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Genetic bases of tolerance to Varroa destructor in honey bees (Apis mellifera L.)

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Abstract

Currently, the Varroa destructor mite is the most serious parasite of honey bees (Apis mellifera) and has become a nearly cosmopolitan species. The mite not only causes damage by feeding on the haemolymph of honey bees, but it also transmits viruses, which have been implicated in colony collapse disorder. The major research goal has been to breed mite-tolerant honey bee lines in order to reduce the amount of pesticide used, because pesticides can promote the evolution of resistance in mites. In this review, we describe different behavioural traits and genes that may be part of the defence against the Varroa mite. Specifically, we review grooming behaviour, Varroa-sensitive hygiene and the suppression of mite reproduction. A large number of candidate genes have been identified by Quantitative Trait Loci studies, and through gene expression studies their function and effect have been elucidated. Results from the studies discussed can be used in apiary practice.

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References

  • Alaux C., Dantec C., Parrinello H. and Le Conte Y. 2011. Nutrigenomics in honey bees: digital gene expression analysis of pollen’s nutritive effects on healthy and Varroa-parasitized bees. BMC Genomics 12: 496

  • Amdam G., Hartfelder K., Norberg K., Hagen A. and Omholt S.W. 2004. Altered physiology in worker honey bees (Hymenoptera: Apidae) infested with the mite Varroa destructor (Acari: Varroidae): a factor in colony loss during overwintering? J. Econ. Entomol. 97: 741-747

    Google Scholar 

  • Andersen S.O., Peter M.G. and Roepstorff P. 1996. Cuticular sclerotisation in insects. Comp. Biochem. Physiol. 113: 689-705

    Google Scholar 

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

    Google Scholar 

  • Aizen M.A., Garibaldi L.A., Cunningham S.A. and Klein A.M. 2009. How much does agriculture depend on pollinators? Lesson from long-term trends in crop production. Ann. Bot. 103: 1579-1588

    Google Scholar 

  • Arechavaleta-Velasco M.E., Alcala-Escamilla K., Robles-Rios C., Tsuruda J.M. and Hunt G.J. 2012. Fine-scale linkage mapping reveals a small set of candidate genes influencing honey bee grooming behaviour in response to Varroa mites. PLoS ONE 7: e47269

  • Ashida M. and Brey P.T. 1998. Recent advances in research on the insect prophenoloxidase cascade. In: Molecular Mechanisms of Immune Responses in Insects (Brey P.T. and Hultmark D., Eds), Chapman and Hall, London UK. pp 135-172

  • Aumeier P., Rosenkranz P. and Goncalves L.S. 2000. A comparison of the hygienic response of Africanised and European (Apis mellifera carnica) honey bees to Varroa infested brood in tropical Brazil. Genet. Mol. Biol. 23: 787-791

    Google Scholar 

  • Beggs K.T., Hamilton I.S., Kurshan P.T., Mustard J.A. and Mercer A.R. 2005. Characterisation of a D2 like dopamine receptor (AmDOP3) in honey bee, Apis mellifera. Insect. Biochem. Mol. Biol. 35: 873-882

    Google Scholar 

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

    Google Scholar 

  • Blenau W., Erber J. and Baumann A. 1998. Characterisation of a dopamine D1 receptor from Apis mellifera: cloning, functional expression, pharmacology, and mRNA localisation in the brain. J. Neurochem. 70: 15-23

    Google Scholar 

  • Boecking O. and Ritter W. 1993. Grooming and removal behaviour of Apis mellifera intermissa in Tunisia against Varroa jacobsoni. J. Apicult. Res. 32: 127-134

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

    Google Scholar 

  • Boecking O. and Genersch E. 2008. Varroosis - the on-going crisis in bee keeping. J. Verbraucherschutz Lebensmittelsicherheit 3: 221-228

    Google Scholar 

  • Bowen-Walker P.L., Martin S.J. and Gunn A. 1999. The transmission of deformed wing virus between honeybees (Apis mellifera L.) by the ectoparasitic mite Varroa jacobsoni Oud. J. Invert. Pathol. 73: 101-106

    Google Scholar 

  • Bull J.C., Ryabov E.V., Prince G., Mead A., Zhang C., Baxter L.A., Pell J.K., Osborne J.L. and Chandler D. 2012. A strong immune response in young adult honeybees masks their increased susceptibility to infection compared to older bees. PLOS Pathogenes 8: e1003083

    Google Scholar 

  • Büchler R. 1994. Varroa tolerance in honey bees - occurrence, characters and breeding. Bee World 49: 6-18

