Apidologie

, Volume 45, Issue 2, pp 248–256 | Cite as

Four quantitative trait loci associated with low Nosema ceranae (Microsporidia) spore load in the honeybee Apis mellifera

  • Qiang Huang
  • Per Kryger
  • Yves Le Conte
  • H. Michael G. Lattorff
  • F. Bernhard Kraus
  • Robin F. A. Moritz
Original article

Abstract

Nosema ceranae has been recently introduced into the honeybee Apis mellifera as a novel microsporidian gut parasite. To locate the genetic region involved in N. ceranae infection tolerance, we fed N. ceranae spores to haploid drones of a F1 hybrid queen produced from a cross between a queen of a Nosema-resistant bred strain and drones of susceptible colonies. The spore loads of the infected F1 drones were used as the phenotype to identify quantitative trait loci (QTLs) associated with N. ceranae spore load. One hundred forty-eight infected drones were individually genotyped with microsatellite markers at an average marker distance of 20 cM along the genome. Four QTLs were significantly associated with low spore load, explaining 20.4 % of total spore load variance. Moreover, a candidate gene Aubergine (Aub) within the major QTL region was significantly overexpressed in drones with low spore loads than in those with high spore loads. Our results confirm the genetic basis of Nosema tolerance in the selected strain and show that both additive effects and epistatic interactions among the QTLs interfere with the tested phenotype.

Keywords

Apis mellifera drone Nosema QTL 

Supplementary material

13592_2013_243_MOESM1_ESM.pdf (368 kb)
ESM 1(PDF 367 kb)

