A second generation genetic map of the bumblebee Bombus terrestris (Linnaeus, 1758) reveals slow genome and chromosome evolution in the Apidae

BackgroundThe bumblebee Bombus terrestris is an ecologically and economically important pollinator and has become an important biological model system. To study fundamental evolutionary questions at the genomic level, a high resolution genetic linkage map is an essential tool for analyses ranging from quantitative trait loci (QTL) mapping to genome assembly and comparative genomics. We here present a saturated linkage map and match it with the Apis mellifera genome using homologous markers. This genome-wide comparison allows insights into structural conservations and rearrangements and thus the evolution on a chromosomal level.ResultsThe high density linkage map covers ~ 93% of the B. terrestris genome on 18 linkage groups (LGs) and has a length of 2'047 cM with an average marker distance of 4.02 cM. Based on a genome size of ~ 430 Mb, the recombination rate estimate is 4.76 cM/Mb. Sequence homologies of 242 homologous markers allowed to match 15 B. terrestris with A. mellifera LGs, five of them as composites. Comparing marker orders between both genomes we detect over 14% of the genome to be organized in synteny and 21% in rearranged blocks on the same homologous LG.ConclusionsThis study demonstrates that, despite the very high recombination rates of both A. mellifera and B. terrestris and a long divergence time of about 100 million years, the genomes' genetic architecture is highly conserved. This reflects a slow genome evolution in these bees. We show that data on genome organization and conserved molecular markers can be used as a powerful tool for comparative genomics and evolutionary studies, opening up new avenues of research in the Apidae.

[1]  R. Reinhardt,et al.  Analysis of a normalised expressed sequence tag (EST) library from a key pollinator, the bumblebee Bombus terrestris , 2010, BMC Genomics.

[2]  W. Jordan,et al.  Differential gene expression in queen–worker caste determination in bumble-bees , 2005, Proceedings of the Royal Society B: Biological Sciences.

[3]  The Honeybee Genome Sequencing Consortium,et al.  Erratum: Insights into social insects from the genome of the honeybee Apis mellifera , 2006, Nature.

[4]  M. Solignac,et al.  Control of reproductive dominance by the thelytoky gene in honeybees , 2007, Biology Letters.

[5]  H. Velthuis,et al.  Diploid males in the bumble bee Bombus terrestris , 1994 .

[6]  R. Whetten,et al.  Construction of an AFLP genetic map with nearly complete genome coverage in Pinus taeda , 1999, Theoretical and Applied Genetics.

[7]  V. HayoH.W. A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination * , 2006 .

[8]  J. Cornuet,et al.  A third-generation microsatellite-based linkage map of the honey bee, Apis mellifera, and its comparison with the sequence-based physical map , 2007, Genome Biology.

[9]  R. Moritz,et al.  Male flight distance and population substructure in the bumblebee Bombus terrestris. , 2009, The Journal of animal ecology.

[10]  Jack A. M. Leunissen,et al.  Turning CFCs into salt. , 1996, Nucleic Acids Res..

[11]  Rongling Wu,et al.  Statistical Genetics of Quantitative Traits: Linkage, Maps and QTL , 2007 .

[12]  Colin N. Dewey,et al.  Discovery of functional elements in 12 Drosophila genomes using evolutionary signatures , 2007, Nature.

[13]  Eric Depiereux,et al.  2× genomes - depth does matter , 2010, Genome Biology.

[14]  C. Fenster,et al.  Quantitative trait locus analyses and the study of evolutionary process , 2004, Molecular ecology.

[15]  D. Grattapaglia,et al.  A microsatellite-based consensus linkage map for species of Eucalyptus and a novel set of 230 microsatellite markers for the genus , 2006, BMC Plant Biology.

[16]  C. Michener,et al.  The oldest fossil bee: Apoid history, evolutionary stasis, and antiquity of social behavior. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Seán G. Brady,et al.  The history of early bee diversification based on five genes plus morphology , 2006, Proceedings of the National Academy of Sciences.

[18]  Melanie A. Huntley,et al.  Evolution of genes and genomes on the Drosophila phylogeny , 2007, Nature.

