Abstract
Introduced social wasps (Vespula spp.) are a pest in many parts of the world. Recently, a mite species (Pneumolaelaps niutirani) was described and associated with disease symptoms in wasps. The mite does not appear to directly parasitise the wasps, but has been observed in high abundance, feeding on exudates from the mouths of larvae. We investigated the viral and fungal pathogens community in these mites and wasps. We found known viruses including Moku virus in both wasps and mites. Moku virus replicated in mites, likely indicating parasitism. Deformed wing virus, commonly found in wasps, was also detected in mite samples. Furthermore, the presence of putative viral transcripts related to 38 distinct viruses, including seven viruses previously isolated from arthropods, indicated that there may be many more viruses associated with the mite that are potentially shared with Vespula wasps. We also found generalist entomopathogenic fungus Aspergillus to infect both mites and wasps. Twelve distinct Aspergillus species were observed, all of which were found in wasp larvae from nests displaying symptoms of disease, with only one species in larvae from apparently healthy nests. Aspergillus novofumigatus was the most common of these species observed in wasps. Six Aspergillus species, including A. novofumigatus were detected in mites. Aspergillus loads were significantly higher in larvae from diseased nests. Our exploratory study indicates that mites can harbour both viruses and fungi that infect wasps, providing avenues of research into biological control using mites as infection vectors.
This is a preview of subscription content, log in via an institution to check access.
Images by Robert Brown
Similar content being viewed by others
Data accessibility
Supplementary information, scripts and data can be downloaded from GitHub at https://doi.org/10.5281/zenodo.3484105; RNA-seq reads can be accessed on the NCBI SRA repository (BioProject ID PRJNA576756, http://www.ncbi.nlm.nih.gov/bioproject/576756).
References
Andreadis TG (2007) Microsporidian parasites of mosquitoes. J Am Mosq Control Assoc 23:3–29. https://doi.org/10.2987/8756-971X(2007)23%5b3:MPOM%5d2.0.CO;2
Barlow ND, Beggs JR, Barron MC (2002) Dynamics of common wasps in New Zealand beech forests: a model with density dependence and weather. J Anim Ecol 71:663–671. https://doi.org/10.1046/j.1365-2656.2002.00630.x
Buchfink B, Xie C, Huson DH (2015) Fast and sensitive protein alignment using DIAMOND. Nat Methods 12:59–60. https://doi.org/10.1038/nmeth.3176
Chen Y, Pettis JS, Evans JD, Kramer M, Feldlaufer MF (2004) Transmission of Kashmir bee virus by the ectoparasitic mite Varroa destructor. Apidologie 35:441–448. https://doi.org/10.1051/apido:2004031
de Miranda JR, Bailey L, Ball BV, Blanchard P, Budge GE, Chejanovsky N, Chen Y-P, Gauthier L, Genersch E, de Graaf DC, Ribière M, Ryabov E, Smet LD, van der Steen JJM (2013) Standard methods for virus research in Apis mellifera. J Apic Res 52:1–56. https://doi.org/10.3896/IBRA.1.52.4.22
Dobelmann J, Loope KJ, Wilson-Rankin E, Quinn O, Baty JW, Gruber MAM, Lester PJ (2017) Fitness in invasive social wasps: the role of variation in viral load, immune response and paternity in predicting nest size and reproductive output. Oikos 126:1208–1218. https://doi.org/10.1111/oik.04117
Fan QH, Zhang ZQ, Brown R, France S, Bennett S (2016) New Zealand Pneumolaelaps (Acari: Laelapidae): description of a new species, key to species and notes on biology. Syst Appl Acarol 21:119–138. https://doi.org/10.11158/saa.21.1.8
