Skip to main content
SpringerLink
Log in

Horizontal Transmission of Microbial Symbionts Within a Guild of Fly Parasitoids

  • Host Microbe Interactions
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Many insects harbor facultative microbial symbionts which affect the ecology of their hosts in diverse ways. Most symbionts are transmitted vertically with high fidelity, whereas horizontal transmission occurs rarely. Parasitoid larvae feed on a single host and are in close physical contact with it, providing an ecological opportunity for symbionts’ horizontal transmission, but there is little empirical evidence documenting this. Here we studied horizontal transmission of three bacterial symbionts—Rickettsia, Sodalis, and Wolbachia—between three fly pupal ectoparasitoid species: Spalangia cameroni, S. endius, and Muscidifurax raptor. Muscidifurax raptor readily parasitized and successfully developed on the Spalangia spp., while the inverse did not happen. The two Spalangia spp. attacked each other and conspecifics in very low rates. Symbiont horizontal transmissions followed by stable vertical transmission in the recipient species were achieved, in low percentages, only between conspecifics: Wolbachia from infected to uninfected M. raptor, Rickettsia in S. endius, and Sodalis in S. cameroni. Low frequency of horizontal transmissions occurred in the interspecific combinations, but none of them persisted in the recipient species beyond F4, at most. Our study is one of few to demonstrate symbionts’ horizontal transmission between hosts within the same trophic level and guild and highlights the rarity of such events.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data Availability

N/A

References

  1. Perlmutter JI, Bordenstein SR (2020) Microorganisms in the reproductive tissues of arthropods. Nat Rev Microbiol 18:97–111. https://doi.org/10.1038/s41579-019-0309-z

  2. Russell SL, Chappell L, Sullivan W (2019) A symbiont’s guide to the germline. Curr Top Dev Biol 135:315–351. https://doi.org/10.1016/BS.CTDB.2019.04.007

    Article  CAS  PubMed  Google Scholar 

  3. Dedeine F, Vavre F, Fleury F, Loppin B, Hochberg ME, Bouletreau M (2001) Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc Natl Acad Sci U S A 98:6247–6252. https://doi.org/10.1073/pnas.101304298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Oliver KM, Martinez AJ (2014) How resident microbes modulate ecologically-important traits of insects. Curr Opin Insect Sci 4:1–7. https://doi.org/10.1016/j.cois.2014.08.001

    Article  PubMed  Google Scholar 

  5. Russell SL (2019) Transmission mode is associated with environment type and taxa across bacteria-eukaryote symbioses: a systematic review and meta-analysis. FEMS Microbiol Lett:366. https://doi.org/10.1093/femsle/fnz013

  6. Bright M, Bulgheresi S (2010) A complex journey: transmission of microbial symbionts. Nat Rev Microbiol 8:218–230. https://doi.org/10.1038/nrmicro2262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Chrostek E, Pelz-Stelinski K, Hurst GDD, Hughes GL (2017) Horizontal transmission of intracellular insect symbionts via plants. Front Microbiol 8. https://doi.org/10.3389/fmicb.2017.02237

  8. Faria VG, Paulo TF, Sucena É (2016) Testing cannibalism as a mechanism for horizontal transmission of Wolbachia in Drosophila. Symbiosis 68:79–85. https://doi.org/10.1007/s13199-015-0354-y

    Article  CAS  Google Scholar 

  9. Su Q, Hu G, Yun Y, Peng Y (2019) Horizontal transmission of Wolbachia in Hylyphantes graminicola is more likely via intraspecies than interspecies transfer. Symbiosis 79:123–128. https://doi.org/10.1007/s13199-019-00623-5

    Article  Google Scholar 

  10. Vavre F, Fleury F, Lepetit D, Fouillet P, Bouletreau M (1999) Phylogenetic evidence for horizontal transmission of Wolbachia in host-parasitoid associations. Mol Biol Evol 16:1711–1723. https://doi.org/10.1093/oxfordjournals.molbev.a026084

  11. Cordaux R, Michel-Salzat A, Bouchon D (2001) Wolbachia infection in crustaceans: novel hosts and potential routes for horizontal transmission. J Evol Biol 14:237–243. https://doi.org/10.1046/j.1420-9101.2001.00279.x

    Article  CAS  Google Scholar 

  12. Qi L-D, Sun J-T, Hong X-Y, Li Y-X (2019) Diversity and phylogenetic analyses reveal horizontal transmission of endosymbionts between whiteflies and their parasitoids. J Econ Entomol 112:894–905. https://doi.org/10.1093/jee/toy367

