Hostname: page-component-89b8bd64d-7zcd7 Total loading time: 0 Render date: 2026-05-12T04:18:34.222Z Has data issue: false hasContentIssue false
  • English
  • Français

Impact of host sex and group composition on parasite dynamics in experimental populations

Published online by Cambridge University Press:  18 February 2016

C. P. TADIRI ,
M. E. SCOTT  and
G. F. FUSSMANN
C. P. TADIRI*
Affiliation:
Department of Biology, McGill University, 1205 Avenue Docteur Penfield, Montreal, QC H3A 1B1, Canada
M. E. SCOTT
Affiliation:
Institute of Parasitology and Centre for Host-Parasite Interactions, McGill University (Macdonald Campus), 21,111 Lakeshore Drive, Ste. Anne-de-Bellevue, QC, H9X 3V9, Canada
G. F. FUSSMANN
Affiliation:
Department of Biology, McGill University, 1205 Avenue Docteur Penfield, Montreal, QC H3A 1B1, Canada
*
* Corresponding author. McGill University Stewart Biology Building, 1205 Avenue Docteur Penfield, Room W3/2, Montréal, QC H3A 1B1, Canada. E-mail: christina.tadiri@mail.mcgill.ca
Get access Rights & Permissions [Opens in a new window]

Summary

To better understand the spread of disease in nature, it is fundamentally important to have broadly applicable model systems with readily available species which can be replicated and controlled in the laboratory. Here we used an experimental model system of fish hosts and monogenean parasites to determine whether host sex, group size and group composition (single-sex or mixed-sex) influenced host-parasite dynamics at an individual and group level. Parasite populations reached higher densities and persisted longer in groups of fish compared with isolated hosts and reached higher densities on isolated females than on isolated males. However, individual fish within groups had similar burdens to isolated males regardless of sex, indicating that females may benefit more than males by being in a group. Relative condition was positively associated with high parasite loads for isolated males, but not for isolated females or grouped fish. No difference in parasite dynamics between mixed-sex groups and single-sex groups was detected. Overall, these findings suggest that while host sex influences dynamics on isolated fish, individual fish in groups have similar parasite burdens, regardless of sex. We believe our experimental results contribute to a mechanistic understanding of host-parasite dynamics, although we are cautious about directly extrapolating these results to other systems.

Keywords

Epidemic dynamicshost-parasite dynamicsguppiesGyrodactylus

Information

Type
Research Article
Information
Parasitology , Volume 143 , Issue 4 , April 2016 , pp. 523 - 531
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

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.)

