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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.


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.
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Fig5: 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.

Mentions: Here, a diverse complement of methods was used to identify miRNAs in the bumblebee genomes, including sequencing of miRNAs in B. terrestris, a homology search of A. mellifera miRNAs from miRBase [154], and miRNA prediction using miRCat [155] and miR-abela [156]. These methods identified 130 and 115 miRNAs in B. terrestris and B. impatiens, respectively (Additional file 2), including a number of previously uncharacterized miRNAs in B. terrestris. Of these bumblebee miRNAs, 17 miRNAs had not previously been identified in A. mellifera. Comparing new miRNAs back to the A. mellifera genome revealed that two miRNAs are conserved across the two bumblebee species and A. mellifera, but 14 miRNAs were unique to one of the two bumblebee species, with five being unique to B. terrestris and one potentially representing a unique duplicated miRNA in B. impatiens (Figure 5).Figure 5


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)

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

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

Fig5: 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.
Mentions: Here, a diverse complement of methods was used to identify miRNAs in the bumblebee genomes, including sequencing of miRNAs in B. terrestris, a homology search of A. mellifera miRNAs from miRBase [154], and miRNA prediction using miRCat [155] and miR-abela [156]. These methods identified 130 and 115 miRNAs in B. terrestris and B. impatiens, respectively (Additional file 2), including a number of previously uncharacterized miRNAs in B. terrestris. Of these bumblebee miRNAs, 17 miRNAs had not previously been identified in A. mellifera. Comparing new miRNAs back to the A. mellifera genome revealed that two miRNAs are conserved across the two bumblebee species and A. mellifera, but 14 miRNAs were unique to one of the two bumblebee species, with five being unique to B. terrestris and one potentially representing a unique duplicated miRNA in B. impatiens (Figure 5).Figure 5

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.