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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.


Related in: MedlinePlus

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.
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Fig4: 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.

Mentions: Both bumblebee genomes contain components of all major immune pathways described in insects and exhibit a similar immune repertoire to A. mellifera (Additional file 2). The total number of immune genes in bumblebees is similar to A. mellifera, and therefore also considerably lower than in Dipteran model species (Figure 4). While numeric representation of immune components is similar, the bumblebee immune repertoire is not however completely undifferentiated from that of the honeybee. Both Bombus species have only a single copy of the antimicrobial peptide (AMP) defensin, which is present in two copies in A. mellifera, and have an expanded set of serine protease inhibitors. In B. terrestris, there are five, highly similar (average 75% sequence similarity), putative serpin 3/4-like genes, while only a single ortholog is identified in A. mellifera. A homolog of the apoptosis-involved caspase decay, which has not been described in either A. mellifera or the parasitoid wasp N. vitripennis, and a Hymenoptera-specific clade of caspases that are most similar to Ice in Drosophila are also present. A recently duplicated species-specific peptidoglycan receptor protein (PGRP) is present in B. impatiens. Further in-depth analyses are reported in a companion paper on immune genes [145]. Quantitative expression analyses in B. terrestris confirm expression changes of many immune-related genes following immune-stimulation. Interacting with parasites, including those that are co-evolving, make immune genes an interesting focus of molecular evolution studies. In the bumblebees, patterns of evolutionary selection differ across immune system components, with certain genes showing lineage-specific patterns of selection. Broadly however, the comparative analysis of immune genes present in the two bumblebee genomes show a reduced immune complement is not the result of honeybee-specific traits or those relating to complex social defenses in advanced eusocial organisms, such as hygienic behavior, but is instead basal in the bees and independent of the level of sociality [145].Figure 4


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)

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

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

Fig4: 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.
Mentions: Both bumblebee genomes contain components of all major immune pathways described in insects and exhibit a similar immune repertoire to A. mellifera (Additional file 2). The total number of immune genes in bumblebees is similar to A. mellifera, and therefore also considerably lower than in Dipteran model species (Figure 4). While numeric representation of immune components is similar, the bumblebee immune repertoire is not however completely undifferentiated from that of the honeybee. Both Bombus species have only a single copy of the antimicrobial peptide (AMP) defensin, which is present in two copies in A. mellifera, and have an expanded set of serine protease inhibitors. In B. terrestris, there are five, highly similar (average 75% sequence similarity), putative serpin 3/4-like genes, while only a single ortholog is identified in A. mellifera. A homolog of the apoptosis-involved caspase decay, which has not been described in either A. mellifera or the parasitoid wasp N. vitripennis, and a Hymenoptera-specific clade of caspases that are most similar to Ice in Drosophila are also present. A recently duplicated species-specific peptidoglycan receptor protein (PGRP) is present in B. impatiens. Further in-depth analyses are reported in a companion paper on immune genes [145]. Quantitative expression analyses in B. terrestris confirm expression changes of many immune-related genes following immune-stimulation. Interacting with parasites, including those that are co-evolving, make immune genes an interesting focus of molecular evolution studies. In the bumblebees, patterns of evolutionary selection differ across immune system components, with certain genes showing lineage-specific patterns of selection. Broadly however, the comparative analysis of immune genes present in the two bumblebee genomes show a reduced immune complement is not the result of honeybee-specific traits or those relating to complex social defenses in advanced eusocial organisms, such as hygienic behavior, but is instead basal in the bees and independent of the level of sociality [145].Figure 4

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.


Related in: MedlinePlus