Simulated vector transmission differentially influences dynamics of two viral variants of deformed wing virus in honey bees () Open Access

Abstract

Understanding how vectors alter the interactions between viruses and their hosts is a fundamental question in virology and disease ecology. In honey bees, transmission of deformed wing virus (DWV) by parasitic mites has been associated with elevated disease and host mortality, and transmission has been hypothesized to lead to increased viral titres or select for more virulent variants. Here, we mimicked transmission by serially passaging a mixed population of two DWV variants, A and B, by injection through reared honey bee pupae and tracking these viral populations through five passages. The DWV-A and DWV-B variant proportions shifted dynamically through passaging, with DWV-B outcompeting DWV-A after one passage, but levels of both variants becoming equivalent by Passage 5. Sequencing analysis revealed a dominant, recombinant DWV-B strain (DWV-A derived 5′ IRES region with the rest of the genome DWV-B), with low nucleotide diversity that decreased through passaging. DWV-A populations had higher nucleotide diversity compared to DWV-B, but this also decreased through passaging. Selection signatures were found across functional regions of the DWV-A and DWV-B genomes, including amino acid mutations in the putative capsid protein region. Simulated vector transmission differentially impacted two closely related viral variants which could influence viral interactions with the host, demonstrating surprising plasticity in vector-host-viral dynamics.

Funding
This study was supported by the:
  • Huck Institutes of the Life Sciences
    • Principle Award Recipient: AllysonM Ray
  • College of Agricultural Sciences, Pennsylvania State University
    • Principle Award Recipient: AllysonM Ray
  • U.S. Department of Agriculture (Award #1010032)
    • Principle Award Recipient: JasonL Rasgon
  • U.S. Department of Agriculture (Award #4716)
    • Principle Award Recipient: ChristinaM Grozinger
  • Animal and Plant Health Inspection Service (Award #16-8130-0501)
    • Principle Award Recipient: ChristinaM Grozinger
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001687
2021-11-24
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/102/11/jgv001687.html?itemId=/content/journal/jgv/10.1099/jgv.0.001687&mimeType=html&fmt=ahah

References

  1. Anderson RM, May RM. Coevolution of hosts and parasites. Parasitology 1982; 85:411–426 [View Article]
    [Google Scholar]
  2. Schmid-Hempel P. Evolutionary Parasitology: the Integrated Study of Infections, Immunology, Ecology, and Genetics Oxford University Press; 2011
    [Google Scholar]
  3. Institute of Medicine (US) Forum on Microbial Threats Vector-Borne Diseases: Understanding the Environmental, Human Health, and Ecological Connections, Workshop Summary National Academies Press (US; 2008
    [Google Scholar]
  4. Genersch E, Aubert M. Emerging and re-emerging viruses of the honey bee (Apis mellifera L.). Vet Res 2010; 41:54 [View Article] [PubMed]
    [Google Scholar]
  5. McMahon DP, Wilfert L, Paxton RJ, Brown MJF. Emerging viruses in bees: from molecules to ecologyviruses in bees: from molecules to ecology. Adv Virus Res 2018; 101:251–291 [View Article]
    [Google Scholar]
  6. Chen YP, Siede R. Honey Bee Viruses. Adv Virus Res 2007; 70:33–80 [View Article] [PubMed]
    [Google Scholar]
  7. Grozinger CM, Flenniken ML. Bee viruses: ecology, pathogenicity, and impacts. Annu Rev Entomol 2019; 64:205–226 [View Article]
    [Google Scholar]
  8. Lanzi G, Miranda JRD, Boniotti MB, Cameron CE, Lavazza A et al. Molecular and biological characterization of deformed wing virus of hobiological characterization of deformed wing virus of honeybees (Apis mellifera L.). J Virol 2006; 80:4998–5009 [View Article]
    [Google Scholar]
