Skip to main content
    • Aa
    • Aa

Fitness effects and transmission routes of a microsporidian parasite infecting Drosophila and its parasitoids

  • P. H. FUTERMAN (a1), S. J. LAYEN (a1), M. L. KOTZEN (a1), C. FRANZEN (a2), A. R. KRAAIJEVELD (a1) and H. C. J. GODFRAY (a1)...

A microsporidian infection was discovered in laboratory cultures of Drosophila species. Ultrastructural examination suggested it belonged to the poorly characterized species Tubulinosema kingi, and morphological and sequence data are presented. We explored how T. kingi affected the fitness of Drosophila melanogaster and D. subobscura, as well as the fitness of 2 of their parasitoids, Asobara tabida and Pachycrepoideus vindemiae. In Drosophila, infections caused changes in most of the traits we looked at that were associated with fitness, in particular causing a 34–55% reduction in early-life fecundity. Parasitoid fitness was affected more severely by infection than that of their hosts, with pupal mortality in particular increasing by 75–89%. We investigated the most important routes of transmission for T. kingi in a laboratory setting. Letting Drosophila larvae feed on medium contaminated with spores from infected dead flies resulted in 100% infection. Low levels of transmission (<10%) were found between larvae, and vertically between mothers and their offspring. Parasitoids developing in infected hosts all became infected, but infected adults were neither able to transmit the pathogen to their offspring nor to their offspring's Drosophila host, either directly, or via contamination of the ovipositor or other body parts. A field survey of Drosophila and their parasitoids in southern England revealed no natural infections. We discuss the potential importance of Microsporidia in parasitoid-host interactions, and for those working with Drosophila in the laboratory.

Corresponding author
NERC Centre for Population Biology, Division of Biology, Imperial College London, Silwood Park Campus, Ascot, Berkshire SL5 7PY, UK. Tel: +44-(0)20 75942544. Fax: +44-(0)133 873173. E-mail:
Hide All
Agnew, P., Bedhomme, S., Haussy, C. and Michalakis, Y. ( 1999). Age and size at maturity of the mosquito Culex pipiens infected by the microsporidian parasite Vavraia culicis. Proceedings of the Royal Society of London, B266, 947952.

Van Alphen, J. J. M. and Thunnissen, I. ( 1983). Host selection and sex allocation by Pachycrepoideus vindemiae Rondani (Pteromalidae) as a facultative hyperparasitoid of Asobara tabida Nees (Braconidae; Alysiinae) and Leptopilina heterotoma (Thomson)(Cynipoidea; Eucoilidae). Netherlands Journal of Zoology33, 497514.

Armstrong, E. ( 1976). Transmission and infectivity studies on Nosema kingi in Drosophila willistoni and other Drosophilids. Zeitschrift für Parasitenkunde50, 161165.

Armstrong, E. ( 1977). Transmission of Nosema kingi to offspring of Drosophila willistoni during copulation. Zeitschrift für Parasitenkunde53, 311315.

Armstrong, E. and Bass, L. ( 1989a). Effects of Nosema kingi on the development and weight of adult Drosophila melanogaster (OR-R-Strain). Journal of Invertebrate Pathology53, 102106.

Armstrong, E. and Bass, L. ( 1989b). Nosema kingi: Effects on fecundity, fertility and longevity of Drosophila melanogaster. Journal of Experimental Zoology250, 8286.

Armstrong, E., Bass, L., Staker, K. and Harrell, L. ( 1986). A comparison of the biology of a Nosema in Drosophila melanogaster to Nosema kingi in Drosophila willistoni. Journal of Invertebrate Pathology48, 124126.

Baker, M. D., Vossbrinck, C. R., Maddox, J. V. and Undeen, A. H. ( 1994). Phylogenetic relationships among Vairimorpha and Nosema species (Microspora) based on ribosomal RNA sequence data. Journal of Invertebrate Pathology64, 100106.

Becnel, J. J. and Andreadis, T. G. ( 1999). Microsporidia in insects. In The Microsporidia and Microsporidiosis ( ed. Wittner, M. and Weiss, L. M.), pp. 447501. ASM Press, Washington DC.

Becnel, J. J., Garcia, J. J. and Johnson, M. A. ( 1995). Edhazardia aedis (Microspora: Culicosporidae) effects on the reproductive capacity of Aedes aegypti (Diptera: Culicidae). Journal of Medical Entomology32, 549553.

Belshaw, R., Fitton, M., Herniou, E., Gimeno, C. and Quicke, D. L. J. ( 1998). A phylogenetic reconstruction of the Ichneumonoidea (Hymenoptera) based on the D2 variable region of 28S ribosomal RNA. Systematic Entomology23, 109123.

Boheene, C. K., Geden, C. J. and Becnel, J. J. ( 2003). Development of microsporidia-infected Muscidifurax raptor (Hymenoptera: Pteromalidae) at different temperatures. Biological Control26, 17.

Canning, E. U., Refardt, D., Vossbrinck, C. R., Okamura, B. and Curry, A. ( 2002). New diplokaryotic microsporidia (Phylum Microsporidia) from freshwater bryozoans (Bryozoa, Phylactolaemata). European Journal of Protistology38, 247265.

Clark, M. E., Anderson, C., Cande, J. and Karr, T. ( 2005). Widespread prevalence of Wolbachia in laboratory stocks and implications for Drosophila research. Genetics170, 16671675.

Dunn, A. M., Terry, R. S. and Smith, J. E. ( 2001). Transovarial transmission in the microsporidia. Advances in Parasitology48, 57100.

Franzen, C. ( 2004). Microsporidia: how can they invade other cells? Trends in Parasitology20, 275279.

Franzen, C., Fischer, S., Schroeder, J., Schölmerich, J. and Schneuwly, S. ( 2005). Morphological and molecular investigations of Tubulinosema ratisbonensis gen. nov., sp. nov. (Microsporidia: Tubulinosematidae fam. nov.), a parasite infecting a laboratory colony of Drosophila melanogaster (Diptera: Drosophilidae). Journal of Eukaryotic Microbiology52, 141152.

Gatehouse, H. S. and Malone, L. A. ( 1998). The ribosomal RNA gene region of Nosema apis (Microspora): DNA sequence for small and large subunit rRNA genes and evidence for a tandem repeat unit size. Journal of Invertebrate Pathology71, 97105.

Geden, C. J., Ferreira De Almeida, M. A. and Pires do Prado, A. ( 2003). Effects of Nosema disease on fitness of the parasitoid Tachinaephagus zealandicus (Hymenoptera: Encyrtidae). Environmental Entomology32, 11391145.

Geden, C. J., Long, S. J., Rutz, D. A. and Becnel, J. J. ( 1995). Nosema disease of the parasitoid Muscidifurax raptor (Hymenoptera: Pteromalidae): prevalence, patterns of transmission, management, and impact. Biological Control5, 607614.

Hirt, R. P., LogsdonJr, J. M., Healy, B., Dorey, M. W., Doolittle, W. F. and Embley, T. M. ( 1999). Microsporidia are related to fungi: evidence from the largest subunit of RNA polymerase II and other proteins. Proceedings of the National Academy of Sciences, USA96, 580585.

Hoffmann, J. A. and Reichhart, J.-M. ( 2002). Drosophila innate immunity: an evolutionary perspective. Nature Immunology3, 121126.

Jaenike, J. ( 1995). Interactions between mycophagous Drosophila and their nematode parasites: from physiological to community ecology. Oikos72, 235244.

Kraaijeveld, A. R. and van Alphen, J. J. M. ( 1993). Successful invasion of North America by two Palearctic Drosophila species (Diptera: Drosophilidae): a matter of immunity to local parasitoids? Netherlands Journal of Zoology43, 235241.

Kraaijeveld, A. R., van Alphen, J. J. M. and Godfray, H. C. J. ( 1998). The coevolution of host resistance and parasitoid virulence. Parasitology116, S29S45.

Kraaijeveld, A. R. and Van Der Wel, N. N. ( 1994). Geographic variation in reproductive success of the parasitoid Asobara tabida in larvae of several Drosophila species. Ecological Entomology19, 221229.

Müller, A., Trammer, T., Chioralia, G., Seitz, H. M., Diehl, V. and Franzen, C. ( 2000). Ribosomal RNA of Nosema algerae and phylogenetic relationship to other microsporidia. Parasitology Research86, 1823.

Müller, C. B. and Brodeur, J. ( 2002). Intraguild predation in biological control and conservation biology. Biological Control25, 216223.

Nappi, A. J. ( 1981). Cellular immune response of Drosophila melanogaster against Asobara tabida. Parasitology83, 319324.

Pell, J. and Canning, E. ( 1993). Light microscope and ultrastructural observations of a microsporidian parasite of Mesocyclops rarus (Copepoda: Cyclopoda) in Tanzania. Journal of Invertebrate Pathology61, 275280.

Polis, G. A., Myers, C. A. and Holt, R. D. ( 1989). The ecology and evolution of intraguild predation: potential competitors that eat each other. Annual Review of Ecology and Systematics20, 297330.

Rosenheim, J. A., Kaya, H. K., Ehler, L. E., Marois, J. J. and Jaffee, B. A. ( 1995). Intraguild predation among biological-control agents: theory and evidence. Biological Control5, 303335.

Roxström-Lindquist, K., Terenius, O. and Faye, I. ( 2004). Parasite-specific immune response in adult Drosophila melanogaster: a genomic study. EMBO Reports5, 207212.

Schuld, M., Madel, G. and Schmuck, R. ( 1999). Impact of Vairimorpha sp. (Microsporidia: Burnellidae) on Trichogramma chilonis (Hymenoptera, Trichogrammatidae), a hymenopteran parasitoid of the cabbage moth, Plutella xylostella (Lepidoptera, Yponomeutidae). Journal of Invertebrate Pathology74, 120126.

Street, D. A. and Henry, J. E. ( 1993). Ultrastructural study of Nosema acridophagus Henry (Microspora: Nosematidae) from grasshopper. Parasitology Research79, 173177.

Terry, R. S., Smith, J. E., Sharpe, R. G., Rigaud, T., Littlewood, D. T. J., Ironside, J. E., Rollinson, D., Bouchin, D., Macneil, C., Dick, J. T. A. and Dunn, A. M. ( 2004). Widespread vertical transmission and associated host sex-ratio distortion within the eukaryotic phylum Microspora. Proceedings of the Royal Society of London, B271, 17831789.

Tzou, P., De Gregorio, E. and Lemaitre, B. ( 2002). How Drosophila combats microbial infection: a model to study innate immunity and host-pathogen interactions. Current Opinion in Microbiology5, 102110.

Vossbrinck, C. R., Baker, M. D., Didier, E. S., Debrunner-Vossbrinck, B. A. and Shadduck, J. A. ( 1993). Ribosomal DNA sequences of Encephalitozoon hellem and Encephalitozoon cuniculi: species identification and phylogenetic construction. Journal of Eukaryotic Microbiology40, 354362.

Williams, B. A. P., Hirt, R. P., Lucocq, J. M. and Embley, T. M. ( 2002). A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature, London418, 865869.

Wilson, G. G. ( 1974). Effects of larval age at innoculation, and dosage of microsporidian (Nosema fumiferanae) spores, on mortality of spruce budworm (Choristoneura fumiferana). Canadian Journal of Zoology52, 993996.

Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *


Type Description Title
Supplementary Materials

Futerman supplementary material
Supplementary figure S1

 PDF (454 KB)
454 KB


Altmetric attention score

Full text views

Total number of HTML views: 3
Total number of PDF views: 16 *
Loading metrics...

Abstract views

Total abstract views: 111 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 17th October 2017. This data will be updated every 24 hours.