[19]  References , 1971 .

[20]  T. A. Hall,et al.  BIOEDIT: A USER-FRIENDLY BIOLOGICAL SEQUENCE ALIGNMENT EDITOR AND ANALYSIS PROGRAM FOR WINDOWS 95/98/ NT , 1999 .

[21]  B. Baer Bumblebees as model organisms to study male sexual selection in social insects , 2003, Behavioral Ecology and Sociobiology.

[22]  D. D. Kosambi The estimation of map distances from recombination values. , 1943 .

[23]  D. Galbraith,et al.  Reference standards for determination of DNA content of plant nuclei. , 1999, American journal of botany.

[24]  T. Anderson,et al.  Genomic linkage map of the human blood fluke Schistosoma mansoni , 2009, Genome Biology.

[25]  J. Cornuet,et al.  A Microsatellite-Based Linkage Map of the Honeybee, Apis mellifera L. , 2004, Genetics.

[26]  K. Katoh,et al.  MAFFT version 5: improvement in accuracy of multiple sequence alignment , 2005, Nucleic acids research.

[27]  Rongling Wu,et al.  Comprar Statistical Genetics of Quantitative Traits · Linkage, Maps and QTL | Casella, George | 9780387203348 | Springer , 2007 .

[28]  Z. Sha,et al.  Construction of Genetic Linkage Maps and Comparative Genome Analysis of Catfish Using Gene-Associated Markers , 2009, Genetics.

[29]  Readman Chiu,et al.  A high-resolution whole-genome cattle-human comparative map reveals details of mammalian chromosome evolution. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[30]  UNEXPECTED CONSEQUENCES OF POLYANDRY FOR PARASITISM AND FITNESS IN THE BUMBLEBEE, BOMBUS TERRESTRIS , 2001, Evolution; international journal of organic evolution.

[31]  M. Solignac,et al.  Novel microsatellite DNA loci for Bombus terrestris (Linnaeus, 1758) , 2009, Molecular ecology resources.

[32]  P. Schmid-Hempel,et al.  Variation in genomic recombination rates among animal taxa and the case of social insects , 2007, Heredity.

[33]  P. Schmid-Hempel,et al.  Natural variation in the genetic architecture of a host–parasite interaction in the bumblebee Bombus terrestris , 2007, Molecular ecology.

[34]  H. Scherthan,et al.  Emerging patterns of comparative genome organization in some mammalian species as revealed by Zoo-FISH. , 1998, Genome research.

[35]  Susan J. Brown,et al.  Genetic Linkage Maps of the Red Flour Beetle, Tribolium castaneum, Based on Bacterial Artificial Chromosomes and Expressed Sequence Tags , 2005, Genetics.

[36]  S. Lidgard,et al.  Quantitative analyses of the early angiosperm radiation , 1988, Nature.

[37]  L. Steinmetz,et al.  High-resolution mapping of meiotic crossovers and non-crossovers in yeast , 2008, Nature.

[38]  R. Moritz,et al.  Recombination Rate and AT-content Show Opposite Correlations in Mammalian and Other Animal Genomes , 2008, Evolutionary Biology.

[39]  Anthony Levasseur,et al.  Ancestral animal genomes reconstruction. , 2007, Current opinion in immunology.

[40]  Xiaoping Chen,et al.  A SSR-based composite genetic linkage map for the cultivated peanut (Arachis hypogaea L.) genome , 2010, BMC Plant Biology.

[41]  J. Tomkins,et al.  Construction and characterization of a BAC-library for a key pollinator, the bumblebee Bombus terrestris L. , 2009, Insectes Sociaux.

[42]  Fengtang Yang,et al.  Comparative genome maps of the pangolin, hedgehog, sloth, anteater and human revealed by cross-species chromosome painting: further insight into the ancestral karyotype and genome evolution of eutherian mammals , 2006, Chromosome Research.

[43]  A. R. Wagner Molecular Biology and Evolution , 2001 .

[44]  J. Cornuet,et al.  Size homoplasy and mutational processes of interrupted microsatellites in two bee species, Apis mellifera and Bombus terrestris (Apidae). , 1995, Molecular biology and evolution.

[45]  D. Tautz,et al.  Tri‐ and tetranucleotide microsatellite loci in honey bees (Apis mellifera)  —  a step towards quantitative genotyping , 1999, Molecular ecology.

[46]  S. Wing Evolution and Expansion of Flowering Plants , 2000 .

[47]  L. Gianfranceschi,et al.  Creating a saturated reference map for the apple (Malus × domestica Borkh.) genome , 2003, Theoretical and Applied Genetics.

[48]  P. Stam,et al.  Construction of integrated genetic linkage maps by means of a new computer package: JOINMAP. , 1993 .

[49]  A. Chakravarti A graphical representation of genetic and physical maps: the Marey map. , 1991, Genomics.

[50]  H. Hoshiba,et al.  Chromosome Evolution of Bees and Wasps (Hymenoptera, Apocrita) on the Basis of C-banding Pattern Analyses , 1993 .

[51]  P. Pevzner,et al.  Reconstructing the genomic architecture of ancestral mammals: lessons from human, mouse, and rat genomes. , 2004, Genome research.

[52]  P. Schmid-Hempel,et al.  THE GENETIC ARCHITECTURE OF IMMUNE DEFENSE AND REPRODUCTION IN MALE BOMBUS TERRESTRIS BUMBLEBEES , 2007, Evolution; international journal of organic evolution.

[53]  P. Lindhout,et al.  Comparison and integration of four barley genetic maps. , 1996, Genome.

[54]  J. Aerts,et al.  Construction of bovine whole-genome radiation hybrid and linkage maps using high-throughput genotyping , 2007, Animal genetics.

[55]  M. Matz,et al.  Construction of a high-resolution genetic linkage map and comparative genome analysis for the reef-building coral Acropora millepora , 2009, Genome Biology.

[56]  H. Hines Historical biogeography, divergence times, and diversification patterns of bumble bees (Hymenoptera: Apidae: Bombus). , 2008, Systematic biology.

[57]  P. Pevzner,et al.  Genome rearrangements in mammalian evolution: lessons from human and mouse genomes. , 2003, Genome research.

[58]  T. Glenn,et al.  A genetic linkage map for the saltwater crocodile (Crocodylus porosus) , 2009, BMC Genomics.

[59]  N. Archidiacono,et al.  Primate chromosome evolution: Ancestral karyotypes, marker order and neocentromeres , 2008, Chromosome Research.

[60]  M. Haberl,et al.  Five hundred and fifty microsatellite markers for the study of the honeybee (Apis mellifera L.) genome , 2003 .

[61]  K. Lange,et al.  How many polymorphic genes will it take to span the human genome? , 1982, American journal of human genetics.

[62]  T. Ryan Gregory,et al.  Eukaryotic genome size databases , 2006, Nucleic Acids Res..

[63]  Tomohito Itoh,et al.  A comprehensive radiation hybrid map of the bovine genome comprising 5593 loci. , 2005, Genomics.

[64]  Roeland E. Voorrips,et al.  Software for the calculation of genetic linkage maps , 2001 .

[65]  Richard Reinhardt,et al.  The European sea bass Dicentrarchus labrax genome puzzle: comparative BAC-mapping and low coverage shotgun sequencing , 2010, BMC Genomics.

[66]  C. Kearns Bumblebees—Their Behavior and Ecology , 2004 .

[67]  T. Murray,et al.  Cryptic species diversity in a widespread bumble bee complex revealed using mitochondrial DNA RFLPs , 2008, Conservation Genetics.

[68]  R. Agarwala,et al.  A 4,103 marker integrated physical and comparative map of the horse genome , 2008, Cytogenetic and Genome Research.

[69]  D. Goulson Bumblebees: their behaviour and ecology. , 2003 .

[70]  P. Pevzner,et al.  Dynamics of Mammalian Chromosome Evolution Inferred from Multispecies Comparative Maps , 2005, Science.