  9. Annoscia D, Del Piccolo F, Covre F, Nazzi F. Mite infestation during development alters the in-hive behaviour of adult honeybees. Apidologie 2015; 46:306–314 [View Article]
    [Google Scholar]
  10. Natsopoulou ME, McMahon DP, Paxton RJ. Parasites modulate within-colony activity and accelerate the temporal polyethism schedule of a social insect, the honey bee. Behav Ecol Sociobiol 2016; 70:1019–1031 [View Article]
    [Google Scholar]
  11. Traniello IM, Bukhari SA, Kevill J, Ahmed AC, Hamilton AR et al. Meta-analysis of honey bee neurogenomic response links Deformed wing virus type A to precocious behavioral maturation. Sci Rep 20201–12
    [Google Scholar]
  12. Benaets K, Geystelen AV, Cardoen D, Smet LD, Graaf DCD et al. Covert deformed wing virus infections have long-term deleterious effects on honeybee foraging and survival. Proceedings of the Royal Society B 2017284
    [Google Scholar]
  13. de Miranda JR, Genersch E. Deformed wing virus. J Invertebr Pathol 2010; 103:S48–S61
    [Google Scholar]
  14. Chen Y, Evans J, Feldlaufer M. Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera. J Invertebr Pathol 2006; 92:152–159 [View Article] [PubMed]
    [Google Scholar]
  15. Bowen-Walker PL, Martin SJ, Gunn A. The transmission of deformed wing virus between honeybees (Apis mellifera L.) by the ectoparasitic mite Varroa jacobsoni oud. J Invertebr Pathol 1999; 73:101–106 [View Article] [PubMed]
    [Google Scholar]
  16. Nazzi F, Le Conte Y. Ecology of Varroa destructor, the major ectoparasite of the Western Honey Bee, Apis mellifera. Annu Rev Entomol 2016; 61:417–432 [View Article] [PubMed]
    [Google Scholar]
  17. Oldroyd BP. Coevolution while you wait: Varroa jacobsoni, a new parasite of western honeybees. Trend Ecol Evol 1999; 14:312–315 [View Article]
    [Google Scholar]
  18. Annoscia D, Brown SP, Prisco GD, Paoli ED, Fabbro SD et al. Haemolymph removal by Varroa mite destabilizes the dynamical interaction between immune effectors and virus in bees, as predicted by Volterras model. Proc Roy Soc B 2019; 286:20190331
    [Google Scholar]
  19. Ramsey SD, Ochoa R, Bauchan G, Gulbronson C, Mowery JD et al. Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proceed National Acad Sci 2019
    [Google Scholar]
  20. Locke B, Semberg E, Forsgren E, De Miranda JR. Persistence of subclinical deformed wing virus infections in honeybees following Varroa mite removal and a bee population turnover. PLoS ONE 2017; 12:1–10
    [Google Scholar]
  21. Dainat B, Evans JD, Chen YP, Gauthier L, Neumann P. Predictive markers of honey bee colony collapse. PLoS One 2012; 7:e32151
    [Google Scholar]
  22. Doke MA, Frazier M, Grozinger CM. Overwintering honey bees: biology and management. Curr Opin Insect Sci 2015; 10:185–193 [View Article] [PubMed]
    [Google Scholar]
  23. Natsopoulou ME, McMahon DP, Doublet V, Frey E, Rosenkranz P et al. The virulent, emerging genotype B of Deformed wing virus is closely linked to overwinter honeybee worker loss. Sci Rep 2017; 7:1–9 [View Article]
    [Google Scholar]
  24. Martin SJ, Highfield AC, Brettell L, Villalobos EM, Budge GE et al. Global honey bee viral landscape altered by a parasitic mite. Science 2012; 336:1304–1307
    [Google Scholar]
  25. Wilfert L, Long G, Leggett HC, Schmid-Hempel P, Butlin R et al. Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites. Science 2016; 351:594–597 [View Article] [PubMed]
    [Google Scholar]
  26. Di Prisco G, Annoscia D, Margiotta M, Ferrara R, Varricchio P et al. A mutualistic symbiosis between a parasitic mite and a pathogenic virus undermines honey bee immunity and health. Proc Natl Acad Sci U S A 2016; 113:3203–3208 [View Article]
    [Google Scholar]
  27. Nazzi F, Brown SP, Annoscia D, Del Piccolo F, Di Prisco G et al. Synergistic parasite-pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies. PLoS Pathog 2012; 8:e1002735 [View Article] [PubMed]
