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Meta-analysis of honey bee neurogenomic response links Deformed wing virus type A to precocious behavioral maturation

  • 1.

    Steffan-Dewenter, I., Potts, S. G. & Packer, L. Pollinator diversity and crop pollination services are at risk. Trends in Ecology & Evolution 20, 651–652 (2005).

    • Article
    • Google Scholar
  • 2.

    Klein, A.-M. et al. Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences 274, 303–313 (2007).

  • 3.

    vanEngelsdorp, D. et al. A survey of honey bee colony losses in the U.S., Fall 2007 to Spring 2008. Plos One 3, e4071 (2008).

  • 4.

    vanEngelsdorp, D. et al. Colony collapse disorder: a descriptive study. Plos One 4, e6481 (2009).

  • 5.

    Ellis, J. D., Evans, J. D. & Pettis, J. Colony losses, managed colony population decline, and Colony Collapse Disorder in the United States. Journal of Apicultural Research 49, 134–136 (2010).

  • 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.

    Xie, X., Huang, Z. Y. & Zeng, Z. Why do Varroa mites prefer nurse bees? Scientific Reports 6, 28228 (2016).

  • 8.

    Lee, K. V. et al. A national survey of managed honey bee 2013–2014 annual colony losses in the USA. Apidologie 46, 292–305 (2015).

    • Article
    • Google Scholar
  • 9.

    Dietemann, V. et al. Varroa destructor: research avenues towards sustainable control. Journal of Apicultural Research 51, 125–132 (2012).

    • Article
    • Google Scholar
  • 10.

    Francis, R. M., Nielsen, S. L. & Kryger, P. Varroa-virus interaction in collapsing honey bee colonies. Plos One 8, e57540 (2013).

  • 11.

    Allen, M. & Ball, B. The incidence and world distribution of honey bee viruses. Bee World 77, 141–162 (1996).

    • Article
    • Google Scholar
  • 12.

    Grozinger, C. M. & Flenniken, M. L. Bee viruses: ecology, pathogenicity, and impacts. Annual Review of Entomology 64, 205–226 (2019).

  • 13.

    Chen, Y., Pettis, J. S., Evans, J. D., Kramer, M. & Feldlaufer, M. F. Transmission of Kashmir bee virus by the ectoparasitic mite Varroa destructor. Apidologie 35, 441–448 (2004).

    • Article
    • Google Scholar
  • 14.

    Shen, M., Yang, X., Cox-Foster, D. & Cui, L. The role of varroa mites in infections of Kashmir bee virus (KBV) and deformed wing virus (DWV) in honey bees. Virology 342, 141–149 (2005).

  • 15.

    Shen, M., Cui, L., Ostiguy, N. & Cox-Foster, D. Intricate transmission routes and interactions between picorna-like viruses (Kashmir bee virus and sacbrood virus) with the honeybee host and the parasitic varroa mite. Journal of General Virology 86, 2281–2289 (2005).

  • 16.

    Di Prisco, G. et al. Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera. Journal of General Virology 92, 151–155 (2011).

  • 17.

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

  • 18.

    Bailey, L. & Ball, B. V. Viruses. In Honey Bee Pathology 10–34 (Elsevier, 1991).

  • 19.

    Lanzi, G. et al. Molecular and biological characterization of deformed wing virus of honeybees (Apis mellifera L.). Journal of Virology 80, 4998–5009 (2006).

  • 20.

    Mordecai, G. J., Wilfert, L., Martin, S. J., Jones, I. M. & Schroeder, D. C. Diversity in a honey bee pathogen: first report of a third master variant of the Deformed Wing Virus quasispecies. The ISME Journal 10, 1264–1273 (2016).

  • 21.

    Martin, S. J. et al. Global honey bee viral landscape altered by a parasitic mite. Science (New York, N.Y.) 336, 1304–6 (2012).

  • 22.

    Kevill, J. L. et al. DWV-A lethal to honey bees (Apis mellifera): a colony level survey of DWV variants (A, B, and C) in England, Wales, and 32 states across the US. Viruses 11, 426 (2019).

  • 23.

    Natsopoulou, M. E. et al. The virulent, emerging genotype B of Deformed wing virus is closely linked to overwinter honeybee worker loss. Scientific Reports 7, 5242 (2017).

  • 24.

    Highfield, A. C. et al. Deformed wing virus implicated in overwintering honeybee colony losses. Applied and environmental microbiology 75, 7212–20 (2009).

  • 25.

