Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-20T06:34:45.997Z Has data issue: false hasContentIssue false
  • English
  • Français

Can host ecology and kin selection predict parasite virulence?

Published online by Cambridge University Press:  24 April 2014

ALYSSA M. GLEICHSNER  and
DENNIS J. MINCHELLA
ALYSSA M. GLEICHSNER*
Affiliation:
Department of Biological Sciences, Purdue University, 915 West State Street, West Lafayette, IN 47907, USA
DENNIS J. MINCHELLA
Affiliation:
Department of Biological Sciences, Purdue University, 915 West State Street, West Lafayette, IN 47907, USA
*
* Corresponding author: Purdue University, 915 West State Street, West Lafayette, IN 47907, USA. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Parasite virulence, or the damage a parasite does to its host, is measured in terms of both host costs (reductions in host growth, reproduction and survival) and parasite benefits (increased transmission and parasite numbers) in the literature. Much work has shown that ecological and genetic factors can be strong selective forces in virulence evolution. This review uses kin selection theory to explore how variations in host ecological parameters impact the genetic relatedness of parasite populations and thus virulence. We provide a broad overview of virulence and population genetics studies and then draw connections to existing knowledge about natural parasite populations. The impact of host movement (transporting parasites) and host resistance (filtering parasites) on the genetic structure and virulence of parasite populations is explored, and empirical studies of these factors using Plasmodium and trematode systems are proposed.

Keywords

Virulencekin selectionparasitehost movementresistance
Type
Review Article
Information
Parasitology , Volume 141 , Issue 8 , July 2014 , pp. 1018 - 1030
Check for updates
Copyright
Copyright © Cambridge University Press 2014 

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

Alizon, S. and Lion, S. (2011). Within-host parasite cooperation and the evolution of virulence. Proceedings of the Royal Society of London, Series B 278, 3738–3747. doi: 10.1098/rspb.2011.0471.Google Scholar
Alizon, S., de Roode, J. C. and Michalakis, Y. (2013). Multiple infections and the evolution of virulence. Ecology Letters 16, 556–567. doi: 10.1111/ele.12076.CrossRefGoogle ScholarPubMed
Allan, B. F., Keesing, F. and Ostfeld, R. S. (2003). Effect of forest fragmentation on lyme disease risk. Conservation Biology 17, 267–272. doi: 10.1046/j.1523-1739.2003.01260.x.CrossRefGoogle Scholar
Anderson, R. M. and May, R. M. (1981). The population dynamics of microparasites and their invertebrate hosts. Philosophical Transactions of the Royal Society of London 291, 451–524.Google Scholar
Anderson, T. J. C., Haubold, B., Williams, J. T., Estrada-Franco, J. G., Richardson, L., Mollinedo, R., Bockarie, M., Mokili, J., Mharakurwa, S., French, N., Witworth, J., Velez, I. D., Brockman, A. H., Nosten, F., Ferreira, M. U. and Day, K. P. (2000). Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum . Molecular Biology and Evolution 17, 1467–1482.CrossRefGoogle ScholarPubMed
Andrén, H. (1994). Effects of habitat fragmentation on birds and mammals in landscapes with different proportions of suitable habitat: a review. Oikos 71, 355–366.Google Scholar
Archie, E. A., Luikard, G. and Ezenwa, V. O. (2009). Infecting epidemiology with genetics: a new frontier in disease ecology. Trends in Ecology and Evolution 24, 21–30. doi: 10.1016/j.tree.2008.08.008.Google Scholar