    Google Scholar 

  • Campbell E.M., Budge G.E. and Bowman A.S. 2010. Gene-knockdown in the honey bee mite Varroa destructor by a non-invasive approach: studies on a glutathione S-transferase. Parasites Vectors 3: 73

    Google Scholar 

  • Cardoen D., Ernst U.R., Vaerenbergh M.V., Boerjan B., de Graaf D.C., Wenseleers T., Schoofs L. and Verleyen P. 2011. Differential proteomics in dequeened honeybee colonies reveals lower viral load in hemolymph of fertile worker bees. PLos One 6: e20043

    Google Scholar 

  • Cociancich S., Ghazi A., Hetruc C., Hoffmann J.A. and Letellier L. 1993. Insect defensin, an inducible antibacterial peptide, forms voltage-dependent channels in Micrococcus luteus. J. Biol. Chem. 268: 19239-19245

    Google Scholar 

  • Cornman R.S., Schatz M.C., Johnston J.S., Chen Y.-P., Pettis J., Hunt G., Bourgeois L., Elsik C., Anderson D., Grozinger C.M. and Evans J.D. 2010. Genomic survey of the ectoparasitic mite Varroa destructor, a major pest of the honey bee Apis mellifera. BMC Genomics 11: 602

    Google Scholar 

  • Cremer S., Armitage S. and Schmid-Hempel P. 2007. Social immunity. Curr. Biol. 17: R693-R702

  • De Guzman L.I. and Delfinado-Baker M. 1996. A new species of Varroa (Acari: Varroidae) associated with Apis koschevnikovi (Apidae: Hymenoptera) in Borneo. Int. J. Acarol. 22: 23-27

    Google Scholar 

  • Dekkers J.C.M. 2004. Commercial application of marker- and gene-assisted selection in livestock: Strategies and lessons. J. Anim. Science 82: E313-E328

  • Delaplane K.S. and Mayer D.F. 2000. Crop Pollination by Bees. CAB, New York

  • Delfinado-Baker M. and Aggarwal K. 1987. A new Varroa (Acari: Varroidae) from the nest of Apis cerana (Apidae). Int. J. Acarol. 13: 233-237

    Google Scholar 

  • Delfinado-Baker M., Rath W. and Boecking O. 1992. Phoretic bee mites and honey bee grooming behaviour. Int. J. Acarol. 18: 315-322

    Google Scholar 

  • Erler S., Popp M. and Lattott H.M.G. 2011. Dynamics of immune system gene expression upon bacterial challenge and wounding in a social insect (Bombus terrestris). PLoS ONE 6: e18126

  • Evans J.D. 2006. Beepath: An ordered quantitative-PCR array for exploring honey bee immunity and disease. J. Invert. Pathol. 93: 135-139

    Google Scholar 

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

    Google Scholar 

  • Evans J.D. and Spivak M. 2010. Socialized medicine: Individual and communal disease barriers in honey bees. J. Invert. Pathol. 103: S62-S72

    Google Scholar 

  • Food and Agriculture Organization of the United Nations (FAO) 2009. FAOSTAT. http://faostat.fao.org. Accessed 10 Apr 2009

  • Fraczek R., Zóltowska K. and Lipinski Z. 2009. The activity of nineteen hydrolases in extracts from Varroa destructor and in haemolymph of Apis mellifera carnica worker bees. J. Apicult. Sci. 53: 43-51

    Google Scholar 

  • Fries I. and Bommarco R. 2007. Possible host-parasite adaptation in honey bee infested by Varroa destructor mites. Apidologie 38: 525-533

  • Fuchs S. 1994. Nonreproducing Varroa jacobsoni Oud. in honey bee worker cells - status of mites or effects of brood cells? Exp. Appl. Acarol. 18: 309-317

  • Gallai N., Salles J.-M., Settele J. and Vaissière B.E. 2009. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol. Econ. 68: 810-821

    Google Scholar 

  • Garbian Y., Maori E., Kalev H., Shafir S. and Sela I. 2012. Bidirectional transfer of RNAi between honey bee and Varroa destructor: Varroa gene silencing reduces Varroa population. PLOS Pathogens 8: e1003035

  • Garrido C. and Rosenkranz P. 2003. The reproductive program of female Varroa destructor mites is triggered by its host, Apis mellifera. Exp. Appl. Acarol. 31: 269-273

    Google Scholar 

  • Gregorc A., Evans J.D., Scharf M. and Ellis J.D. 2011. Gene expression in honey bee (Apis mellifera) larvae exposed to pesticides and Varroa mite (Varroa destructor). J. Insect Physiol. 58: 1042-1049

