
Smagghe, Guy
Stolle, Eckart
Van Vaerenbergh, Matthias
Waterhouse, Robert M
Bornberg-Bauer, Erich
Klasberg, Steffen
Bennett, Anna K
Câmara, Francisco
Guigó, Roderic
Hoff, Katharina
Mariotti, Marco
Munoz-Torres, Monica
Murphy, Terence
Santesmasses, Didac
Amdam, Gro V
Beckers, Matthew
Beye, Martin
Biewer, Matthias
Bitondi, Márcia MG
Blaxter, Mark L
Bourke, Andrew FG
Brown, Mark JF
Buechel, Severine D
Cameron, Rossanah
Cappelle, Kaat
Carolan, James C
Christiaens, Olivier
Ciborowski, Kate L
Clarke, David F
Colgan, Thomas J
Collins, David H
Cridge, Andrew G
Dalmay, Tamas
Dreier, Stephanie
du Plessis, Louis
Duncan, Elizabeth
Erler, Silvio
Evans, Jay
Falcon, Tiago
Flores, Kevin
Freitas, Flávia CP
Fuchikawa, Taro
Gempe, Tanja
Hartfelder, Klaus
Hauser, Frank
Helbing, Sophie
Humann, Fernanda C
Irvine, Frano
Jermiin, Lars S
Johnson, Claire E
Johnson, Reed M
Jones, Andrew K
Kadowaki, Tatsuhiko
Kidner, Jonathan H
Koch, Vasco
Köhler, Arian
Kraus, F Bernhard
Lattorff, H Michael G
Leask, Megan
Lockett, Gabrielle A
Mallon, Eamonn B
Antonio, David S Marco
Marxer, Monika
Meeus, Ivan
Moritz, Robin FA
Nair, Ajay
Näpflin, Kathrin
Nissen, Inga
Niu, Jinzhi
Nunes, Francis MF
Oakeshott, John G
Osborne, Amy
Otte, Marianne
Pinheiro, Daniel G
Rossié, Nina
Rueppell, Olav
Santos, Carolina G
Schmid-Hempel, Regula
Schmitt, Björn D
Schulte, Christina
Simões, Zilá LP
Soares, Michelle PM
Swevers, Luc
Winnebeck, Eva C
Wolschin, Florian
Yu, Na
Zdobnov, Evgeny M
Aqrawi, Peshtewani K
Blankenburg, Kerstin P
Coyle, Marcus
Francisco, Liezl
Hernandez, Alvaro G
Holder, Michael
Hudson, Matthew E
Jackson, LaRonda
Jayaseelan, Joy
Joshi, Vandita
Kovar, Christie
Lee, Sandra L
Mata, Robert
Mathew, Tittu
Newsham, Irene F
Ngo, Robin
Okwuonu, Geoffrey
Pham, Christopher
Pu, Ling-Ling
Saada, Nehad
Santibanez, Jireh
Simmons, DeNard
Thornton, Rebecca
Venkat, Aarti
Walden, Kimberly KO
Wu, Yuan-Qing
Debyser, Griet
Devreese, Bart
Asher, Claire
Blommaert, Julie
Chipman, Ariel D
Chittka, Lars
Fouks, Bertrand
Liu, Jisheng
O’Neill, Meaghan P
Sumner, Seirian
Puiu, Daniela
Qu, Jiaxin
Salzberg, Steven L
Scherer, Steven E
Muzny, Donna M
Richards, Stephen
Robinson, Gene E
Gibbs, Richard A
Schmid-Hempel, Paul
Worley, Kim C
author_sort Sadd, Ben M
collection PubMed
description BACKGROUND: The shift from solitary to social behavior is one of the major evolutionary transitions. Primitively eusocial bumblebees are uniquely placed to illuminate the evolution of highly eusocial insect societies. Bumblebees are also invaluable natural and agricultural pollinators, and there is widespread concern over recent population declines in some species. High-quality genomic data will inform key aspects of bumblebee biology, including susceptibility to implicated population viability threats. RESULTS: We report the high quality draft genome sequences of Bombus terrestris and Bombus impatiens, two ecologically dominant bumblebees and widely utilized study species. Comparing these new genomes to those of the highly eusocial honeybee Apis mellifera and other Hymenoptera, we identify deeply conserved similarities, as well as novelties key to the biology of these organisms. Some honeybee genome features thought to underpin advanced eusociality are also present in bumblebees, indicating an earlier evolution in the bee lineage. Xenobiotic detoxification and immune genes are similarly depauperate in bumblebees and honeybees, and multiple categories of genes linked to social organization, including development and behavior, show high conservation. Key differences identified include a bias in bumblebee chemoreception towards gustation from olfaction, and striking differences in microRNAs, potentially responsible for gene regulation underlying social and other traits. CONCLUSIONS: These two bumblebee genomes provide a foundation for post-genomic research on these key pollinators and insect societies. Overall, gene repertoires suggest that the route to advanced eusociality in bees was mediated by many small changes in many genes and processes, and not by notable expansion or depauperation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13059-015-0623-3) contains supplementary material, which is available to authorized users.