    Shah, K. S., Evans, E. C. & Pizzorno, M. C. Localization of deformed wing virus (DWV) in the brains of the honeybee, Apis mellifera Linnaeus. Virology Journal 6, 182 (2009).

  • 26.

    Iqbal, J. & Mueller, U. Virus infection causes specific learning deficits in honeybee foragers. Proceedings of the Royal Society B: Biological Sciences 274, 1517–21 (2007).

  • 27.

    Wells, T. et al. Flight performance of actively foraging honey bees is reduced by a common pathogen. Environmental Microbiology Reports 8, 728–737 (2016).

  • 28.

    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. Applied and environmental microbiology 78, 981–7 (2012).

  • 29.

    McNeill, M. S., Kapheim, K. M., Brockmann, A., McGill, T. A. W. W. & Robinson, G. E. Brain regions and molecular pathways responding to food reward type and value in honey bees. Genes, Brain and Behavior 15, 305–317 (2015).

    • Article
    • Google Scholar
  • 30.

    Shpigler, H. Y. et al. Honey bee neurogenomic responses to affiliative and agonistic social interactions. Genes, Brain and Behavior 18, e12509 (2018).

    • Article
    • Google Scholar
  • 31.

    Kovac, H. & Crailsheim, K. Lifespan of Apis Mellifera Carnica Pollm. infested by Varroa Jacobsoni Oud. in relation to season and extent of infestation. Journal of Apicultural Research 27, 230–238 (1988).

    • Article
    • Google Scholar
  • 32.

    Doublet, V. et al. Unity in defence: honeybee workers exhibit conserved molecular responses to diverse pathogens. BMC Genomics 18, 207 (2017).

  • 33.

    Benaets, K. et al. Covert deformed wing virus infections have long-term deleterious effects on honeybee foraging and survival. Proceedings of the Royal Society B: Biological Sciences 284, 20162149 (2017).

  • 34.

    Huang, Z.-Y. & Robinson, G. E. Regulation of honey bee division of labor by colony age demography. Behavioral Ecology and Sociobiology 39, 147–158 (1996).

    • Article
    • Google Scholar
  • 35.

    Ushitani, T., Perry, C. J., Cheng, K. & Barron, A. B. Accelerated behavioural development changes fine-scale search behaviour and spatial memory in honey bees (Apis mellifera L.). Journal of Experimental Biology 219, 412–8 (2016).

  • 36.

    Peng, F. et al. A simple computational model of the bee mushroom body can explain seemingly complex forms of olfactory learning and memory. Current Biology 27, 224–230 (2017).

  • 37.

    Eden, E., Navon, R., Steinfeld, I., Lipson, D. & Yakhini, Z. GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 10, 48 (2009).

  • 38.

    Seeley, T. D. Adaptive significance of the age polyethism schedule in honeybee colonies. Behavioral Ecology and Sociobiology 11, 287–293 (1982).

    • Article
    • Google Scholar
  • 39.

    Winston, M. L. The Biology of the Honey Bee. (Harvard University Press, 1991).

  • 40.

    Shpigler, H. Y. et al. Behavioral, transcriptomic and epigenetic responses to social challenge in honey bees. Genes, Brain and Behavior 16, 579–591 (2017).

  • 41.

    Traniello, I. M., Chen, Z., Bagchi, V. A. & Robinson, G. E. Valence of social information is encoded in different subpopulations of mushroom body Kenyon cells in the honeybee brain. Proceedings of the Royal Society B: Biological Sciences 286, 20190901 (2019).

  • 42.

    Khamis, A. M. et al. Insights into the transcriptional architecture of behavioral plasticity in the honey bee Apis mellifera. Scientific Reports 5, 11136 (2015).

  • 43.

    Alaux, C. et al. Regulation of brain gene expression in honey bees by brood pheromone. Genes, Brain and Behavior 8, 309–319 (2009).

  • 44.

    Thurmond, J. et al. FlyBase 2.0: the next generation. Nucleic Acids Research 47, D759–D765 (2019).

  • 45.

    Kevill, J. et al. ABC assay: method development and application to quantify the role of three DWV master variants in overwinter colony losses of European honey bees. Viruses 9, 314 (2017).

  • 46.

    Xiong, W. C., Okano, H., Patel, N. H., Blendy, J. A. & Montell, C. repo encodes a glial-specific homeo domain protein required in the Drosophila nervous system. Genes & Development 8, 981–94 (1994).

  • 47.