Article purchase

Temporarily unavailable

References

REFERENCES

Anderson, R. M. and May, R. M. (1979). Population biology of infectious diseases: Part I. Nature 280, 361–367.Google Scholar
Apolloni, A., Poletto, C., Ramasco, J. J., Jensen, P. and Colizza, V. (2014). Metapopulation epidemic models with heterogeneous mixing and travel behaviour. Theoretical Biology and Medical Modelling 11, 3.Google Scholar
Arino, J. and Van den Driessche, P. (2006). Disease spread in metapopulations. Nonlinear Dynamics and Evolution Equations 48, 1–13.Google Scholar
Bagge, A. M., Poulin, R. and Valtonen, E. T. (2004). Fish population size, and not density, as the determining factor of parasite infection: a case study. Parasitology 128, 305–313.Google Scholar
Bakke, T. A., Cable, J. and Harris, P. D. (2007). The biology of gyrodactylid monogeneans: the ‘russian-doll killers’. In Advances in Parasitology, Vol. 64 (ed. Baker, J. R., M., R. and Rollinson, D.), pp. 161–376, 459–460. Academic Press, Cambridge, MA.Google Scholar
Ben-Zion, Y., Cohen, Y. and Shnerb, N. M. (2010). Modeling epidemics dynamics on heterogenous networks. Journal of Theoretical Biology 264, 197–204.Google Scholar
Bonte, D., Lens, L., Maelfait, J.-P., Hoffmann, M. and Kuijken, E. (2003). Patch quality and connectivity influence spatial dynamics in a dune wolfspider. Oecologia 135, 227–233.Google Scholar
Boots, M., Best, A., Miller, M. R. and White, A. (2009). The role of ecological feedbacks in the evolution of host defence: what does theory tell us? Philosophical Transactions of the Royal Society B: Biological Sciences 364, 27–36.Google Scholar
Brooks, C. P., Antonovics, J. and Keitt, T. H. (2008). Spatial and temporal heterogeneity explain disease dynamics in a spatially explicit network model. American Naturalist 172, 149–159.CrossRefGoogle Scholar
Cable, J. and van Oosterhout, C. (2007 a). The impact of parasites on the life history evolution of guppies (Poecilia reticulata): the effects of host size on parasite virulence. International Journal for Parasitology 37, 1449–1458.Google Scholar
Cable, J. and van Oosterhout, C. (2007 b). The role of innate and acquired resistance in two natural populations of guppies (Poecilia reticulata) infected with the ectoparasite Gyrodactylus turnbulli . Biological Journal of the Linnean Society 90, 647–655.Google Scholar
Colizza, V. and Vespignani, A. (2008). Epidemic modeling in metapopulation systems with heterogeneous coupling pattern: theory and simulations. Journal of Theoretical Biology 251, 450–467.CrossRefGoogle Scholar
Cornell, S. J., Isham, V. S. and Grenfell, B. T. (2004). Stochastic and spatial dynamics of nematode parasites in farmed ruminants. Proceedings of the Royal Society of London B: Biological Sciences 271, 1243–1250.Google Scholar
Croft, D., Krause, J. and James, R. (2004). Social networks in the guppy (Poecilia reticulata). Proceedings of the Royal Society of London B: Biological Sciences 271(Suppl 6), S516–S519.Google Scholar
Croft, D. P., Albanese, B., Arrowsmith, B. J., Botham, M., Webster, M. and Krause, J. (2003). Sex-biased movement in the guppy (Poecilia reticulata). Oecologia 137, 62–68.Google Scholar
Dargent, F., Scott, M. E., Hendry, A. P. and Fussmann, G. F. (2013). Experimental elimination of parasites in nature leads to the evolution of increased resistance in hosts. Proceedings of the Royal Society of London B: Biological Sciences 280. doi: 10.1098/rspb.2013.2371.Google Scholar
Dargent, F., Rolshausen, G., Hendry, A. P., Scott, M. E. and Fussmann, G. F. (2015). Parting ways: parasite release in nature leads to sex-specific evolution of defence. Journal of Evolutionary Biology 29, 23–24.Google Scholar
Dennis, R. L. H. and Eales, H. T. (1997). Patch occupancy in Coenonympha tullia (Muller, 1764) (Lepidoptera: Satyrinae): habitat quality matters as much as patch size and isolation. Journal of Insect Conservation 1, 167–176.Google Scholar
Fleishman, E., Ray, C., Sjögren-Gulve, P., Boggs, C. L. and Murphy, D. D. (2002). Assessing the roles of patch quality, area, and isolation in predicting metapopulation dynamics. Conservation Biology 16, 706–716.CrossRefGoogle Scholar
Franzén, M. and Nilsson, S. G. (2010). Both population size and patch quality affect local extinctions and colonizations. Proceedings of the Royal Society of London B: Biological Sciences 277, 79–85.Google Scholar
