Co-infection alters population dynamics of infectious disease

Nature Communications

Volumn 6, Issue , 2015, Pages

  Susi, Hanna ^a   Barrès, Benoit ^a   Vale, Pedro F ^b   Laine, Anna Liisa ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GENOTYPE; HERB; INFECTIOUS DISEASE; PATHOGEN; POPULATION DYNAMICS;

ARTICLE; CONTROLLED STUDY; DISEASE TRANSMISSION; GENOTYPE; MIXED INFECTION; NONHUMAN; PLANTAGO LANCEOLATA; PODOSPHAERA; PODOSPHAERA PLANTAGINIS; POPULATION DYNAMICS; PROPAGULE; ASCOMYCETES; BAYES THEOREM; COMMUNICABLE DISEASE; FUNGUS SPORE; HOST PATHOGEN INTERACTION; MICROBIOLOGY; PHENOTYPE; PHYSIOLOGY; PLANT DISEASE; PLANTAGO; STATISTICAL MODEL; STATISTICS AND NUMERICAL DATA;

PLANTAGO LANCEOLATA; PODOSPHAERA PLANTAGINIS;

ASCOMYCOTA; BAYES THEOREM; COINFECTION; COMMUNICABLE DISEASES; HOST-PATHOGEN INTERACTIONS; LINEAR MODELS; PHENOTYPE; PLANT DISEASES; PLANTAGO; POPULATION DYNAMICS; SPORES, FUNGAL;

EID: 84927160317     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6975     Document Type: Article

References (48)