    [Google Scholar]
  28. Wood GR, Fannon JM, Moore JD, Bull JC et al. A virulent strain of deformed wing virus (DWV) of honeybees (Apis mellifera) prevails after Vvarroa destructor-mediated, or in vitro, transmission. PLoS Pathog 2014; 10:e1004230 [View Article]
    [Google Scholar]
  29. Manley R, Temperton B, Doyle T, Gates D, Hedges S. Knock-on community impacts of a novel vector: spillover of emerging DWV-B from Varroa -infested honeybees to wild bumblebees. Ecol Lett 2019; 22:1306–1315 [View Article]
    [Google Scholar]
  30. Mondet F, de Miranda JR, Kretzschmar A, Le Conte Y, Mercer AR. On the front line: quantitative virus dynamics in Honeybee (Apis mellifera L.) colonies along a new expansion front of the parasite Varroa destructor. PLoS Pathog 2014; 10:e1004323 [View Article] [PubMed]
    [Google Scholar]
  31. Singh R, Levitt AL, Rajotte EG, Holmes EC, Ostiguy N et al. RNA viruses in hymenopteran pollinators: Evidence of inter-taxa virus transmission via pollen and potential impact on non-Apis hymenopteran species. PLoS ONE 2010; 5:12 [View Article] [PubMed]
    [Google Scholar]
  32. Tehel A, Brown MJF, Paxton RJ. Impact of managed honey bee viruses on wild bees. Curr Opin Virol 2016; 19:16–22 [View Article] [PubMed]
    [Google Scholar]
  33. Ongus JR, Peters D, Bonmatin JM, Bengsch E, Vlak JM et al. Complete sequence of a picorna-like virus of the genus Iflavirus replicating in the mite Varroa destructor. J Gen Virol 2004; 85:3747–3755 [View Article] [PubMed]
    [Google Scholar]
  34. Gisder S, Aumeier P, Genersch E. Deformed wing virus: replication and viral load in mites (Varroa destructor). J Gen Virol 2009; 90:463–467 [View Article]
    [Google Scholar]
  35. McMahon DP, Natsopoulou ME, Doublet V, Fürst M, Weging S et al. Elevated virulence of an emerging viral genotype as a driver of honeybee loss. Proceedings of the Royal Society B 2016; 283:1833
    [Google Scholar]
  36. Ryabov E, Childers AK, Chen Y, Madella S, Nessa A et al. Recent spread of Varroa destructor virus-1, a honey bee pathogen, in the United States. Sci Rep 2017; 7:1–10 [View Article]
    [Google Scholar]
  37. Moore J, Jironkin A, Chandler D, Burroughs N, Evans DJ et al. Recombinants between Deformed wing virus and Varroa destructor virus-1 may prevail in Varroa destructor -infested honeybee colonies. J Gen Virol 2011; 92:156–161 [View Article] [PubMed]
    [Google Scholar]
  38. Mordecai GJ, Wilfert L, Martin SJ, Jones IM, Schroeder DC. Diversity in a honey bee pathogen: First report of a third master variant of the Deformed Wing Virus quasispecies. ISME J 2016; 10:1264–1273 [View Article] [PubMed]
    [Google Scholar]
  39. Mordecai GJ, Brettell LE, Martin SJ, Dixon D, Jones IM et al. Superinfection exclusion and the long-term survival of honey bees in Varroa-infested colonies. ISME J 2016; 10:1182–1191 [View Article] [PubMed]
    [Google Scholar]
  40. Brettell LE, Schroeder DC, Martin SJ. RNAseq analysis reveals virus diversity within Hawaiian apiary insect communities. Viruses 2019; 11:397 [View Article]
    [Google Scholar]
  41. Tehel A, Vu Q, Bigot D, Gogol-döring A, Koch P et al. The two prevalent genotypes of an emerging equally low pupal mortality and equally high wing deformities in host honey bees. Viruses 2019; 11:1–18
    [Google Scholar]
  42. Brettell LE, Mordecai GJ, Schroeder DC, Jones IM, Da Silva JR et al. A comparison of deformed wing virus in deformed and asymptomatic honey bees. Insects 2017; 8: [View Article]
    [Google Scholar]
  43. Kevill JL, Souza DFS, Sharples C 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 2019; 11: [View Article] [PubMed]
    [Google Scholar]
  44. Neumann P, Yañez O, Fries I, De Miranda JR. Varroa invasion and virus adaptation. Trends Parasitol 2012; 28:353–354 [View Article] [PubMed]
    [Google Scholar]