    Shah, A. K., Kreibich, C. D., Amdam, G. V. & Münch, D. Metabolic enzymes in glial cells of the honeybee brain and their associations with aging, starvation and food response. Plos One 13, e0198322 (2018).

  • 48.

    Brutscher, L. M., Daughenbaugh, K. F. & Flenniken, M. L. Virus and dsRNA-triggered transcriptional responses reveal key components of honey bee antiviral defense. Scientific Reports 7, 6448 (2017).

  • 49.

    Johnson, R. M., Evans, J. D., Robinson, G. E. & Berenbaum, M. R. Changes in transcript abundance relating to colony collapse disorder in honey bees (Apis mellifera). Proceedings of the National Academy of Sciences of the United States of America 106, 14790–5 (2009).

  • 50.

    Brutscher, L. M. & Flenniken, M. L. RNAi and antiviral defense in the honey bee. Journal of Immunology Research 2015, 941897 (2015).

  • 51.

    Drakesmith, H. & Prentice, A. Viral infection and iron metabolism. Nature Reviews Microbiology 6, 541–552 (2008).

  • 52.

    Liu, G. et al. Aldehyde dehydrogenase 1 defines and protects a nigrostriatal dopaminergic neuron subpopulation. The Journal of Clinical Investigation 124, 3032–3046 (2014).

  • 53.

    Pesch, Y.-Y., Riedel, D., Patil, K. R., Loch, G. & Behr, M. Chitinases and Imaginal disc growth factors organize the extracellular matrix formation at barrier tissues in insects. Scientific Reports 6, 18340 (2016).

  • 54.

    Chupp, G. L. et al. A chitinase-like protein in the lung and circulation of patients with severe asthma. New England Journal of Medicine 357, 2016–2027 (2007).

  • 55.

    Lee, C. G. et al. Role of chitin and chitinase/chitinase-like proteins in inflammation, tissue remodeling, and injury. Annual Review of Physiology 73, 479–501 (2011).

  • 56.

    Kawada, M., Hachiya, Y., Arihiro, A. & Mizoguchi, E. Role of mammalian chitinases in inflammatory conditions. The Keio Journal of Medicine 56, 21–7 (2007).

  • 57.

    Wiley, C. A. et al. Role for mammalian chitinase 3-like protein 1 in traumatic brain injury. Neuropathology 35, 95–106 (2015).

  • 58.

    Falcon, T. et al. Exploring integument transcriptomes, cuticle ultrastructure, and cuticular hydrocarbons profiles in eusocial and solitary bee species displaying heterochronic adult cuticle maturation. Plos One 14, e0213796 (2019).

  • 59.

    Varela, P. F., Llera, A. S., Mariuzza, R. A. & Tormo, J. Crystal structure of imaginal disc growth factor-2. Journal of Biological Chemistry 277, 13229–13236 (2002).

  • 60.

    Kim, M. A. et al. Neural ganglia transcriptome and peptidome associated with sexual maturation in female Pacific abalone (Haliotis discus hannai). Genes 10, 268 (2019).

  • 61.

    Perry, C. J., Søvik, E., Myerscough, M. R. & Barron, A. B. Rapid behavioral maturation accelerates failure of stressed honey bee colonies. Proceedings of the National Academy of Sciences of the United States of America 112, 3427–32 (2015).

  • 62.

    Khoury, D. S., Myerscough, M. R. & Barron, A. B. A quantitative model of honey bee colony population dynamics. Plos One 6, e18491 (2011).

  • 63.

    Yañez, O. et al. Deformed wing virus and drone mating flights in the honey bee (Apis mellifera): implications for sexual transmission of a major honey bee virus. Apidologie 43, 17–30 (2012).

    • Article
    • Google Scholar
  • 64.

    Chu, H. M., Tan, Y., Kobierski, L. A., Balsam, L. B. & Comb, M. J. Activating transcription factor-3 stimulates 3′,5′-cyclic adenosine monophosphate-dependent gene expression. Molecular Endocrinology 8, 59–68 (1994).

  • 65.

    Schulz, D. J., Huang, Z.-Y. & Robinson, G. E. Effects of colony food shortage on behavioral development in honey bees. Behavioral Ecology and Sociobiology 42, 295–303 (1998).

    • Article
    • Google Scholar
  • 66.

    Goblirsch, M., Huang, Z. Y. & Spivak, M. Physiological and behavioral changes in honey bees (Apis mellifera) induced by Nosema ceranae infection. Plos One 8, e58165 (2013).

