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The genomes of two key bumblebee species with primitive eusocial organization.

Sadd BM, Barribeau SM, Bloch G, de Graaf DC, Dearden P, Elsik CG, Gadau J, Grimmelikhuijzen CJ, Hasselmann M, Lozier JD, Robertson HM, Smagghe G, Stolle E, Van Vaerenbergh M, Waterhouse RM, Bornberg-Bauer E, Klasberg S, Bennett AK, Câmara F, Guigó R, Hoff K, Mariotti M, Munoz-Torres M, Murphy T, Santesmasses D, Amdam GV, Beckers M, Beye M, Biewer M, Bitondi MM, Blaxter ML, Bourke AF, Brown MJ, 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 FC, 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 HM, Leask M, Lockett GA, Mallon EB, Antonio DS, Marxer M, Meeus I, Moritz RF, Nair A, Näpflin K, Nissen I, Niu J, Nunes FM, Oakeshott JG, Osborne A, Otte M, Pinheiro DG, Rossié N, Rueppell O, Santos CG, Schmid-Hempel R, Schmitt BD, Schulte C, Simões ZL, Soares MP, 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 KK, 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 - Genome Biol. (2015)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: School of Biological Sciences, Illinois State University, Normal, IL, 61790, USA. bmsadd@ilstu.edu.

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.

No MeSH data available.


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.
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Fig1: 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.

Mentions: The ‘primitively eusocial’ bumblebees (Bombus spp., Bombini) share some traits with advanced eusocial bees, yet lack particular aspects that would qualify them as advanced eusocial organisms (Table 1). In comparison to honeybees, they have queen-worker caste differentiation based mainly on body size and physiology, annual colonies of hundreds rather than many thousands of individuals, and worker offspring that have lost the ability to mate, but can reproduce readily by laying haploid (male) eggs [20]. Bumblebees typically exhibit an annual colony cycle (Figure 1), although perennial colonies have been recorded in some bumblebee species such as the neotropical B. atratus [21], and social parasitic cuckoo bumblebees do not found their own colonies. There is a clear value to investigating bumblebees as they hold a key, intermediate position on the eusocial spectrum.Table 1


The genomes of two key bumblebee species with primitive eusocial organization.

Sadd BM, Barribeau SM, Bloch G, de Graaf DC, Dearden P, Elsik CG, Gadau J, Grimmelikhuijzen CJ, Hasselmann M, Lozier JD, Robertson HM, Smagghe G, Stolle E, Van Vaerenbergh M, Waterhouse RM, Bornberg-Bauer E, Klasberg S, Bennett AK, Câmara F, Guigó R, Hoff K, Mariotti M, Munoz-Torres M, Murphy T, Santesmasses D, Amdam GV, Beckers M, Beye M, Biewer M, Bitondi MM, Blaxter ML, Bourke AF, Brown MJ, 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 FC, 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 HM, Leask M, Lockett GA, Mallon EB, Antonio DS, Marxer M, Meeus I, Moritz RF, Nair A, Näpflin K, Nissen I, Niu J, Nunes FM, Oakeshott JG, Osborne A, Otte M, Pinheiro DG, Rossié N, Rueppell O, Santos CG, Schmid-Hempel R, Schmitt BD, Schulte C, Simões ZL, Soares MP, 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 KK, 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 - Genome Biol. (2015)

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.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4414376&req=5

Fig1: 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.
Mentions: The ‘primitively eusocial’ bumblebees (Bombus spp., Bombini) share some traits with advanced eusocial bees, yet lack particular aspects that would qualify them as advanced eusocial organisms (Table 1). In comparison to honeybees, they have queen-worker caste differentiation based mainly on body size and physiology, annual colonies of hundreds rather than many thousands of individuals, and worker offspring that have lost the ability to mate, but can reproduce readily by laying haploid (male) eggs [20]. Bumblebees typically exhibit an annual colony cycle (Figure 1), although perennial colonies have been recorded in some bumblebee species such as the neotropical B. atratus [21], and social parasitic cuckoo bumblebees do not found their own colonies. There is a clear value to investigating bumblebees as they hold a key, intermediate position on the eusocial spectrum.Table 1

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: School of Biological Sciences, Illinois State University, Normal, IL, 61790, USA. bmsadd@ilstu.edu.

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.

No MeSH data available.