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Pupal cannibalism by worker honey bees contributes to the spread of deformed wing virus

  • 1.

    Grassly, N. C. & Fraser, C. Mathematical models of infectious disease transmission. Nat. Rev. Microbiol. 6, 477–487 (2008).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 2.

    Cressler, C. E., McLeod, D. V., Rozins, C., Van Den Hoogen, J. & Day, T. The adaptive evolution of virulence: A review of theoretical predictions and empirical tests. Parasitology 143, 915–930 (2016).

    PubMed 
    Article 

    Google Scholar 

  • 3.

    Lanzi, G. et al. Molecular and biological characterization of deformed wing virus of honeybees (Apismellifera L.). J. Virol. 80, 4998–5009 (2006).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 4.

    Dainat, B., Evans, J. D., Chen, Y. P., Gauthier, L. & Neumann, P. Dead or alive: Deformed wing virus and Varroa destructor reduce the life span of winter honeybees. Appl. Environ. Microbiol. 78, 981–987 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 5.

    Highfield, A. C. et al. Deformed wing virus implicated in overwintering honeybee colony losses. Appl. Environ. Microbiol. 75, 7212–7220 (2009).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 6.

    Le Conte, Y., Ellis, M. & Ritter, W. Varroa mites and honey bee health: Can Varroa explain part of the colony losses?. Apidologie 41, 353–363 (2010).

    Article 

    Google Scholar 

  • 7.

    De Miranda, J. R. & Genersch, E. Deformed wing virus. J. Invertebr. Pathol. 103, S48–S61 (2010).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • 8.

    Martin, S. J. & Brettell, L. E. Deformed wing virus in honeybees and other insects. Annu. Rev. Virol. 6, 49–69 (2019).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 9.

    Sumpter, D. J. & Martin, S. J. The dynamics of virus epidemics in Varroa-infested honey bee colonies. J. Anim. Ecol. 73, 51–63 (2004).

    Article 

    Google Scholar 

  • 10.

    Ramsey, S. D. et al. Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proc. Natl. Acad. Sci. 116, 1792–1801 (2019).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 11.

    Yang, X. & Cox-Foster, D. L. Impact of an ectoparasite on the immunity and pathology of an invertebrate: Evidence for host immunosuppression and viral amplification. Proc. Natl. Acad. Sci. 102, 7470–7475 (2005).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 12.

    Rosenkranz, P., Aumeier, P. & Ziegelmann, B. Biology and control of Varroa destructor. J. Invertebr. Pathol. 103, S96–S119 (2010).

    PubMed 
    Article 

    Google Scholar 

  • 13.

    Wilfert, L. et al. Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites. Science 351, 594–597 (2016).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 14.

    Dalmon, A. et al. Evidence for positive selection and recombination hotspots in deformed wing virus (DWV). Sci. Rep. 7, 1–12 (2017).

    Article 
    CAS 

    Google Scholar 

  • 15.

    Martin, S. J. et al. Global honey bee viral landscape altered by a parasitic mite. Science 336, 1304–1306 (2012).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 16.

    Moore, J. et al. Recombinants between deformed wing virus and Varroa destructor virus-1 may prevail in Varroa destructor-infested honeybee colonies. J. Gen. Virol. 92, 156–161 (2011).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 17.

    Ryabov, E. V. et al. A virulent strain of deformed wing virus (DWV) of honeybees (Apis mellifera) prevails after Varroa destructor-mediated, or in vitro, transmission. PLoS Pathog. 10, e1004230 (2014).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 18.

    Ryabov, E. V. et al. Dynamic evolution in the key honey bee pathogen deformed wing virus: Novel insights into virulence and competition using reverse genetics. PLoS Biol. 17, e3000502 (2019).

    MathSciNet 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 19.

    Mondet, F. et al. Specific cues associated with honey bee social defence against Varroa destructor infested brood. Sci. Rep. 6, 25444 (2016).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 20.

    Spivak, M. & Danka, R. G. Perspectives on hygienic behavior in Apismellifera and other social insects. Apidologie https://doi.org/10.1007/s13592-020-00784-z (2020).

    Article 

    Google Scholar 

  • 21.

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

    Article 

    Google Scholar 

  • 22.

    Baracchi, D., Fadda, A. & Turillazzi, S. Evidence for antiseptic behaviour towards sick adult bees in honey bee colonies. J. Insect Physiol. 58, 1589–1596 (2012).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 23.

