Skip to main content
SpringerLink
Log in

High-resolution linkage map for two honeybee chromosomes: the hotspot quest

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Meiotic recombination is a fundamental process ensuring proper disjunction of homologous chromosomes and allele shuffling in successive generations. In many species, this cellular mechanism occurs heterogeneously along chromosomes and mostly concentrates in tiny fragments called recombination hotspots. Specific DNA motifs have been shown to initiate recombination in these hotspots in mammals, fission yeast and drosophila. The aim of this study was to check whether recombination also occurs in a heterogeneous fashion in the highly recombinogenic honeybee genome and whether this heterogeneity can be connected with specific DNA motifs. We completed a previous picture drawn from a routine genetic map built with an average resolution of 93 kb. We focused on the two smallest honeybee chromosomes to increase the resolution and even zoomed at very high resolution (3.6 kb) on a fragment of 300 kb. Recombination rates measured in these fragments were placed in relation with occurrence of 30 previously described motifs through a Poisson regression model. A selection procedure suitable for correlated variables was applied to keep significant motifs. These fine and ultra-fine mappings show that recombination rate is significantly heterogeneous although poorly contrasted between high and low recombination rate, contrarily to most model species. We show that recombination rate is probably associated with the DNA methylation state. Moreover, three motifs (CGCA, GCCGC and CCAAT) are good candidates of signals promoting recombination. Their influence is however moderate, doubling at most the recombination rate. This discovery extends the way to recombination dissection in insects.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Arnheim N, Calabrese P, Nordborg M (2003) Hot and cold spots of recombination in the human genome: the reason we should find them and how this can be achieved. Am J Hum Genet 73(1):5–16

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Barnes TM, Kohara Y, Coulson A, Hekimi S (1995) Meiotic recombination, noncoding DNA and genomic organization in Caenorhabditis elegans. Genetics 141(1):159–179

    CAS  PubMed  Google Scholar 

  • Baudat F, Buard J, Grey C, Fledel-Alon A, Ober C, Przeworski M, Coop G, de Massy B (2010) PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327(5967):836–840

    Article  CAS  PubMed  Google Scholar 

  • Beaume N, Chowdhury S (2011) G-Quadruplexes evolution: lessons from bacterial genomes. In: 5th Indo-French bioinformatics meeting, centre for DNA fingerprinting and diagnostics (CDFD), Hyderabad 500 001, India

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc: Ser B (Methodol) 57(1):289–300

    Google Scholar 

  • Berg IL, Neumann R, Sarbajna S, Odenthal-Hesse L, Butler NJ, Jeffreys AJ (2011) Variants of the protein PRDM9 differentially regulate a set of human meiotic recombination hotspots highly active in African populations. Proc Natl Acad Sci USA 108(30):12378–12383

    Article  CAS  PubMed  Google Scholar 

  • Bessoltane N, Toffano-Nioche C, Solignac M, Mougel F (2012) Fine scale analysis of crossover and non-crossover and detection of recombination sequence motifs in the honeybee (Apis mellifera). PLoS ONE 7(5):e36229

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Beye M, Gattermeier I, Hasselmann M, Gempe T, Schioett M, Baines JF, Schlipalius D, Mougel F, Emore C, Rueppell O, Sirvio A, Guzman-Novoa E, Hunt G, Solignac M, Page RE Jr (2006) Exceptionally high levels of recombination across the honey bee genome. Genome Res 16(11):1339–1344

    Article  CAS  PubMed  Google Scholar 

  • Billings T, Parvanov ED, Baker CL, Walker M, Paigen K, Petkov PM (2013) DNA binding specificities of the long zinc-finger recombination protein PRDM9. Genome Biol 14(4):R35

    Article  PubMed  Google Scholar 

  • Bleazard T, Ju YS, Sung J, Seo JS (2013) Fine-scale mapping of meiotic recombination in Asians. BMC Genet 14:19

    Article  PubMed Central  PubMed  Google Scholar 

  • Broman KW, Weber JL (2000) Characterization of human crossover interference. Am J Hum Genet 66(6):1911–1926

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Buhler C, Borde V, Lichten M (2007) Mapping meiotic single-strand DNA reveals a new landscape of DNA double-strand breaks in Saccharomyces cerevisiae. PLoS Biol 5(12):e324

    Article  PubMed Central  PubMed  Google Scholar 

  • Capra JA, Paeschke K, Singh M, Zakian VA (2010) G-quadruplex DNA sequences are evolutionarily conserved and associated with distinct genomic features in Saccharomyces cerevisiae. PLoS Comput Biol 6(7):e1000861

    Article  PubMed Central  PubMed  Google Scholar 

  • Chakravarti A, Buetow K, Antonarakis S, Waber P, Boehm C, Kazazian H (1984) Nonuniform recombination within the human beta-globin gene cluster. Am J Hum Genet 36:1239–1258

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chakravarti A, Elbein S, Permutt M (1986) Evidence for increased recombination near the human insulin gene: implication for disease association studies. Proc Natl Acad Sci USA 83:1045–1049

    Article  CAS  PubMed  Google Scholar 

  • Chan AH, Jenkins PA, Song YS (2012) Genome-wide fine-scale recombination rate variation in Drosophila melanogaster. PLoS Genet 8(12):e1003090

    Article  PubMed Central  PubMed  Google Scholar 

  • Cirulli ET, Kliman RM, Noor MA (2007) Fine-scale crossover rate heterogeneity in Drosophila pseudoobscura. J Mol Evol 64(1):129–135

    Article  CAS  PubMed  Google Scholar 

  • Comeron JM, Ratnappan R, Bailin S (2012) The many landscapes of recombination in Drosophila melanogaster. PLoS Genet 8(10):e1002905

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Coop G, Wen X, Ober C, Pritchard JK, Przeworski M (2008) High-resolution mapping of crossovers reveals extensive variation in fine-scale recombination patterns among humans. Science 319(5868):1395–1398

    Article  CAS  PubMed  Google Scholar 

  • Crawford DC, Bhangale T, Li N, Hellenthal G, Rieder MJ, Nickerson DA, Stephens M (2004) Evidence for substantial fine-scale variation in recombination rates across the human genome. Nat Genet 36(7):700–706

    Article  CAS  PubMed  Google Scholar 

  • de Givry S, Bouchez M, Chabrier P, Milan D, Schiex T (2005) CARTHAGENE: multipopulation integrated genetic and radiated hybrid mapping. Bioinformatics 21(8):1703–1704

    Article  PubMed  Google Scholar 

  • DE Miller, Takeo S, Nandanan K, Paulson A, Gogol MM, Noll AC, Perera AG, Walton KN, Gilliland WD, Li H, Staehling KK, Blumenstiel JP, Hawley RS (2012) A whole-chromosome analysis of meiotic recombination in Drosophila melanogaster. G3 (Bethesda) 2(2):249–260

    Article  CAS  Google Scholar 

  • Drouaud J, Camilleri C, Bourguignon PY, Canaguier A, Berard A, Vezon D, Giancola S, Brunel D, Colot V, Prum B, Quesneville H, Mezard C (2006) Variation in crossing-over rates across chromosome 4 of Arabidopsis thaliana reveals the presence of meiotic recombination “hot spots”. Genome Res 16(1):106–114

    Article  CAS  PubMed  Google Scholar 

  • Duret L, Arndt PF (2008) The impact of recombination on nucleotide substitutions in the human genome. PLoS Genet 4(5):e1000071

    Article  PubMed Central  PubMed  Google Scholar 

  • Foret S, Kucharski R, Pittelkow Y, Lockett GA, Maleszka R (2009) Epigenetic regulation of the honey bee transcriptome: unravelling the nature of methylated genes. BMC genomics 10:472

    Article  PubMed Central  PubMed  Google Scholar 

  • Friedman J, Hastie T, Tibshirani R (2010) Regularization paths for generalized linear models via coordinate descent. J Stat Softw 33(1):1–22

    PubMed Central  PubMed  Google Scholar 

  • Groeneveld LF, Atencia R, Garriga RM, Vigilant L (2012) High diversity at PRDM9 in chimpanzees and bonobos. PLoS ONE 7(7):e39064

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hasselmann M, Beye M (2006) Pronounced differences of recombination activity at the sex determination locus of the honeybee, a locus under strong balancing selection. Genetics 174(3):1469–1480

    Article  CAS  PubMed  Google Scholar 

  • Heil CS, Noor MA (2012) Zinc finger binding motifs do not explain recombination rate variation within or between species of Drosophila. PLoS ONE 7(9):e45055

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hinch AG, Tandon A, Patterson N, Song Y, Rohland N, Palmer CD, Chen GK, Wang K, Buxbaum SG, Akylbekova EL, Aldrich MC, Ambrosone CB, Amos C, Bandera EV, Berndt SI, Bernstein L, Blot WJ, Bock CH, Boerwinkle E, Cai Q, Caporaso N, Casey G, Cupples LA, Deming SL, Diver WR, Divers J, Fornage M, Gillanders EM, Glessner J, Harris CC, Hu JJ, Ingles SA, Isaacs W, John EM, Kao WH, Keating B, Kittles RA, Kolonel LN, Larkin E, Le Marchand L, McNeill LH, Millikan RC, Murphy A, Musani S, Neslund-Dudas C, Nyante S, Papanicolaou GJ, Press MF, Psaty BM, Reiner AP, Rich SS, Rodriguez-Gil JL, Rotter JI, Rybicki BA, Schwartz AG, Signorello LB, Spitz M, Strom SS, Thun MJ, Tucker MA, Wang Z, Wiencke JK, Witte JS, Wrensch M, Wu X, Yamamura Y, Zanetti KA, Zheng W, Ziegler RG, Zhu X, Redline S, Hirschhorn JN, Henderson BE, Taylor HA Jr, Price AL, Hakonarson H, Chanock SJ, Haiman CA, Wilson JG, Reich D, Myers SR (2011) The landscape of recombination in African Americans. Nature 476(7359):170–175

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hubert R, MacDonald M, Gusella J, Arnheim N (1994) High resolution localization of recombination hot spots using sperm typing. Nat Genet 7(3):420–424

    Article  CAS  PubMed  Google Scholar 

  • Hunt GJ, Page RE Jr (1995) Linkage map of the honey bee, Apis mellifera, based on RAPD markers. Genetics 139(3):1371–1382

    CAS  PubMed  Google Scholar 

  • Jensen-Seaman MI, Furey TS, Payseur BA, Lu Y, Roskin KM, Chen CF, Thomas MA, Haussler D, Jacob HJ (2004) Comparative recombination rates in the rat, mouse, and human genomes. Genome Res 14(4):528–538

    Article  CAS  PubMed  Google Scholar 

  • Jiang H, Li N, Gopalan V, Zilversmit MM, Varma S, Nagarajan V, Li J, Mu J, Hayton K, Henschen B, Yi M, Stephens R, McVean G, Awadalla P, Wellems TE, Su XZ (2011) High recombination rates and hotspots in a Plasmodium falciparum genetic cross. Genome Biol 12(4):R33

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kong A, Gudbjartsson DF, Sainz J, Jonsdottir GM, Gudjonsson SA, Richardsson B, Sigurdardottir S, Barnard J, Hallbeck B, Masson G, Shlien A, Palsson ST, Frigge ML, Thorgeirsson TE, Gulcher JR, Stefansson K (2002) A high-resolution recombination map of the human genome. Nat Genet 31(3):241–247

    CAS  PubMed  Google Scholar 

  • Kong A, Thorleifsson G, Gudbjartsson DF, Masson G, Sigurdsson A, Jonasdottir A, Walters GB, Jonasdottir A, Gylfason A, Kristinsson KT, Gudjonsson SA, Frigge ML, Helgason A, Thorsteinsdottir U, Stefansson K (2010) Fine-scale recombination rate differences between sexes, populations and individuals. Nature 467(7319):1099–1103

    Article  CAS  PubMed  Google Scholar 

  • Koren A, Ben-Aroya S, Kupiec M (2002) Control of meiotic recombination initiation: a role for the environment? Curr Genet 42(3):129–139

    Article  CAS  PubMed  Google Scholar 

  • Lake CM, Nielsen RJ, Hawley RS (2011) The Drosophila zinc finger protein trade embargo is required for double strand break formation in meiosis. PLoS Genet 7(2):e1002005

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lyko F, Foret S, Kucharski R, Wolf S, Falckenhayn C, Maleszka R (2010) The honey bee epigenomes: differential methylation of brain DNA in queens and workers. PLoS Biol 8(11):e1000506

    Article  PubMed Central  PubMed  Google Scholar 

  • Mancera E, Bourgon R, Brozzi A, Huber W, Steinmetz LM (2008) High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454(7203):479–485

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mani P, Yadav VK, Das SK, Chowdhury S (2009) Genome-wide analyses of recombination prone regions predict role of DNA structural motif in recombination. PLoS ONE 4(2):e4399

    Article  PubMed Central  PubMed  Google Scholar 

  • Mantovani R (1999) The molecular biology of the CCAAT-binding factor NF-Y. Gene 239(1):15–27

    Article  CAS  PubMed  Google Scholar 

  • McVean GA, Myers SR, Hunt S, Deloukas P, Bentley, Donnelly P (2004) The fine-scale structure of recombination rate variation in the human genome. Science 304(5670):581–584

    Article  CAS  PubMed  Google Scholar 

  • Myers S, Bottolo L, Freeman C, McVean G, Donnelly P (2005) A fine-scale map of recombination rates and hotspots across the human genome. Science 310(5746):321–324

    Article  CAS  PubMed  Google Scholar 

  • Myers S, Freeman C, Auton A, Donnelly P, McVean G (2008) A common sequence motif associated with recombination hot spots and genome instability in humans. Nat Genet 40(9):1124–1129

    Article  CAS  PubMed  Google Scholar 

  • Myers S, Bowden R, Tumian A, Bontrop RE, Freeman C, MacFie TS, McVean G, Donnelly P (2010) Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science 327(5967):876–879

    Article  CAS  PubMed  Google Scholar 

  • Niehuis O, Gibson JD, Rosenberg MS, Pannebakker BA, Koevoets T, Judson AK, Desjardins CA, Kennedy K, Duggan D, Beukeboom LW, van de Zande L, Shuker DM, Werren JH, Gadau J (2010) Recombination and its impact on the genome of the haplodiploid parasitoid wasp Nasonia. PLoS ONE 5(1):e8597

    Article  PubMed Central  PubMed  Google Scholar 

  • Paigen K, Petkov P (2010) Mammalian recombination hot spots: properties, control and evolution. Nat Rev 11(3):221–233

    Article  CAS  Google Scholar 

  • Paigen K, Szatkiewicz JP, Sawyer K, Leahy N, Parvanov ED, Ng SH, Graber JH, Broman KW, Petkov PM (2008) The recombinational anatomy of a mouse chromosome. PLoS Genet 4(7):e1000119

    Article  PubMed Central  PubMed  Google Scholar 

  • Pan J, Sasaki M, Kniewel R, Murakami H, Blitzblau HG, Tischfield SE, Zhu X, Neale MJ, Jasin M, Socci ND, Hochwagen A, Keeney S (2011) A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell 144(5):719–731

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing. http://www.R-project.org. Accessed Dec 2011

  • Rice P, Longden I, Bleasby A (2000) EMBOSS: the European molecular biology open software suite. Trends Genet 16(6):276–277

    Article  CAS  PubMed  Google Scholar 

  • Robertson HM, Reese JT, Milshina NV, Agarwala R, Solignac M, Walden KK, Elsik CG (2007) Manual superscaffolding of honey bee (Apis mellifera) chromosomes 12–16: implications for the draft genome assembly version 4, gene annotation, and chromosome structure. Insect Mol Biol 16(4):401–410

    Article  CAS  PubMed  Google Scholar 

  • Rockman MV, Kruglyak L (2009) Recombinational landscape and population genomics of Caenorhabditis elegans. PLoS Genet 5(3):e1000419

    Article  PubMed Central  PubMed  Google Scholar 

  • Shifman S, Bell JT, Copley RR, Taylor MS, Williams RW, Mott R, Flint J (2006) A high-resolution single nucleotide polymorphism genetic map of the mouse genome. PLoS Biol 4(12):e395

    Article  PubMed Central  PubMed  Google Scholar 

  • Sigurdsson MI, Smith AV, Bjornsson HT, Jonsson JJ (2009) HapMap methylation-associated SNPs, markers of germline DNA methylation, positively correlate with regional levels of human meiotic recombination. Genome Res 19(4):581–589

    Article  CAS  PubMed  Google Scholar 

  • Singh ND, Aquadro CF, Clark AG (2009) Estimation of fine-scale recombination intensity variation in the white-echinus interval of D. melanogaster. J Mol Evol 69(1):42–53

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Singh ND, Stone EA, Aquadro CF, Clark AG (2013) Fine-scale heterogeneity in crossover rate in the garnet-scalloped region of the Drosophila melanogaster X chromosome. Genetics 194(2):375–387

    Article  CAS  PubMed  Google Scholar 

  • Solignac M, Vautrin D, Baudry E, Mougel F, Loiseau A, Cornuet JM (2004) A microsatellite-based linkage map of the honeybee Apis mellifera L. Genetics 167(1):253–262

    Article  CAS  PubMed  Google Scholar 

  • Solignac M, Mougel F, Vautrin D, Monnerot M, Cornuet JM (2007) A third-generation microsatellite-based linkage map of the honey bee, Apis mellifera, and its comparison with the sequence-based physical map. Genome Biol 8(4):R66

    Article  PubMed Central  PubMed  Google Scholar 

  • Steiner WW, Smith GR (2005) Natural meiotic recombination hot spots in the Schizosaccharomyces pombe genome successfully predicted from the simple sequence motif M26. Mol Cell Biol 25(20):9054–9062

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Steiner WW, Steiner EM, Girvin AR, Plewik LE (2009) Novel nucleotide sequence motifs that produce hotspots of meiotic recombination in Schizosaccharomyces pombe. Genetics 182(2):459–469