Garigliany M, Agrebi NE, Franssen M, Hautier L, Saegerman C (2019) Moku virus detection in honey bees, Belgium, 2018. Transbound Emerg Dis 66:43–46. https://doi.org/10.1111/tbed.13055
Glare TR, Harris RJ, Donovan BJ (1996) Aspergillus flavus as a pathogen of wasps, Vespula spp., in New Zealand. N Z J Zool 23:339–344. https://doi.org/10.1080/03014223.1996.9518093
Grozinger CM, Flenniken ML (2019) Bee viruses: ecology, pathogenicity, and impacts. Annu Rev Entomol 64:205–226. https://doi.org/10.1146/annurev-ento-011118-111942
Gruber MAM, Cooling M, Baty JW, Buckley K, Friedlander A, Quinn O, Russell JFEJ, Sébastien A, Lester PJ (2017) Single-stranded RNA viruses infecting the invasive Argentine ant, Linepithema humile. Sci Rep 7:3304. https://doi.org/10.1038/s41598-017-03508-z
Gruber MAM, Quinn O, Baty JW, Dobelmann J, Haywood J, Wenseleers T, Lester PJ (2019) Fitness and microbial networks of the common wasp, Vespula vulgaris (Hymenoptera: Vespidae), in its native and introduced ranges. Ecol Entomol. https://doi.org/10.1111/een.12732
Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M, MacManes MD, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey CN, Henschel R, LeDuc RD, Friedman N, Regev A (2013) De novo transcript sequence reconstruction from RNA-Seq: reference generation and analysis with Trinity. Nat Protoc. https://doi.org/10.1038/nprot.2013.084
Harris RJ, Harcourt SJ, Glare TR, Rose EAF, Nelson TJ (2000) Susceptibility of Vespula vulgaris (Hymenoptera: Vespidae) to generalist entomopathogenic fungi and their potential for wasp control. J Invertebr Pathol 75:251–258. https://doi.org/10.1006/jipa.2000.4928
Hay DB, Hart BJ, Douglas AE (1993) Effects of the fungus Aspergillus penicillioides on the house dust mite Dermatophagoides pteronyssinus: an experimental re-evaluation. Med Vet Entomol 7:271–274
Hunter PE, Husband RW (1973) Pneumolaelaps (Acarina: Laelapidae) mites from North America and Greenland. Fla Entomol 56:77–91. https://doi.org/10.2307/3493231
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199
Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357–360. https://doi.org/10.1038/nmeth.3317
Lester PJ, Beggs JR (2019) Invasion success and management strategies for social Vespula Wasps. Annu Rev Entomol 64:51–71. https://doi.org/10.1146/annurev-ento-011118-111812
Lester PJ, Bosch PJ, Gruber MAM, Kapp EA, Peng L, Brenton-Rule EC, Buchanan J, Stanislawek WL, Archer M, Corley JC, Masciocchi M, Oystaeyen AV, Wenseleers T (2015) No evidence of enemy release in pathogen and microbial communities of common wasps (Vespula vulgaris) in their native and introduced range. PLoS One 10:e0121358. https://doi.org/10.1371/journal.pone.0121358
Lester PJ, Haywood J, Archer ME, Shortall CR (2017) The long-term population dynamics of common wasps in their native and invaded range. J Anim Ecol 86:337–347. https://doi.org/10.1111/1365-2656.12622
Levitt AL, Singh R, Cox-Foster DL, Rajotte E, Hoover K, Ostiguy N, Holmes EC (2013) Cross-species transmission of honey bee viruses in associated arthropods. Virus Res 176:232–240. https://doi.org/10.1016/j.virusres.2013.06.013
Loope KJ, Baty JW, Lester PJ, Wilson-Rankin EE (2019) Pathogen shifts in a honeybee predator following the arrival of the Varroa mite. Proc R Soc B Biol Sci 286:20182499. https://doi.org/10.1098/rspb.2018.2499
MacIntyre P, Hellstrom J (2015) An evaluation of the costs of pest wasps (Vespula species) in New Zealand. Int Pest Control 57:162–163
McMenamin AJ, Brutscher LM, Glenny W, Flenniken ML (2016) Abiotic and biotic factors affecting the replication and pathogenicity of bee viruses. Curr Opin Insect Sci 16:14–21. https://doi.org/10.1016/j.cois.2016.04.009
