Skip to main content Accessibility help

The expression of virulence for a mixed-mode transmitted parasite in a diapausing host


Many parasites survive harsh periods together with their hosts. Without the possibility of horizontal transmission during host diapause, parasite persistence depends entirely on host survival. We therefore hypothesize that a parasite should be avirulent during its host's diapausing stage. In contrast, the parasite may express higher virulence, i.e. parasite-induced fitness reduction of the host, during host life stages with good opportunities for horizontal transmission. Here we study the effects of a vertically and horizontally transmitted microsporidium parasite, Hamiltosporidium tvaerminnensis, on the quantity and survival of resting eggs of its host Daphnia magna. We find that the parasite did not affect egg volume, hatching success and time to hatching of the Daphnia's resting eggs, although it did strongly reduce the number of resting eggs produced by infected females, revealing high virulence during the non-diapause phase of the host's life cycle. These results also explain another aspect of this system – namely the strong decline in natural population prevalence across diapause. This decline is not caused by mortality in infected resting stages, as was previously hypothesized, but because infected female hosts produce lower rates of resting eggs. Together, these results help explain the epidemiological dynamics of a microsporidian disease and highlight the adaptive nature of life stage-dependent parasite virulence.

Corresponding author
* Corresponding author: University of Basel, Zoological Institute, Vesalgasse 1, 4051 Basel, Switzerland. E-mail:
Hide All
Agnew, P. and Koella, J. C. (1999). Constraints on the reproductive value of vertical transmission for a microsporidian parasite and its female-killing behaviour. Journal of Animal Ecology 68, 10101019.
Alizon, S., Hurford, A., Mideo, N. and Van Baalen, M. (2009). Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. Journal of Evolutionary Biology 22, 245259. doi: 10.1111/j.1420-9101.2008.01658.x.
Altermatt, F. and Ebert, D. (2010). Populations in small, ephemeral habitat patches may drive dynamics in a Daphnia magna metapopulation. Ecology 91, 29752982.
Anderson, R. M. and May, R. M. (1982). Coevolution of hosts and parasites. Parasitology 85, 411426.
Andreadis, T. G. (1983). Life-cycle and epizootiology of Amblyospora sp. (Microspora, Amblyosporidae) in the mosquito, Aedes cantator . Journal of Protozoology 30, 509518. doi: 10.1111/J.1550-7408.1983.Tb01412.X.
Andreadis, T. G. (2005). Evolutionary strategies and adaptations for survival between mosquito-parasitic microsporidia and their intermediate copepod hosts: a comparative examination of Amblyospora connectius and Hyalinocysta chapmani (Microsporidia: Amblyosporidae). Folia Parasitologica 52, 2335.
Andreadis, T. G. and Hall, D. W. (1979). Development, ultrastructure, and mode of transmission of Amblyospora sp. (Microspora) in the mosquito. Journal of Protozoology 26, 444452. doi: 10.1111/J.1550-7408.1979.Tb04651.X.
Arbaciauskas, K. (2004). Seasonal phenotypes of Daphnia: post-diapause and directly developing offspring. Journal of Limnology 63, 715.
Bates, D., Maechler, M. and Dai, B. (2008). lme4: linear mixed-effects models using S4 classes. R package version 0.999375-28.
Bauer, L. S. and Nordin, G. L. (1989 a). Effect of Nosema fumiferanae (Microsporida) on fecundity, fertility, and progeny performance of Choristoneura fumiferana (Lepidoptera, Tortricidae). Environmental Entomology 18, 261265.
Bauer, L. S. and Nordin, G. L. (1989 b). Response of spruce budworm (Lepidoptera, Tortricidae) infected with Nosema fumiferanae (Microsporida) to Bacillus thuringiensis treatments. Environmental Entomology 18, 816821.
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 Entomology 32, 549553.
Bedhomme, S., Agnew, P., Vital, Y., Sidobre, C. and Michalakis, Y. (2005). Prevalence-dependent costs of parasite virulence. PloS Biology 3, 14031408. Art. e262. doi: 10.1371/journal.pbio.0030262.