1. Mideo, N., Alizon, S. & Day, T. Linking within- and between-host dynamics in the evolutionary epidemiology of infectious diseases. Trends Ecol. Evol. 23, 511-517 (2008).
2. Hamilton, W. D. Altruism and related phenomena, mainly in social insects. Annu. Rev. Ecol. Syst. 3, 192-232 (1972).
3. Levin, B. R. & Bull, J. J. Short-sighted evolution and the virulence of pathogenic microorganisms. Trends Microbiol. 2, 76-81 (1994).
4. Antia, R., Levin, B. R. & May, R. M. Within-host population dynamics and the evolution and maintenance of microparasite virulence. Am. Nat. 144, 457-472 (1994).
5. Criscione, C. D., Poulin, R. & Blouin, M. S. Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Mol. Ecol. 14, 2247-2257 (2005).
6. Lopez-Villavicencio, M. et al. Multiple infections by the anther smut pathogen are frequent and involve related strains. PLoS Pathog. 3, e176 (2007).
7. Schmid-Hempel, P. & Funk, C. R. The distribution of genotypes of the trypanosome parasite, Crithidia bombi, in populations of its host, Bombus terrestris. Parasitology 129, 147-158 (2004).
8. Tollenaere, C. et al. SNP Design from 454 sequencing of Podosphaera plantaginis transcriptome reveals a genetically diverse pathogen metapopulation with high levels of mixed-genotype infection. PLoS ONE 7, e52492 (2012).
9. Karvonen, A., Rellstab, C., Louhi, K.-R. & Jokela, J. Synchronous attack is advantageous: mixed genotype infections lead to higher infection success in trematode parasites. Proc. R. Soc. B 279, 171-176 (2012).
10. Lopez-Villavicencio, M. et al. Competition, cooperation among kin and virulence in multiple infections. Evolution 65, 1357-1366 (2011).
11. de Roode, J. C., Helinski, M. E. H., Anwar, M. A. & Read, A. F. Dynamics of multiple infection and within-host competition in genetically diverse malaria infections. Am. Nat. 166, 531-534 (2005).
12. Mideo, N. Parasite adaptations to within-host competition. Trends Parasitol. 25, 261-268 (2009).
13. de Roode, J. C. et al. Virulence and competitive ability in genetically diverse malaria infections. Proc. Natl Acad. Sci. USA 102, 7624-7628 (2005).
14. Laine, A.-L. Context-dependent effects of induced resistance under co-infection in a plant-pathogen interaction. Evol. Appl. 4, 696-707 (2011).
15. Choisy, M. & de Roode, J. C. Mixed infections and the evolution of virulence: effects of resource competition, parasite plasticity, and impaired host immunity. Am. Nat. 175, E105-E118 (2010).
16. Alizon, S. & van Baalen, M. Multiple infections, immune dynamics, and the evolution of virulence. Am. Nat. 172, E150-E168 (2008).
17. Telfer, S. et al. Species interactions in a parasite community drive infection risk in a wildlife population. Science 330, 243-246 (2010).
18. Jung, H. W., Tschaplinski, T. J., Wang, L., Glazebrook, J. & Greenberg, J. T. Priming in systemic plant immunity. Science 324, 89-91 (2009).
19. Ebert, D. & Bull, J. J. Challenging the trade-off model for the evolution of virulence: is virulence management feasible? Trends Microbiol. 11, 15-20 (2003).
20. Seabloom, E. W., Borer, E. T., Mitchell, C. E. & Power, A. G. Viral diversity and prevalence gradients in North American Pacific Coast grasslands. Ecology 91, 721-732 (2010).
21. Jousimo, J. et al. Ecological and evolutionary effects of fragmentation on infectious disease dynamics. Science 344, 1289-1293 (2014).
22. Laine, A. L. Resistance variation within and among host populations in a plant-pathogen metapopulation: implications for regional pathogen dynamics. J. Ecol. 92, 990-1000 (2004).
23. Laine, A. L. Pathogen fitness components and genotypes differ in their sensitivity to nutrient and temperature variation in a wild plant-pathogen association. J. Evol. Biol. 20, 2371-2378 (2007).
24. Laine, A. L. Spatial scale of local adaptation in a plant-pathogen metapopulation. J. Evol. Biol. 18, 930-938 (2005).
25. Matthews, L. & Woolhouse, M. New approaches to quantifying the spread of infection. Nat. Rev. Microbiol. 3, 529-536 (2005).
26. Laine, A. L. & Hanski, I. Large-scale spatial dynamics of a specialist plant pathogen in a fragmented landscape. J. Ecol. 94, 217-226 (2006).
27. Jones, J. D. G. & Dangl, J. L. The plant immune system. Nature 444, 323-329 (2006).
28. Lass, S. et al. Generating super-shedders: co-infection increases bacterial load and egg production of a gastrointestinal helminth. J. R. Soc. Interface 10, 20120588 (2013).
29. Paull, S. H. et al. From superspreaders to disease hotspots: linking transmission across hosts and space. Front. Ecol. Environ. 10, 75-82 (2012).
30. Lambrechts, L. et al. Impact of daily temperature fluctuations on dengue virus transmission by Aedes aegypti. Proc. Natl Acad. Sci. USA 108, 7460-7465 (2011).
31. Kilpatrick, A. M., Meola, M. A., Moudy, R. M. & Kramer, L. D. Temperature, viral genetics, and the transmission of West Nile virus by Culex pipiens mosquitoes. PLoS Pathog. 4, e1000092 (2008).
32. Fellous, S., Duncan, A. B., Quillery, E., Vale, P. F. & Kaltz, O. Genetic influence on disease spread following arrival of infected carriers. Ecol. Lett. 15, 186-192 (2012).
33. Vale, P. F., Choisy, M. & Little, T. J. Host nutrition alters the variance in parasite transmission potential. Biol Lett. 9, 20121145 (2013).
34. Ferrari, N., Cattadori, I. M., Nespereira, J., Rizzoli, A. & Hudson, P. J. The role of host sex in parasite dynamics: field experiments on the yellow-necked mouse Apodemus flavicollis. Ecol. Lett. 7, 88-94 (2004).
35. Perkins, S. E., Cattadori, I. M., Tagliapietra, V., Rizzoli, A. P. & Hudson, P. J. Empirical evidence for key hosts in persistence of a tick-borne disease. Int. J. Parasitol. 33, 909-917 (2003).
36. Vale, P., Fenton, A. & Brown, S. Limiting damage during infection: lessons from infection tolerance for novel therapeutics. PLoS Biol. 12, e1001769 (2014).
37. Wargo, A. R., Huijben, S., de Roode, J. C., Shepherd, J. & Read, A. F. Competitive release and facilitation of drug-resistant parasites after therapeutic chemotherapy in a rodent malaria model. Proc. Natl Acad. Sci. USA 104, 19914-19919 (2007).
38. Lloyd-Smith, J. O., Schreiber, S. J., Kopp, P. E. & Getz, W. M. Superspreading and the effect of individual variation on disease emergence. Nature 438, 355-359 (2005).
39. Ojanen, S. P., Nieminen, M., Meyke, E., Pöyry, J. & Hanski, I. Long-term metapopulation study of the Glanville fritillary butterfly (Melitaea cinxia): survey methods, data management, and long-term population trends. Ecol. Evol. 3, 3713-3737 (2013).
40. Ovaskainen, O. & Laine, A. L. Inferring evolutionary signals from ecological data in a plant-pathogen metapopulation. Ecology 87, 880-891 (2006).
41. Nicot, P. C., Bardin, M. & Dik, A. J. in The Powdery Mildews: A Comprehensive Treatise (eds Bélanger, R. R., Bushnell, R. B., Dik, A. J. & Carver, T. J. W.) 83-99 (American Phytopathological Society, 2002).
42. Bevan, J. R., Crute, I. R. & Clarke, D. D. Diversity and variation in expression of resistance to Erysiphe fischeri in Senecio vulgaris. Plant Pathol. 42, 647-653 (1993).
43. Littell, R. C., Milliken, G. A., Stroup, W. W., Wolfinger, R. D. & Schabenberger, O. SAS for Mixed Models 2nd edn (SAS Institute Inc., 2006).
44. SAS Institute Inc. System Requirements for SAS 9.2 Foundation for Microsoft Windows (SAS Institute Inc., 2011).
45. Baddeley, A. & Turner, R. Spatstat: an R package for analyzing spatial point patterns. J. Stat.Softw. 12, 1-42 (2005).
46. Laine, A. L. Evolution of host resistance: looking for coevolutionary hotspots at small spatial scales. Proc. R. Soc. B 273, 267-273 (2006).
47. R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2014).
48. Bates, D. M., Maechler, M. & Bolker, B. lme4: linear mixed-effects models using S4 classes. R package version 1.0-6 (2014).