Mordecai GJ, Brettell LE, Pachori P, Villalobos EM, Martin SJ, Jones IM, Schroeder DC (2016) Moku virus; a new Iflavirus found in wasps, honey bees and Varroa. Sci Rep 6:34983. https://doi.org/10.1038/srep34983
Pertea M, Pertea GM, Antonescu CM, Chang T-C, Mendell JT, Salzberg SL (2015) StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 33:290–295. https://doi.org/10.1038/nbt.3122
Quinn O, Gruber MAM, Brown RL, Baty JW, Bulgarella M, Lester PJ (2018) A metatranscriptomic analysis of diseased social wasps (Vespula vulgaris) for pathogens, with an experimental infection of larvae and nests. PLoS One. https://doi.org/10.1371/journal.pone.0209589
Rigaud T, Perrot-Minnot M-J, Brown MJF (2010) Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence. Proc R Soc B Biol Sci 277:3693–3702. https://doi.org/10.1098/rspb.2010.1163
Roberts A, Pachter L (2012) Streaming fragment assignment for real-time analysis of sequencing experiments. Nat Methods 10:71. https://doi.org/10.1038/nmeth.2251
Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140. https://doi.org/10.1093/bioinformatics/btp616
Rose EAF, Harris RJ, Glare TR (1999) Possible pathogens of social wasps (Hymenoptera: Vespidae) and their potential as biological control agents. N Z J Zool 26:179–190. https://doi.org/10.1080/03014223.1999.9518188
Royce LA, Krantz GW (1989) Observations on pollen processing by Pneumolaelaps longanalis (Acari: Laelapidae), a mite associate of bumblebees. Exp Appl Acarol 7:161–165. https://doi.org/10.1007/BF01270436
Santamaria J, Villalobos EM, Brettell LE, Nikaido S, Graham JR, Martin S (2018) Evidence of Varroa-mediated Deformed wing virus spillover in Hawaii. J Invertebr Pathol 151:126–130. https://doi.org/10.1016/j.jip.2017.11.008
Schwarz RS, Huang Q, Evans JD (2015) Hologenome theory and the honey bee pathosphere. Curr Opin Insect Sci 10:1–7. https://doi.org/10.1016/j.cois.2015.04.006
Sébastien A, Lester PJ, Hall RJ, Wang J, Moore NE, Gruber MAM (2015) Invasive ants carry novel viruses in their new range and form reservoirs for a honeybee pathogen. Biol Let 11:20150610. https://doi.org/10.1098/rsbl.2015.0610
Solter LF, Becnel JJ, Oi DH (2012) Microsporidian entomopathogens. In: Vega FE, Kaya HK (eds) Insect pathology, chapter 7, 2nd edn. Academic Press, San Diego, pp 221–263. https://doi.org/10.1016/B978-0-12-384984-7.00007-5
Spradbery P (1974) wasps. an account of the biology and natural history of solitary and social wasps. Q Rev Biol 49:159. https://doi.org/10.1086/408041
St. Leger RJ, Screen SE, Shams-Pirzadeh B (2000) Lack of host specialization in Aspergillus flavus. Appl Environ Microbiol 66:320–324
Yue C, Genersch E (2005) RT-PCR analysis of Deformed wing virus in honeybees (Apis mellifera) and mites (Varroa destructor). J Gen Virol 86:3419–3424. https://doi.org/10.1099/vir.0.81401-0
Acknowledgements
This work was supported by Victoria University of Wellington, and the Ministry of Business, Innovation and Employment (New Zealand’s Biological Heritage NSC, C09X1501 & Victoria University of Wellington, Internal grant). We thank Emily Remnant for useful discussions on viral discovery in RNA-Seq data, as well as two anonymous reviewers for their comments on the manuscript. No potential conflict of interest was reported by the authors.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Felden, A., Baty, J.W., Bulgarella, M. et al. Viral and fungal pathogens associated with Pneumolaelaps niutirani (Acari: Laelapidae): a mite found in diseased nests of Vespula wasps. Insect. Soc. 67, 83–93 (2020). https://doi.org/10.1007/s00040-019-00730-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00040-019-00730-y