Ben-Ami, F., Rigaud, T. and Ebert, D. (2011). The expression of virulence during double infections by different parasites with conflicting host exploitation and transmission strategies. Journal of Evolutionary Biology 24, 13071316. doi: 10.1111/j.1420-9101.2011.02264.x.
Bieger, A. and Ebert, D. (2009). Expression of parasite virulence at different host population densities under natural conditions. Oecologia (Berlin) 160, 247255.
Boersma, M., Boriss, H. and Mitchell, S. E. (2000). Maternal effects after sexual reproduction in Daphnia magna . Journal of Plankton Research 22, 279285. doi: 10.1093/Plankt/22.2.279.
Brown, M. J. F., Schmid-Hempel, R. and Schmid-Hempel, P. (2003). Strong context-dependent virulence in a host-parasite system: reconciling genetic evidence with theory. Journal of Animal Ecology 72, 9941002.
Bull, J. J. (1994). Perspective – Virulence. Evolution 48, 14231437.
Bull, J. J., Molineux, I. J. and Rice, W. R. (1991). Selection of benevolence in a host-parasite system. Evolution 45, 875882.
Caceres, C. E., Hartway, C. and Paczolt, K. A. (2009). Inbreeding depression varies with investment in sex in a facultative parthenogen. Evolution 63, 24742480. doi: 10.1111/J.1558-5646.2009.00707.X.
Dawkins, R. (1982). The Extended Phenotype: The Gene as the Unit of Selection. WH Freeman, Oxford, UK.
De Meester, L. (1993). Inbreeding and outbreeding depression in Daphnia . Oecologia (Berlin) 96, 8084.
De Meester, L., Cousyn, C. and Vanoverbeke, J. (1998). Chemical interactions, maternal effects and the hatching of Daphnia diapausing eggs. Archiv für Hydrobiologie Special Issue Advances in Limnology, 52, 263272.
Dunn, A. M. and Smith, J. E. (2001). Microsporidian life cycles and diversity: the relationship between virulence and transmission. Microbes and Infection 3, 381388.
Ebert, D. (2013). The epidemiology and evolution of symbionts with mixed-mode transmission. Annual Review of Ecology, Evolution, and Systematics 44, 623643.
Ebert, D., Zschokke-Rohringer, C. D. and Carius, H. J. (1998). Within- and between-population variation for resistance of Daphnia magna to the bacterial endoparasite Pasteuria ramosa . Proceedings of the Royal Society B: Biological Sciences 265, 21272134.
Ebert, D., Hottinger, J. W. and Pajunen, V. I. (2001). Temporal and spatial dynamics of parasites in a Daphnia metapopulation: which factors explain parasite richness? Ecology 82, 34173434.
Ebert, D., Altermatt, F. and Lass, S. (2007). A short term benefit for outcrossing in a Daphnia metapopulation in relation to parasitism. Journal of the Royal Society Interface 4, 777785.
Evseeva, N. V. (1996). Diapause of copepods as an element for stabilizing the parasite system of some fish helminths. Hydrobiologia 320, 229233. doi: 10.1007/Bf00016824.
Fine, P. E. M. (1975). Vectors and vertical transmission: an epidemiologic perspective. Annals of the New York Academy of Sciences 266, 173194.
Futerman, P. H., Layen, S. J., Kotzen, M. L., Franzen, C., Kraaijeveld, A. R. and Godfray, H. C. J. (2006). Fitness effects and transmission routes of a microsporidian parasite infecting Drosophila and its parasitoids. Parasitology 132, 479492.
Gill, D. E. and Mock, B. A. (1985). Ecological and evolutionary dynamics of parasites: The case of Trypanosoma diemyctyli in the red-spotted newt Notophthalmus viridescens . In Ecology and Genetics of Host-Parasite Interactions (ed. Rollinson, D. and Anderson, R. M.), pp. 157183. Academic Press, London, UK.
Haag, K. L., Larsson, J. I. R., Refardt, D. and Ebert, D. (2011). Cytological and molecular description of Hamiltosporidium tvaerminnensis gen. et sp nov., a microsporidian parasite of Daphnia magna, and establishment of Hamiltosporidium magnivora comb. nov. Parasitology 138, 447462. doi: 10.1017/s0031182010001393.
Haag, K. L., Sheikh-Jabbari, E., Ben-Ami, F. and Ebert, D. (2013 a). Microsatellite and single-nucleotide polymorphisms indicate recurrent transitions to asexuality in a microsporidian parasite. Journal of Evolutionary Biology 26, 11171128. doi: 10.1111/Jeb.12125.
Haag, K. L., Traunecker, E. and Ebert, D. (2013 b). Single-nucleotide polymorphisms of two closely related microsporidian parasites suggest a clonal population expansion after the last glaciation. Molecular Ecology 22, 314326. doi: 10.1111/mec.12126.