    Traynor, K. S. et al. Varroa destructor: A complex parasite, crippling honey bees worldwide. Trends Parasitol. 36, 592–606 (2020).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 24.

    Sun, Q. & Zhou, X. Corpse management in social insects. Int. J:. Biol. Sci. 9, 313 (2013).

    Google Scholar 

  • 25.

    Van Allen, B. G. et al. Cannibalism and infectious disease: Friends or foes?. Am. Nat. 190, 299–312 (2017).

    PubMed 
    Article 

    Google Scholar 

  • 26.

    Bourke, A. F. Queen behaviour, reproduction and egg cannibalism in multiple-queen colonies of the ant Leptothorax acervorum. Anim. Behav. 42, 295–310 (1991).

    Article 

    Google Scholar 

  • 27.

    Pulliainen, U., Helanterä, H., Sundström, L. & Schultner, E. The possible role of ant larvae in the defence against social parasites. Proc. R. Soc. B 286, 20182867 (2019).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 28.

    Evans, H. & West-Eberhard, M. The Wasps (Univ. Michigan, 1970).

    Google Scholar 

  • 29.

    Schmickl, T. & Crailsheim, K. Cannibalism and early capping: Strategy of honeybee colonies in times of experimental pollen shortages. J. Comp. Physiol. A 187, 541–547 (2001).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 30.

    Webster, T. C., Peng, Y. S. & Duffey, S. S. Conservation of nutrients in larval tissue by cannibalizing honey bees. Physiol. Entomol. 12, 225–231 (1987).

    CAS 
    Article 

    Google Scholar 

  • 31.

    Woyke, J. Cannibalism and brood-rearing efficiency in the honeybee. J. Apic. Res. 16, 84–94 (1977).

    Article 

    Google Scholar 

  • 32.

    Chouvenc, T. Limited survival strategy in starving subterranean termite colonies. Insectes Soc. 67, 71–82 (2020).

    Article 

    Google Scholar 

  • 33.

    Raina, A. K., Park, Y. I. & Lax, A. Defaunation leads to cannibalism in primary reproductives of the Formosan subterranean termite, Coptotermes formosanus (Isoptera: Rhinotermitidae). Ann. Entomol. Soc. Am. 97, 753–756 (2004).

    Article 

    Google Scholar 

  • 34.

    Schmickl, T. & Crailsheim, K. Inner nest homeostasis in a changing environment with special emphasis on honey bee brood nursing and pollen supply. Apidologie 35, 249–263 (2004).

    Article 

    Google Scholar 

  • 35.

    Meunier, J. Social immunity and the evolution of group living in insects. Philos. Trans. R. Soc. B Biol. Sci. 370, 20140102 (2015).

    Article 

    Google Scholar 

  • 36.

    Rueppell, O., Hayworth, M. K. & Ross, N. Altruistic self-removal of health-compromised honey bee workers from their hive. J. Evol. Biol. 23, 1538–1546 (2010).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 37.

    Halling, L. & Oldroyd, B. P. Do policing honeybee (Apis mellifera) workers target eggs in drone comb?. Insectes Soc. 50, 59–61 (2003).

    Article 

    Google Scholar 

  • 38.

    Santomauro, G., Oldham, N. J., Boland, W. & Engels, W. Cannibalism of diploid drone larvae in the honey bee (Apis mellifera) is released by odd pattern of cuticular substances. J. Apic. Res. 43, 69–74 (2004).

    Article 

    Google Scholar 

  • 39.

    Imdorf, A., Rickli, M., Kilchenmann, V., Bogdanov, S. & Wille, H. Nitrogen and mineral constituents of honey bee worker brood during pollen shortage. Apidologie 29, 315–325 (1998).

    Article 

    Google Scholar 

  • 40.

    Rudolf, V. H. & Antonovics, J. Disease transmission by cannibalism: Rare event or common occurrence?. Proc. R. Soc. B Biol. Sci. 274, 1205–1210 (2007).

    Article 

    Google Scholar 

  • 41.

    Chapman, J. W. et al. Age-related cannibalism and horizontal transmission of a nuclear polyhedrosis virus in larval Spodoptera frugiperda. Ecol. Entomol. 24, 268–275 (1999).

    Article 

    Google Scholar 

  • 42.

    Hamano, K. et al. Waterborne and cannibalism-mediated transmission of the Yellow head virus in Penaeus monodon. Aquaculture 437, 161–166 (2015).

    Article 

    Google Scholar 

  • 43.

