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Within-host interference competition can prevent invasion of rare parasites

Published online by Cambridge University Press:  15 May 2017

Benjamin J. Z. Quigley ,
Sam P. Brown ,
Helen C. Leggett ,
Pauline D. Scanlan  and
Angus Buckling
Benjamin J. Z. Quigley*
Affiliation:
Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK
Sam P. Brown
Affiliation:
School of Biology, Georgia Institute of Technology, 311 Ferst Drive, Atlanta, Georgia 30332-0230, USA
Helen C. Leggett
Affiliation:
Department of Genetics, University of Cambridge, Cambridge CB2 3EH, UK
Pauline D. Scanlan
Affiliation:
APC Microbiome Institute, University College Cork, T12 YT20, Ireland
Angus Buckling
Affiliation:
Department of Biosciences, University of Exeter, Penryn, Cornwall TR10 9EX, UK
*
Author for correspondence: Benjamin J. Z. Quigley, E-mail: benjaminjzq@gmail.com
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Abstract

Competition between parasite species or genotypes can play an important role in the establishment of parasites in new host populations. Here, we investigate a mechanism by which a rare parasite is unable to establish itself in a host population if a common resident parasite is already present (a ‘priority effect’). We develop a simple epidemiological model and show that a rare parasite genotype is unable to invade if coinfecting parasite genotypes inhibit each other's transmission more than expected from simple resource partitioning. This is because a rare parasite is more likely to be in multiply-infected hosts than the common genotype, and hence more likely to pay the cost of reduced transmission. Experiments competing interfering clones of bacteriophage infecting a bacterium support the model prediction that the clones are unable to invade each other from rare. We briefly discuss the implications of these results for host-parasite ecology and (co)evolution.

Keywords

Multiplicity of infection (MOI)interference competitionpositive frequency dependencebacteriaphage
Type
Research Article
Information
Parasitology , Volume 145 , Issue 6 , May 2018 , pp. 770 - 774
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Copyright
Copyright © Cambridge University Press 2017 

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References

Balmer, O, et al. (2009) Intraspecific competition between co-infecting parasite strains enhances host survival in African trypanosomes. Ecology 90, 3367–3378.CrossRefGoogle ScholarPubMed
Benmayor, R, et al. (2009) Host mixing and disease emergence. Current Biology 19, 764–767.CrossRefGoogle ScholarPubMed
Buckling, A and Brockhurst, MA (2008) Kin selection and the evolution of virulence. Heredity 100, 484–488.CrossRefGoogle ScholarPubMed
Buckling, A and Rainey, PB (2002) Antagonistic coevolution between a bacterium and a bacteriophage. Proceedings of the Royal Society B 269, 931–936.CrossRefGoogle Scholar
Brown, S, Hochberg, M and Grenfell, B (2002) Does multiple infection select for raised virulence? Trends in Microbiology 10, 401–405.CrossRefGoogle ScholarPubMed
Connell, JH and Slatyer, RO (1977) Mechanisms of succession in natural communities and their role in community stability and organization. American Naturalist 111, 1119–1144.CrossRefGoogle Scholar
Cox, F (2001) Concomitant infections, parasites and immune responses. Parasitology 122, S23–S38.CrossRefGoogle ScholarPubMed
Dittmar, D, Castro, A and Haines, H (1982) Demonstration of interference between dengue virus types in cultured mosquito cells using monoclonal antibody probes. Journal of General Virology 59, 273–282.CrossRefGoogle ScholarPubMed
Dobson, AP (1985) The population dynamics of competition between parasites. Parasitology 91, 317–347.CrossRefGoogle ScholarPubMed
Eswarappa, SM, Estrela, S and Brown, SP (2012) Within-host dynamics of multi-species infections: facilitation, competition and virulence. PloS ONE 7, e38730.CrossRefGoogle ScholarPubMed
Fenton, A (2008) Worms and germs: the population dynamic consequences of microparasite-macroparasite co-infection. Parasitology 135, 1545–1560.CrossRefGoogle ScholarPubMed
Futuyma, D and Moreno, G (1988) The evolution of ecological specialization. Annual Review of Ecology and Systematics 19, 207–233.CrossRefGoogle Scholar
Gandon, S, van Baalen, M and Jansen, VAA (2002) The evolution of parasite virulence, superinfection, and host resistance. American Naturalist 159, 658–669.CrossRefGoogle ScholarPubMed
Gomez, P, Ashby, B and Buckling, A (2015) Population mixing promotes arms race host-parasite coevolution. Proceedings of the Royal Society B 282, 2297.Google ScholarPubMed
Gómez, P, et al. (2016) Local adaptation of a bacterium is as important as its presence in structuring a natural microbial community. Nature Communications 7, 12453.CrossRefGoogle ScholarPubMed
Graham, AL (2008) Ecological rules governing helminth-microparasite coinfection. Proceedings of the National Academy of Sciences USA 105, 566–570.CrossRefGoogle ScholarPubMed
Gupta, S, Swinton, J and Anderson, RM (1994) Theoretical studies of the effects of heterogeneity in the parasite population on the transmission dynamics of malaria. Proceedings of the Royal Society B 256, 231–238.Google ScholarPubMed
Hart, AR and Cloyd, MW (1990) Interference patterns of human immunodeficiency viruses HIV-1 and HIV-2. Virology 177, 1–10.CrossRefGoogle ScholarPubMed
Heineman, RH, Springman, R and Bull, JJ (2008) Optimal foraging by bacteriophages through host avoidance. American Naturalist 171, E149–E157.CrossRefGoogle ScholarPubMed
Hoverman, JT, Hoye, BJ and Johnson, PTJ (2013) Does timing matter? How priority effects influence the outcome of parasite interactions within hosts. Oecologia 173, 1471–1480.CrossRefGoogle ScholarPubMed
Inglis, RF, et al. (2009) Spite and virulence in the bacterium Pseudomonas aeruginosa. Proceedings of the National Academy of Sciences of the United States of America 106, 5703–5707.CrossRefGoogle ScholarPubMed
Kawecki, TJ (1998) Red Queen meets Santa Rosalia: Arms Races and the evolution of host specialization in organisms with parasitic lifestyles. American Naturalist 152, 635–651.CrossRefGoogle ScholarPubMed
Keeling, MJ and Rohani, P (2008) Modeling Infectious Diseases in Humans and Animals. Princeton, NJ: Princeton University Press.CrossRefGoogle Scholar
Leggett, HC, et al. (2013 a). Experimental evolution of adaptive phenotypic plasticity in a parasite. Current Biology 23, 139–142.CrossRefGoogle Scholar
Leggett, HC, et al. (2013 b). Generalism and the evolution of parasite virulence. Trends in Ecology and Evolution 28, 592–596.CrossRefGoogle ScholarPubMed
Leggett, HC, et al. (2017) Fast-killing parasites can be favoured in spatially structured populations. Philosophical Transactions of the Royal Society B, 372, 20160096.CrossRefGoogle ScholarPubMed
Lello, J, et al. (2004) Competition and mutualism among the gut helminths of a mammalian host. Nature 428, 840–844.CrossRefGoogle ScholarPubMed
Lenski, R, et al. (1991) Long-term experimental evolution in Escherichia Coli .1. adaptation and divergence during 2,000 generations. American Naturalist 138, 1315–1341.CrossRefGoogle Scholar
Mideo, N (2009) Parasite adaptations to within-host competition. Trends in Parasitology 25, 261–268.CrossRefGoogle ScholarPubMed
Morgan, AD, Gandon, S and Buckling, A (2005) The effect of migration on local adaptation in a coevolving host-parasite system. Nature 437, 253–256.CrossRefGoogle Scholar
Onderdonk, A, et al. (1981) Competition between congenic Escherichia coli K-12 strains in vivo. Infection and Immunity 32, 74–79.CrossRefGoogle ScholarPubMed
Pedersen, AB and Fenton, A (2007) Emphasizing the ecology in parasite community ecology. Trends in Ecology and Evolution 22, 133–139.CrossRefGoogle ScholarPubMed
Poullain, V, et al. (2008) The evolution of specificity in evolving and co-evolving antagonistic interactions between a bacteria and its phage. Evolution 62, 1–11.Google Scholar
Ramiro, RS, et al. (2016) Facilitation through altered resource availability in a mixed-species rodent malaria infection. Ecology Letters 19, 1041–1050.CrossRefGoogle Scholar
Read, AF (2001) The ecology of genetically diverse infections. Science 292, 1099–1102.CrossRefGoogle ScholarPubMed
Roberts, M and Dobson, AP (1995) The population dynamics of communities of parasitic helminths. Mathematical Bioscience 126, 191–215.CrossRefGoogle ScholarPubMed
Scanlan, P, et al. (2011) Genetic basis of infectivity evolution in a bacteriophage. Molecular Ecology 20, 981–989.CrossRefGoogle Scholar
Shrestha, S, et al. (2013) Identifying the interaction between influenza and pneumococcal pneumonia using incidence data. Science Translational Medicine 5, 191ra84.CrossRefGoogle ScholarPubMed
Sugita, K (1981) Interference between virulent and avirulent strains of Sendai virus. Journal of General Virology 55, 95–107.CrossRefGoogle ScholarPubMed
Sutherland, JP (1974) Multiple stable points in natural communities. American Naturalist 108, 859–873.CrossRefGoogle Scholar
Telfer, S, et al. (2010) Species interactions in a parasite community drive infection risk in a wildlife population. Science 330, 243–246.CrossRefGoogle Scholar
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