Ballabeni, P. and Ward, P. I. (1993). Local adaptation of the trematode Diplostomum phoxini to the European minnow Phoxinus phoxinus, its second intermediate host. Functional Ecology 7, 84–90.Google Scholar
Barrett, L. G., Bell, T., Dwyer, G. and Bergelson, J. (2011). Cheating, trade-offs and the evolution of aggressiveness in a natural pathogen population. Ecology Letters 14, 1149–1157. doi: 10.1111/j.1461-0248.2011.01687.x.Google Scholar
Bartholomew, J. L. (1998). Host resistance to infection by the myxosporean parasite Ceratomyxa shasta: a review. Journal of Aquatic Animal Health 10, 112–120.2.0.CO;2>CrossRefGoogle Scholar
Bashey, F., Young, S. K., Hawlena, H. and Lively, C. M. (2012). Spiteful interactions between sympatric natural isolates of Xenorhabdus bovienii benefit kin and reduce virulence. Journal of Evolutionary Biology 25, 431–437. doi: 10.1111/j.1420-9101.2011.02441.x.Google Scholar
Ben-Ami, F., Mouton, L. and Ebert, D. (2008). The effects of multiple infections on the expression and evolution of virulence in a Daphnia-endoparasite system. Evolution 62, 1700–1711. doi: 10.1111/j.1558-5646.2008.00391.x.Google Scholar
Bayne, C. (2009). Successful parasitism of vector snail Biomphalaria glabrata by the human blood fluke (trematode) Schistosoma mansoni: a 2009 assessment. Molecular and Biochemical Parasitology 165, 8–18. doi: 10.1016/j.molbiopara.2009.01.005.Google Scholar
Bell, A. S., De Roode, J. C., Sim, D. and Read, A. F. (2006). Within-host competition in genetically diverse malaria infections: parasite virulence and competitive success. Evolution 60, 1358–1371. doi: 10.1111/j.0014-3820.2006.tb01215.x.Google Scholar
Best, A., Webb, S., White, A. and Boots, M. (2011). Host resistance and coevolution in spatially structured populations. Proceedings of the Royal Society B: Biological Sciences 278, 2216–2222. doi: 10.1098/rspb.2010.1978.CrossRefGoogle ScholarPubMed
Blouin, M. S., Dame, J. B., Tarrant, C. A. and Coutney, C. H. (1992). Unusual populations genetics of a parasitic nematode: mtDNA variation within and among populations. Evolution 46, 470–476.Google Scholar
Blouin, M. S., Yowell, C. A., Courtney, C. H. and Dame, J. B. (1995). Host movement and the genetic structure of populations of parasitic nematodes. Genetics 141, 1007–1014.CrossRefGoogle ScholarPubMed
Boots, M. and Mealor, M. (2007). Local interactions select for lower pathogen infectivity. Science 315, 1284–1286. doi: 10.1126/science.1137126.Google Scholar
Boots, M. and Sasaki, A. (1999). ‘Small worlds’ and the evolution of virulence: infection occurs locally and at a distance. Proceedings of the Royal Society B: Biological Sciences 266, 1933–1938. doi: 10.1098/rspb.1999.0869.Google Scholar
Blanchet, S., Rey, O., Etienne, R., Lek, S. and Loot, G. (2010). Species-specific responses to landscape fragmentation: implications for management strategies. Evolutionary Applications 3, 291–304. doi: 10.1111/j.1752-4571.2009.00110.x.Google Scholar
Buckling, A. and Brockhurst, M. A. (2008). Kin selection and the evolution of virulence. Heredity 100, 484–488. doi: 10.1038/sj.hdy.6801093.CrossRefGoogle ScholarPubMed
Campino, S., Auburn, S., Kivinen, K., Zongo, I., Ouedraogo, J., Mangano, V., Djimde, A., Doumbo, O. K., Kiara, S. M., Nzila, A., Borrmann, S., Marsh, K., Michon, P., Mueller, I., Siba, P., Jiang, H., Su, X., Amaratunga, C., Socheat, D., Fairhurst, R. M., Imwong, M., Anderson, T., Nosten, F., White, N. H., Gwilliam, R., Deloukas, P., MacInnis, B., Newbold, C. I., Rockett, K., Clark, T. G. and Kwiatkowski, D. P. (2011). Population genetic analysis of Plasmodium falciparum parasites using a customized Illumina GoldenGate genotyping assay. PLoS One 6. doi: 10.1371/journal.pone.0020251.Google Scholar
