Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2015 Apr 24;16(1):76.
doi: 10.1186/s13059-015-0623-3.

The genomes of two key bumblebee species with primitive eusocial organization

Ben M Sadd  1   2 , Seth M Barribeau  3   4 , Guy Bloch  5 , Dirk C de Graaf  6 , Peter Dearden  7 , Christine G Elsik  8   9 , Jürgen Gadau  10 , Cornelis J P Grimmelikhuijzen  11 , Martin Hasselmann  12 , Jeffrey D Lozier  13 , Hugh M Robertson  14 , Guy Smagghe  15 , Eckart Stolle  16 , Matthias Van Vaerenbergh  17 , Robert M Waterhouse  18   19   20   21 , Erich Bornberg-Bauer  22 , Steffen Klasberg  23 , Anna K Bennett  24 , Francisco Câmara  25   26 , Roderic Guigó  27   28 , Katharina Hoff  29 , Marco Mariotti  30   31 , Monica Munoz-Torres  32   33 , Terence Murphy  34 , Didac Santesmasses  35   36 , Gro V Amdam  37   38 , Matthew Beckers  39 , Martin Beye  40 , Matthias Biewer  41   42 , Márcia M G Bitondi  43 , Mark L Blaxter  44 , Andrew F G Bourke  45 , Mark J F Brown  46 , Severine D Buechel  47 , Rossanah Cameron  48 , Kaat Cappelle  49 , James C Carolan  50 , Olivier Christiaens  51 , Kate L Ciborowski  52 , David F Clarke  53 , Thomas J Colgan  54 , David H Collins  55 , Andrew G Cridge  56 , Tamas Dalmay  57 , Stephanie Dreier  58 , Louis du Plessis  59   60   61 , Elizabeth Duncan  62 , Silvio Erler  63 , Jay Evans  64 , Tiago Falcon  65 , Kevin Flores  66 , Flávia C P Freitas  67 , Taro Fuchikawa  68   69 , Tanja Gempe  70 , Klaus Hartfelder  71 , Frank Hauser  72 , Sophie Helbing  73 , Fernanda C Humann  74 , Frano Irvine  75 , Lars S Jermiin  76 , Claire E Johnson  14 , Reed M Johnson  77 , Andrew K Jones  78 , Tatsuhiko Kadowaki  79 , Jonathan H Kidner  80 , Vasco Koch  81 , Arian Köhler  82 , F Bernhard Kraus  83   84 , H Michael G Lattorff  85   86 , Megan Leask  87 , Gabrielle A Lockett  88 , Eamonn B Mallon  89 , David S Marco Antonio  90 , Monika Marxer  91 , Ivan Meeus  92 , Robin F A Moritz  93 , Ajay Nair  94 , Kathrin Näpflin  95 , Inga Nissen  96 , Jinzhi Niu  97 , Francis M F Nunes  98 , John G Oakeshott  99 , Amy Osborne  100 , Marianne Otte  101 , Daniel G Pinheiro  102 , Nina Rossié  103 , Olav Rueppell  104 , Carolina G Santos  105 , Regula Schmid-Hempel  106 , Björn D Schmitt  107 , Christina Schulte  108 , Zilá L P Simões  109 , Michelle P M Soares  110 , Luc Swevers  111 , Eva C Winnebeck  112 , Florian Wolschin  113   114 , Na Yu  115 , Evgeny M Zdobnov  116   117 , Peshtewani K Aqrawi  118 , Kerstin P Blankenburg  119 , Marcus Coyle  120 , Liezl Francisco  121 , Alvaro G Hernandez  122 , Michael Holder  123 , Matthew E Hudson  124 , LaRonda Jackson  125 , Joy Jayaseelan  126 , Vandita Joshi  127 , Christie Kovar  128 , Sandra L Lee  129 , Robert Mata  130 , Tittu Mathew  131 , Irene F Newsham  132 , Robin Ngo  133 , Geoffrey Okwuonu  134 , Christopher Pham  135 , Ling-Ling Pu  136 , Nehad Saada  137 , Jireh Santibanez  138 , DeNard Simmons  139 , Rebecca Thornton  140 , Aarti Venkat  141 , Kimberly K O Walden  142 , Yuan-Qing Wu  143 , Griet Debyser  144 , Bart Devreese  145 , Claire Asher  146 , Julie Blommaert  147 , Ariel D Chipman  148 , Lars Chittka  149 , Bertrand Fouks  150   151 , Jisheng Liu  152   153 , Meaghan P O'Neill  154 , Seirian Sumner  155 , Daniela Puiu  156 , Jiaxin Qu  157 , Steven L Salzberg  158 , Steven E Scherer  159 , Donna M Muzny  160 , Stephen Richards  161 , Gene E Robinson  162 , Richard A Gibbs  163 , Paul Schmid-Hempel  164 , Kim C Worley  165
Affiliations

The genomes of two key bumblebee species with primitive eusocial organization

Ben M Sadd et al. Genome Biol. .

Abstract

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.

PubMed Disclaimer

Figures

Figure 1
Figure 1
An illustrative colony cycle of bumblebee species living in temperate regions (a). This is representative of the colony cycles of Bombus terrestris (b) and B. impatiens (c). Queen bumblebees emerge from hibernation, establish a nest as a single foundress and provision it with pollen and nectar. Egg batches are laid that develop into female worker offspring. Once these offspring have developed and emerged as adults they take over foraging duties from the queen, and tend to developing brood. After sustained colony growth, males and new queens are produced. These sexuals leave the colony and mate. The new queens hibernate while males and the remainder of the colony perish.
Figure 2
Figure 2
Bumblebee orthology with selected Hymenopterans and representative species from other insect orders. The maximum likelihood phylogenetic tree built from the concatenated alignments of 2,294 single-copy orthologs recovers the expected phylogeny rooted with the human body louse, Pediculus humanus. The tree highlights the pairs of closely-related bumblebees (Bombus terrestris and Bombus impatiens), honeybees (Apis mellifera and Apis florea), and fungus-growing ants (Atta cephalotes and Acromyrmex echinatior). It also shows slow average rates of molecular evolution in the Hymenopterans, similar to the flour beetle, Tribolium castaneum, but much slower than the silk moth, Bombyx mori, the malaria mosquito, Anopheles gambiae, and the fruit fly, Drosophila melanogaster. The bars represent the total gene counts in each species partitioned according to their homology to genes in the other species and other arthropods: from universally present single-copy orthologs (dark blue, left) to lineage-specific orthologs, and genes with no detectable orthology (gray, right). A small fraction made up of about 100 to 150 genes in each of the bee and ant species exhibit orthology only to genes from the most closely-related species (red, green, purple). The inset boxplots show the distributions of percent amino acid identities between pairs of Bombus, Apis, and Attini (ants) universal single-copy orthologs, where the identity is much higher between the bumblebee orthologs than between the honeybees or the ants.
Figure 3
Figure 3
Section of the phylogenetic tree of the Bombus terrestris, Apis mellifera, and Drosophila melanogaster gustatory receptors (GRs) showing the impressive B. terrestris-specific expansion. This is a corrected distance tree. B. terrestris and A. mellifera proteins are highlighted in orange and blue, respectively, as are the branches leading to them to emphasize gene lineages. Bootstrap support level in percentage of 10,000 replications of uncorrected distance analysis is shown above major branches. The full phylogenetic tree of GRs can be found in Additional file 1.
Figure 4
Figure 4
Immune gene counts in bumblebees relative to selected insects. Number of genes belonging to 29 categories of immune genes are presented in the cells. Heat colours in a cell reflect the number of genes in that category relative to those other species (light blue: fewer - dark red: more). The tree represents a clustering analysis using Euclidean distances based on the number of genes within these groups. AMP = Antimicrobial peptide, APHAG = Autophagy, CASP = Caspase, CASPA = Caspase A, CAT = Catalase, CLIP = CLIP serine protease, CTL = C-type lectin, FREP = Fibrinogen-like, GALE = Galectin, GNBP = Gram-negative binding protein/Beta-glucan recognition protein, IAP = IAP repeat, IGG = Immunoglobulin, IMDPATH = Imd pathway, JAKSTAT = JAK/STAT pathway, LYS = Lysozyme, ML = MD-2-related lipid recognition, NIMROD = nimrod, PGRP = Peptidoglycan recognition protein, PPO = Prophenoloxidase, PRDX = Peroxidase, REL = Relish, SCR = Scavenger receptor, SOD = Superoxide dismutase, SPZ = Spatzle, SRPN = Serine protease inhibitor, SRRP = Small RNA regulatory pathway, TEP = Thioester-containing protein, TOLL = Toll genes, TOLLPATH = Toll pathway.
Figure 5
Figure 5
Venn diagram of the distribution of unique and shared miRNAs across the two bumblebee species investigated and Apis mellifera. A total of 116 miRNAs were found in the genomes of all three species. Strikingly, 103 miRNAs of the 219 in A. mellifera were not found in the genome of either bumblebee species.
See this image and copyright information in PMC

Comment in

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Maynard Smith J, Szathmary E. The major evolutionary transitions. Nature. 1995;374:227–232. - PubMed
    1. Bourke AF. The validity and value of inclusive fitness theory. Proc R Soc B. 2011;278:3313–3320. - PMC - PubMed
    1. Crozier R, Pamilo P. Evolution of social insect colonies: Sex allocation and kin selection. Oxford: Oxford University Press; 1996.
    1. Hughes WO, Oldroyd BP, Beekman M, Ratnieks FL. Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science. 2008;320:1213–1216. - PubMed
    1. Hamilton WD. The genetical evolution of social behaviour I. J Theor Biol. 1964;7:1–16. - PubMed

Publication types

MeSH terms