    Article  PubMed  Google Scholar 

  13. Werren J, Skinner S, Huger A (1986) Male-killing bacteria in a parasitic wasp. Science 231:990–992. https://doi.org/10.1126/science.3945814

  14. Huigens ME, Luck RF, Klaassen RHG, Maas MFPM, Timmermans MJTN, Stouthamer R (2000) Infectious parthenogenesis. Nature 405:178–179. https://doi.org/10.1038/35012066

    Article  CAS  PubMed  Google Scholar 

  15. Parratt SR, Frost CL, Schenkel MA, Rice A, Hurst GDD, King KC (2016) Superparasitism drives heritable symbiont epidemiology and host sex ratio in a wasp. PLoS Pathog 12:e1005629. https://doi.org/10.1371/journal.ppat.1005629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Huigens ME, de Almeida RP, Boons PAH, Luck RF, Stouthamer R (2004) Natural interspecific and intraspecific horizontal transfer of parthenogenesis-inducing Wolbachia in Trichogramma wasps. Proc R Soc B-Biological Sci 271:509–515

    Article  CAS  Google Scholar 

  17. Chiel E, Zchori-Fein E, Inbar M, Gottlieb Y, Adachi-Hagimori T, Kelly SE, Asplen MK, Hunter MS (2009) Almost there: transmission routes of bacterial symbionts between trophic levels. PLoS One 4:e4767 https://doi.org/10.1371/journal.pone.0004767

  18. Duron O, Wilkes TE, Hurst GDD (2010) Interspecific transmission of a male-killing bacterium on an ecological timescale. Ecol Lett 13:1139–1148. https://doi.org/10.1111/j.1461-0248.2010.01502.x

    Article  PubMed  Google Scholar 

  19. Heath BD, Butcher RDJ, Whitfield WGF, Hubbard SF (1999) Horizontal transfer of Wolbachia between phylogenetically distant insect species by a naturally occurring mechanism. Curr Biol 9:313–316. https://doi.org/10.1038/ismej.2016.164

  20. Ahmed MZ, Li SJ, Xue X, Yin XJ, Ren SX, Jiggins FM, Greeff JM, Qiu BL (2015) The intracellular bacterium Wolbachia uses parasitoid wasps as phoretic vectors for efficient horizontal transmission. PLoS Pathog 11:e1004672. https://doi.org/10.1371/journal.ppat.1004672

    Article  CAS  PubMed Central  Google Scholar 

  21. Gehrer L, Vorburger C (2012) Parasitoids as vectors of facultative bacterial endosymbionts in aphids. Biol Lett 8:613–615. https://doi.org/10.1098/rsbl.2012.0144

    Article  PubMed  PubMed Central  Google Scholar 

  22. Jaenike J, Polak M, Fiskin A, Helou M, Minhas M (2007) Interspecific transmission of endosymbiotic Spiroplasma by mites. Biol Lett 3:23–25. https://doi.org/10.1098/rsbl.2006.0577

    Article  CAS  PubMed  Google Scholar 

  23. Chiel E, Kuslitzky W (2016) Diversity and abundance of house fly pupal parasitoids in Israel, with first records of two Spalangia species. Environ Entomol 45:283–291. https://doi.org/10.1093/ee/nvv180

    Article  PubMed  Google Scholar 

  24. Wylie HG, Bouletreau M, David J et al (1971) Observations on intraspecific larval competition in three hymenopterous parasites of fly puparia. Can Entomol 103:137–142. https://doi.org/10.4039/Ent103137-1

    Article  Google Scholar 

  25. Wylie HG (1972) Larval competition among three hymenopterous parasite species on multiparasitized housefly (Diptera) pupae. Can Entomol 104:1181–1190. https://doi.org/10.4039/Ent1041181-8

    Article  Google Scholar 

  26. Propp GD, Morgan PB (1983) Multiparasitism of house fly, Musca domestica L., pupae by Spalangia endius Walker and Muscidifurax raptor Girault and Sanders (Hymenoptera: Pteromalidae). Environ Entomol 12:1232–1238. https://doi.org/10.1093/ee/12.4.1232

    Article  Google Scholar 

  27. Betelman K, Caspi-Fluger A, Shamir M, Chiel E (2017) Identification and characterization of bacterial symbionts in three species of filth fly parasitoids. FEMS Microbiol Ecol 93. https://doi.org/10.1093/femsec/fix107

  28. Kyei-Poku GK, Giladi M, Coghlin P, Mokady O, Zchori-Fein E, Floate KD (2006) Wolbachia in wasps parasitic on filth flies with emphasis on Spalangia cameroni. Entomol Exp Appl 121:123–135

