Hostname: page-component-848d4c4894-pjpqr Total loading time: 0 Render date: 2024-06-18T21:06:40.847Z Has data issue: false hasContentIssue false
  • English
  • Français

Ecological and genetic determinants of multiple infection and aggregation in a microbial host-parasite system

Published online by Cambridge University Press:  08 September 2008

D. FELS ,
M. VIGNON  and
O. KALTZ
D. FELS
Affiliation:
UPMC Univ Paris 06, Laboratoire de Parasitologie Evolutive – UMR 7103, 7 quai St-Bernard, 75252 Paris, France
M. VIGNON
Affiliation:
UPMC Univ Paris 06, Laboratoire de Parasitologie Evolutive – UMR 7103, 7 quai St-Bernard, 75252 Paris, France
O. KALTZ*
Affiliation:
UPMC Univ Paris 06, Laboratoire de Parasitologie Evolutive – UMR 7103, 7 quai St-Bernard, 75252 Paris, France
*
*Corresponding author. Tel: +33 (0)1 44 27 38 23. Fax: +33 (0)1 44 27 35 16. E-mail: oliver.kaltz@gmail.com
Get access Rights & Permissions [Opens in a new window]

Summary

The number of parasites colonizing a host (termed ‘multiple infection’) is an important determinant of host-parasite interactions. In theory, multiple infection is determined by random mass action in genetically and spatially homogeneous populations of host and parasite. In real populations, deviations from these assumptions may strongly influence levels of multiple infection. We carried out inoculation experiments in microcosms of the freshwater protozoan Paramecium caudatum and its bacterial parasite Holospora undulata. Increasing parasite dose produced higher levels of (multiple) infection; more susceptible host genotypes also were more multiply infected. An overall pattern of parasite aggregation (excess of uninfected individuals and of individuals carrying larger numbers of parasites) indicated deviations from random mass-action transmission. Homogenizing spatial distributions of parasite and host in our microcosms did not affect aggregation, whereas aggregation was more pronounced in old than in new host clones. Thus, variation in susceptibility may arise over time within clonal populations. When sequentially inoculated, already established infections increased the probability of additional infection in generally resistant host clones, but decreased it in more susceptible clones. Hence, the role of multiple infection as a driver of epidemiological or evolutionary processes may vary among populations, depending on their precise genetic composition or infection history.

