Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-11T07:15:13.477Z Has data issue: false hasContentIssue false

Applying predator-prey theory to modelling immune-mediated, within-host interspecific parasite interactions

Published online by Cambridge University Press:  15 February 2010

ANDY FENTON*
Affiliation:
School of Biological Sciences, University of Liverpool, Crown Street, LiverpoolL69 7ZB, UK
SARAH E. PERKINS
Affiliation:
Center for Infectious Disease Dynamics, 208 Mueller Lab, Penn State University, State College, PA, 16803, USA
*
*Corresponding author: School of Biological Sciences, University of Liverpool, Crown Street, LiverpoolL69 7ZB, UK. Tel: +0151 795 4473. Fax: +0151 795 4408. E-mail: a.fenton@liverpool.ac.uk

Summary

Predator-prey models are often applied to the interactions between host immunity and parasite growth. A key component of these models is the immune system's functional response, the relationship between immune activity and parasite load. Typically, models assume a simple, linear functional response. However, based on the mechanistic interactions between parasites and immunity we argue that alternative forms are more likely, resulting in very different predictions, ranging from parasite exclusion to chronic infection. By extending this framework to consider multiple infections we show that combinations of parasites eliciting different functional responses greatly affect community stability. Indeed, some parasites may stabilize other species that would be unstable if infecting alone. Therefore hosts' immune systems may have adapted to tolerate certain parasites, rather than clear them and risk erratic parasite dynamics. We urge for more detailed empirical information relating immune activity to parasite load to enable better predictions of the dynamic consequences of immune-mediated interspecific interactions within parasite communities.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2010

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

Abbas, A. K., Murphy, K. M. and Sher, A. (1996). Functional diversity of helper T lymphocytes. Nature, London 383, 787793.CrossRefGoogle ScholarPubMed
Antia, R., Bergstrom, C. T., Pilyugin, S. S., Kaech, S. M. and Ahmed, R. (2003). Models of CD8+ responses: 1. What is the antigen-independent proliferation program. Journal of Theoretical Biology 221, 585598.Google Scholar
Antia, R. and Koella, J. (2004). Theoretical immunology – Parasitic turncoat. Nature, London 429, 511513Google Scholar
Antia, R., Koella, J. C. and Perrot, V. (1996). Models of the within-host dynamics of persistent mycobacterial infections. Proceedings of the Royal Society of London, B 263, 257263.Google Scholar
Antia, R. and Lipsitch, M. (1997). Mathematical models of parasite responses to host immune defences. Parasitology 115, S155S167.Google Scholar
Bassetti, S., Bischoff, W. E. and Sherertz, R. J. (2005). Are SARS superspreaders cloud adults? Emerging Infectious Diseases 11, 637638.CrossRefGoogle ScholarPubMed
Behnke, J. M. (2008). Structure in parasite component communities in wild rodents: predictability, stability, associations and interactions … or pure randomness? Parasitology 135, 751766.CrossRefGoogle ScholarPubMed
Ben-Smith, A., Wahid, F. N., Lammas, D. A. and Behnke, J. M. (1999). The relationship between circulating and intestinal Heligmosomoides polygyrus-specific IgG(1) and IgA and resistance to primary infection. Parasite Immunology 21, 383395.Google Scholar
Bentwich, Z., Kalinkovich, A., Weisman, Z., Borkow, G., Beyers, N. and Beyers, A. D. (1999). Can eradication of helminthic infections change the face of AIDS and tuberculosis? Immunology Today 20, 485487.Google Scholar
Bonsall, M. B. and Hassell, M. P. (1997). Apparent competition structures ecological assemblages. Nature, London 388, 371373.CrossRefGoogle Scholar
Borer, E. T., Anderson, K., Blanchette, C. A., Broitman, B., Cooper, S. D., Halpern, B. S., Seabloom, E. W. and Shurin, J. B. (2002). Topological approaches to food web analyses: a few modifications may improve our insights. Oikos 99, 397401.Google Scholar
Bottomley, C., Isham, V. and Basanez, M. G. (2007). Population biology of multispecies helminth infection: competition and coexistence. Journal of Theoretical Biology 244, 8195.CrossRefGoogle ScholarPubMed
Brady, M. T., O'Neill, S. M., Dalton, J. P. and Mills, K. H. G. (1999). Fasciola hepatica suppresses a protective Th1 response against Bordetella pertussis. Infection and Immunity 67, 53725378.CrossRefGoogle ScholarPubMed
Buric, N., Mudrinic, M. and Vasovic, N. (2001). Time delay in a basic model of the immune response. Chaos Solitons & Fractals 12, 483489.CrossRefGoogle Scholar
Callard, R. E. and Yates, A. J. (2005). Immunology and mathematics: crossing the divide. Immunology 115, 2133.Google Scholar
Carpenter, S. R., Cottingham, K. L. and Stow, C. A. (1994). Fitting predator-prey models to time series with observation errors. Ecology 75, 12541264.Google Scholar
Christensen, N. O., Nansen, P., Fagbemi, B. O. and Monrad, J. (1987). Heterologous antagonistic and synergistic interactions between helminths and between helminths and protozoans in concurrent experimental infection of mammalian hosts. Parasitology Research 73, 387410.CrossRefGoogle ScholarPubMed
Cox, F. E. G. (2001). Concomitant infections, parasites and immune responses. Parasitology 122, S23S38.CrossRefGoogle ScholarPubMed
Ebert, D. (1994). Virulence and local adaptation of a horizontally transmitted parasite. Science 265, 10841086.CrossRefGoogle ScholarPubMed
Fenton, A. (2008). Worms and germs: the population dynamic consequences of microparasite-macroparasite co-infection. Parasitology 135, 15451560.CrossRefGoogle ScholarPubMed
Fenton, A., Lamb, T. and Graham, A. L. (2008). Optimality analysis of Th1/Th2 immune responses during microparasite-macroparasite co-infection, with epidemiological feedbacks. Parasitology 135, 841853.CrossRefGoogle ScholarPubMed
Fenton, A., Lello, J. and Bonsall, M. B. (2006). Pathogen responses to host immunity: the impact of time delays and memory on the evolution of virulence. Proceedings of the Royal Society of London B 273, 20832090.Google Scholar
Ferguson, N. M., Galvani, A. P. and Bush, R. M. (2003). Ecological and immunological determinants of influenza evolution. Nature, London 422, 428433.Google Scholar
Gause, G. F. (1934). The Struggle for Existence. Williams and Wilkins, Baltimore, MD, USA.Google Scholar
Gause, G. F. (1935). Experimental demonstration of Volterra's periodic oscillations in the numbers of animals. Journal of Experimental Biology 12, 4448.Google Scholar
Gause, G. F. (1936). Further studies of interaction between predators and prey. The Journal of Animal Ecology 5, 118.CrossRefGoogle Scholar
Gog, J. R. and Grenfell, B. T. (2002). Dynamics and selection of many-strain pathogens. Proceedings of the National Academy of Sciences, USA 99, 1720917214.CrossRefGoogle ScholarPubMed
Graham, A. L. (2008). Ecological rules governing helminth-microparasite coinfection. Proceedings of the National Academy of Sciences, USA 105, 566570.CrossRefGoogle ScholarPubMed
Gupta, S., Swinton, J. and Anderson, R. M. (1994). Theoretical studies of the effects of heterogeneity in the parasite population on the transmission dynamics of malaria. Proceedings of the Royal Society of London, B 256, 231238.Google Scholar
Harrison, G. W. (1995). Comparing predator-prey models to Luckinbill's experiment with Didinium and Paramecium. Ecology 76, 357374.CrossRefGoogle Scholar
Holmes, J. C. (1961). Effects of concurrent infections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala). 1. General effects and comparison with crowding. Journal of Parasitology 47, 209216.Google Scholar
Holmes, J. C. (1962). Effects of concurrent infections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala). Effects on growth. Journal of Parasitology 48, 8796.Google Scholar
Holt, R. D. (1977). Predation, apparent competition, and structure of prey communities. Theoretical Population Biology 12, 197229.CrossRefGoogle ScholarPubMed
Holt, R. D. (1983). Optimal foraging and the form of the predator isocline. American Naturalist 122, 521541.CrossRefGoogle Scholar
Holt, R. D. and Dobson, A. P. (2006). Extending the principles of community ecology to address the epidemiology of host-pathogen systems. In Disease Ecology: Community Structure and Pathogen Dynamics (ed. Collinge, S. K. and Ray, C.), pp. 6–27. Oxford University Press, Oxford, UK.Google Scholar
Holt, R. D. and Lawton, J. H. (1994). The ecological consequences of shared natural enemies. Annual Review of Ecology and Systematics 25, 495520.CrossRefGoogle Scholar
Jost, C. and Arditi, R. (2001). From pattern to process: identifying predator-prey models from time-series data. Population Ecology 43, 229243.Google Scholar
Keymer, A. (1982). Density-dependent mechanisms in the regulation of intestinal helminth populations. Parasitology 84, 573587.Google Scholar
Koelle, K., Rodo, X., Pascual, M., Yunus, M. and Mostafa, G. (2005). Refractory periods and climate forcing in cholera dynamics. Nature, London 436, 696700.CrossRefGoogle ScholarPubMed
Lamb, T. J., Graham, A. L., Le Goff, L. and Allen, J. E. (2005). Co-infected C57BL/6 mice mount appropriately polarized and compartmentalized cytokine responses to Litomosoides sigmodontis and Leishmania major but disease progression is altered. Parasite Immunology 27, 317324.CrossRefGoogle ScholarPubMed
Lello, J., Boag, B., Fenton, A., Stevenson, I. R. and Hudson, P. J. (2004). Competition and mutualism among the gut helminths of a mammalian host. Nature, London 428, 840844.CrossRefGoogle ScholarPubMed
Liesenfeld, O., Dunay, I. R. and Erb, K. J. (2004). Infection with Toxoplasma gondii reduces established and developing Th2 responses induced by Nippostrongylus brasiliensis infection. Infection and Immunity 72, 38123822.CrossRefGoogle ScholarPubMed
Marshall, B. G., Mitchell, D. M., Shaw, R. J., Marais, F., Watkins, R. M. and Coker, R. J. (1999). HIV and tuberculosis co-infection in an inner London hospital – a prospective anonymized seroprevalence study. Journal of Infection 38, 162166.Google Scholar
May, R. M. (1974). Stability and Complexity in Model Ecosystems. Princeton University Press, Princeton, NJ, USA.Google Scholar
Murdoch, W. W., Briggs, C. J. and Nisbet, R. M. (2003). Consumer-Resource Dynamics. Princeton University Press, Princeton, NJ, USA.Google Scholar
Nowak, M. A. and May, R. M. (2000). Virus Dynamics: Mathematical Principles of Immunology and Virology. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Otterstatter, M. C. and Thomson, J. D. (2006). Within-host dynamics of an intestinal pathogen of bumble bees. Parasitology 133, 749761.CrossRefGoogle ScholarPubMed
Pedersen, A. B. and Fenton, A. (2007). Emphasising the ecology in parasite community ecology. Trends in Ecology & Evolution 22, 133139.Google Scholar
Perelson, A. S. (2002). Modelling viral and immune system dynamics. Nature Reviews Immunology 2, 2836.CrossRefGoogle ScholarPubMed
Pilyugin, S. S. and Antia, R. (2000). Modeling immune responses with handling time. Bulletin of Mathematical Biology 62, 869890.CrossRefGoogle ScholarPubMed
Read, A. F., Graham, A. L. and Raberg, L. (2008). Animal defenses against infectious agents: is damage control more important than pathogen control? PLoS Biology 6, 26382641.CrossRefGoogle ScholarPubMed
Riley, S., Donnelly, C. A. and Ferguson, N. M. (2003). Robust parameter estimation techniques for stochastic within-host macroparasite models. Journal of Theoretical Biology 225, 419430.CrossRefGoogle ScholarPubMed
Rohani, P., Green, C. J., Mantilla-Beniers, N. B. and Grenfell, B. T. (2003). Ecological interference between fatal diseases. Nature, London 422, 885888.Google Scholar
Shen, Z., Ning, F., Zhou, W. G., He, X., Lin, C. Y., Chin, D. P., Zhu, Z. H. and Schuchat, A. (2004). Superspreading SARS events, Beijing, 2003. Emerging Infectious Diseases 10, 256260.CrossRefGoogle ScholarPubMed
Sole, R. V. and Montoya, J. M. (2001). Complexity and fragility in ecological networks. Proceedings of the Royal Society of London, B 268, 20392045.CrossRefGoogle ScholarPubMed
Tompkins, D. M. and Hudson, P. J. (1999). Regulation of nematode fecundity in the ring-necked pheasant (Phasianus colchicus): not just density dependence. Parasitology 118, 417423.CrossRefGoogle Scholar
Volterra, V. (1926). Fluctuations in the abundance of a species considered mathematically. Nature, London 118, 558560.Google Scholar
Wodarz, D. (2006). Ecological and evolutionary principles in immunology. Ecology Letters 9, 694705.Google Scholar
Zinkernagel, R. M. (1996). Immunology taught by viruses. Science 271, 173178.CrossRefGoogle ScholarPubMed
Supplementary material: File

Fenton supplementary material

Appendix.doc

Download Fenton supplementary material(File)
File 256 KB