Fraser, B. A., Ramnarine, I. W. and Neff, B. D. (2009). Selection at the MHC class IIB locus across guppy (Poecilia reticulata) populations. Heredity 104, 155–167.Google Scholar
Gheorghiu, C., Cable, J., Marcogliese, D. J. and Scott, M. E. (2007). Effects of waterborne zinc on reproduction, survival and morphometrics of Gyrodactylus turnbulli (Monogenea) on guppies (Poecilia reticulata). International Journal for Parasitology 37, 375–381.Google Scholar
Gog, J. R., Pellis, L., Wood, J. L. N., McLean, A. R., Arinaminpathy, N. and Lloyd-Smith, J. O. (2015). Seven challenges in modeling pathogen dynamics within-host and across scales. Epidemics 10, 45–48.Google Scholar
Gotanda, K., Delaire, L., Raeymaekers, J. M., Pérez-Jvostov, F., Dargent, F., Bentzen, P., Scott, M., Fussmann, G. and Hendry, A. (2013). Adding parasites to the guppy-predation story: insights from field surveys. Oecologia 172, 155–166.CrossRefGoogle Scholar
Grenfell, B. and Harwood, J. (1997). (Meta)population dynamics of infectious diseases. Trends in Ecology and Evolution 12, 395–399.Google Scholar
Hagenaars, T. J., Donnelly, C. A. and Ferguson, N. M. (2004). Spatial heterogeneity and the persistence of infectious diseases. Journal of Theoretical Biology 229, 349–359.CrossRefGoogle ScholarPubMed
Hanski, I. (1999). Metapopulation Ecology. Oxford University Press, Oxford.Google Scholar
Harris, P. D. and Lyles, A. M. (1992). Infections of Gyrodactylus bullatarudis and Gyrodactylus turnbulli on guppies (Poecilia reticulata) in Trinidad. Journal of Parasitology 78, 912–914.Google Scholar
Houde, A. E. and Torio, A. J. (1992). Effect of parasitic infection on male color pattern and female choice in guppies. Behavioral Ecology 3, 346–351.Google Scholar
Johnson, M. B., Lafferty, K. D., van Oosterhout, C. and Cable, J. (2011). Parasite transmission in social interacting hosts: monogenean epidemics in guppies. PLoS ONE 6, e22634.Google Scholar
Kearn, G. C. (1994). Evolutionary expansion of the Monogenea. International Journal for Parasitology 24, 1227–1271.Google Scholar
Kolluru, G. R., Grether, G. F., South, S. H., Dunlop, E., Cardinali, A., Liu, L. and Carapiet, A. (2006). The effects of carotenoid and food availability on resistance to a naturally occurring parasite (Gyrodactylus turnbulli) in guppies (Poecilia reticulata). Biological Journal of the Linnean Society 89, 301–309.Google Scholar
Kolluru, G. R., Grether, G. F., Dunlop, E. and South, S. H. (2009). Food availability and parasite infection influence mating tactics in guppies (Poecilia reticulata). Behavioral Ecology 20, 131–137.Google Scholar
Le Cren, E. D. (1951). The length-weight relationship and seasonal cycle in gonad weight and condition in the perch (Perca fluviatilis). Journal of Animal Ecology 20, 201–219.Google Scholar
May, R. M. and Anderson, R. M. (1979). Population biology of infectious diseases: Part II. Nature 280, 455–461.Google Scholar
Peig, J. and Green, A. J. (2010). The paradigm of body condition: a critical reappraisal of current methods based on mass and length. Functional Ecology 24, 1323–1332.Google Scholar
Pérez-Jvostov, F., Hendry, A. P., Fussmann, G. F. and Scott, M. E. (2015). An experimental test of antagonistic effects of competition and parasitism on host performance in semi-natural mesocosms. Oikos. doi: 10.1111/oik.02499.Google Scholar
Poulin, R. and Rohde, K. (1997). Comparing the richness of metazoan ectoparasite communities of marine fishes: controlling for host phylogeny. Oecologia 110, 278–283.Google Scholar
R Development Core Team (2014). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Richards, E. L., van Oosterhout, C. and Cable, J. (2010). Sex-specific differences in shoaling affect parasite transmission in guppies. PLoS ONE 5, e13285.Google Scholar
Richards, E. L., van Oosterhout, C. and Cable, J. (2012). Interactions between males guppies facilitates the transmission of the monogenean ectoparasite Gyrodactylus turnbulli . Experimental Parasitology 132, 483–486.Google Scholar
Richards, G. R. and Chubb, J. C. (1998). Longer-term population dynamics of Gyrodactylus bullatarudis and G. turnbulli (Monogenea) on adult guppies Poecilia reticulata in 50-l experimental arenas. Parasitology Research 84, 753–756.Google Scholar
Rosà, R., Pugliese, A., Villani, A. and Rizzoli, A. (2003). Individual-based vs. deterministic models for macroparasites: host cycles and extinction. Theoretical Population Biology 63, 295–307.Google Scholar
Schelkle, B., Doetjes, R. and Cable, J. (2011). The salt myth revealed: treatment of gyrodactylid infections on ornamental guppies, Poecilia reticulata . Aquaculture 311, 74–79.Google Scholar
Schooley, R. and Branch, L. (2007). Spatial heterogeneity in habitat quality and cross-scale interactions in metapopulations. Ecosystems 10, 846–853.Google Scholar
Schulenburg, H., Kurtz, J., Moret, Y. and Siva-Jothy, M. T. (2009). Introduction. Ecological immunology. Philosophical Transactions of the Royal Society B: Biological Sciences 364, 3–14.Google Scholar
Scott, M. E. (1982). Reproductive potential of Gyrodactylus bullatarudis (Monogenea) on guppies (Poecilia reticulata). Parasitology 85, 217–236.Google Scholar
Scott, M. E. (1985 a). Dynamics of challenge infections of Gyrodactylus bullatarudis Turnbull (Monogenea) on guppies, Poecilia reticulata (Peters). Journal of Fish Diseases 8, 495–503.Google Scholar
Scott, M. E. (1985 b). Experimental epidemiology of Gyrodactylus bullatarudis (Monogenea) on guppies (Poecilia reticuata): short- and long-term studies. In Ecology and Genetics of Host-Parasite Interactions (ed. Rollinson, D. and Anderson, R. M.), pp. 21–38. Academic Press, New York.Google Scholar
Scott, M. E. (1988). The impact of infection and disease on animal populations: implications for conservation biology. Conservation Biology 2, 40–56.Google Scholar
Scott, M. E. (1991). Heligmosomoides polygyrus (Nematoda): susceptible and resistant strains of mice are indistinguishable following natural infection. Parasitology 103, 429–438.Google Scholar
Scott, M. E. (2006). High transmission rates restore expression of genetically determined susceptibility of mice to nematode infections. Parasitology 132, 669–679.Google Scholar
Scott, M. E. and Anderson, R. M. (1984). The population dynamics of Gyrodactylus bullatarudis (Monogenea) within laboratory populations of the fish host Poecilia reticulata . Parasitology 89, 159–194.Google Scholar
Scott, M. E. and Robinson, M. A. (1984). Challenge infections of Gyrodactylus bullatarudis (Monogenea) on guppies, Poecilia reticulata (Peters), following treatment. Journal of Fish Biology 24, 581–586.Google Scholar
Singh, B. K., Rao, J. S., Ramaswamy, R. and Sinha, S. (2004). The role of heterogeneity on the spatiotemporal dynamics of host–parasite metapopulation. Ecological Modelling 180, 435–443.Google Scholar
Smith, K. F., Dobson, A. P., McKenzie, F. E., Real, L. A., Smith, D. L. and Wilson, M. L. (2005). Ecological theory to enhance infectious disease control and public health policy. Frontiers in Ecology and the Environment 3, 29–37.Google Scholar
Smith, K. F., Acevedo-Whitehouse, K. and Pedersen, A. B. (2009). The role of infectious diseases in biological conservation. Animal Conservation 12, 1–12.Google Scholar
Stephenson, J. F., van Oosterhout, C., Mohammed, R. S. and Cable, J. (2014). Parasites of Trinidadian guppies: evidence for sex- and age-specific trait-mediated indirect effects of predators. Ecology 96, 489–498.Google Scholar
Tadiri, C. P., Dargent, F. and Scott, M. E. (2013). Relative host body condition and food availability influence epidemic dynamics: a Poecilia reticulata-Gyrodactylus turnbulli host-parasite model. Parasitology 140, 343–351.Google Scholar
Thomas, J. A., Bourn, N. A. D., Clarke, R. T., Stewart, K. E., Simcox, D. J., Pearman, G. S., Curtis, R. and Goodger, B. (2001). The quality and isolation of habitat patches both determine where butterflies persist in fragmented landscapes. Proceedings of the Royal Society of London B: Biological Sciences 268, 1791–1796.Google Scholar
Van Oosterhout, C., Harris, P. D. and Cable, J. (2003). Marked variation in parasite resistance between two wild populations of the Trinidadian guppy, Poecilia reticulata (Pisces: Poeciliidae). Biological Journal of the Linnean Society 79, 645–651.Google Scholar
Wilson, K. and Cotter, S. C. (2008). Density-dependent prophylaxis in insects. Phenotypic Plasticity of Insects: Mechanisms and Consequences (eds Ananthakrishnan, T. & Whitman, D.), pp. 381–420. Science Pub Inc, Plymouth, UK.Google Scholar