Skip to main content

Advertisement

Log in

Breeding for hygienic behaviour in honeybees (Apis mellifera) using free-mated nucleus colonies

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

Abstract

Gains in hygienic behaviour based on maternal selection of queens were evaluated among four commercial beekeeping operations in northern Alberta, Canada over four generations. While the proportion of breeding colonies expressing the trait increased with each subsequent generation, levels of hygienic behaviour among progeny remained relatively unchanged. Estimated breeding values for the final generation of progeny confirmed only a slight effect of selection; the expected average increase in the removal of frozen brood in the next generation was determined to be 0.17% at 24 h and 0.34% at 48 h. This modest increase may be explained by the low (24 h, h 2 = 0.17) to moderate (48 h, h 2 = 0.25) heritability of hygienic behaviour in our population. Our work implies that year-to-year comparisons of breeding colonies may not be an accurate predictor of selection gains within honeybee populations and that honey producers in this region may need to focus selection within elite breeding populations.

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.

Institutional subscriptions

Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.

Similar content being viewed by others

References

  • Alippi, A.M. (1994) Sensibilidad in vitro de Bacillus larvae frente a diferentes agentes antimicrobianos. Vida Apícola. 66, 20–24

    Google Scholar 

  • Anderson, D.L., Trueman, J.W.H. (2000) Varroa jacobsoni (Acari: Varroidae) is more than one species. Exp. Appl. Acarol. 24, 165–189

    Article  PubMed  CAS  Google Scholar 

  • Boecking, O., Bienefeld, K., Drescher, W. (2000) Heritability of the Varroa-specific hygienic behaviour in honey bees (Hymenoptera: Apidae). J. Anim. Breed. Genet. 117, 417–424

    Article  Google Scholar 

  • Brødsgaard, C.J., Hansen, H., Brødsgaard, H.F., Jakobsen J. (2001) Beekeeping in Denmark, a survey based on questionnaires to skilled beekeepers and bee inspectors. Danmarks JordbrugsForskning report no. 45. Tjele, Denmark

  • Chan, W.T.Q., Melathopoulos, A.P., Pernal, S.F., Foster, L.J. (2009) The innate immune and systemic response in honey bees to a bacterial pathogen, Paenibacillus larvae. BMC Genomics 10, 387–346

    Article  Google Scholar 

  • de Guzman, L.I., Rinderer, T., Stelzer, J.A., Beaman, L., Delatte, G.T., Harper, C. (2002) Hygienic behavior by honey bees from far-eastern Russia. Am. Bee J. 142, 58–60

    Google Scholar 

  • Elliott, A.C., Reisch, J.S. (2006) Implementing a multiple comparison test for proportions in a 2xC crosstabulation in SAS®. In: Proceedings of the SAS User's Group International 31, San Francisco, CA, 26–29 March 2006. pp 204–231

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

    Article  CAS  Google Scholar 

  • Fries, I., Raina, S. (2003) American foulbrood and African honey bees (Hymenoptera: Apidae). J. Econ. Entomol. 96, 1641–1646

    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  PubMed  CAS  Google Scholar 

  • Gilliam, M., Taber III, S., Richardson, G.V. (1983) Hygienic behavior of honey bees in relation to chalkbrood disease. Apidologie 14, 29–39

    Article  Google Scholar 

  • Guzmán-Novoa, E., Page Jr., R. (1999) Selective breeding of honey bees (Hymenoptera: Apidae) in Africanized areas. J. Econ. Entomol. 92, 521–525

    Google Scholar 

  • Harbo, J.R., Harris, J.W. (1999) Heritability in honey bees (Hymenoptera: Apidae) of characteristics associated with resistance to Varroa jacobsoni (Mesostigmata: Varroidae). J. Econ. Entomol. 92, 261–265

    Google Scholar 

  • Harris, D.L., Newman, S. (1994) Breeding for profit: synergism between genetic improvement and livestock production (a review). J. Anim. Sci. 72, 2178–2200

    PubMed  CAS  Google Scholar 

  • Honey Bee Genome Sequencing Consortium (HBGSC) (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443, 931–949

    Article  Google Scholar 

  • Hwang, Y.-J., Roe, B., Teisl, M.F. (2005) An empirical analysis of United States consumers’ concerns about eight food production and processing technologies. AgBioForum 8, 40–49

    Google Scholar 

  • Ibrahim, A., Reuter, G.S., Spivak, M. (2007) Field trial of honey bee colonies bred for mechanisms of resistance against Varroa destructor. Apidologie 38, 67–76

    Article  Google Scholar 

  • Kamel, S.M., Strange, J.P., Sheppard, W.S. (2003) A scientific note on hygienic behavior in Apis mellifera lamarckii and A. m. carnica in Egypt. Apidologie 34, 189–190

    Article  Google Scholar 

  • Lapidge, K.L., Oldroyd, B.P., Spivak, M. (2002) Seven suggestive quantitative trait loci influence hygienic behaviour of honey bees. Naturwissenschaften 89, 565–568

    PubMed  CAS  Google Scholar 

  • Littell, R.C., Milliken, G.A., Stroup, W.W., Wolfinger, R.D. (1996) SAS System for Mixed Models. SAS Institute Inc. Cary, NC.

  • Madsen P., Jensen J. (2006) A User’s Guide to DMU. A package for analyzing multivariate mixed models. Version 6, release 4.6. University of Aarhus, Faculty Agricultural Sciences (DJF), Dept of Genetics and Biotechnology, Research Centre Foulum, Tjele, Denmark

  • Melathopoulos, A.P., Farney, W.G. (2002) The Canadian beekeeper pest management survey. Hivelights 15, 13, 16

    Google Scholar 

  • Miyagi, T., Peng, C.Y.S., Chuang, R.Y., Mussen, E.C., Spivak, M.S., Doi, R.H. (2000) Verification of oxytetracycline-resistant American foulbrood pathogen Paenibacillus larvae in the United States. J. Invertbr. Pathol. 75, 95–96

    Article  CAS  Google Scholar 

  • Momont, J.P., Rothenbuhler, W.C. (1971) Behaviour genetics of nest cleaning in honey bees. VI. Interactions of age and genotype of bees, and nectar flow. J. Apic. Res. 10, 11–21

    Google Scholar 

  • Moritz, R.F.A., Southwick, E.E., Harbo, J.B. (1987) Genetic analysis of defensive behaviour of honeybee colonies (Apis mellifera L.) in a field test. Apidologie 18, 27–42

    Article  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  PubMed  CAS  Google Scholar 

  • Palacio, M.A., Figini, E.E., Ruffinengo, S.R., Rodriguez, E.M., Hoyo, M.L., Bedascarrasburne, E.L. (2000) Changes in a population of Apis mellifera L. selected for hygienic behavior and its relation to brood disease tolerance. Apidologie 31, 471–478

    Article  Google Scholar 

  • Panasiuk, B., Skowronek, W., Gerula, D. (2009) Effect of period of the season and environmental conditions on rate of cleaning cells with dead brood. J. Apic. Sci. 53, 95–102

    Google Scholar 

  • Rothenbuhler, W.C. (1958) Genetics and breeding of the honey bee. Annu. Rev. Entomol. 3, 161–180

    Article  Google Scholar 

  • Rothenbuhler, W.C. (1964a) 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 

  • Rothenbuhler, W.C. (1964b) Behaviour genetics of nest cleaning in honey bees. IV. Responses of F1 and backcross generations to disease-killed brood. Am. Zool. 4, 111–123

    PubMed  CAS  Google Scholar 

  • SAS Institute (2001) Proprietary Software, Release 8.2. SAS Institute, Cary, NC.

  • Spivak, M. (1996) Honey bee hygienic behavior and defence against Varroa jacobsoni. Apidologie 27, 245–260

    Article  Google Scholar 

  • Spivak, M., Downey, D. (1998) Field assays for hygienic behavior in honey bees (Apidae: Hymenoptera). J. Econ. Entomol. 91, 64–70

    Google Scholar 

  • Spivak, M., Gilliam, M. (1993) Facultative expression of hygienic behaviour of honey bees in relation to disease resistance. J. Apic. Res. 32, 147–157

    Google Scholar 

  • Spivak, M., Gilliam, M. (1998a) Hygienic behavior of honey bees and its application for control of brood diseases and Varroa; Part I. Hygienic behavior and resistance to American foulbrood. Bee World 79, 124–134

    Google Scholar 

  • Spivak, M., Gilliam, M. (1998b) Hygienic behavior of honey bees and its application for control of brood diseases and Varroa; Part II. Studies on hygienic behaviour since the Rothenbuhler era. Bee World 79, 169–186

    Google Scholar 

  • Spivak, M., Reuter, G.S. (1998) Honey bee hygienic behavior. Am. Bee J. 138, 283–286

    Google Scholar 

  • Spivak, M., Reuter, G.S. (2001a) Resistance to American foulbrood disease by honey bee colonies Apis mellifera bred for hygienic behavior. Apidologie 32, 555–565

