Advertisement

Oecologia

, Volume 186, Issue 2, pp 555–564 | Cite as

The influence of related and unrelated co-infections on parasite dynamics and virulence

  • A. M. Gleichsner
  • K. Reinhart
  • D. J. Minchella
Community ecology – original research

Abstract

Many parasitic infections increase the morbidity and mortality of host populations. Interactions between co-infecting parasites can influence virulence, the damage done to a host. Previous studies investigating the impacts of parasite co-infection on hosts have been limited by their inability to control parasite dosage, use consistent virulence metrics, or verify co-infection status. This study used molecular tools, known infection dosage, and multiple assessments over time to test whether parasite relatedness can predict virulence in co-infections, as well as whether competitive interactions between different parasite strains within a host are predictable over time. In addition, we examined the impacts of other parasite traits, such as infectivity, as alternative predictors of virulence and competition outcomes. Hosts with single-strain (related) parasite infections were found to have lower virulence in terms of host and parasite reproduction, supporting kin selection predictions. However, these infections also resulted in higher host mortality. We argue that mortality should not be used as a measurement of virulence in parasite systems that castrate hosts. Hosts were more susceptible to mixed strain (unrelated) parasite infections, indicating that co-infections may make resistance more costly to hosts. Co-infections were dynamic, with changes in parasite dominance over the course of the infection. The more infective parasite strain appeared to suppress the less infective strain, ultimately increasing host longevity. Our findings suggest that unrelated, or more diverse, parasite infections are associated with higher virulence, but that studies must consider their methodology and possible alternative explanations beyond kin selection to understand virulence outcomes.

Keywords

Virulence Parasite Kin selection Schistosoma mansoni Competition 

Notes

Acknowledgements

We thank the anonymous reviewers and editorial team for their helpful comments and suggestions regarding this manuscript. We also thank the Biomedical Research Institute for providing the parasites and hosts used in this experiment.

Author contribution statement

AMG and DJM conceived and designed the experiment, AMG and KR performed the experiments and analyzed the data. AMG, KR, and DJM wrote the manuscript.

References

  1. Alizon S (2012) Parasite co-transmission and evolutionary epidemiology of virulence. Evolution 67(4):921–933CrossRefPubMedGoogle Scholar
  2. Alizon S, de Roode JC, Michalakis Y (2013) Multiple infections and the evolution of virulence. Ecol Lett 16:556–567.  https://doi.org/10.1111/ele.12076 CrossRefPubMedGoogle Scholar
  3. Anderson RM, May RM (1982) Coevolution of hosts and parasites. Parasitology 85:411–426.  https://doi.org/10.1007/978-1-4614-3265-4 CrossRefPubMedGoogle Scholar
  4. Bell AS, de Roode JC, Sim D, Read AF (2006) Within-host competition in genetically diverse malaria infections: parasite virulence and competitive success. Evolution 60:1358–1371.  https://doi.org/10.1554/05-611.1 CrossRefPubMedGoogle Scholar
  5. Bremermann HJ, Pickering J (1983) A game-theoretical model of parasite virulence. J Theor Biol 100:411–426.  https://doi.org/10.1016/0022-5193(83)90438-1 CrossRefPubMedGoogle Scholar
  6. Cheever AW, Duvall RH, Hallack TA Jr, Minker RG, Malley JD, Malley KG (1987) Variation of hepatic fibrosis and granuloma size among mouse strains infected with Schistosoma mansoni. Am Soc Trop Med Hyg 37(1):85–97.  https://doi.org/10.4269/ajtmh.1987.37.85 CrossRefGoogle Scholar
  7. Combes C (2001) Parasitism: the ecology and evolution of intimate interactions. The University of Chicago Press, ChicagoGoogle Scholar
  8. Dabo A, Durand P, Morand S et al (1997) Distribution and genetic diversity of Schistosoma haematobium within its bulinid intermediate hosts in Mali. Acta Trop 66:15–26CrossRefPubMedGoogle Scholar
  9. Davies CM, Webster JP, Kruger O, Munatsi A, Ndamba J, Woolhouse MEJ (1999) Host—parasite population genetics: a cross-sectional comparison of Bulinus globosus and Schistosoma haematobium. Parasitology 119:295–302CrossRefPubMedGoogle Scholar
  10. Davies CM, Webster JP, Woolhouse ME (2001) Trade-offs in the evolution of virulence in an indirectly transmitted macroparasite. Proc R Soc B 268:251–257.  https://doi.org/10.1098/rspb.2000.1367 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Davies CM, Fairbrother E, Webster JP (2002) Mixed strain schistosome infections of snails and the evolution of parasite virulence. Parasitology 124:31–38CrossRefPubMedGoogle Scholar
  12. de Roode JC, Pansini R, Cheesman SJ et al (2005) Virulence and competitive ability in genetically diverse malaria infections. Proc Natl Acad Sci USA 102:7624–7628.  https://doi.org/10.1073/pnas.0500078102 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Eppert A, Lewis FA, Grzywacz C et al (2002) Distribution of schistosome infections in molluscan hosts at different levels of parasite prevalence. J Parasitol 88:232–236CrossRefPubMedGoogle Scholar
  14. Ford AF, Schall JJ (2011) Relative clonal proportions over time in mixed-genotype infections of the lizard malaria parasite Plasmodium mexicanum. Int J Parasitol 41:731–738.  https://doi.org/10.1016/j.ijpara.2011.01.010 CrossRefPubMedGoogle Scholar
  15. Frank SA (1996) models of parasite virulence. Q Rev Biol 71:37–78CrossRefPubMedGoogle Scholar
  16. Ganz HH, Ebert D (2010) Benefits of host genetic diversity for resistance to infection depend on parasite diversity. Ecology 91(5):1263–1268CrossRefPubMedPubMedCentralGoogle Scholar
  17. Gasser RB, Morahan G, Mitchell GF (1991) Sexing single larval stages of Schistosoma mansoni by polymerase chain reaction. Mol Biochem Parasitol 47:255–258CrossRefPubMedGoogle Scholar
  18. Gleichsner AM, Minchella DJ (2014) Can host ecology and kin selection predict parasite virulence? Parasitology 141:1018–1030.  https://doi.org/10.1017/S0031182014000389 CrossRefPubMedGoogle Scholar
  19. Gleichsner AM, Thiele EA, Minchella DJ (2015) It’s all about those bases: the need for incorporating parasite genetic heterogeneity into the development of schistosome vaccines. PLoS Negl Trop Dis 9(6):e0003805.  https://doi.org/10.1371/journal.pntd.0003805 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Gower CM, Webster JP (2005) Intraspecific competition and the evolution of virulence in a parasitic trematode. Evolution 59:544.  https://doi.org/10.1554/04-475 CrossRefPubMedGoogle Scholar
  21. Holt RD, Dobson AP (2006) Extending the principles of community ecology to address the epidemiology of host-pathogen systems. In: Collinge SK, Ray C (eds) Disease ecology: community structure and pathogen dynamics. Oxford University Press, Oxford, pp 28–40Google Scholar
  22. Izhar R, Routtu J, Ben-ami F (2015) Host age modulates within-host parasite competition. Biol Lett.  https://doi.org/10.1098/rsbl.2015.0131 PubMedPubMedCentralGoogle Scholar
  23. Jensen K, Little T, Skorping A, Ebert D (2006) Empirical support for optimal virulence in a castrating parasite. PLoS Biol 4(7):e197CrossRefPubMedPubMedCentralGoogle Scholar
  24. Jones-Nelson O, Thiele EA, Minchella DJ (2011) Transmission dynamics of two strains of Schistosoma mansoni utilizing novel intermediate and definitive hosts. Paristol Res 109:675–687.  https://doi.org/10.1007/s00436-011-2299-2 CrossRefGoogle Scholar
