The genomes of two key bumblebee species with primitive eusocial organization

Ben M Sadd, Seth M Barribeau, Guy Bloch, Dirk C de Graaf, Peter Dearden, Christine G Elsik, Jürgen Gadau, Cornelis JP Grimmelikhuijzen, Martin Hasselmann, Jeffrey D Lozier, Hugh M Robertson, Guy Smagghe, Eckart Stolle, Matthias Van Vaerenbergh, Robert M Waterhouse, Erich Bornberg-Bauer, Steffen Klasberg, Anna K Bennett, Francisco Câmara, Roderic Guigó, Katharina Hoff, Marco Mariotti, Monica Munoz-Torres, Terence Murphy, Didac Santesmasses, Gro V Amdam, Matthew Beckers, Martin Beye, Matthias Biewer, Márcia MG Bitondi, Mark L Blaxter, Andrew FG Bourke, Mark JF Brown, Severine D Buechel, Rossanah Cameron, Kaat Cappelle, James C Carolan, Olivier Christiaens, Kate L Ciborowski, David F Clarke, Thomas J Colgan, David H Collins, Andrew G Cridge, Tamas Dalmay, Stephanie Dreier, Louis du Plessis, Elizabeth Duncan, Silvio Erler, Jay Evans, Tiago Falcon, Kevin Flores, Flávia CP Freitas, Taro Fuchikawa, Tanja Gempe, Klaus Hartfelder, Frank Hauser, Sophie Helbing, Fernanda C Humann, Frano Irvine, Lars S Jermiin, Claire E Johnson, Reed M Johnson, Andrew K Jones, Tatsuhiko Kadowaki, Jonathan H Kidner, Vasco Koch, Arian Köhler, F Bernhard Kraus, H Michael G Lattorff, Megan Leask, Gabrielle A Lockett, Eamonn B Mallon, David S Marco Antonio, Monika Marxer, Ivan Meeus, Robin FA Moritz, Ajay Nair, Kathrin Näpflin, Inga Nissen, Jinzhi Niu, Francis MF Nunes, John G Oakeshott, Amy Osborne, Marianne Otte, Daniel G Pinheiro, Nina Rossié, Olav Rueppell, Carolina G Santos, Regula Schmid-Hempel, Björn D Schmitt, Christina Schulte, Zilá LP Simões, Michelle PM Soares, Luc Swevers, Eva C Winnebeck, Florian Wolschin, Na Yu, Evgeny M Zdobnov, Peshtewani K Aqrawi, Kerstin P Blankenburg, Marcus Coyle, Liezl Francisco, Alvaro G Hernandez, Michael Holder, Matthew E Hudson, LaRonda Jackson, Joy Jayaseelan, Vandita Joshi, Christie Kovar, Sandra L Lee, Robert Mata, Tittu Mathew, Irene F Newsham, Robin Ngo, Geoffrey Okwuonu, Christopher Pham, Ling-Ling Pu, Nehad Saada, Jireh Santibanez, DeNard Simmons, Rebecca Thornton, Aarti Venkat, Kimberly KO Walden, Yuan-Qing Wu, Griet Debyser, Bart Devreese, Claire Asher, Julie Blommaert, Ariel D Chipman, Lars Chittka, Bertrand Fouks, Jisheng Liu, Meaghan P O’Neill, Seirian Sumner, Daniela Puiu, Jiaxin Qu, Steven L Salzberg, Steven E Scherer, Donna M Muzny, Stephen Richards, Gene E Robinson, Richard A Gibbs, Paul Schmid-Hempel, Kim C Worley

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. 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. 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.