    Möckel, N., Gisder, S. & Genersch, E. Horizontal transmission of deformed wing virus: Pathological consequences in adult bees (Apis mellifera) depend on the transmission route. J. Gen. Virol. 92, 370–377 (2011).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • 44.

    Ryabov, E. V. et al. Development of a honey bee RNA virus vector based on the genome of a deformed wing virus. Viruses 12, 374 (2020).

    CAS 
    PubMed Central 
    Article 
    PubMed 

    Google Scholar 

  • 45.

    Posada-Florez, F. et al. Deformed wing virus type A, a major honey bee pathogen, is vectored by the mite Varroa destructor in a non-propagative manner. Sci. Rep. 9, 1–10 (2019).

    CAS 
    Article 

    Google Scholar 

  • 46.

    Bull, J. C. et al. A strong immune response in young adult honeybees masks their increased susceptibility to infection compared to older bees. PLoS Pathog. 8, e1003083 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 47.

    Shi, M. et al. Redefining the invertebrate RNA virosphere. Nature 540, 539–543 (2016).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 48.

    Masterman, R., Ross, R., Mesce, K. & Spivak, M. Olfactory and behavioral response thresholds to odors of diseased brood differ between hygienic and non-hygienic honey bees (Apis mellifera L.). J. Comp. Physiol. A 187, 441–452 (2001).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 49.

    Crailsheim, K. Trophallactic interactions in the adult honeybee (Apis mellifera L.). Apidologie 29, 97–112 (1998).

    Article 

    Google Scholar 

  • 50.

    Nixon, H. & Ribbands, C. R. Food transmission within the honeybee community. Proc. R. Soc. Lond. Ser. B Biol. Sci. 140, 43–50 (1952).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 51.

    Arathi, H. & Spivak, M. Influence of colony genotypic composition on the performance of hygienic behaviour in the honeybee, Apis mellifera L. Anim. Behav. 62, 57–66 (2001).

    Article 

    Google Scholar 

  • 52.

    Knecht, D. & Kaatz, H. Patterns of larval food production by hypopharyngeal glands in adult worker honey bees. Apidologie 21, 457–468 (1990).

    Article 

    Google Scholar 

  • 53.

    Li, Z. et al. Transcriptional and physiological responses of hypopharyngeal glands in honeybees (Apis mellifera L.) infected by Nosema ceranae. Apidologie 50, 51–62 (2019).

    CAS 
    Article 

    Google Scholar 

  • 54.

    Lass, A. & Crailsheim, K. Influence of age and caging upon protein metabolism, hypopharyngeal glands and trophallactic behavior in the honey bee (Apis mellifera L.). Insectes Soc. 43, 347–358 (1996).

    Article 

    Google Scholar 

  • 55.

    Chiou, S.-S. & Chen, W.-J. Mutations in the NS3 gene and 3′-NCR of Japanese encephalitis virus isolated from an unconventional ecosystem and implications for natural attenuation of the virus. Virology 289, 129–136 (2001).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 56.

    Steel, A., Gubler, D. J. & Bennett, S. N. Natural attenuation of dengue virus type-2 after a series of island outbreaks: A retrospective phylogenetic study of events in the South Pacific three decades ago. Virology 405, 505–512 (2010).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 57.

    de Souza, F. S., Allsopp, M. H. & Martin, S. J. Deformed wing virus prevalence and load in honeybees in South Africa. Arch. Virol. 166, 237–241 (2020).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 58.

    Martin, S. J. et al. Varroa destructor reproduction and cell re-capping in mite-resistant Apis mellifera populations. Apidologie 51, 369–381 (2020).

    CAS 
    Article 

    Google Scholar 

  • 59.

    Kulhanek, K. et al. Survey-derived best management practices for backyard beekeepers improve colony health and reduce mortality. PLoS ONE 16, e0245490 (2021).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 60.

    Peck, D. T. & Seeley, T. D. Mite bombs or robber lures? The roles of drifting and robbing in Varroa destructor transmission from collapsing honey bee colonies to their neighbors. PLoS ONE 14, e0218392 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 61.

    Ryabov, E. V. et al. Recent spread of Varroa destructor virus-1, a honey bee pathogen, in the United States. Sci. Rep. 7, 1–10 (2017).

    CAS 
    Article 

    Google Scholar 

  • 62.

    Abràmoff, M. D., Magalhães, P. J. & Ram, S. J. Image processing with ImageJ. Biophoton. Int. 11, 36–42 (2004).

    Google Scholar 


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