  45. Gisder S, Möckel N, Eisenhardt D, Genersch E. In vivo evolution of viral virulence: switching of deformed wing virus between hosts results in virulence changes and sequence shifts. Environ Microbiol 2018; 20:4612–4628 [View Article]
    [Google Scholar]
  46. Remnant EJ, Mather N, Gillard TL, Yagound B, Beekman M et al. Direct transmission by injection affects competition among RNA viruses in honeybees. Proc Royal Soc B 2019; 286:20182452
    [Google Scholar]
  47. Yañez O, Chávez-galarza J, Tellgren-roth C, Pinto MA, Neumann P et al. The honeybee (Apis mellifera) developmental state shapes the genetic composition of the deformed wing virus-a quasispecies during serial transmission. Sci Rep 2020; 10:1–12
    [Google Scholar]
  48. Winston ML. The Biology of the Honey Bee Harvard University Press; 1991
    [Google Scholar]
  49. Schmehl DR, Tomé H, Mortensen AN, Martins GF, Ellis JD. Protocol for the in vitro rearing of honey bee (Apis mellifera L.) workers. J Apic Res 2016; 55:113–129
    [Google Scholar]
  50. Pertea M, Kim D, Pertea GM, Leek JT, Salzberg SL. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat Protoc 2016; 11:1650–1667 [View Article] [PubMed]
    [Google Scholar]
  51. Li H. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 2011; 27:2987–2993
    [Google Scholar]
  52. Li H. Seqtk: a fast and lightweight tool for processing FASTA or FASTQ sequences; 2013
  53. Grabherr MG, Hass BJ, Yassour M, Levin JZ, Thompson DA et al. Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat Biotechnol 2013; 29:644–652
    [Google Scholar]
  54. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 2011; 7:539 [View Article]
    [Google Scholar]
  55. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ. Jalview Version 2 — a multiple sequence alignment editor and analysis workbench. Bioinform 2009; 25:1189–1191 [View Article]
    [Google Scholar]
  56. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article]
    [Google Scholar]
  57. Bowen CD, Renner DW, Johnston CM, Szpara ML. In vitro evolution of herpes simplex virus 1 (HSV-1) reveals selection for syncytia and other minor variants in cell culture. Virus Evol 2020; 6:1–15 [View Article]
    [Google Scholar]
  58. Cingolani P, Platts A, Wang LL, Coon M, Nguyen T et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 2012; 6:80–92 [View Article]
    [Google Scholar]
  59. Škubník K, Nováček J, Füzik T, Přidal A, Paxton RJ et al. Structure of deformed wing virus, a major honey bee pathogen. Proc Natl Acad Sci U S A 2017; 114:3210–3215 [View Article]
    [Google Scholar]
  60. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM et al. UCSF Chimera — A Visualization System for Exploratory Research and Analysis. J Comput Chem 2004
    [Google Scholar]
  61. Kassambara A, Kosinski M, Biecek P. survminer: Drawing Survival Curves using “ggplot2.”; 2020
  62. Core Team R. R: A language and environment for statistical computing. R Foundation for Statistical Computing Vienna, Austria: 2020
    [Google Scholar]
  63. Therneau T. A Package for Survival Analysis in S 2015
    [Google Scholar]
  64. Organtini LJ, Shingler KL, Ashley RE, Capaldi EA, Durrani K et al. Honey bee deformed wing virus structures reveal that conformational changes accompany genome release. J Virol 2017; 91:10–13 [View Article]
    [Google Scholar]
  65. Cooper VS, Reiskind MH, Miller JA, Shelton KA, Walther BA et al. Timing of transmission and the evolution of virulence of an insect virus. Proc Roy Soc London Ser B Biol Sci 2002; 269:1161–1165 [View Article]
    [Google Scholar]
  66. Norton AM, Remnant EJ, Buchmann G, Beekman M. Accumulation and competition amongst deformed wing virus genotypes in naïve aaustralian honeybees provides insight into the increasing global prevalence of gcompetition amongst deformed wing virus genotypes in naïve australian honeybees provides insight into the increasing global prevalence of genotype b. Front Microbiol 2020; 11:1–14 [View Article]