    Google Scholar 

  • Gregory P.G., Evans J.D., Rinderer T. and de Guzman L. 2005. Conditional immune-gene suppression of honeybees parasitized by Varroa mites. J. Insect Science 5: 7

    Google Scholar 

  • Hall M., Wang R., Antwerpen R., Sottrup-Jensen L. and Söderhäll K. 1999. The crayfish plasma clotting protein: a vitellogenin-related protein responsible for clot formation in crustacean blood. Proc. Natl Acad. Sci. 96: 1965-1970

    Google Scholar 

  • Harbo J.R. and Hoopingarner R.A. 1997. Honey bee (Hymenoptera: Apidae) in the United States that express resistance to Varroa jacobsoni (Mesostigmata: Varroidae). J. Econ. Entomol. 90: 893-898

    Google Scholar 

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

    Google Scholar 

  • Harbo J.R. and Harris J.W. 2005. Suppressed mite reproduction explained by the behaviour of adult bees. J. Apicult. Res. 44: 21-23

    Google Scholar 

  • Harris J.W. 2007. Bees with Varroa Sensitive Hygiene preferentially remove mite infested pupae aged ≤ five days post capping. J. Apicult. Res. Bee World 46: 134-139

    Google Scholar 

  • Humphries M.A., Mustard J.A., Hunter S.J., Mercer A., Ward V. and Ebert P.R. 2003. Invertebrate D2 type dopamine receptor exhibits age-based plasticity of expression in the mushroom bodies of the honeybee brain. J. Neurobiol. 55: 315-330

    Google Scholar 

  • Hunt G.J. and Page R.E.J. 1995. A linkage map of the honey bee, Apis mellifera, based on RAPD markers. Genetics 139: 1371-1382

  • Ilyasov R.A., Gaifullina L.R., Saltykova E.S., Poskryakov A.V. and Nikolenko A.G. 2012. Review of the expression of antimicrobial peptide defensin in honey bees Apis mellifera L. J. Apicult. Sci. 56: 115-124

    Google Scholar 

  • Klaudiny J., Albert S., Bachanová K., Kopernicky J. and Simúth J. 2005. Two structurally different defensin genes, one of them encoding a novel defensin isoform, are expressed in honeybee Apis mellifera. Insect Biochem. Mol. Biol. 35: 11-22

    Google Scholar 

  • Kraus B. and Hunt G. 1995. Differentiation of Varroa jacobsoni Oud. populations by random amplification of polymorphic DNA (RAPD). Apidologie 26: 283-290

    Google Scholar 

  • Kurtz J. 2005. Specific memory within innate immune systems. Trends Immunol. 26: 186-192

    Google Scholar 

  • Lai-Fook J. 1966. The repair of wounds in the integument of insects. J. Insect Physiol. 12: 195-226

    Google Scholar 

  • Lapidge K., Oldroyd B.P. and Spivak M. 2002. Seven suggestive quantitative trait loci influence hygienic behaviour of honey bees. Naturwissenschaften 89: 565-568

    Google Scholar 

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

    Google Scholar 

  • Lee G.M., Brown M.J.F. and Oldroyd B.P. 2013. Inbred and outbred honey bee (Apis mellifera) have similar innate immune response. Insect. Soc. 60: 97-102

    Google Scholar 

  • Lobo N.F., Ton L.Q., Hill C.A., Emore C., Romero-Severson J., Hunt G.J. and Collins F.H. 2003. Genomic analysis in the sting-2 quantitative trait locus for defensive behavior in the honey bee, Apis mellifera. Genome Res. 13: 2588-2593

    Google Scholar 

  • Locke B. and Fries I. 2011. Characteristics of honey bee colonies (Apis mellifera) in Sweden surviving Varroa destructor infestation. Apidologie 42: 533-542

  • Lourenco A.P., Zufelato M.S., Bitondi M.M.G. and Simoes Z.L.P. 2005. Molecular characterisation of a cDNA encoding prophenoloxidase and its expression in Apis mellifera. Insect Biochem. Mol. Biol. 35: 541-552

    Google Scholar 

  • Lourenco A.P., Martins J.R., Bitondi M.M.G. and Simoes L.P. 2009. Trade-off between immune stimulation and expression of storage protein genes. Arch. Insect. Biochem. Physiol. 71: 70-87

    Google Scholar 

  • Lowenberger C.A., Smarth C.T., Bulet P., Ferdig M.T., Severson D.W., Hoffmann J.A. and Christensen B.M. 1999. Insect immunity: molecular cloning, expression, and characterisation of cDNAs and genomic DNA encoding three isoforms of insect defensin in Aedes aegypti. Insect Mol. Biol. 8: 107-118