    Article  Google Scholar 

  • Spivak, M., Reuter, G.S. (2001b) Varroa destructor infestation in untreated honey bee (Hymenoptera: Apidae) colonies selected for hygienic behavior. J. Econ. Entomol. 94, 326–331

    Article  PubMed  CAS  Google Scholar 

  • Spivak, M., Reuter, G.S., Lee, K., Ranum, B. (2009) The future of the MN hygienic stock of bees is in good hands! Am. Bee J. 149, 965–967

    Google Scholar 

  • Stanimirović, Z., Stevanović, J., Mirilović, M., Stojić, V. (2008) Heritability of hygienic behaviour in grey honey bees (Apis mellifera carnica). Acta Veter. (Beograd). 58, 593–601

    Article  Google Scholar 

  • Szabo, T.I., Heikel, D.T. (1987) Patterns of honey bee colony gain in Alberta. Canada. J. Apic. Res. 26, 47–52

    Google Scholar 

  • Thompson, T.S., Pernal, S.F., Noot, D.K., Melathopoulos, A.P., van den Heever, J.P. (2007) Degradation of incurred tylosin to desmycosin: implications for residue analysis of honey. Anal. Chim. Acta 586, 304–311

    Article  PubMed  CAS  Google Scholar 

  • Unger, P., Guzmán-Novoa, E. (2009) Maternal effects on the hygienic behavior of Russian × Ontario hybrid honeybees (Apis mellifera L.). J. Hered. 101, 91–96

    Article  Google Scholar 

  • vanEngelsdorp, D., Otis, G.W. (2000) Application of a modified selection index for honey bees (Hymenoptera: Apidae). J. Econ. Entomol. 93, 1606–1612

    Article  CAS  Google Scholar 

  • Wegener, H.C. (2003) Antibiotics in animal feed and their role in resistance development. Curr. Opin. Microbiol. 6, 439–445

    Article  PubMed  CAS  Google Scholar 

  • Woodrow, A.W., Holst, E.C. (1942) The mechanism of colony resistance to American foulbrood. J. Econ. Entomol. 35, 327–330

    Google Scholar 

  • Zar, J.H. (1999) Biostatistical analysis, 4th edn. Prentice-Hall, Upper Saddle River, NJ

    Google Scholar 

Download references

Acknowledgements

Expert advice was kindly provided by Ernesto Guzmán-Novoa, Jeff Harris and Marla Spivak. Technical support was provided by Sterling Smith. We also thank Robert Albright, German Cucatto, Devon Coupland, Brendan and Andrew Dickson, Bill Farney, Julio Flores, Amanda Van Haga, Felis Jiménez, Christel Leonhardt, Ricardo Madge, Andres Mendez, Peter Mills, Erik Moller, Felix Valdez Pulodo, Marina and Ricardo Sanchez and Ryan Scorgie for helping conduct the many colony assessments. Marla Spivak graciously supplied the Minnesota benchmark, and along with Susan Cobey, conducted instrumental inseminations. We thank Gus Rouse for his donation of benchmark queens. Most importantly, we owe considerable thanks to the cooperating beekeepers who not only supplied colonies and breeding material, but who contributed considerable labour to the project: Rob Dickson, Denis McKenna, Mark Paradis, Peter Jessing, Fernando Sanchez, Mike Williams and Gilbert Wolfe. The project was supported financially by the Alberta Crop Industry Development Fund (Project #2002C030R), the Matching Investment Initiative of Agriculture and Agri-Food Canada, the Canadian Bee Research Fund, Bee Maid Honey, Medivet Pharmaceuticals and the Alberta Beekeepers’ Association.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stephen F. Pernal.

Additional information

Elevage d’abeilles ( Apis mellifera ) présentant un comportement hygiénique à partir de nuclei issus d’une reproduction naturelle.

Héritabilité / comportement hygiénique / corrélation génétique / résistance / loque américaine / Varroa destructor

Zucht auf Hygieneverhalten bei Honigbienen ( Apis mellifera ) mittels Begattungskästchen in freier Paarung

Heritabilität; Hygieneverhalten; genetische Korrelation; Widerstandsfähigkeit; Amerikanische Faulbrut; Varroa destructor

Manuscript editor: Marla Spivak

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pernal, S.F., Sewalem, A. & Melathopoulos, A.P. Breeding for hygienic behaviour in honeybees (Apis mellifera) using free-mated nucleus colonies. Apidologie 43, 403–416 (2012). https://doi.org/10.1007/s13592-011-0105-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13592-011-0105-x

Keywords

Navigation