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spelling pubmed-44143762015-04-30 The genomes of two key bumblebee species with primitive eusocial organization Sadd, Ben M Barribeau, Seth M Bloch, Guy de Graaf, Dirk C Dearden, Peter Elsik, Christine G Gadau, Jürgen Grimmelikhuijzen, Cornelis JP Hasselmann, Martin Lozier, Jeffrey D Robertson, Hugh M Smagghe, Guy Stolle, Eckart Van Vaerenbergh, Matthias Waterhouse, Robert M Bornberg-Bauer, Erich Klasberg, Steffen Bennett, Anna K Câmara, Francisco Guigó, Roderic Hoff, Katharina Mariotti, Marco Munoz-Torres, Monica Murphy, Terence Santesmasses, Didac Amdam, Gro V Beckers, Matthew Beye, Martin Biewer, Matthias Bitondi, Márcia MG Blaxter, Mark L Bourke, Andrew FG Brown, Mark JF Buechel, Severine D Cameron, Rossanah Cappelle, Kaat Carolan, James C Christiaens, Olivier Ciborowski, Kate L Clarke, David F Colgan, Thomas J Collins, David H Cridge, Andrew G Dalmay, Tamas Dreier, Stephanie du Plessis, Louis Duncan, Elizabeth Erler, Silvio Evans, Jay Falcon, Tiago Flores, Kevin Freitas, Flávia CP Fuchikawa, Taro Gempe, Tanja Hartfelder, Klaus Hauser, Frank Helbing, Sophie Humann, Fernanda C Irvine, Frano Jermiin, Lars S Johnson, Claire E Johnson, Reed M Jones, Andrew K Kadowaki, Tatsuhiko Kidner, Jonathan H Koch, Vasco Köhler, Arian Kraus, F Bernhard Lattorff, H Michael G Leask, Megan Lockett, Gabrielle A Mallon, Eamonn B Antonio, David S Marco Marxer, Monika Meeus, Ivan Moritz, Robin FA Nair, Ajay Näpflin, Kathrin Nissen, Inga Niu, Jinzhi Nunes, Francis MF Oakeshott, John G Osborne, Amy Otte, Marianne Pinheiro, Daniel G Rossié, Nina Rueppell, Olav Santos, Carolina G Schmid-Hempel, Regula Schmitt, Björn D Schulte, Christina Simões, Zilá LP Soares, Michelle PM Swevers, Luc Winnebeck, Eva C Wolschin, Florian Yu, Na Zdobnov, Evgeny M Aqrawi, Peshtewani K Blankenburg, Kerstin P Coyle, Marcus Francisco, Liezl Hernandez, Alvaro G Holder, Michael Hudson, Matthew E Jackson, LaRonda Jayaseelan, Joy Joshi, Vandita Kovar, Christie Lee, Sandra L Mata, Robert Mathew, Tittu Newsham, Irene F Ngo, Robin Okwuonu, Geoffrey Pham, Christopher Pu, Ling-Ling Saada, Nehad Santibanez, Jireh Simmons, DeNard Thornton, Rebecca Venkat, Aarti Walden, Kimberly KO Wu, Yuan-Qing Debyser, Griet Devreese, Bart Asher, Claire Blommaert, Julie Chipman, Ariel D Chittka, Lars Fouks, Bertrand Liu, Jisheng O’Neill, Meaghan P Sumner, Seirian Puiu, Daniela Qu, Jiaxin Salzberg, Steven L Scherer, Steven E Muzny, Donna M Richards, Stephen Robinson, Gene E Gibbs, Richard A Schmid-Hempel, Paul Worley, Kim C Genome Biol Research BACKGROUND: The shift from solitary to social behavior is one of the major evolutionary transitions. Primitively eusocial bumblebees are uniquely placed to illuminate the evolution of highly eusocial insect societies. Bumblebees are also invaluable natural and agricultural pollinators, and there is widespread concern over recent population declines in some species. High-quality genomic data will inform key aspects of bumblebee biology, including susceptibility to implicated population viability threats. RESULTS: We report the high quality draft genome sequences of Bombus terrestris and Bombus impatiens, two ecologically dominant bumblebees and widely utilized study species. Comparing these new genomes to those of the highly eusocial honeybee Apis mellifera and other Hymenoptera, we identify deeply conserved similarities, as well as novelties key to the biology of these organisms. Some honeybee genome features thought to underpin advanced eusociality are also present in bumblebees, indicating an earlier evolution in the bee lineage. Xenobiotic detoxification and immune genes are similarly depauperate in bumblebees and honeybees, and multiple categories of genes linked to social organization, including development and behavior, show high conservation. Key differences identified include a bias in bumblebee chemoreception towards gustation from olfaction, and striking differences in microRNAs, potentially responsible for gene regulation underlying social and other traits. CONCLUSIONS: These two bumblebee genomes provide a foundation for post-genomic research on these key pollinators and insect societies. Overall, gene repertoires suggest that the route to advanced eusociality in bees was mediated by many small changes in many genes and processes, and not by notable expansion or depauperation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13059-015-0623-3) contains supplementary material, which is available to authorized users. BioMed Central 2015-04-24 2015 /pmc/articles/PMC4414376/ /pubmed/25908251 http://dx.doi.org/10.1186/s13059-015-0623-3 Text en © Sadd et al.; licensee BioMed Central. 2015 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Sadd, Ben M
Barribeau, Seth M
Bloch, Guy
de Graaf, Dirk C
Dearden, Peter
Elsik, Christine G
Gadau, Jürgen
Grimmelikhuijzen, Cornelis JP
Hasselmann, Martin
Lozier, Jeffrey D
Robertson, Hugh M
Smagghe, Guy
Stolle, Eckart
Van Vaerenbergh, Matthias
Waterhouse, Robert M
Bornberg-Bauer, Erich
Klasberg, Steffen
Bennett, Anna K
Câmara, Francisco
Guigó, Roderic
Hoff, Katharina
Mariotti, Marco
Munoz-Torres, Monica
Murphy, Terence
Santesmasses, Didac
Amdam, Gro V
Beckers, Matthew
Beye, Martin
Biewer, Matthias
Bitondi, Márcia MG
Blaxter, Mark L
Bourke, Andrew FG
Brown, Mark JF
Buechel, Severine D
Cameron, Rossanah
Cappelle, Kaat
Carolan, James C
Christiaens, Olivier
Ciborowski, Kate L
Clarke, David F
Colgan, Thomas J
Collins, David H
Cridge, Andrew G
Dalmay, Tamas
Dreier, Stephanie
du Plessis, Louis
Duncan, Elizabeth
Erler, Silvio
Evans, Jay
Falcon, Tiago
Flores, Kevin
Freitas, Flávia CP
Fuchikawa, Taro
Gempe, Tanja
Hartfelder, Klaus
Hauser, Frank
Helbing, Sophie
Humann, Fernanda C
Irvine, Frano
Jermiin, Lars S
Johnson, Claire E
Johnson, Reed M
Jones, Andrew K
Kadowaki, Tatsuhiko
Kidner, Jonathan H
Koch, Vasco
Köhler, Arian
Kraus, F Bernhard
Lattorff, H Michael G
Leask, Megan
Lockett, Gabrielle A
Mallon, Eamonn B
Antonio, David S Marco
Marxer, Monika
Meeus, Ivan
Moritz, Robin FA
Nair, Ajay
Näpflin, Kathrin
Nissen, Inga
Niu, Jinzhi
Nunes, Francis MF
Oakeshott, John G
Osborne, Amy
Otte, Marianne
Pinheiro, Daniel G
Rossié, Nina
Rueppell, Olav
Santos, Carolina G
Schmid-Hempel, Regula
Schmitt, Björn D
Schulte, Christina
Simões, Zilá LP
Soares, Michelle PM
Swevers, Luc
Winnebeck, Eva C
Wolschin, Florian
Yu, Na
Zdobnov, Evgeny M
Aqrawi, Peshtewani K
Blankenburg, Kerstin P
Coyle, Marcus
Francisco, Liezl
Hernandez, Alvaro G
Holder, Michael
Hudson, Matthew E
Jackson, LaRonda
Jayaseelan, Joy
Joshi, Vandita
Kovar, Christie
Lee, Sandra L
Mata, Robert
Mathew, Tittu
Newsham, Irene F
Ngo, Robin
Okwuonu, Geoffrey
Pham, Christopher
Pu, Ling-Ling
Saada, Nehad
Santibanez, Jireh
Simmons, DeNard
Thornton, Rebecca
Venkat, Aarti
Walden, Kimberly KO
Wu, Yuan-Qing
Debyser, Griet
Devreese, Bart
Asher, Claire
Blommaert, Julie
Chipman, Ariel D
Chittka, Lars
Fouks, Bertrand
Liu, Jisheng
O’Neill, Meaghan P
Sumner, Seirian
Puiu, Daniela
Qu, Jiaxin
Salzberg, Steven L
Scherer, Steven E
Muzny, Donna M
Richards, Stephen
Robinson, Gene E
Gibbs, Richard A
Schmid-Hempel, Paul
Worley, Kim C
The genomes of two key bumblebee species with primitive eusocial organization
title The genomes of two key bumblebee species with primitive eusocial organization
title_full The genomes of two key bumblebee species with primitive eusocial organization
title_fullStr The genomes of two key bumblebee species with primitive eusocial organization
title_full_unstemmed The genomes of two key bumblebee species with primitive eusocial organization
title_short The genomes of two key bumblebee species with primitive eusocial organization
title_sort genomes of two key bumblebee species with primitive eusocial organization
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4414376/
https://www.ncbi.nlm.nih.gov/pubmed/25908251
http://dx.doi.org/10.1186/s13059-015-0623-3
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AT hauserfrank thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT helbingsophie thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT humannfernandac thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT irvinefrano thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT jermiinlarss thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT johnsonclairee thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT johnsonreedm thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT jonesandrewk thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT kadowakitatsuhiko thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT kidnerjonathanh thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT kochvasco thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT kohlerarian thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT krausfbernhard thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT lattorffhmichaelg thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT leaskmegan thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT lockettgabriellea thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT malloneamonnb thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT antoniodavidsmarco thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT marxermonika thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT meeusivan thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT moritzrobinfa thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT nairajay thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT napflinkathrin thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT nisseninga thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT niujinzhi thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT nunesfrancismf thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT oakeshottjohng thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT osborneamy thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT ottemarianne thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT pinheirodanielg thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT rossienina thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT rueppellolav thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT santoscarolinag thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT schmidhempelregula thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT schmittbjornd thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT schultechristina thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT simoeszilalp thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT soaresmichellepm thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT sweversluc thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT winnebeckevac thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT wolschinflorian thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT yuna thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT zdobnovevgenym thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT aqrawipeshtewanik thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT blankenburgkerstinp thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT coylemarcus thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT franciscoliezl thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT hernandezalvarog thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT holdermichael thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT hudsonmatthewe thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT jacksonlaronda thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT jayaseelanjoy thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT joshivandita thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT kovarchristie thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT leesandral thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT matarobert thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT mathewtittu thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT newshamirenef thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT ngorobin thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT okwuonugeoffrey thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT phamchristopher thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT pulingling thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT saadanehad thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT santibanezjireh thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT simmonsdenard thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT thorntonrebecca thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT venkataarti thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT waldenkimberlyko thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT wuyuanqing thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT debysergriet thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT devreesebart thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT asherclaire thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT blommaertjulie thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT chipmanarield thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT chittkalars thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT fouksbertrand thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT liujisheng thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT oneillmeaghanp thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT sumnerseirian thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT puiudaniela thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT qujiaxin thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT salzbergstevenl thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT schererstevene thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT muznydonnam thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT richardsstephen thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT robinsongenee thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT gibbsricharda thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT schmidhempelpaul thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT worleykimc thegenomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT saddbenm genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT barribeausethm genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT blochguy genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT degraafdirkc genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT deardenpeter genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT elsikchristineg genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT gadaujurgen genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT grimmelikhuijzencornelisjp genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT hasselmannmartin genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT lozierjeffreyd genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT robertsonhughm genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT smaggheguy genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT stolleeckart genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT vanvaerenberghmatthias genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT waterhouserobertm genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT bornbergbauererich genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT klasbergsteffen genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT bennettannak genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT camarafrancisco genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT guigoroderic genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT hoffkatharina genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT mariottimarco genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT munoztorresmonica genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT murphyterence genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT santesmassesdidac genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT amdamgrov genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT beckersmatthew genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT beyemartin genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT biewermatthias genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT bitondimarciamg genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT blaxtermarkl genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT bourkeandrewfg genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT brownmarkjf genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT buechelseverined genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT cameronrossanah genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT cappellekaat genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT carolanjamesc genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT christiaensolivier genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT ciborowskikatel genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT clarkedavidf genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT colganthomasj genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT collinsdavidh genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT cridgeandrewg genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT dalmaytamas genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT dreierstephanie genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT duplessislouis genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT duncanelizabeth genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT erlersilvio genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT evansjay genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT falcontiago genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT floreskevin genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT freitasflaviacp genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT fuchikawataro genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT gempetanja genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT hartfelderklaus genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT hauserfrank genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT helbingsophie genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT humannfernandac genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT irvinefrano genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT jermiinlarss genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT johnsonclairee genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT johnsonreedm genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT jonesandrewk genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT kadowakitatsuhiko genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT kidnerjonathanh genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT kochvasco genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT kohlerarian genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT krausfbernhard genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT lattorffhmichaelg genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT leaskmegan genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT lockettgabriellea genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT malloneamonnb genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT antoniodavidsmarco genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT marxermonika genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT meeusivan genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT moritzrobinfa genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT nairajay genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT napflinkathrin genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT nisseninga genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT niujinzhi genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT nunesfrancismf genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT oakeshottjohng genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT osborneamy genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT ottemarianne genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT pinheirodanielg genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT rossienina genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT rueppellolav genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT santoscarolinag genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT schmidhempelregula genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT schmittbjornd genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT schultechristina genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT simoeszilalp genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT soaresmichellepm genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT sweversluc genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT winnebeckevac genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT wolschinflorian genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT yuna genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT zdobnovevgenym genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT aqrawipeshtewanik genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT blankenburgkerstinp genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT coylemarcus genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT franciscoliezl genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT hernandezalvarog genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT holdermichael genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT hudsonmatthewe genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT jacksonlaronda genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT jayaseelanjoy genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT joshivandita genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT kovarchristie genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT leesandral genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT matarobert genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT mathewtittu genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT newshamirenef genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT ngorobin genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT okwuonugeoffrey genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT phamchristopher genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT pulingling genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT saadanehad genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT santibanezjireh genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT simmonsdenard genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT thorntonrebecca genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT venkataarti genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT waldenkimberlyko genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT wuyuanqing genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT debysergriet genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT devreesebart genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT asherclaire genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT blommaertjulie genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT chipmanarield genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT chittkalars genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT fouksbertrand genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT liujisheng genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT oneillmeaghanp genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT sumnerseirian genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT puiudaniela genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT qujiaxin genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT salzbergstevenl genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT schererstevene genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT muznydonnam genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT richardsstephen genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT robinsongenee genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT gibbsricharda genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT schmidhempelpaul genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization
AT worleykimc genomesoftwokeybumblebeespecieswithprimitiveeusocialorganization