    Google Scholar 

  • Martel A.-C., Zeggane S., Auriéres C., Drajnudel P., Faucon J.-P. and Aubert M.F.A. 2007. Acaricide residues in honey and was after treatment of honey bee colonies with Apivar® or Asuntol® 50. Apidologie 38: 534-544

    Google Scholar 

  • Milum V.G. 1947. Grooming dance and associated activities of the honey bee. III. Acad. Sci. Trans. 40: 194-196

    Google Scholar 

  • Mondragon L., Martin S. and Vandame R. 2006. Grooming dance and associated activities of the honey bee. III. Apidologie 37: 67-74

    Google Scholar 

  • Moretto G., Gonçalves L.S. and De Jong D. 1993. Heritability of Africanised and European honey bee defensive behaviour against the mite Varroa jacobsoni. Rev. Bras. Genet. 16: 71-77

    Google Scholar 

  • Moritz R.F.A. and Evans J.D. 2007. Virology and the honey bee. In: Honeybee Breeding and Genomics for Resistance to Virus Infections (Aubert M., Ball B., Fries I., Moritz R.F.A., Milani N. and Bernadellie I., Eds), European Commission, Brussels. pp 347-370

  • Moritz R.F.A., de Miranda J., Fries I., Le Conte Y., Neumann P. and Paxton R. 2010. Research strategies to improve honeybee health in Europe. Apidologie 41: 227-242

  • Mustard J.A., Pham P.M. and Smith B.H. 2010. Modulation of motor behaviour by dopamine and the D1-like dopamine receptor AmDOP2 in the honey bee. J. Insect Physiol. 56: 422-430

    Google Scholar 

  • Navajas M., Migeon A., Alaux C., Martin-Magniette M.L., Robinson G.E., Evans J.D., Cros-Arteil S., Crauser D. and Le Conte Y. 2008. Differential gene expression of the honey bee Apis mellifera associated with Varroa destructor infection. BMC Genomics 9: 301

  • Neve K.A., Seamans J.K. and Trantham-Davidson H. 2004. Dopamine receptor signalling. J. Recept. Signal Transduct. Res. 24: 165-205

    Google Scholar 

  • Oudemans A.C. 1904. On a new genus and species of parasitic acari. Notes Leyden Museum 24: 216-222

    Google Scholar 

  • Oxley P.R., Spivak M. and Oldroyd B.P. 2010. Six quantitative trait loci influence task thresholds for hygienic behaviour in honeybees (Apis mellifera). Mol. Ecol. 19: 1453-1461

    Google Scholar 

  • Peng Y.S. 1988. The resistance mechanism of the Asian honey bee Apis cerana to the mite Varroa jacobsoni. In: Africanized Honeybees and Bee Mites (Needham G.R., Page R.E., Delfinado-Baker M. and Bowman C.E., Eds), Ellis Horwood, Chichester. pp 426-429

  • Peng Y.S., Fang Y., Xu S. and Ge L. 1987. The resistance mechanism of the Asian honey bee, Apis cerana Fabr., to an ectoparasitic mite Varroa jacobsoni Oudemans. J. Invert. Pathol. 49: 54-60

  • Pettis J.S. 2004. A scientific note on Varroa destructor resistance to coumapos in the United States. Apidologie 35: 91-92

    Google Scholar 

  • Rawlings R.D. and Barrett A.J. 1993. Evolutionary families of peptides. Biochem. J. 290: 205-218

    Google Scholar 

  • Richard F.J., Aubert A. and Grozinger C.M. 2008. Modulation of social interactions by immune stimulation in honey bee, Apis mellifera, workers. BMC Biology 6: 50

    Google Scholar 

  • Rosenkranz P. 1999. Honey bee (Apis mellifera L.) tolerance to Varroa jacobsoni Oud. in South America. Apidologie 30: 159-172

    Google Scholar 

  • Rosenkranz P., Tewarson N.C., Singh A. and Engels W. 1993. Differential hygienic behaviour towards Varroa jacobsoni in capped worker brood of Apis cerana depends on alien scent adhering to the mites. J. Apicult. Res. 32: 89-93

    Google Scholar 

  • Rosenkranz P., Aumeier P. and Ziegelmann B. 2010. Biology and control of Varroa destructor. J. Invert. Pathol. 103: S96-S119

    Google Scholar 

  • Rothenbuhler W. 1964. Behaviour genetics of nest cleaning behaviour in honeybees I. Response of four inbred lines to disease killed brood. Anim. Behav. 12: 578-583