Choisy, M. and de Roode, J. (2010). Mixed infections and the evolution of virulence: effects of resource competition, parasite plasticity, and impaired host immunity. American Naturalist 175, 105–118. doi: 10.1086/651587.Google Scholar
Coluzzi, M., Petrarca, V. and Di Deco, M. A. (1985). Chromosomal inversion intergradation and incipient speciation in Anopheles gambiae . Bollettino di Zoologia 52, 45–63. doi: 10.1080/11250008509440343.Google Scholar
Combes, C. (2001). Parasitism: the Ecology and Evolution of Intimate Interactions. University of Chicago Press, Chicago, IL, USA.Google Scholar
Cooper, L. A., Richards, C. S., Lewis, F. A. and Minchella, D. J. (1994). Schistosoma mansoni: relationship between low fecundity and reduced susceptibility to parasite infection in the snail Biomphalaria glabrata . Experimental Parasitology 79, 21–28.CrossRefGoogle ScholarPubMed
Cotner, L. A. and Schooley, R. L. (2011). Habitat occupancy by riparian muskrats reveals tolerance to urbanization and invasive vegetation. Journal of Wildlife Management 75, 1637–1645. doi: 10.1002/jwmg.197.Google Scholar
Criscione, C. D. and Blouin, M. S. (2005). Effective sizes of macroparasite populations: a conceptual model. Trends in Parasitology 21, 212–217. doi: 10.1016/j.pt.2005.03.002.Google Scholar
Cristóbal-Azkarate, J., Hervier, B., Vegas-Carrillo, S., Osorio-Sarabia, D., Rodríquez-Luna, E. and Veà, J. J. (2010). Parasitic infections of three Mexican howler monkey groups (Alouatta palliata mexicana) living in forest fragments in Mexico. Primates 51, 231–239. doi: 10.1007/s10329-010-0193-7.CrossRefGoogle ScholarPubMed
Curtis, J., Sorensen, R. E. and Minchella, D. J. (2002). Schistosome genetic diversity: the implications of population structure as detected with microsatellite markers. Parasitology 125, 51–59. doi: 10.1017/S0031182002002020.Google Scholar
Dabo, A., Durand, P., Morand, S., Diakite, M., Langand, J., Imbert-Establet, D., Doumbo, O. and Jourdane, J. (1997). Distribution and genetic diversity of Schistosoma haematobium within its bulinid intermediate hosts in Mali. Acta Tropica 66, 15–26.Google Scholar
Davies, C. M., Webster, J. P. and Woolhouse, M. E. J. (2001). Trade-offs in the evolution of virulence in an indirectly transmitted macroparasite. Proceedings of the Royal Society of London Biology 268, 251–257. doi: 10.1098/rspb.2000.1367.Google Scholar
Davies, C. M., Fairbrother, E. and Webster, J. P. (2002). Mixed strain schistosome infections of snails and the evolution of parasite virulence. Parasitology 124, 31–38. doi: http://dx.doi.org/10.1017/S0031182001008873.Google Scholar
Decaestecker, E., Gaba, S., Raeymaekers, J. A. M., Stoks, R., Van Kerckhoven, L., Ebert, D. and De Meester, L. (2007). Host-parasite ‘Red Queen’ dynamics archived in pond sediment. Nature 450, 870–874. doi: 10.1038/nature06291.Google Scholar
de Roode, J. C. and Altizer, S. (2009). Virulence-transmission relationships in natural populations of monarch butterflies. Evolution 64, 502–514. doi: 10.1111/j.1558-5646.2009.00845.x.Google Scholar
de Roode, J. C., Culleton, R., Bell, A. S. and Read, A. F. (2004). Competitive release of drug resistance following drug treatment of mixed Plasmodium chabaudi infections. Malaria Journal 3, 33. doi: 10.1186/1475–2875-3-33.Google Scholar