  25. Karvonen A, Rellstab C, Louhi K-R, Jokela J (2011) Synchronous attack is advantageous: mixed genotype infections lead to higher infection success in trematode parasites. Proc Biol Sci.  https://doi.org/10.1098/rspb.2011.0879 PubMedPubMedCentralGoogle Scholar
  26. Koene JM, Ter Maat A (2004) Energy budgets in the simultaneously hermaphroditic pond snail, Lymnaea stagnalis: a trade-off between growth and reproduction during development. Belg J Zool 134:41–45Google Scholar
  27. Koskella B, Lin DM, Buckling A, Thompson JN (2012) The costs of evolving resistance in heterogeneous parasite environments. Proc R Soc B.  https://doi.org/10.1098/rspb.2011.2259 PubMedGoogle Scholar
  28. Leggett HC, Brown SP, Reece SE (2014) War and peace: social interactions in infections. Phil Trans R Soc B 369:20130365.  https://doi.org/10.1098/rstb.2013.0365 CrossRefPubMedPubMedCentralGoogle Scholar
  29. May RM, Nowak MA (1994) Superinfection, metapopulation dynamics, and the evolution of diversity. J Theor Biol 170:95–114CrossRefPubMedGoogle Scholar
  30. May RM, Nowak MA (1995) Coinfection and the evolution of parasite virulence. Proc R Soc B 261:209–215.  https://doi.org/10.1098/rspb.1995.0138 CrossRefPubMedGoogle Scholar
  31. Minchella DJ (1985) Host life-history variation in response to parasitism. Parasitology 90:205–216CrossRefGoogle Scholar
  32. Oliver L, Stirewalt MA (1952) An efficient method for exposure of mice to cercariae of Schistosoma mansoni. J Parasitol 38:19–23CrossRefGoogle Scholar
  33. Partridge L, Harvey PH (1988) The ecological context of life history evolution. Science 241(4872):1449CrossRefPubMedGoogle Scholar
  34. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/
  35. Read AF, Taylor LH (2001) The ecology of genetically diverse infections. Science 292(5519):1099–1102CrossRefPubMedGoogle Scholar
  36. Reznick D (1983) The structure of guppy life histories: the tradeoff between growth and reproduction. Ecology 64(4):862–873CrossRefGoogle Scholar
  37. Richards CS, Knight M, Lewis FA (1992) Genetics of Biomphalaria glabrata and its effect on the outcome of Schistosoma mansoni infection. Parasitol Today 8(5):1771–1774.  https://doi.org/10.1016/0169-4758(92)90015-T CrossRefGoogle Scholar
  38. Rigaud T, Perrot-Minnot M-J, Brown MJF (2010) Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence. Proc R Soc B.  https://doi.org/10.1098/rspb.2010.1163 PubMedPubMedCentralGoogle Scholar
  39. Sandland GJ, Minchella DJ (2003) Costs of immune defense: an enigma wrapped in an environmental cloak? Trends Parasitol 19(12):571–574.  https://doi.org/10.1016/j.pt.2003.10.006 CrossRefPubMedGoogle Scholar
  40. Silva LK, Liu S, Blanton RE (2005) Microsatellite analysis of pooled Schistosoma mansoni DNA: an approach for studies of parasite populations. Parasitology 132:331–338.  https://doi.org/10.1017/S0031182005009066 CrossRefPubMedGoogle Scholar
  41. Standley CJ, Kabatereine NB, Lange CN et al (2010) Molecular epidemiology and phylogeography of Schistosoma mansoni around Lake Victoria. Parasitology 137:1937–1949.  https://doi.org/10.1017/S0031182010000788 CrossRefPubMedGoogle Scholar
  42. Stohler R, Curtis J, Minchella DJ (2004) A comparison of microsatellite polymorphism and heterozygosity among field and laboratory populations of Schistosoma mansoni. Int J Parasitol 34:595–601.  https://doi.org/10.1016/j.ijpara.2003.11.026 CrossRefPubMedGoogle Scholar
  43. Tavilire HF, Blouin MS, Steinauer ML (2015) Genotypic variation in host response to infection affects parasite reproductive rate. Int J Parasitol 46:123–131.  https://doi.org/10.1016/j.ijpara.2015.10.001 CrossRefGoogle Scholar
  44. Thiele EA, Minchella DJ (2013) Molecular assessment of trematode co-infection and intraspecific competition in molluscan intermediate hosts. Mol Biochem Parasitol 187:52–59.  https://doi.org/10.1016/j.molbiopara.2012.12.003 CrossRefPubMedGoogle Scholar
  45. Thiele EA, Sorensen RE, Gazzinelli A, Minchella DJ (2008) Genetic diversity and population structuring of Schistosoma mansoni in a Brazilian village. Int J Parasitol 38:389–399.  https://doi.org/10.1016/j.ijpara.2007.07.011 CrossRefPubMedGoogle Scholar
  46. Valentim CLL, LoVerde PT, Anderson TJC, Criscione CD (2009) Efficient genotyping of Schistosoma mansoni miracidia following whole genome amplification. Mol Biochem Parasitol 166:81–84.  https://doi.org/10.1016/j.molbiopara.2009.02.010 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Van Rooij JM, Bruggemann JH, Videler JJ, Breeman AM (1995) Plastic growth of the herbivorous reef fish Sparisoma viride: field evidence for a trade-off between growth and reproduction. MEPS 122:93–105CrossRefGoogle Scholar
  48. 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 266:391–396.  https://doi.org/10.1098/rspb.1999.0650 CrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  • A. M. Gleichsner
    • 1
    • 2
  • K. Reinhart
    • 1
  • D. J. Minchella
    • 1
  1. 1.Department of Biological SciencesPurdue UniversityWest LafayetteUSA
  2. 2.Department of Biological SciencesState University of New York, College at PlattsburghPlattsburghUSA

Personalised recommendations