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Grant support

The sequencing, annotation, and assembly of the B. impatiens genome was supported by National Institutes of Health (NIH) Pioneer Award DP1 OD006416 (GER). The B. terrestris genome sequencing, assembly and project coordination was supported by NIH grant U54 HG003273 (RAG). Contributions from members of the CGE lab were supported by Agriculture and Food Research Initiative Competitive grant no. 2010-65106-21301 from the USDA National Institute of Food and Agriculture. GVA was supported by the Research Council of Norway (NFR) and the PEW Charitable Trust. MB was supported by a student fellowship from the University of East Anglia, UK. GB was supported by the Israel Science Foundation (ISF). DHC was supported by a studentship funded by the Biotechnology and Biological Sciences Research Council, UK, and the University of East Anglia. JDL was supported by the University of Alabama College of Arts and Sciences. ZPLS was supported by a Sao Paulo Research Foundation grant (FAPESP number 11/03171-5). RMW was supported by Marie Curie International Outgoing Fellowship PIOF-GA-2011-303312 and by Swiss National Science Foundation awards 31003A-125350 and 31003A-143936 to EMZ. BMS was supported by a New Faculty Initiative Grant (NFIG) from Illinois State University College of Arts and Sciences. MHasselmann received financial support from the DFG. The work of FC, RG, and MM was supported by the Instituto Nacional de Bioinformatica (INB) from ISCIII in Spain. We thank Justin Reese and Christopher Childers for setting up genome annotation tools at Hymenoptera Genome Database.

Analysis of institutional authors

Guigo, RAuthorMariotti, MAuthorSantesmasses, DAuthorCâmara Ferreira, FranciscoAuthorGuigó Serra, RodericAuthor

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December 19, 2018
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Article

The genomes of two key bumblebee species with primitive eusocial organization

Publicated to:Genome Biology. 16 76- - 2015-04-24 16(), DOI: 10.1186/s13059-015-0623-3

Authors: Sadd, BM; Barribeau, SM; Bloch, G; de Graaf, DC; Dearden, P; Elsik, CG; Gadau, J; Grimmelikhuijzen, CJP; Hasselmann, M; Lozier, JD; Robertson, HM; Smagghe, G; Stolle, E; Van Vaerenbergh, M; Waterhouse, RM; Bornberg-Bauer, E; Klasberg, S; Bennett, AK; Câamara, F; Guigó, R; Hoff, K; Mariotti, M; Munoz-Torres, M; Murphy, T; Santesmasses, D; Amdam, GV; Beckers, M; Beye, M; Biewer, M; Bitondi, MMG; Blaxter, ML; Bourke, AFG; Brown, MJF; Buechel, SD; Cameron, R; Cappelle, K; Carolan, JC; Christiaens, O; Ciborowski, KL; Clarke, DF; Colgan, TJ; Collins, DH; Cridge, AG; Dalmay, T; Dreier, S; du Plessis, L; Duncan, E; Erler, S; Evans, J; Falcon, T; Flores, K; Freitas, FCP; Fuchikawa, T; Gempe, T; Hartfelder, K; Hauser, F; Helbing, S; Humann, FC; Irvine, F; Jermiin, LS; Johnson, CE; Johnson, RM; Jones, AK; Kadowaki, T; Kidner, JH; Koch, V; Köhler, A; Kraus, FB; Lattorff, HMG; Leask, M; Lockett, GA; Mallon, EB; Antonio, DSM; Marxer, M; Meeus, I; Moritz, RFA; Nair, A; Näpflin, K; Nissen, I; Niu, J; Nunes, FMF; Oakeshott, JG; Osborne, A; Otte, M; Pinheiro, DG; Rossié, N; Rueppell, O; Santos, CG; Schmid-Hempel, R; Schmitt, BD; Schulte, C; Simoes, ZLP; Soares, MPM; Swevers, L; Winnebeck, EC; Wolschin, F; Yu, N; Zdobnov, EM; Aqrawi, PK; Blankenburg, KP; Coyle, M; Francisco, L; Hernandez, AG; Holder, M; Hudson, ME; Jackson, L; Jayaseelan, J; Joshi, V; Kovar, C; Lee, SL; Mata, R; Mathew, T; Newsham, IF; Ngo, R; Okwuonu, G; Pham, C; Pu, LL; Saada, N; Santibanez, J; Simmons, D; Thornton, R; Venkat, A; Walden, KKO; Wu, YQ; Debyser, G; Devreese, B; Asher, C; Blommaert, J; Chipman, AD; Chittka, L; Fouks, B; Liu, J; O'Neill, MP; Sumner, S; Puiu, D; Qu, J; Salzberg, SL; Scherer, SE; Muzny, DM; Richards, S; Robinson, GE; Gibbs, RA; Schmid-Hempel, P; Worley, KC