    Article  Google Scholar 

  29. Brown LD, Macaluso KR (2016) Rickettsia felis, an emerging flea-borne rickettsiosis. Curr Trop Med reports 3:27–39. https://doi.org/10.1007/s40475-016-0070-6

    Article  Google Scholar 

  30. Semiatizki A, Weiss B, Bagim S, Rohkin-Shalom S, Kaltenpoth M, Chiel E (2020) Effects, interactions, and localization of Rickettsia and Wolbachia in the house fly parasitoid, Spalangia endius. Microb Ecol 80:1–11. https://doi.org/10.1007/s00248-020-01520-x

    Article  Google Scholar 

  31. Gibson GA (2000) Illustrated key to the native and introduced chalcidoid parasitoids of filth flies in America north of Mexico (Hymenoptera: Chalcidoidea). https://doi.org/10.13140/RG.2.2.19059.32809

  32. Gibson GA (2009) Revision of new world spalangiinae (Hymenoptera: Pteromalidae). Zootaxa 2259:1–159. https://doi.org/10.11646/zootaxa.2259.1.1

  33. Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–190. https://doi.org/10.1146/annurev.genet.41.110306.130119

  34. Schuler H, Bertheau C, Egan SP, Feder JL, Riegler M, Schlick-Steiner BC, Steiner FM, Johannesen J, Kern P, Tuba K, Lakatos F, Köppler K, Arthofer W, Stauffer C (2013) Evidence for a recent horizontal transmission and spatial spread of Wolbachia from endemic Rhagoletis cerasi (Diptera: Tephritidae) to invasive Rhagoletis cingulata in Europe. Mol Ecol 22:4101–4111. https://doi.org/10.1111/mec.12362

    Article  CAS  PubMed  Google Scholar 

  35. Shaikevich E, Bogacheva A, Rakova V, Ganushkina L, Ilinsky Y (2019) Wolbachia symbionts in mosquitoes: intra- and intersupergroup recombinations, horizontal transmission and evolution. Mol Phylogenet Evol 134:24–34. https://doi.org/10.1016/j.ympev.2019.01.020

    Article  PubMed  Google Scholar 

  36. Tolley SJA, Nonacs P, Sapountzis P (2019) Wolbachia horizontal transmission events in ants: what do we know and what can we learn? Front Microbiol 10. https://doi.org/10.3389/fmicb.2019.00296

  37. Ahmed MZ, Breinholt JW, Kawahara AY (2016) Evidence for common horizontal transmission of Wolbachia among butterflies and moths. BMC Evol Biol 16:118. https://doi.org/10.1186/s12862-016-0660-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Bailly-Bechet M, Martins-Simões P, Szöllosi GJ et al (2017) How long does wolbachia remain on board? Mol Biol Evol 34:1183–1193. https://doi.org/10.1093/molbev/msx073

    Article  CAS  PubMed  Google Scholar 

  39. Braig HR, Guzman H, Tesh RB, O’Neill SL (1994) Replacement of the natural Wolbachia symbiont of Drosophila simulans with a mosquito counterpart. Nature 367:453–455. https://doi.org/10.1038/367453a0

    Article  CAS  PubMed  Google Scholar 

  40. Fujii Y, Kageyama D, Hoshizaki S, Ishikawa H, Sasaki T (2001) Transfection of Wolbachia in Lepidoptera: the feminizer of the adzuki bean borer Ostrinia scapulalis causes male killing in the Mediterranean flour moth Ephestia kuehniella. Proc R Soc B-Biological Sci 268:855–859. https://doi.org/10.1098/rspb.2001.1593

  41. Grenier S, Bernard P, Heddi A, Lassabliére F, Jager C, Louis C, Khatchadourian C (1998) Successful horizontal transfer of Wolbachia symbionts between Trichogramma wasps. Proc R Soc Lond Ser B Biol Sci 265:1441–1445. https://doi.org/10.1098/rspb.1998.0455

    Article  Google Scholar 

  42. Xi Z, Khoo CCH, Dobson SL (2006) Interspecific transfer of Wolbachia into the mosquito disease vector Aedes albopictus. Proc R Soc B Biol Sci 273:1317–1322. https://doi.org/10.1098/rspb.2005.3405

    Article  Google Scholar 

  43. McCutcheon JP, Boyd BM, Dale C (2019) The life of an insect endosymbiont from the cradle to the grave. Curr Biol 29:R485–R495. https://doi.org/10.1016/j.cub.2019.03.032