[71]  T. Markow,et al.  Analysis of Drosophila Species Genome Size and Satellite DNA Content Reveals Significant Differences Among Strains as Well as Between Species , 2007, Genetics.

[72]  L Nardi,et al.  Plant Genome Size Estimation by Flow Cytometry: Inter-laboratory Comparison , 1998 .

[73]  P. Schmid-Hempel,et al.  A core linkage map of the bumblebee Bombus terrestris. , 2006, Genome.

[74]  O. Rueppell,et al.  Comparative linkage mapping suggests a high recombination rate in all honeybees. , 2010, The Journal of heredity.

[75]  Denis Milan,et al.  Piggy-BACing the human genome II. A high-resolution, physically anchored, comparative map of the porcine autosomes. , 2005, Genomics.

[76]  L. Chittka,et al.  The dynamics of social learning in an insect model, the bumblebee (Bombus terrestris) , 2007, Behavioral Ecology and Sociobiology.

[77]  Gary Stone,et al.  Towards the delineation of the ancestral eutherian genome organization: comparative genome maps of human and the African elephant (Loxodonta africana) generated by chromosome painting , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[78]  Yaqin Ma,et al.  BatchPrimer3: A high throughput web application for PCR and sequencing primer design , 2008, BMC Bioinformatics.

[79]  M. Daly,et al.  MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. , 1987, Genomics.

[80]  K. Kjer,et al.  Ancient rapid radiations of insects: challenges for phylogenetic analysis. , 2008, Annual review of entomology.

[81]  J. Nadeau,et al.  Lengths of chromosomal segments conserved since divergence of man and mouse. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[82]  T. Laverty,et al.  The Ecology and Sociobiology of Bumble Bees , 1984 .

[83]  B. Robertson,et al.  Determination of DNA Content of Aquatic Bacteria by Flow Cytometry , 2001, Applied and Environmental Microbiology.

[84]  R. Voorrips MapChart: software for the graphical presentation of linkage maps and QTLs. , 2002, The Journal of heredity.

[85]  A. Wille,et al.  A linkage analysis of sex determination in Bombus terrestris (L.) (Hymenoptera: Apidae) , 2001, Heredity.

[86]  R. Crozier,et al.  Infection with the trypanosome Crithidia bombi and expression of immune-related genes in the bumblebee Bombus terrestris. , 2010, Developmental and comparative immunology.

[87]  J. Willis,et al.  A genetic map in the Mimulus guttatus species complex reveals transmission ratio distortion due to heterospecific interactions. , 2001, Genetics.

[88]  J. Cornuet,et al.  Characterization of (GT)n and (CT)n microsatellites in two insect species: Apis mellifera and Bombus terrestris. , 1993, Nucleic acids research.

[89]  P. Mardulyn,et al.  Multiple molecular data sets suggest independent origins of highly eusocial behavior in bees (Hymenoptera:Apinae). , 2001, Systematic biology.

[90]  T. Speed,et al.  Statistical analysis of crossover interference using the chi-square model. , 1995, Genetics.

[91]  A. Meyer,et al.  A Microsatellite-Based Genetic Linkage Map of the Cichlid Fish, Astatotilapia burtoni (Teleostei): A Comparison of Genomic Architectures Among Rapidly Speciating Cichlids , 2009, Genetics.

[92]  M. Engel A Giant Honey Bee from the Middle Miocene of Japan (Hymenoptera: Apidae) , 2006 .

[93]  R. E. Page,et al.  The Gene csd Is the Primary Signal for Sexual Development in the Honeybee and Encodes an SR-Type Protein , 2003, Cell.

[94]  P. Schmid-Hempel,et al.  Microsatellite loci for Bombus spp. , 2006 .

[95]  Thomas Faraut,et al.  Addressing chromosome evolution in the whole-genome sequence era , 2008, Chromosome Research.

[96]  J. Feder,et al.  Evidence for Broad-Scale Conservation of Linkage Map Relationships Between Rhagoletis pomonella (Diptera: Tephritidae) and Drosophila melanogaster (Diptera: Drosophilidae) , 2001 .