References

  1. Behrens, D., Huang, Q., Geßner, C., Rosenkranz, P., Frey, E., et al. (2011) Three QTL in the honey bee Apis mellifera L. suppress reproduction of the parasitic mite Varroa destructor. Ecol. Evol . doi:10.1002/ece3.17 PubMedCentralPubMedGoogle Scholar
  2. Broman, K.W., Wu, H., Sen, S., Churchill, G.A. (2003) QTL mapping in experimental crosses. Bioinformatics 19, 889–890PubMedCrossRefGoogle Scholar
  3. Chen, Y.P., Evans, J.D., Zhou, L., Boncristiani, H., Kimura, K., Xiao, T.G., et al. (2009) Asymmetrical coexistence of Nosema ceranae and Nosema apis in honey bees. J. Invertebr. Pathol. 101, 204–209PubMedCrossRefGoogle Scholar
  4. Cronin, S.J.F., Nehme, N.T., Limmer, S., Liegeois, S., Pospislik, J.A., et al. (2009) Genome-wide RNAi screen identifies genes involved in intestinal pathogenic bacterial infection. Science 325, 340–343PubMedCentralPubMedCrossRefGoogle Scholar
  5. Forsgren, E., Fries, I. (2010) Comparative virulence of Nosema ceranae and Nosema apis in individual European honey bees. Vet. Pathol. 170, 212–217Google Scholar
  6. Fries, I., Feng, F., Silva, A., Slemenda, S.B., Pieniazek, N.J. (1996) Nosema ceranae n sp (Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae). Eur. J. Protistol. 32, 356–365CrossRefGoogle Scholar
  7. Fries, I., Martin, R., Meana, A., García-Palencia, P., Higes, M. (2006) Natural infections of Nosema ceranae in European honey bees. J. Apic. Res. 45, 230–233CrossRefGoogle Scholar
  8. Gisder, S., Hedtke, K., Möckel, N., Frielitz, M.C., Linde, A., et al. (2010) Five-year cohort study of Nosema spp. in Germany: does climate shape virulence and assertiveness of Nosema ceranae? Appl. Environ. Microbiol. 9, 3032–3038CrossRefGoogle Scholar
  9. Hamiduzzaman, M.M., Guzman-Novoa, E., Goodwin, P.H. (2010) A multiplex PCR assay to diagnose and quantify Nosema infections in honey bees (Apis mellifera). J. Invertebr. Pathol. 105, 151–155PubMedCrossRefGoogle Scholar
  10. Higes, M., Martin-Hernandez, R., Garrido-Bailón, E., González-Porto, A.V., García-Palencia, P., et al. (2009) Honeybee colony collapse due to Nosema ceranae in professional apiaries. Environ. Microbiol. Rep. 1, 110–113PubMedCrossRefGoogle Scholar
  11. Higes, M., García-Palencia, P., Martín-hernández, R., Meana, A. (2007) Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia). J. Invertebr. Pathol. 94, 211–217PubMedCrossRefGoogle Scholar
  12. Higes, M., Martín, R., Meana, A. (2006) Nosema ceranae, a new microsporidian parasite in honeybees in Europe. J. Invertebr. Pathol. 92, 93–95PubMedCrossRefGoogle Scholar
  13. Higes, M., Martin-Hernandez, R., Botias, C., Bailon, E.G., Gonzalez-Porto, A.V., et al. (2008) How natural infection by Nosema ceranae causes honeybee colony collapse. Environ. Microbiol. 10, 2659–2669PubMedCrossRefGoogle Scholar
  14. Huang, Q., Kryger, P., Le Conte, Y., Moritz, R.F.A. (2012) Survival and immune response of drones of a Nosemosis tolerant honey bee strain towards N. ceranae infections. J. Invertebr. Pathol. 109, 297–302PubMedCrossRefGoogle Scholar
  15. Hunt, G.J., Guzmán-Novoa, E., Fondrk Jr., M.K., Page, R.E. (1998) Quantitative trait loci for honey bee stinging behavior and body size. Genetics 148, 1203–1213PubMedGoogle Scholar
  16. Kawaoka, S., Minami, K., Katsuma, S., Mita, K., Shimada, T. (2008) Developmentally synchronized expression of two Bombyx mori Piwi subfamily genes, SIWI and BmAGO3 in germ-line cells. Biochem. Biophys. Res. Commun. 367, 755–760PubMedCrossRefGoogle Scholar
  17. Liao, Z., Jia, Q.D., Li, F., Han, Z.J. (2010) Identification of two Piwi genes and their expression profile in honeybee, Apis mellifera. Arch. Insect Biochem. Physiol. 74, 91–102PubMedGoogle Scholar
  18. Moritz, R.F.A. (1984) The effect of different diluents on insemination success in the honeybee using mixed semen. J. Apic. Res. 23, 164–167Google Scholar
  19. 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, 1452–1461PubMedCrossRefGoogle Scholar
  20. R Devolopment Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org
  21. Rebai, A., Goffinet, B., Mangin, B. (1995) Comparing power of different methods for QTL detection. Biometrics 51, 87–99PubMedCrossRefGoogle Scholar
  22. Teo, C.H., Pui, H.P., Othman, R.Y., Harikrishna, J.A. (2011) Comparative analysis of Argonaute gene sequences in bananas (Musa sp.) shows conserved species-specific Ago-7 PIWI domains. Genet. Resour. Crop. Evol. 58, 713–725CrossRefGoogle Scholar
  23. Traynor, K. (2008) Bee breeding around the world. Am. Bee J. 148, 135–139Google Scholar
  24. Walsh, P.S., Metzger, D.A., Higuchi, R. (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques 10, 506–513PubMedGoogle Scholar
  25. Wang, S., Basten, C.J., Zeng Z.B. (2011) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NC. ( http://statgen.ncsu.edu/qtlcart/WQTLCart.htm)
  26. Zander, E. (1909) Tierische Parasiten als Krankenheitserreger bei der Biene. Münchener Bienenzeitung 31, 196–204Google Scholar

Copyright information

© INRA, DIB and Springer-Verlag France 2013

Authors and Affiliations

  • Qiang Huang
    • 1
    • 2
  • Per Kryger
    • 3
  • Yves Le Conte
    • 4
  • H. Michael G. Lattorff
    • 1
    • 5
  • F. Bernhard Kraus
    • 1
    • 6
  • Robin F. A. Moritz
    • 1
    • 7
    • 8
  1. 1.Institut für Biology/Zoologie, Molekulare ÖkologieMartin-Luther-Universität Halle-WittenbergHalleGermany
  2. 2.Honeybee Research InstituteJiangxi Agricultural UniversityNanchangChina
  3. 3.Department of Agroecology, Section of Entomology and Plant PathologyAarhus UniversitySlagelseDenmark
  4. 4.INRA, UR 406 Abeilles et Environnement, Laboratoire de Biologie et Protection de l’abeilleAvignon Cedex 9France
  5. 5.Institut für Biology/Zoologie, TierphysiologieMartin-Luther-Universität Halle -WittenbergHalleGermany
  6. 6.Department of Laboratory MedicineUniversity Hospital Halle (Saale)Halle (Saale)Germany
  7. 7.RoBeeTechUniversitatea de Stiinte Agricole si Medicina Vetereinaria Cluj-NapocaCluj-NapocaRomania
  8. 8.Department of Zoology and EntomologyUniversity of PretoriaPretoriaSouth Africa

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