  44. Taylor GP, Coghlin PC, Floate KD, Perlman SJ (2011) The host range of the male-killing symbiont Arsenophonus nasoniae in filth fly parasitioids. J Invertebr Pathol 106:371–379. https://doi.org/10.1016/j.jip.2010.12.004

    Article  PubMed  Google Scholar 

  45. Nadal-Jimenez P, Griffin JS, Davies L, Frost CL, Marcello M, Hurst GDD (2019) Genetic manipulation allows in vivo tracking of the life cycle of the son-killer symbiont, Arsenophonus nasoniae , and reveals patterns of host invasion, tropism and pathology. Environ Microbiol 21:3172–3182. https://doi.org/10.1111/1462-2920.14724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. de Jonge N, Michaelsen TY, Ejbye-Ernst R et al (2020) Housefly (Musca domestica L.) associated microbiota across different life stages. Sci Rep 10. https://doi.org/10.1038/s41598-020-64704-y

  47. Junqueira ACM, Ratan A, Acerbi E, Drautz-Moses DI, Premkrishnan BNV, Costea PI, Linz B, Purbojati RW, Paulo DF, Gaultier NE, Subramanian P, Hasan NA, Colwell RR, Bork P, Azeredo-Espin AML, Bryant DA, Schuster SC (2017) The microbiomes of blowflies and houseflies as bacterial transmission reservoirs. Sci Rep 7:1–15. https://doi.org/10.1038/s41598-017-16353-x

    Article  CAS  Google Scholar 

  48. Zhang B, McGraw E, Floate KD, James P, Jorgensen W, Rothwell J (2009) Wolbachia infection in Australasian and North American populations of Haematobia irritans (Diptera: Muscidae). Vet Parasitol 162:350–353. https://doi.org/10.1016/j.vetpar.2009.03.012

    Article  PubMed  Google Scholar 

  49. Mingchay P, Sai-Ngam A, Phumee A, Bhakdeenuan P, Lorlertthum K, Thavara U, Tawatsin A, Choochote W, Siriyasatien P (2014) Wolbachia supergroups a and B in natural populations of medically important filth flies (Diptera: Muscidae, Calliphoridae, and Sarcophagidae) in Thailand. Southeast Asian J Trop Med Public Health 45:309–318. PMID: 24968670.

  50. Böckmann EA, Tormos J, Beitia F, Fischer K (2012) Offspring production and self-superparasitism in the solitary ectoparasitoid Spalangia cameroni (Hymenoptera: Pteromalidae) in relation to host abundance. Bull Entomol Res 102:131–137. https://doi.org/10.1017/S0007485311000447

    Article  PubMed  Google Scholar 

  51. Bautista CR, Rodríguez T, Rojas C et al (2018) Molecular detection of Anaplasma marginale in stable flies Stomoxys calcitrans (Diptera: Muscidae) feeding on a tick-free bovine herd. Vet Mex 5:1–7. https://doi.org/10.21753/vmoa.5.1.436

    Article  Google Scholar 

  52. Baldacchino F, Muenworn V, Desquesnes M, Desoli F, Charoenviriyaphap T, Duvallet G (2013) Transmission of pathogens by Stomoxys flies (Diptera, Muscidae): a review. Parasite 20:26. https://doi.org/10.1051/PARASITE/2013026

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank Maya Lapid for the professional processing and arrangement of the figures.

Funding

The study was supported by the Israel Science Foundation, grant # 435/18 to Elad Chiel.

Author information

Author notes

  1. Noam Tzuri, Ayelet Caspi-Fluger and Kfir Betelman contributed equally to this work.

Authors and Affiliations

  1. Department of Biology and Environment, University of Haifa-Oranim, 3600600, Tivon, Israel

    Noam Tzuri, Ayelet Caspi-Fluger, Kfir Betelman, Sarit Rohkin Shalom & Elad Chiel

Authors
  1. Noam Tzuri
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ayelet Caspi-Fluger
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kfir Betelman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sarit Rohkin Shalom
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Elad Chiel
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the experiments design; NT, ACF, KB, and SRS collected the data; NT, KF, and EC analyzed the data; EC led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.

Corresponding author

Correspondence to Elad Chiel.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interests.

Ethics Approval

N/A

Consent to Participate

N/A

Consent for Publication

N/A (?)

Code Availability

N/A

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tzuri, N., Caspi-Fluger, A., Betelman, K. et al. Horizontal Transmission of Microbial Symbionts Within a Guild of Fly Parasitoids. Microb Ecol 81, 818–827 (2021). https://doi.org/10.1007/s00248-020-01618-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-020-01618-2

Keywords

Search

Navigation