Affiliations

Arizona State Univ, Sch Life Sci, Tempe, AZ 85287 USA - Author
be - Author
Box 56, Dunedin, 9054, New Zealand - Author
Center for Functional and Comparative Insect Genomics, Department of Biology, University of Copenhagen, Copenhagen, Denmark - Author
CSIRO, Land & Water Flagship, Canberra, ACT, Australia - Author
Ctr Genom Regulat CRG, Barcelona 08003, Spain - Author
Department of Biology, East Carolina University, Greenville, NC, 27858, USA - Author
Department of Biology, Georgetown University, Washington, DC, 20057, USA - Author
Department of Ecology, Evolution, and Behavior, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel - Author
Division of Animal Sciences, Division of Plant Sciences, and MU Informatics Institute, University of Missouri, Columbia, MO, 65211, USA - Author
E Carolina Univ, Dept Biol, Greenville, NC 27858 USA - Author
edu - Author
Ernst Moritz Arndt Univ Greifswald, Inst Math & Comp Sci, D-17487 Greifswald, Germany - Author
ETH, Inst Integrat Biol, Expt Ecol, CH-8092 Zurich, Switzerland - Author
Experimental Ecology, Institute of Integrative Biology, Eidgenössiche Technische Hochschule (ETH) Zürich, CH-8092, Zürich, Switzerland - Author
Georgetown Univ, Dept Biol, Washington, DC 20057 USA - Author
Hebrew Univ Jerusalem, Alexander Silberman Inst Life Sci, Dept Ecol Evolut & Behav, Jerusalem, Israel - Author
Illinois State Univ, Sch Biol Sci, Normal, IL 61790 USA - Author
Laboratory for Evolution and Development, Genetics Otago and the National Research Centre for Growth and Development, Department of Biochemistry, University of Otago, P - Author
Laboratory of Zoophysiology, Faculty of Sciences, Ghent University, Krijgslaan 281, S2, 9000, Ghent, Belgium - Author
Maynooth Univ, Dept Biol, Co, Kildare, Ireland - Author
MIT & Harvard, Broad Inst, Cambridge Ctr 7, Cambridge, MA 02142 USA - Author
MIT, Comp Sci & Artificial Intelligence Lab, Cambridge, MA 02139 USA - Author
Natl Lib Med, Natl Ctr Biotechnol Informat, Bethesda, MD 20894 USA - Author
Norwegian Univ Food Sci, Dept Chem Biotechnol & Food Sci, N-1432 As, Norway - Author
O - Author
Royal Holloway Univ London, Sch Biol Sci, London, England - Author
School of Biological Sciences, Illinois State University, Normal, IL, 61790, USA - Author
School of Life Sciences, Arizona State University, Tempe, AZ, 85287, USA - Author
Swiss Inst Bioinformat, CH-1211 Geneva, Switzerland - Author
Trin Coll Dublin, Sch Nat Sci, Dept Zool, Dublin, Ireland - Author
Univ Alabama, Dept Biol Sci, Tuscaloosa, AL 35487 USA - Author
Univ Bristol, Sch Biol Sci, Bristol BS8 1TQ, Avon, England - Author
Univ Calif Berkeley, Lawrence Berkeley Natl Lab, Genom Div, Berkeley, CA 94720 USA - Author
Univ Cologne, Inst Genet, Cologne, Germany - Author
Univ Copenhagen, Dept Biol, Ctr Funct & Comparat Insect Gen, Copenhagen, Denmark - Author
Univ Dusseldorf, Inst Evolut Genet, D-40225 Dusseldorf, Germany - Author
Univ E Anglia, Sch Biol Sci, Norwich NR4 7TJ, Norfolk, England - Author
Univ E Anglia, Sch Comp Sci, Norwich NR4 7TJ, Norfolk, England - Author
Univ Edinburgh, Ashworth Labs, Inst Evolutionary Biol & Edinburgh Gen, Edinburgh EH9 3FL, Midlothian, Scotland - Author
Univ Geneva, Sch Med, Dept Genet Med & Dev, CH-1211 Geneva, Switzerland - Author
Univ Ghent, Fac Biosci Engn, Dept Crop Protect, Lab Agrozool, B-9000 Ghent, Belgium - Author
Univ Ghent, Fac Sci, Lab Zoophysiol, B-9000 Ghent, Belgium - Author
Univ Halle Wittenberg, Inst Biol, Wittenberg, Germany - Author
Univ Hohenheim, Inst Anim Sci, D-70599 Stuttgart, Germany - Author
Univ Illinois, Dept Entomol, Urbana, IL 61801 USA - Author
Univ Missouri, Div Plant Sci, Div Anim Sci, Columbia, MO 65211 USA - Author
Univ Missouri, MU Informat Inst, Columbia, MO 65211 USA - Author
Univ Munster, Inst Evolut & Biodivers, D-48149 Munster, Germany - Author
Univ Otago, Dept Biochem, Labo Evolut & Dev Genet, Dunedin 9054, New Zealand - Author
Univ Otago, Dept Biochem, Natl Res Ctr Growth & Dev, Dunedin 9054, New Zealand - Author
Univ Sao Paulo, Dept Biol, Fac Filosofia Ciencias & Letras Ribeirao Preto, BR-14040901 Ribeirao Preto, Brazil - Author
UPF, Barcelona, Spain - Author
Zool Soc London, Inst Zool, London NW1 4RY, England - Author
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Abstract