de Roode, J. C., Pansini, R., Cheesman, S. J., Helinski, M. E. H., Huijben, S., Wargo, A. R., Bell, A. S., Chan, B. H. K., Walliker, D. and Read, A. F. (2005). Virulence and competitive ability in genetically diverse malaria infections. Proceedings of the National Academy of Sciences USA 102, 7624–7628. doi: 10.1073/pnas.0500078102.Google Scholar
Detwiler, J. T. (2010). The molecular ecology of echinostome trematodes: elucidating the phylogenetics and transmission dynamics of a freshwater helminth parasite. Doctoral dissertation. Purdue University, West Lafayette, IN, USA.Google Scholar
Detwiler, J. T., Bos, D. H. and Minchella, D. J. (2010). Revealing the secret lives of cryptic species: examining the phylogenetic relationships of echinostome parasites in North America. Molecular Phylogenetics and Evolution 55, 611–620. doi: 10.1016/j.ympev.2010.01.004.Google Scholar
Detwiler, J. T., Zajac, A., Minchella, D. J. and Belden, L. K. (2012). Revealing cryptic diversity in a definitive host: echinostomes in muskrats. Journal of Parasitology 98, 1148–1155. doi: http://dx.doi.org/10.1645/GE-3117.1.Google Scholar
Duffy, M. A. and Sivars-Becker, L. (2007). Rapid evolution and ecological host-parasite dynamics. Ecology Letters 10, 44–53. doi: 10.1111/j.1461-0248.2006.00995.x.Google Scholar
Duncan, A. B., Fellous, S. and Kaltz, O. (2011). Reverse evolution: selection against costly resistance in disease-free microcosm populations of Paramecium caudatum . Evolution 65, 3462–3474. doi: 10.1111/j.1558-5646.2011.01388.x.Google Scholar
Ewald, P. W. (2004). Evolution of virulence. Infectious Disease Clinics of North America 18, 1–15. doi: 10.1016/S0891-5520(03)00099-0.Google Scholar
Fahrig, L. (2003). Effects of habitat fragmentation on biodiversity. Annual Review of Ecology, Evolution, and Systematics 34, 487–515.CrossRefGoogle Scholar
Finkelman, F. D., Shea-Donohue, T., Goldhill, J., Sullivan, C. A., Morris, S. C., Madden, K. B., Gause, W. C. and Urban, J. F. Jr. (1997). Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annual Review of Immunology 15, 505–533.Google Scholar
Fournet, S., Kerlan, M. C., Renault, L., Dantec, J. P., Rouaux, C. and Montarry, J. (2013). Selection of nematodes by resistant plants has implications for local adaptation and cross-virulence. Plant Pathology 62, 184–193. doi: 10.1111/j.1365-3059.2012.02617.x.Google Scholar
Gandon, S. and Michalakis, Y. (2000). Evolution of parasite virulence against qualitative and quantitative host resistance. Proceedings of the Royal Society of London Series B 267, 985–990. doi: 10.1098/rspb.2000.1100.Google Scholar
Gardner, M. J., Hall, N., Fung, E., White, O., Berriman, M., Hyman, R. W., Carlton, J. M., Pain, A., Nelson, K. E., Bowman, S., Paulsen, I. T., James, K., Eisen, J. A., Rutherford, K., Salzberg, S. L., Craig, A., Kyes, S., Chan, M., Nene, V., Shallom, S. J., Suh, B., Peterson, J., Angiuoli, S., Pertea, M., Allen, J., Selengut, J., Haft, D., Mather, M. W., Vaidya, A. B., Martin, D. M. A., Fairlamb, A. H., Fraunholz, M. J., Roos, D. S., Ralph, S. A., McFadden, G. I., Cummings, L. M., Subramanian, G. M., Mungall, C., Venter, C. J., Carucci, D. J., Hoffman, S. L., Newbold, C., Davis, R. W., Fraser, C. M. and Barrell, B. (2002). Genome sequence of the human malaria parasite Plasmodium falciparum . Nature 419, 498–511. doi: 10.1038/nature01097.Google Scholar
Gazzinelli, R. T., Ropert, C. and Campos, M. A. (2004). Role of Toll/interleukin-1 receptor signaling pathway in host resistance and pathogenesis during infection with protozoan parasites. Immunological Reviews 201, 9–25. doi: 10.1111/j.0105–2896.2004.00174.x.Google Scholar
Gillespie, T. and Chapman, C. (2008). Forest fragmentation, the decline of an endangered primate, and changes in host-parasite interactions relative to an unfragmented forest. American Journal of Primatology 70, 222–230. doi: 10.1002/ajp.20475.Google Scholar
Gomez-Diaz, E., Boulinier, T., Sertour, N., Cornet, M., Ferquel, E. and McCoy, K. D. (2011). Genetic structure of marine Borrelia garinii and population admixture with the terrestrial cycle of Lyme borreliosis. Environmental Microbiology 13, 2453–2467. doi: 10.1111/j.1462-2920.2011.02515.x.Google Scholar
Gower, C. M. and Webster, J. P. (2005). Intraspecific competition and the evolution of virulence in a parasitic trematode. Evolution 59, 544–553. doi: 10.1111/j.0014-3820.2005.tb01014.x.Google Scholar
Gower, C. W., Gouvras, A. N., Lamberton, P. H. I., Deol, A., Shrivastava, J., Mutombo, P. N., Mbuy, J. V., Norton, A. J., Webster, B. L., Stothard, J. R., Garba, A., Lamine, M. S., Kariuki, C., Lange, C. N., Mkoji, G. M., Kabatereine, N. B., Gabrielli, A. F., Rudge, J. W., Fenwick, A., Sacko, M., Dembele, R., Lwambo, N. J. S., Tchuente, L. T., Rollinson, D. and Webster, J. P. (2013). Population genetic structure of Schistosoma mansoni and Schistosoma haematobium from across six sub-Saharan African countries: implications for epidemiology, evolution and control. Acta Tropica 128, 261–274. doi: 10.1016/j.actatropica.2012.09.014.Google Scholar
Grech, K., Watt, K. and Read, A. F. (2006). Host-parasite interactions for virulence and resistance in a malaria model system. Journal of Evolutionary Biology 19, 1620–1630. doi: 10.1111/j.1420-9101.2006.01116.x.Google Scholar
Gregory, R. D. (1990). Parasites and host geographic range as illustrated by waterfowl. Functional Ecology 4, 645–654.Google Scholar
Greischar, M. A. and Koskella, B. (2007). A synthesis of experimental work on parasite local adaptation. Ecology Letters 10, 418–434. doi: 10.1111/j.1461-0248.2007.01028.x.CrossRefGoogle ScholarPubMed
Hall, M. D. and Ebert, D. (2012). Disentangling the influence of parasite genotype, host genotype, and maternal environment on different stages of bacterial infection in Daphnia magna . Proceedings of the Royal Society B: Biological Sciences 279, 3176–3183. doi: 10.1098/rspb.2012.0509.Google Scholar
Hall, S. R., Smyth, R., Becker, C. R., Duffy, M. A., Knight, C. J., MacIntyre, S., Tessier, A. J. and Cáceres, C. E. (2010). Why are Daphnia in some lakes sicker? Disease ecology, habitat structure, and the plankton. BioScience 60, 363–375. doi: http://dx.doi.org/10.1525/bio.2010.60.5.6.Google Scholar
Hamilton, W. D. (1964). The genetical evolution of social behavior. Journal of Theoretical Biology 7, 1–16.Google Scholar
Harris, C., Lambrechts, L., Rousset, F., Abate, L., Nsango, S. E., Fontenille, D., Morlais, I. and Cohuet, A. (2010). Polymorphisms in Anopheles gambiae immune genes associated with natural resistance to Plasmodium falciparum . PLoS Pathogens 6. doi: 10.1371/journal.ppat.1001112.Google Scholar
Hoa, T. T. T., Zwart, M. P., Phuong, N. T., Oanh, D. T. H., de Jong, M. C. M. and Vlak, J. M. (2011). Mixed-genotype white spot syndrome virus infections of shrimp are inversely correlated with disease outbreaks in ponds. Journal of General Virology 92, 675–680. doi: 10.1099/vir0.026351-0.Google Scholar
Holt, R. A., Subramanian, G. M., Halpern, A., Sutton, G. G., Charlab, R., Nusskern, D. R., Wincker, P., Clark, A. G., Ribeiro, J. M. C., Wides, R., Salzberg, S. L., Loftus, B., Yandell, M., Majoros, W. H., Rusch, D. B., