Skip to main content

Advertisement

SpringerLink
Log in

Evolution of host resistance to parasite infection in the snail–schistosome–human system

  • Published:
Journal of Mathematical Biology Aims and scope Submit manuscript

Abstract

The evolutionary strategies that emerge within populations can be dictated by numerous factors, including interactions with other species. In this paper, we explore the consequences of such a scenario using a host–parasite system of human concern. By analyzing the dynamical behaviors of a mathematical model we investigate the evolutionary outcomes resulting from interactions between Schistosoma mansoni and its snail and human hosts. The model includes two types of snail hosts representing resident and mutant types. Using this approach, we focus on establishing evolutionary stable strategies under conditions where snail hosts express different life-histories and when drug treatment is applied to an age-structured population of human hosts. Results from this work demonstrate that the evolutionary trajectories of host–parasite interactions can be varied, and at times, counter-intuitive, based on parasite virulence, host resistance, and drug treatment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Anderson RM, May RM (1978) Regulation and stability of host-parasite population interactions. I. Regulatory processes. J Anim Ecol 47: 219–247

    Article  Google Scholar 

  • Anderson RM, May RM (1982) Coevolution of hosts and parasites. Parasitology 85: 411–426

    Article  Google Scholar 

  • Anderson RM, May RM (1991) Infectious diseases of humans. Dynamics and control. Oxford university Press, Oxford

    Google Scholar 

  • Beck K, Keener JP, Ricciardi P (1984) The effects of epidemics on genetic evolution. J Math Biol 19: 79–94

    Article  MathSciNet  MATH  Google Scholar 

  • Boots M, Bowers RG (1999) Three mechanisms of host resistance to microparasites-avoidance, recovery and tolerance—show different evolutionary dynamics. J Theor Biol 201: 13–23

    Article  Google Scholar 

  • Boots M, Haraguchi Y (1999) The evolution of costly resistance in host-parasite systems. Am Nat 153(4): 359–370

    Article  Google Scholar 

  • Bowers RG (1999) A baseline model for the apparent competition between many host types: the evolution of host resistance to microparasites. J Theor Biol 200: 65–67

    Article  Google Scholar 

  • Bowers RG, Turner J (1997) Community structure and the interplay between interspecific infection and competition. J Theor Biol 187: 95–109

    Article  Google Scholar 

  • Bowers RG, Boots M, Begon M (1994) Life-history trade-offs and the evolution of pathogen resistance: competition between host strain. Proc R Soc Lond B 257: 247–253

    Article  Google Scholar 

  • Bowers RG, Hoyle A, White A, Boots M (2005) The geometric theory of adaptive evolution: trade-off and invasion plots. J Theor Biol 233: 363–377

    Article  MathSciNet  Google Scholar 

  • CDC—Schistosomiasis biology (2011). http://www.cdc.gov/parasites/schistosomiasis/biology.html. Accessed July 2011

  • CDC—Schistosomiasis fact sheet (2011). http://www.cdc.gov/parasites/schistosomiasis/epi.html. Accessed July 2011

  • Chan MS, Guyatt HL, Bundy DA, Booth M, Fulford AJ, Medley GF (1995) The development of an age structured model for schistosomiasis transmission dynamics and control and its validation for Schistosoma mansoni. Epidemiol Infect 115: 325–344

    Article  Google Scholar 

  • Chitsulo L, Engels D, Montresor A, Savioli L (2000) The global status of schistosomiasis and its control. Acta Trop 77: 41–51

    Article  Google Scholar 

  • Cioli D (2000) Praziquantel: is there real resistance and are there alternatives?. Curr Opin Infect Dis 13: 659

    Article  Google Scholar 

  • Davies CM, Webster JP, Woolhouse MEJ (2001) Trade-offs in the evolution of virulence in an indirectly transmitted macroparasite. Proc R Coc Lond B 268: 251–257

    Article  Google Scholar 

  • Dieckmann U (2004) Trade-off geometries and frequency-dependent selection. Am Nat 164(6): 765–778

    Article  Google Scholar 

  • Diekmann O, Heesterbeek JAP (2000) Mathematical epidemiology of infectious diseases: model building, analysis and interpretation. Wiley, New York

    Google Scholar 

  • Dobson AP (1988) The population biology of parasite-induced changes in host behavior. Q Rev Biol 63: 139–165

    Article  Google Scholar 

  • Dobson AP, Keymer AE (1985) Life history models. In: Crompton DWT, Nickol B (eds) The biology of the Acanthocephala. Cambridge University Press, Cambridge, pp 347–384

    Google Scholar 

  • Duncan AB, Little TJ (2007) Parasite-driven genetic change in a natural population of Daphnia. Evolution 61(4): 796–803

    Article  Google Scholar 

  • Fallon PG, Mubarak JS, Fookes RE, Niang M, Butterworth AE, Sturrock RF, Doenhoff MJ (1997) Schistosoma mansoni: maturation rate and drug susceptibility of different geographic isolates. Exp Parasitol 86: 29–36

    Article  Google Scholar 

  • Feng Z, Eppert A, Milner FA, Minchella DJ (2004) Estimation of parameters governing the transmission dynamics of Schistosomes. Appl Math Lett 17: 105

    Article  MathSciNet  Google Scholar 

  • Frank SA (1992) A kin selection model for the evolution of virulence. Proc R Soc Lond B 250: 195–197

    Article  Google Scholar 

  • Gerard C, Theron A (1997) Age/size- and time-specific effects of Schistosoma mansoni on energy allocation patterns of its snail host Biomphalaria glabrata. Oecologia 112: 447–452

    Article  Google Scholar 

  • Geritz SAH, Metz JAJ, Kisdi E, Meszena G (1997) The dynamics of adaptation and evolutionary branching. Phys Rev Lett 78: 2024–2027

    Article  Google Scholar 

  • Geritz SAH, van der Meijden E, Metz JAJ (1998) Evolutionarily singular strategies and the adaptive growth and branching of the evolutionary tree. Evol Ecol 12: 35–57

    Article  Google Scholar 

  • Gower CM, Webster JP (2004) Fitness of indirectly transmitted pathogens: restraint and constraint. Evolution 58: 544–553

    Google Scholar 

  • Gower CM, Webster JP (2005) Intraspecific competition and the evolution of virulence in a parasitic trematode. Evolution 59: 544–553

    Google Scholar 

  • Hadeler KP (1984) An integral equation for helminthic infections: stability of the noninfected population. In: Lakeshmikantham V (ed) Trends in theoretical and practical nonlinear differential equations. Lecture notes in pure and applied mathematics, vol 90. Marcel Dekker

  • Hadeler KP, Dietz K (1983) Nonlinear hyperbolic partial differential equations for the dynamics of parasite populations. Comput Math Appl 9(3): 415–430

    Article  MathSciNet  MATH  Google Scholar 

  • Hoyle A, Bowers RG (2008) Can possible evolutionary outcomes be determined directly from the population dynamics?. Theor Popul Biol 74: 311–323

    Article  MATH  Google Scholar 

  • Ismail M, Botros S, Metwally A, William S et al (1999) Resistance to Praziquantel: direct evidence from Schistosoma mansoni isolated from Egyptian villagers. Am J Trop Med Hyg 60(6): 932–935

    Google Scholar 

  • Kraaijeveld AR, Godfray HCJ (1997) Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389: 278–280

    Article  Google Scholar 

  • Massara CL, Peixoto SV, Barros HS, Enk MJ, Carvalho OS, Schall V (2004) Factors associated with Schistosomiasis Mansoni in a population from the municipality of Jaboticatubas, State of Minas Gerais, Brazil. Mem Inst Oswaldo Cruz, Rio de Janeiro 99(Suppl I): 127–134

    Article  Google Scholar 

  • May RM, Anderson RM (1983) Epidemiology and genetics in the coevolution of parasites and hosts. Proc R Soc Lond B 219: 281–313

    Article  MATH  Google Scholar 

  • May RM, Nowak MA (1995) Coinfection and the evolution of virulence. Proc R Soc Lond B 261: 209–215

    Article  Google Scholar 

  • Metz JAJ, Nisbet RM, Geritz SAH (1992) How should we define ‘fitness’ for general ecological scenarios?. Trends Ecol Evol 7: 198–202

    Article  Google Scholar 

  • Metz JAJ, Geritz SAH, Meszena G, Jacobs FJA, Heerwaarden JS (1996) Adaptive dynamics: a geometrical study of the consequences of nearly faithful reproduction. In: van Strien SJ, Verduyn Lunel SM (eds) Stochastic and spatial structures of dynamical systems. North Holland, Amsterdam, pp 183–231

    Google Scholar 

  • Meuleman EA (1972) Host-parasite interrelationships between the freshwater pulmonate Biomphalaria pfeifferi and the trematode Schistosoma mansoni. Neth J Zool 22: 355–427

    Article  Google Scholar 

  • Miller MR, White A, Boots M (2005) The evolution of host resistance: tolerance and control as distinct strategies. J Theor Biol 236: 198–207

    Article  MathSciNet  Google Scholar 

  • Minchella DJ (1985) Host life-history variation in response to parasitism. Parasitology 90: 205–216

    Article  Google Scholar 

  • Minchella DJ, Loverde PT (1981) A cost of increased reproductive effort in the snail Biomphalaria glabrata. Am Nat 118: 876–881

    Article  Google Scholar 

  • Nowak MA, May RM (1994) Superinfection and the evolution of parasite virulence. Proc R Soc Lond B 255: 81–89

    Article  Google Scholar 

  • Pan CT (1965) Studies on the host-parasite relationship between Schistosoma mansoni and the Snail Australorbis glabratus. Am J Trop Med Hyg 14(6): 931–976

    Google Scholar 

  • Rueffler C, van Dooren TJM, Metz JAJ (2004) Adaptive walks on changing landscapes: Levins’ approach extended. Theor Popul Biol 65: 165–178

    Article  MATH  Google Scholar 

  • Rugierri E, Schreiber SJ (2005) The dynamics of the Schoener-Polis-Holt model of intra-guild predation. Math Biosci Eng 2(2): 279–288

    Article  MathSciNet  Google Scholar 

  • Sandland GJ, Minchella DJ (2003a) Costs of immune defense: an enigma wrapped in an environmental cloak?. Trends Parasitol 19: 571–574

    Article  Google Scholar 

  • Sandland GJ, Minchella DJ (2003b) Effects of diet and Echinostoma revolutum infection on energy allocation patterns in juvenile Lymnaea elodes snails. Oecologia 134: 479–486

    Google Scholar 

  • Sandland GJ, Minchella DJ (2004) Life-history plasticity in hosts exposed to differing resources and parasitism. Can J Zool 82: 1672–1677

    Article  Google Scholar 

  • Smith JM (1982) Evolution and the theory of games. Cambridge University Press, Cambridge

    Book  MATH  Google Scholar 

  • Sorensen RE, Minchella DJ (2001) Snail-trematode life history interactions: past trend and future directions. Parasitology 123: S3–S18

    Article  Google Scholar 

  • Sturrock RF (2001) Schistosomiasis epidemiology and control: how did we get here and where should be go?. Mem Inst Oswaldo Cruz, Rio de Janeiro 96(Suppl): 17–27

    Article  Google Scholar 

  • Webster JP, Woolhouse MEJ (1999) Cost of resistance: relationship between reduced fertility and increased resistance in a snail–schistosome host–parasite system. Proc R Soc B: Biol Sci 266: 391–396

    Article  Google Scholar 

  • Xu D, Curtis J, Feng Z, Minchella DJ (2005) On the role of schistosome mating structure in the maintenance of drug resistant strains. Bull Math Biol 67(6): 1207–1226

    Article  MathSciNet  Google Scholar 

  • Zhang P, Feng Z, Milner FA (2007a) A schistosomiasis model with an age-structure in human hosts and its application to treatment strategies. Math Biosci 205(1): 83–107

    Article  MathSciNet  MATH  Google Scholar 

  • Zhang P, Sandland GJ, Feng Z, Xu D, Minchella DJ (2007b) Evolutionary implications for interactions between multiple strains of host and parasite. J Theor Biol 248(2): 225–240

    Article  MathSciNet  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Mathematics, Purdue University, West Lafayette, IN, 47907, USA

    Yiding Yang & Zhilan Feng

  2. Department of Mathematics, Southern Illinois University Carbondale, Carbondale, IL, 62901, USA

    Dashun Xu

  3. Department of Biology, University of Wisconsin–La Crosse, La Crosse, WI, 54601, USA

    Gregory J. Sandland

  4. Department of Biological Sciences, Purdue University, West Lafayette, IN, 47907, USA

    Dennis J. Minchella

Authors
  1. Yiding Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhilan Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dashun Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gregory J. Sandland
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dennis J. Minchella
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhilan Feng.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yang, Y., Feng, Z., Xu, D. et al. Evolution of host resistance to parasite infection in the snail–schistosome–human system. J. Math. Biol. 65, 201–236 (2012). https://doi.org/10.1007/s00285-011-0457-x

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00285-011-0457-x

Keywords

Mathematics Subject Classification (2000)

Search

Navigation