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.

Keywords

Bee apis-melliferaBombus-terrestris linnaeusDna methylationDrosophila-melanogasterHigh-throughputHoney-beeMale courtship behaviorMultiple sequence alignmentPhylogenetic analysesSex-determination pathway

Quality index

Bibliometric impact. Analysis of the contribution and dissemination channel

The work has been published in the journal Genome Biology due to its progression and the good impact it has achieved in recent years, according to the agency WoS (JCR), it has become a reference in its field. In the year of publication of the work, 2015, it was in position 5/161, thus managing to position itself as a Q1 (Primer Cuartil), in the category Biotechnology & Applied Microbiology.

From a relative perspective, and based on the normalized impact indicator calculated from World Citations provided by WoS (ESI, Clarivate), it yields a value for the citation normalization relative to the expected citation rate of: 7.87. This indicates that, compared to works in the same discipline and in the same year of publication, it ranks as a work cited above average. (source consulted: ESI Nov 14, 2024)

This information is reinforced by other indicators of the same type, which, although dynamic over time and dependent on the set of average global citations at the time of their calculation, consistently position the work at some point among the top 50% most cited in its field:

  • Weighted Average of Normalized Impact by the Scopus agency: 7.41 (source consulted: FECYT Feb 2024)
  • Field Citation Ratio (FCR) from Dimensions: 35.74 (source consulted: Dimensions Jul 2025)

Specifically, and according to different indexing agencies, this work has accumulated citations as of 2025-07-16, the following number of citations:

  • WoS: 288
  • Scopus: 203
  • Europe PMC: 173

Impact and social visibility

From the perspective of influence or social adoption, and based on metrics associated with mentions and interactions provided by agencies specializing in calculating the so-called "Alternative or Social Metrics," we can highlight as of 2025-07-16:

  • The use, from an academic perspective evidenced by the Altmetric agency indicator referring to aggregations made by the personal bibliographic manager Mendeley, gives us a total of: 547.
  • The use of this contribution in bookmarks, code forks, additions to favorite lists for recurrent reading, as well as general views, indicates that someone is using the publication as a basis for their current work. This may be a notable indicator of future more formal and academic citations. This claim is supported by the result of the "Capture" indicator, which yields a total of: 578 (PlumX).

With a more dissemination-oriented intent and targeting more general audiences, we can observe other more global scores such as:

  • The Total Score from Altmetric: 98.15.
  • The number of mentions on the social network Facebook: 6 (Altmetric).
  • The number of mentions on the social network X (formerly Twitter): 43 (Altmetric).
  • The number of mentions on Wikipedia: 4 (Altmetric).
  • The number of mentions in news outlets: 9 (Altmetric).

It is essential to present evidence supporting full alignment with institutional principles and guidelines on Open Science and the Conservation and Dissemination of Intellectual Heritage. A clear example of this is:

  • The work has been submitted to a journal whose editorial policy allows open Open Access publication.

Leadership analysis of institutional authors

This work has been carried out with international collaboration, specifically with researchers from: Australia; Belgium; Brazil; China; Denmark; Germany; Greece; Israel; Japan; New Zealand; Norway; Switzerland; United Kingdom; United States of America.