Keywords

multiple infectionaggregationexperimental epidemiologyHolospora undulatainduced resistancemass actionParamecium caudatumspatial distribution
Type
Original Articles
Information
Parasitology , Volume 135 , Issue 12 , October 2008 , pp. 1373 - 1383
Copyright
Copyright © 2008 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Amann, R., Springer, N., Ludwig, W., Görtz, H.-D. and Schlaifer, K.-H. (1991). Identification in situ and phylogeny of uncultured bacterial endosymbionts. Nature, London 351, 161–164.Google Scholar
Anderson, R. and May, R. (1978). Regulation and stability of host-parasite population interactions. I. Regulatory processes. Jounal of Animal Ecology 47, 219–247.Google Scholar
Anderson, R. M. and May, R. M. (1979). Population biology of infectious diseases: Part 1. Nature, London 280, 361–367.Google Scholar
Bell, A. S., de Roode, J. C., Sim, D. and Read, A. F. (2006). Within-host competition in genetically diverse malaria infections: parasite virulence and competitive success. Evolution 60, 1358–1371.Google Scholar
Ben-Ami, F., Mouton, L. and Ebert, D. (2008 a). The effects of multiple infections on the expression and evolution of virulence in a daphnia-endoparasite system. Evolution 62, 1700–1711.CrossRefGoogle Scholar
Ben-Ami, F., Regoes, R. R. and Ebert, D. (2008 b). A quantitative test of the relationship between parasite dose and infection probability across different host-parasite combinations. Proceedings of the Royal Society of London, B 275, 853–859.Google Scholar
Boag, B., Lello, J., Fenton, A., Tompkins, D. M. and Hudson, P. J. (2001). Patterns of parasite aggregation in the wild European rabbit (Oryctolagus cuniculus). International Journal for Parasitology 31, 1421–1428.CrossRefGoogle ScholarPubMed
Boete, C., Paul, R. E. and Koella, J. C. (2004). Direct and indirect immunosuppression by a malaria parasite in its mosquito vector. Proceedings of the Royal Society of London, B 271, 1611–1615.Google Scholar
Brown, M., 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, 994–1002.CrossRefGoogle Scholar
Brown, S. P., Hochberg, M. E. and Grenfell, B. T. (2002). Does multiple infection select for raised virulence? Trends in Microbiology 10, 401–405.Google Scholar
Cox, F. E. (2001). Concomitant infections, parasites and immune responses. Parasitology 122 (Suppl.) S23–S38.Google Scholar
Dohra, H. and Fujishima, M. (1999). Effects of antibiotics on the early infection process of a macronuclear endosymbiotic bacterium Holospora obtusa of Paramecium caudatum. FEMS Microbiology Letters 179, 473–477.Google Scholar
Ebert, D., Zschokke-Rohringer, C. D. and Carius, H. J. (2000). Dose effects and density dependent regulation of two microparasites of Daphnia magna. Oecologia 122, 200–209.Google Scholar
Elston, D. A., Moss, R., Boulinier, T., Arrowsmith, C. and Lambin, X. (2001). Analysis of aggregation, a worked example: numbers of ticks on red grouse chicks. Parasitology 122, 563–569.CrossRefGoogle ScholarPubMed
Engelberth, J., Alborn, H. T., Schmelz, E. A. and Tumlinson, J. H. (2004). Airborne signals prime plants against insect herbivore attack. Proceedings of the National Academy of Sciences, USA 101, 1781–1785.Google Scholar
Fels, D. and Kaltz, O. (2006). Temperature-dependent transmission and latency of Holospora undulata, a micronucleus-specific parasite of the ciliate Paramecium caudatum. Proceedings of the Royal Society of London, B 273, 1031–1038.Google Scholar
Fokin, S. I. (2004). Bacterial endocytobionts of ciliophora and their interactions with the host cell. International Review of Cytology 236, 181–249.CrossRefGoogle ScholarPubMed
Fokin, S. I. and Skovorodkin, I. N. (1997). Experimental analysis of the resistance of Paramecium caudatum (Ciliophora) against infection by bacterium Holospora undulata. European Journal of Protistology 33, 214–218.Google Scholar
Frank, S. A. (2002). Immunology and Evolution of Infectious Disease. Princeton University Press, Princeton, USA.Google Scholar
Galvani, A. P. (2003). Immunity, antigenic heterogeneity, and aggregation of helminth parasites. Journal of Parasitology 89, 232–241.CrossRefGoogle ScholarPubMed
Gandon, S., Jansen, V. A. A. and van Baalen, M. (2001). Host life history and the evolution of parasite virulence. Evolution 55, 1056–1062.CrossRefGoogle ScholarPubMed
Görtz, H.-D. and Dieckmann, J. (1980). Life cycle and infectivity of Holospora elegans Haffkine, a micronucleus-specific symbiont of Paramecium caudatum (Ehrenberg). Protistologia 16, 591–603.Google Scholar
Görtz, H.-D. and Wiemann, M. (1989). Route of infection of the bacteria Holospora elegans and Holospora obtusa into the nuclei of Paramecium caudatum. European Journal of Protistology 24, 101–109.CrossRefGoogle ScholarPubMed