    [Google Scholar]
  67. Dalmon A, Desbiez C, Coulon M, Thomasson M, Le Conte Y et al. Evidence for positive selection and recombination hotspots in Deformed wing virus (DWV). Sci Rep 2017; 7:1–12
    [Google Scholar]
  68. Lamp B, Url A, Seitz K, Eichhorn J, Riedel C et al. Construction and rescue of a molecular clone of Deformed wing virus (DWV). PLoS ONE 2016; 11:1–18 [View Article]
    [Google Scholar]
  69. Ryabov E, Childers AK, Lopez D, Grubbs K, Posada-Florez F et al. Dynamic evolution in the key honey bee pathogen deformed wing virus: Novel insights into virulence and competition using reverse genetics. PLoS Biol 2019; 17:10 [View Article] [PubMed]
    [Google Scholar]
  70. Guo Y, Goodman CL, Stanley DW, Bonning BC. Cell lines for honey bee virus research. Viruses 2020; 12:1–17
    [Google Scholar]
  71. Retel C, Markle H, Becks L, Feulner PGD. Ecological and evolutionary processes shaping viral genetic diversity. Viruses 2019; 11:220 [View Article] [PubMed]
    [Google Scholar]
  72. Sanjuán R, Domingo-Calap P. Mechanisms of viral mutation. Cell Mol Life Sci 2016; 73:4433–4448 [View Article] [PubMed]
    [Google Scholar]
  73. Duffy S, Shackelton L, Holmes E. Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 2008; 9:267–276 [View Article] [PubMed]
    [Google Scholar]
  74. Andino R, Domingo E. Viral quasispecies. Virology 2015; 479–480:46–51 [View Article] [PubMed]
    [Google Scholar]
  75. Domingo E, Escarmís C, Sevilla N, Moya A, Elena SF et al. Basic concepts in RNA virus evolution. FASEB j 1996; 10:859–864 [View Article]
    [Google Scholar]
  76. Alizon S, DeRoode JC, Michalakis Y. Multiple infections and the evolution of virulence. Ecol Lett 2013; 16:556–567 [View Article] [PubMed]
    [Google Scholar]
  77. Shirogane Y, Watanabe S, Yanagi Y. Cooperation between different variants: A unique potential for virus evolution. Virus R 2019; 264:68–73
    [Google Scholar]
  78. Chen YP, Higgins JA, Feldlaufer MF. Quantitative Real-Time Reverse Transcription-PCR analysis of deformed quantitative Real-Time Reverse Transcription-PCR analysis of deformed wing virus infection in the honeybee (Apis mellifera L.). Appl Environ Microbiol 2005; 71:436–441
    [Google Scholar]
  79. Harbo JR, Harris JW. Heritability in honey bees (Hymenoptera: Apidae) of characteristics associated with resistance to Varroa jacobsoni (Mesostigmata: Varroidae). J Econ Entomol 1999; 92:
    [Google Scholar]
  80. Mondet F, Beaurepaire A, McAfee A, Locke B, Alaux C et al. Honey bee survival mechanisms against the parasite Varroa destructor: a sys‐tematic review of phenotypic and genomic research efforts. Int J Parasitol 2020; 50:433–447 [View Article] [PubMed]
    [Google Scholar]
  81. Barribeau SM, Sadd BM, du Plessis L, Schmid-Hempel P. Gene expression differences underlying genotype-by-genotype specificity in a host–parasite system. Proc Natl Acad Sci USA 2014; 111:3496–3501 [View Article]
    [Google Scholar]
  82. de Roode JC, Altizer S. Host – parasite genetic interactions and virulence-transmission relationships in natural populations of monarch butterflies. Evolution 2009; 64:502–514 [View Article] [PubMed]
    [Google Scholar]
  83. Lambrechts L, Chevillon C, Albright RG, Thaisomboonsuk B, Richardson JH et al. Genetic specificity and potential for local adaptation between dengue viruses and mosquito vectors. BMC Evol Biol 2009; 9:1–11 [View Article]
    [Google Scholar]
  84. Posada-Florez F, Childers AK, Heerman MC, Egekwu N, Cook SC 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 2019; 9:1–10
    [Google Scholar]
  85. Bee Informed Partnership National Management Survey 2020
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001687
Loading
/content/journal/jgv/10.1099/jgv.0.001687
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL

Most cited Most Cited RSS feed