  • 67.

    Downey, D. L., Higo, T. T. & Winston, M. L. Single and dual parasitic mite infestations on the honey bee, Apis mellifera L. Insectes Sociaux 47, 171–176 (2000).

    • Article
    • Google Scholar
  • 68.

    Yildirim, K., Petri, J., Kottmeier, R. & Klämbt, C. Drosophila glia: few cell types and many conserved functions. Glia 67, 5–26 (2019).

  • 69.

    Kretzschmar, D. & Pflugfelder, G. Glia in development, function, and neurodegeneration of the adult insect brain. Brain Research Bulletin 57, 121–131 (2002).

  • 70.

    Edwards, T. N. & Meinertzhagen, I. A. The functional organisation of glia in the adult brain of Drosophila and other insects. Progress in Neurobiology 90, 471–497 (2010).

  • 71.

    Dheilly, N. M. et al. Who is the puppet master? Replication of a parasitic wasp-associated virus correlates with host behaviour manipulation. Proceedings of the Royal Society B: Biological Sciences 282, 20142773–20142773 (2015).

  • 72.

    Retallack, H. et al. Zika virus cell tropism in the developing human brain and inhibition by azithromycin. Proceedings of the National Academy of Sciences of the United States of America 113, 14408–14413 (2016).

  • 73.

    Bloch, G., Toma, D. P. & Robinson, G. E. Behavioral rhythmicity, age, division of labor and period expression in the honey bee brain. Journal of Biological Rhythms 16, 444–456 (2001).

  • 74.

    Buenz, E. J., Rodriguez, M. & Howe, C. L. Disrupted spatial memory is a consequence of picornavirus infection. Neurobiology of Disease 24, 266–273 (2006).

  • 75.

    McMahon, D. P. et al. Elevated virulence of an emerging viral genotype as a driver of honeybee loss. Proceedings of the Royal Society B: Biological Sciences 283, 20160811 (2016).

  • 76.

    Rittschof, C. C. et al. Neuromolecular responses to social challenge: common mechanisms across mouse, stickleback fish, and honey bee. Proceedings of the National Academy of Sciences of the United States of America 111, 17929–34 (2014).

  • 77.

    Wallberg, A. et al. A hybrid de novo genome assembly of the honeybee, Apis mellifera, with chromosome-length scaffolds. BMC Genomics 2019 20:1 20, 275 (2019).

    • Google Scholar
  • 78.

    Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).

  • 79.

    Liao, Y., Smyth, G. K. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2014).

  • 80.

    Liao, Y., Smyth, G. K. & Shi, W. The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote. Nucleic Acids Research 41, e108–e108 (2013).

  • 81.

    Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–40 (2010).

  • 82.

    Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing on JSTOR. Journal of the Royal Statistical Society. Series B: Methodological 57, 289–300 (1995).

    • MATH
    • Google Scholar
  • 83.

    Shen, L. GeneOverlap: An R package to test and visualize gene overlaps. (2014).

  • 84.

    Wang, M., Zhao, Y. & Zhang, B. Efficient test and visualization of multi-set intersections. Scientific Reports 5, 16923 (2015).

  • 85.

    Camacho, C. et al. BLAST+: architecture and applications. BMC Bioinformatics 10, 421 (2009).

  • 86.

    Hong, G., Zhang, W., Li, H., Shen, X. & Guo, Z. Separate enrichment analysis of pathways for up- and downregulated genes. Journal of the Royal Society, Interface 11, 20130950 (2014).

  • 87.

    Supek, F., Bošnjak, M., Škunca, N. & Šmuc, T. REVIGO summarizes and visualizes long lists of gene ontology terms. Plos One 6, e21800 (2011).

  • 88.

    Chandrasekaran, S. et al. Behavior-specific changes in transcriptional modules lead to distinct and predictable neurogenomic states. Proceedings of the National Academy of Sciences of the United States of America 108, 18020–5 (2011).

  • 89.

    Celniker, S. E. et al. Unlocking the secrets of the genome. Nature 459, 927–930 (2009).

  • 90.

    Gallo, S. M. et al. REDfly v3.0: toward a comprehensive database of transcriptional regulatory elements in Drosophila. Nucleic Acids Research 39, D118–D123 (2011).

  • 91.

    Murali, T. et al. DroID 2011: a comprehensive, integrated resource for protein, transcription factor, RNA and gene interactions for Drosophila. Nucleic Acids Research 39, D736–D743 (2011).


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