Hall, S. R., Duffy, M. A., Tessier, A. J. and Caceres, C. E. (2005). Spatial heterogeneity of daphniid parasitism within lakes. Oecologia 143, 635–644.CrossRefGoogle ScholarPubMed
Hori, M. and Fujishima, M. (2003). The endosymbiotic bacterium Holospora obtusa enhances heat-shock gene expression of the host Paramecium caudatum. Journal of Eukaryotic Microbiology 50, 293–298.Google Scholar
Jaenike, J. (1996). Population-level consequences of parasite aggregation. Oikos 76, 155–160.Google Scholar
Kaltz, O. and Shykoff, J. A. (2001). Male and female Silene latifolia plants differ in per-contact risk of infection by a sexually transmitted disease. Journal of Ecology 89, 99–109.CrossRefGoogle Scholar
Karvonen, A., Hudson, P. J., Seppala, O. and Valtonen, E. T. (2004). Transmission dynamics of a trematode parasite: exposure, acquired resistance and parasite aggregation. Parasitology Research 92, 183–188.Google Scholar
Kiesecker, J. M., Skelly, D. K., Beard, K. H. and Preisser, E. (1999). Behavioral reduction of infection risk. Proceedings of the National Academy of Sciences, USA 96, 9165–9168.Google Scholar
Lohse, K., Gutierrez, A. and Kaltz, O. (2006). Experimental evolution of resistance in Paramecium caudatum against the bacterial parasite Holospora undulata. Evolution 60, 1177–1186.Google Scholar
Lord, C. C., Barnard, B., Day, K., Hargrove, J. W., McNamara, J. J., Paul, R. E., Trenholme, K. and Woolhouse, M. E. (1999). Aggregation and distribution of strains in microparasites. Philosophical Transactions of the Royal Society of London, B 354, 799–807.Google Scholar
McCallum, H., Barlow, N. and Hone, J. (2001). How should pathogen transmission be modelled? Trends in Ecology and Evolution 16, 295–300.Google Scholar
Millot, L. and Kaltz, O. (2006). Cryopreservation of Holospora undulata, a bacterial parasite of the ciliate Paramecium caudatum. Cryobiology 62, 161–165.Google Scholar
Nakamura, Y., Aki, M., Aikawa, T., Hori, M. and Fujishima, M. (2004). Differences in gene expression of the ciliate Paramecium caudatum caused by endonuclear symbiosis with Holospora obtusa, revealed using differential display reverse transcribed PCR. FEMS Microbiology Letters 240, 209–213.Google Scholar
Nakamura, Y. and Fujishima, M. (2006). Infection with Holospora obtusa changes digestive vacuole formation in the host, Paramecium caudatum. Japanese Journal of Protozoology 39, 91–92.Google Scholar
Poulin, R. (1998). Evolutionary Ecology of Parasites: From Individuals to Communities, Chapman and Hall, London, UK.Google Scholar
Pulkkinen, K. (2007). Microparasite transmission to Daphnia magna decreases in the presence of conspecifics. Oecologia 154, 45–53.Google Scholar
Read, A. F. and Taylor, L. H. (2001). The ecology of genetically diverse infections. Science 292, 1099–1102.Google Scholar
Regoes, R. R., Ebert, D. and Bonhoeffer, S. (2002). Dose-dependent infection rates of parasites produce the Allee effect in epidemiology. Proceedings of the Royal Society of London, B 269, 271–279.CrossRefGoogle ScholarPubMed
Regoes, R. R., Hottinger, J. W., Sygnarski, L. and Ebert, D. (2003). The infection rate of Daphnia magna by Pasteuria ramosa conforms with the mass-action principle. Epidemiology and Infection 131, 957–966.Google Scholar
Restif, O. and Kaltz, O. (2006). Condition-dependent virulence in a horizontally and vertically transmitted bacterial parasite. Oikos 114, 148–158.Google Scholar
Restif, O. and Koella, J. C. (2004). Concurrent evolution of resistance and tolerance to pathogens. American Naturalist 164, E90–102.Google Scholar
SAS (1996). SAS/STAT User's Guide, Release 6.11, SAS Institute, Cary, N.C., USA.Google Scholar
SAS (2003). JMP Statistics and Graphics Guide (Version 5.0.1.2), SAS Institute, Cary, N.C., USA.Google Scholar
Schjørring, S. and Koella, J. (2003). Sub-lethal effects of pathogens can lead to the evolution of lower virulence in multiple infections. Proceedings of the Royal Society of London, B 270.CrossRefGoogle Scholar
Shaw, D. J., Grenfell, B. T. and Dobson, A. P. (1998). Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117, 597–610.Google Scholar
Tanguay, G. V. and Scott, M. E. (1992). Factors generating aggregation of Heligmosomoides polygyrus (Nematoda) in laboratory mice. Parasitology 104, 519–529.Google Scholar
Timms, R., Colegrave, N., Chan, B. H. and Read, A. F. (2001). The effect of parasite dose on disease severity in the rodent malaria parasite Plasmodium chabaudi. Parasitology 123, 1–11.Google Scholar
Traniello, J. F., Rosengaus, R. B. and Savoie, K. (2002). The development of immunity in a social insect: evidence for the group facilitation of disease resistance. Proceedings of the National Academy of Sciences, USA 99, 6838–6842.Google Scholar
Zar, J. H. (1984). Biostatistical Analysis, 2nd Edn. Prentice-Hall, Englewood Cliffs, NJ., USA.Google Scholar