    Article  CAS  PubMed  Google Scholar 

  • Steinmetz M, Stephan D, Fischer Lindahl K (1986) Gene organization and recombinational hotspots in the murine major histocompatibility complex. Cell 44(6):895–904

    Article  CAS  PubMed  Google Scholar 

  • Stevison LS, Noor MA (2010) Genetic and evolutionary correlates of fine-scale recombination rate variation in Drosophila persimilis. J Mol Evol 71(5–6):332–345

    Article  CAS  PubMed  Google Scholar 

  • Tibshirani R (1996) Regression shrinkage and selection via the lasso. J Royal Stat Soc Ser B 58:267–288

    Google Scholar 

  • Tibshirani R, Bien J, Friedman J, Hastie T, Simon N, Taylor J, Tibshirani R (2012) Strong rules for discarding predictors in Lasso-type problems. J Royal Stat Soc Ser B 74:245–266

    Article  Google Scholar 

  • Tiemann-Boege I, Calabrese P, Cochran DM, Sokol R, Arnheim N (2006) High-resolution recombination patterns in a region of human chromosome 21 measured by sperm typing. PLoS Genet 2(5):e70

    Article  PubMed Central  PubMed  Google Scholar 

  • True JR, Mercer JM, Laurie CC (1996) Differences in crossover frequency and distribution among three sibling species of Drosophila. Genetics 142(2):507–523

    CAS  PubMed  Google Scholar 

  • Wahls WP, Davidson MK (2012) New paradigms for conserved, multifactorial, cis-acting regulation of meiotic recombination. Nucleic Acids Res 40(20):9983–9989

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang Y, Leung FC (2009) In silicon prediction of two classes of honeybee genes with CpG deficiency or CpG enrichment and sorting according to gene ontology classes. J Mol Evol 68(6):700–705

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Fan HC, Behr B, Quake SR (2012) Genome-wide single-cell analysis of recombination activity and de novo mutation rates in human sperm. Cell 150(2):402–412

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Weinstock G, Consortium HGS et al (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443(7114):931–949

    Article  CAS  Google Scholar 

  • Wilfert L, Gadau J, Schmid-Hempel P (2007) Variation in genomic recombination rates among animal taxa and the case of social insects. Heredity 98(4):189–197

    Article  CAS  PubMed  Google Scholar 

  • Wong AK, Ruhe AL, Dumont BL, Robertson KR, Guerrero G, Shull SM, Ziegle JS, Millon LV, Broman KW, Payseur BA, Neff MW (2010) A comprehensive linkage map of the dog genome. Genetics 184(2):595–605

    Article  CAS  PubMed  Google Scholar 

  • Yadav VK, Abraham JK, Mani P, Kulshrestha R, Chowdhury S (2008) QuadBase: genome-wide database of G4 DNA–occurrence and conservation in human, chimpanzee, mouse and rat promoters and 146 microbes. Nucleic acids research 36:D381–D385 (Database issue)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yu A, Zhao C, Fan Y, Jang W, Mungall AJ, Deloukas P, Olsen A, Doggett NA, Ghebranious N, Broman KW, Weber JL (2001) Comparison of human genetic and sequence-based physical maps. Nature 409(6822):951–953

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The English form of the manuscript has been revised by Helen McCombie. This work was supported by the European Commission through the 6th framework collaborative project BEESHOP (EU contract number: FOOD-CT-2006-022568). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We are very grateful to Jacques Kemp for providing us large drone samples for very fine scale mapping.

Author information

Authors and Affiliations

  1. Laboratoire Evolution Génomes Spéciation, CNRS, avenue de la Terrasse, 91198, Gif-sur-Yvette Cedex, France

    Florence Mougel, Dominique Vautrin & Michel Solignac

  2. Université Paris Sud, 91405, Orsay Cedex, France

    Florence Mougel & Michel Solignac

  3. Laboratoire de Mathématiques d’Orsay, Université Paris Sud, 91405, Orsay Cedex, France

    Marie-Anne Poursat

  4. GNR Knowledge Centre for Genome Informatics, Institute of Genomics and Integrative Biology, CSIR, Mall Road, Delhi, 110 007, India

    Nicolas Beaume

Authors
  1. Florence Mougel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marie-Anne Poursat
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nicolas Beaume
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dominique Vautrin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michel Solignac
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Florence Mougel.

Additional information

Communicated by A. Aguilera.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mougel, F., Poursat, MA., Beaume, N. et al. High-resolution linkage map for two honeybee chromosomes: the hotspot quest. Mol Genet Genomics 289, 11–24 (2014). https://doi.org/10.1007/s00438-013-0784-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-013-0784-2

Keywords

Search

Navigation