    Google Scholar 

  • Royet J., Reichart J.M. and Hoffmann J.A. 2005. Sensing and signalling during infection in Drosophila. Curr. Opin. Immunol. 17: 11-17

    Google Scholar 

  • Ruttner F., Marx H. and Marx G. 1984. Beobachtungen über eine mögliche Anpassung von Varroa Jacobsoni an Apis mellifera L. in Uruguay. Apidologie 15: 43-62

  • Ruttner F. and Hänel H. 1992. Active defence against Varroa mites in a Carniolan stain of honeybee (Apis mellifera carnica Pollmann). Apidologie 23: 173-187

    Google Scholar 

  • Schmid-Hempel P. 2005. Evolutionary ecology of insect immune defence. Annu. Rev. Entomol. 50: 529-551

    Google Scholar 

  • Spivak M. and Reuter G.S. 1998. Performance of hygienic honey bee colonies in a commercial apiary. Apidologie 29: 291-302

    Google Scholar 

  • Stanimirovic Z., Stevanovic J., Mirilovic M. and Stojic V. 2008. Heritability of hygienic behaviour in grey honey bee (Apis mellifera carnica). Acta Veter. 58: 593-601

    Google Scholar 

  • Stanimirovic Z., Stevanovic J., Aleksic N. and Stojic V. 2010. Heritability of grooming behaviour in grey honey bee (Apis mellifera carnica). Acta Veter. 60: 313-323

    Google Scholar 

  • Strand M.R. 2008. The insect cellular immune response. Insect Science 15: 1-14

    Google Scholar 

  • Stroschein-Stevenson S.L., Foley E., O’Farrell P.H. and Johnson A.D. 2009. Phagocytosis of Candida albicans by RNAi-treated Drosophila S2 cells. Methods Mol. Biol. 470: 347-358

    Google Scholar 

  • Tsurada J.M., Harris J.W., Bourgeois L., Danka R.G. and Hunt G.J. 2012. High-resolution linkage analyses to identify genes that influence Varroa sensitive hygiene behaviour in honey bees. PLoS ONE 7: e48276

  • van Engelsdorp D., Evans J.D., Saegerman C., Mullin C., Haubruge E., Nguyen B.K., Frazier J., Cox-Foster D., Chen Y., Underwood R., Tarpy D.R. and Pettis J.S. 2009. Colony collapse disorder: A descriptive study. PLoS ONE 4: e6481

  • Webster T.C. and Delaplane K.S. 2001 Mites of the Honey Bee. Dadant and Sons Inc., Hamilton Illinois

  • Weinstock G.M., Robinson G.E., Gibbs R.A., Worley K.C., Evans J.D., Maleszka R., Robertson H.M., Weaver D.B., Beye M., Carninci P. et al. 2006. Insights into social insects from the genome of the honey bee Apis mellifera. Nature 443: 931-949

    Google Scholar 

  • Zhang Y., Liu X., Zhang W. and Han R. 2010. Differential gene expression of the honey bee Apis mellifera and Apis cerana induced by Varroa destructor infection. J. Insect Physiol. 56: 1207-1218

  • Zou Z., Lopes D.L., Kanost M.R., Evans J.D. and Jiang H. 2006. Comparative analysis of serine protease-related genes in the honey bee genome: possible involvement in embryonic development and innate immunity. Insect Mol. Biol. 15: 603-614

    Google Scholar 

  • Zufelato M.S., Lourenco A.P., Simoes Z.L.P., Jorge J.A. and Bitondi M.M.G. 2004. Phenoloxidase activity in Apis mellifera honey bee pupae, and ecdysteroid-dependent expression of the prophenoloxidase mRNA. Insect Biochem. Mol. Biol. 34: 1257-1268

    Google Scholar 

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Acknowledgments

The publication is supported by the TÁMOP-4.2.2/B-10/1-2010-0024 project. The project is co-financed by the European Union and the European Social Fund. The manuscript has been proofread by Proof-Reading Service and Dr. Matthew Baranski as native English speaker. Authors thank three anonymous reviewers for their helpful comments.

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  1. Centre for Agricultural and Applied Economic Science, University of Debrecen, Böszörményi Street 138, Debrecen, 4032, Hungary

    E. Zakar, A. Jávor & Sz. Kusza

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Zakar, E., Jávor, A. & Kusza, S. Genetic bases of tolerance to Varroa destructor in honey bees (Apis mellifera L.). Insect. Soc. 61, 207–215 (2014). https://doi.org/10.1007/s00040-014-0347-5

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