Kaltz, O. and Koella, J. C. (2003). Host growth conditions regulate the plasticity of horizontal and vertical transmission in Holospora undulata, a bacterial parasite of the protozoan Paramecium caudatum . Evolution 57, 15351542.
Lass, S. and Ebert, D. (2006). Apparent seasonality of parasite dynamics: analysis of cyclic prevalence patterns. Proceedings of the Royal Society B: Biological Sciences 273, 199206.
Lass, S., Hottinger, J. W., Fabbro, T. and Ebert, D. (2011). Converging seasonal prevalence dynamics in experimental epidemics. BMC Ecology 11, 14. doi: 10.1186/1472-6785-11-14.
Lenski, R. E. and May, R. M. (1994). The evolution of virulence in parasites and pathogens: reconciliation between two competing hypotheses. Journal of Theoretical Biology 169, 253265.
Lipsitch, M., Nowak, M. A., Ebert, D. and May, R. M. (1995). The population dynamics of vertically and horizontally transmitted parasites. Proceedings of the Royal Society, London, Series B 260, 321327.
Lipsitch, M., Siller, S. and Nowak, M. A. (1996). The evolution of virulence in pathogens with vertical and horizontal transmission. Evolution 50, 17291741.
Liu, W. and Niu, C. J. (2010). Polymorphism in resting egg size and hatching strategy in the Rotifer Brachionus calyciflorus pallas . Zoological Science 27, 330337. doi: 10.2108/Zsj.27.330.
Magalon, H., Nidelet, T., Martin, G. and Kaltz, O. (2010). Host growth conditions influence experimental evolution of life history and virulence of a parasite with vertical and horizontal transmission. Evolution 64, 21262138.
Mink, G. I. (1993). Pollen-transmitted and seed-transmitted viruses and viroids. Annual Review of Phytopathology 31, 375402.
Pajunen, V. I. and Pajunen, I. (2007). Habitat characteristics contributing to local occupancy and habitat use in rock pool Daphnia metapopulations. Hydrobiologia 592, 291302.
Pfrender, M. E. and Deng, H. W. (1998). Environmental and genetic control of diapause termination in Daphnia . Advances in Limnology 52, 237251.
Quinn, G. P. and Keogh, M. J. (2002). Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge, UK.
Raina, S. K., Das, S., Rai, M. M. and Khurad, A. M. (1995). Transovarial transmission of Nosema locustae (Microsporida, Nosematidae) in the migratory locust Locusta migratoria migratorioides . Parasitology Research 81, 3844.
Regniere, J. (1984). Vertical transmisison of diseases and population dynamics of insects with discrete generations – a model. Journal of Theoretical Biology 107, 287301.
Rutrecht, S. T. and Brown, M. J. F. (2008). Within colony dynamics of Nosema bombi infections: disease establishment, epidemiology and potential vertical transmission. Apidologie 39, 504514.
Sorrell, I., White, A., Pedersen, A. B., Hails, R. S. and Boots, M. (2009). The evolution of covert, silent infection as a parasite strategy. Proceedings of the Royal Society B: Biological Sciences 276, 22172226.
Stewart, F. M. and Levin, B. R. (1984). The population biology of bacterial viruses: why be temperate? Theoretical Population Biology 26, 93117.
Thomson, H. M. (1958). Some aspects of the epidemiology of a microsporidian parasite of the spruce budworm, Choristoneura fumiferana (Clem.). Canadian Journal of Zoology 36, 309316.
Tinsley, R. C. (1995). Parasitic disease in amphibians: control by the regulation of worm burdens. Parasitology 111, S153S178.
Vizoso, D. B. and Ebert, D. (2004). Within-host dynamics of a microsporidium with horizontal and vertical transmission: Octosporea bayeri in Daphnia magna . Parasitology 128, 3138.
Vizoso, D. B. and Ebert, D. (2005). Phenotypic plasticity of host-parasite interactions in response to the route of infection. Journal of Evolutionary Biology 18, 911921.
Vizoso, D. B., Lass, S. and Ebert, D. (2005). Different mechanisms of transmission of the microsporidium Octosporea bayeri: a cocktail of solutions for the problem of parasite permanence. Parasitology 130, 501509.
Zbinden, M., Lass, S., Refardt, D., Hottinger, J. and Ebert, D. (2005). Octosporea bayeri: Fumidil B inhibits vertical transmission in Daphnia magna . Experimental Parasitology 109, 5861.
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

Sheikh-Jabbari Supplementary Material
Table S1

 Word (21 KB)
21 KB


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed