Skip to main content
Log in

QTL-mapping of individual resistance against American foulbrood in haploid honeybee drone larvae (Apis mellifera)

  • Original article
  • Published:
Apidologie Aims and scope Submit manuscript

Abstract

American foulbrood (AFB) is a severe brood disease in honeybees. Since sustainable treatment is not available, selection of genetically resistant honeybee stock is highly desirable. Using a set of 291 heterozygous microsatellite markers in a bulk segregant analysis with subsequent finemapping of haploid drone offspring from a single honeybee queen, we identified one significant and three suggestive quantitative trait loci as well as one significant epistatic interaction influencing prepupal survival after AFB infection. While we were not able to verify specific genes responsible for tolerance, we suggest that developmental genes may have played an important role. The identified markers can be used as regions of interest in future mapping or expression studies. In order to use them for marker-assisted selection in breeding programmes for AFB-resistant honeybee stock, it will be required to evaluate these loci more extensively under variable experimental conditions.

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

Access this article

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

Instant access to the full article PDF.

Figure 1.
Figure 2.

Similar content being viewed by others

REFERENCES

  • Arechavaleta-Velasco, M.E., Hunt, G.J. (2004) Binary trait loci that influence honey bee (Hymenoptera: Apidae) guarding behavior. Ann. Entomol. Soc. Am. 97, 177–183

    Article  CAS  Google Scholar 

  • Behrens, D., Forsgren, E., Fries, I., Moritz, R.F.A. (2007) Infection of drone larvae (Apis mellifera) with American foulbrood. Apidologie 38, 281–288

    Article  Google Scholar 

  • Behrens, D., Forsgren, E., Fries I., Moritz, R.F.A. (2010) Lethal infection thresholds of Paenibacillus larvae for honeybee drone and worker larvae (Apis mellifera). Environ. Microbiol. 12, 2838–2845

    CAS  PubMed  Google Scholar 

  • Behrens, D., Huang, Q., Geßner, C., Rosenkranz, P., Frey, E., Locke, B., Moritz, R.F.A., Kraus, F.B. (2011) Three QTL in the honeybee Apis mellifera L. suppress reproduction of the parasitic mite Varroa destructor. Ecol. Evol. 1, 451–458

    Article  PubMed  PubMed Central  Google Scholar 

  • Broman, K.W., Wu, H., Sen, S., Churchill, G.A. (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19, 889–890

    Article  CAS  PubMed  Google Scholar 

  • Chandra, S., Hunt, G., Cobey, S., Smith, B. (2001) Quantitative trait loci associated with reversal learning and latent inhibition in honeybees (Apis mellifera). Behav. Genet. 31, 275–285

    Article  CAS  PubMed  Google Scholar 

  • Darvasi, A., Soller, M. (1994) Selective DNA pooling for determination of linkage between a molecular marker and a quantitative trait locus. Genetics 138, 1365–1373

    CAS  PubMed  PubMed Central  Google Scholar 

  • Evans, J.D. (2003) Diverse origins of tetracycline resistance in the honey bee bacterial pathogen Paenibacillus larvae. J. Invertebr. Pathol. 83, 46–50

    Article  CAS  PubMed  Google Scholar 

  • Evans, J.D. (2006) Beepath: an ordered quantitative-PCR array for exploring honey bee immunity and disease. J. Invertebr. Pathol. 93, 135–139

    Article  CAS  PubMed  Google Scholar 

  • Evans, J.D., Aronstein, K., Chen, Y.P., Hetru, C., Imler, J.L., Jiang, H., Kanost, M., Thompson, G.J., Zou, Z., Hultmark D. (2006) Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol. Biol. 15, 645–656

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evans, J.D., Pettis, J.S. (2005) Colony-level impacts of immune responsiveness in honey bees, Apis mellifera. Evolution 59, 2270–2274

    Article  CAS  PubMed  Google Scholar 

  • Genersch, E. (2010) American foulbrood in honeybees and its causative agent, Paenibacillus larvae. J. Invertebr. Pathol. 103, S10-S19

    Article  PubMed  Google Scholar 

  • Genersch, E., Forsgren, E., Pentikäinen, J., Ashiralieva, A., Rauch, S., Kilwinski, J., Fries, I. (2006) Reclassification of Paenibacillus larvae subsp. pulvifaciens and Paenibacillus larvae subsp. larvae as Paenibacillus larvae without subspecies differentiation. Int. J. Syst. Evol. Microbiol. 56, 501–511

    Article  CAS  PubMed  Google Scholar 

  • Graham, A., Munday, M., Kaftanoglu, O., Page, R., Amdam, G., Rueppell, O. (2011) Support for the reproductive ground plan hypothesis of social evolution and major QTL for ovary traits of Africanized worker honey bees (Apis mellifera L.). BMC Evol. Biol. 11, 95

    Article  PubMed  PubMed Central  Google Scholar 

  • Guzmán-Novoa, E., Hunt, G.J., Uribe, J.L., Smith, C., Arechavaleta-Velasco, M.E. (2002) Confirmation of QTL effects and evidence of genetic dominance of honeybee defensive behavior: Results of colony and individual behavioral assays. Behav. Genet. 32, 95–102

    Article  PubMed  Google Scholar 

  • Holloway, B., Sylvester, H.A., Bourgeois, L., Rinderer, T.E. (2012) Association of single nucleotide polymorphisms to resistance to chalkbrood in Apis mellifera. J. Apic. Res. 51, 154–163

    Article  CAS  Google Scholar 

  • Hunt, G.J., Guzmán-Novoa, E., Fondrk, M.K., Page, R.E. (1998) Quantitative trait loci for honey bee stinging behavior and body size. Genet. 148, 1203–1213

    CAS  Google Scholar 

  • Hunt, G.J., Page, J., Fondrk, M.K., Dullum, C.J. (1995) Major quantitative trait loci affecting honey bee foraging behavior. Genetics 141, 1537–1545

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lattorff, H.M.G., Moritz, R.F.A., Crewe, R.M., Solignac, M. (2007) Control of reproductive dominance by the thelytoky gene in honeybees. Biol. Lett. 3, 292–295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Linksvayer, T.A., Rueppell, O., Siegel, A., Kaftanoglu, O., Page, R.E., Amdam, G.V. (2009) The genetic basis of transgressive ovary size in honeybee workers. Genetics 183, 693–707

    Article  PubMed  PubMed Central  Google Scholar 

  • Manichaikul, A., Broman, K.W. (2009) Binary trait mapping in experimental crosses with selective genotyping. Genetics 182, 863–874

    Article  PubMed  PubMed Central  Google Scholar 

  • Michelmore, R.W., Paran, I., Kesseli, R.V. (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc. Natl. Acad. Sci. U S A 88, 9828–9832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mougel, F., Solignac, M., Vautrin, D., Baudry, E., Ogden, J., Tchapla, A., Schweitz, H., Gilbert, H. (2012) Quantitative traits loci (QTL) involved in body colour, wing morphometry, cuticular hydrocarbons and venom components in honeybee. Apidologie 43, 162–181

    Article  CAS  Google Scholar 

  • Oxley, P.R., Spivak, M., Oldroyd, B.P. (2010) Six quantitative trait loci influence task thresholds for hygienic behaviour in honeybees (Apis mellifera). Mol. Ecol. 19, 1452–1461

    Article  CAS  PubMed  Google Scholar 

  • Oxley, P.R., Thompson, G.J., Oldroyd, B.P. (2008) Four QTL influence worker sterility in the honey bee (Apis mellifera). Genetics 179, 1337–1343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Page, R.E., Fondrk, M.K., Hunt, G.J., Guzmán-Novoa, E., Humphries, M.A., Nguyen, K., Greene, A.S. (2000) Genetic dissection of honeybee (Apis mellifera L.) foraging behavior. J. Hered. 91, 474–479

    Article  PubMed  Google Scholar 

  • Palmer, K., Oldroyd, B.P. (2003) Evidence for intra-colonial genetic variance in resistance to American foulbrood of honey bees (Apis mellifera): further support for the parasite/pathogen hypothesis for the evolution of polyandry. Naturwissenschaften 90, 265–268

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org/ (accessed on 21 February 13)

  • Rose, R.I., Briggs, J.D. (1969) Resistance to American foulbrood in honey bees. IX. Effects of honey bee larval food on the growth and viability of Bacillus larvae. J. Invertebr. Pathol. 13, 74–80

    Article  Google Scholar 

  • Rothenbuhler, W.C. (1964) Behaviour genetics of nest cleaning in honey bees. I. Responses of four inbred lines to disease-killed brood. Anim. Behav. 12, 578–583

    Article  Google Scholar 

  • Rueppell, O., Chandra, S.B.C., Pankiw, T., Fondrk, M.K., Beye, M. et al. (2006) The genetic architecture of sucrose responsiveness in the honey bee (Apis mellifera L). Genetics 172, 243–251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rueppell, O., Metheny, J.D., Linksvayer, T., Fondrk, M.K., Page, Jr. R.E., Amdam, G.V. (2011) Genetic architecture of ovary size and asymmetry in European honeybee workers. Heredity 106, 894–903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rüppell, O., Pankiw, T., Page, Jr. R.E. (2004) Pleiotropy, epistasis and new QTL: the genetic architecture of honey bee foraging behavior. J. Hered. 95, 481–491

    Article  PubMed  Google Scholar 

  • Slate, J. (2005) Quantitative trait locus mapping in natural populations: progress, caveats and future directions. Mol. Ecol. 14, 363–379

    Article  CAS  PubMed  Google Scholar 

  • Solignac, M., Mougel, F., Vautrin, D., Monnerot, M., Cornuet, J.M. (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, R66

    Article  PubMed  PubMed Central  Google Scholar 

  • Solignac, M., Vautrin, D., Loiseau, A., Mougel, F., Baudry, E., Estoup, A., Garnery, L., Haberl, M., Cornuet, J.M. (2003) Five hundred and fifty microsatellite markers for the study of the honeybee (Apis mellifera L.) genome. Mol. Ecol. Notes 3, 307–311

    Article  CAS  Google Scholar 

  • Thompson, V.C., Rothenbuhler, W.C. (1957) Resistance to American foulbrood in honey bees. II. Differential protection of larvae by adults of different genetic lines. J. Econ. Entomol. 50, 731–737

    Google Scholar 

  • Weinstock, G.M., Robinson, G.E. (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443, 931–949

    Article  CAS  Google Scholar 

  • Wilson, W.T. (1974) Residues of oxytetracycline in honey stored by Apis mellifera. Environ. Entomol. 3, 674–676

    CAS  Google Scholar 

Download references

ACKNOWLEDGEMENTS

We thank Petra Leibe and Denise Kleber for technical assistance in the lab, H. Michael G. Lattorff for help with the genomic database, Qiang Huang for advice with R/qtl and Eva Forsgren for providing the spore solution. This work was supported by the European Commission through the 6th framework collaborative Specific Targeted Research Project BEE SHOP (Bees in Europe and Sustainable Honey Production; EU contract number: FOOD-CT-2006-022568) and by the German Ministry for Education and Science (BMBF) through the FUGATO-plus project FUGAPIS (Functional genome analysis of disease resistance in honeybees, Apis mellifera; project number: 0315125A).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dieter Behrens.

Additional information

Manuscript editor: Yves Le Conte

Cartographie de loci à effets quantitatifs de la résistance individuelle contre la loque américaine chez des larves d’abeilles mâles haploïdes ( Apis mellifera )

Paenibacillus larvae / pathologie des invertébrés / résistance aux maladies / locus à effet quantitatif / microsatellites

QTL-Kartierung der individueller Resistenz gegen Amerikanische Faulbrut in haploiden Drohnenlarven der Honigbiene ( Apis mellifera )

Paenibacillus larvae / Invertebratenpathologie / Krankheitsresistenz / Loci quantitativer Eigenschaften / Mikrosatelliten

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 156 kb)

ESM 2

(PDF 70 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Behrens, D., Moritz, R.F.A. QTL-mapping of individual resistance against American foulbrood in haploid honeybee drone larvae (Apis mellifera). Apidologie 45, 409–417 (2014). https://doi.org/10.1007/s13592-013-0255-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13592-013-0255-0

Keywords

Navigation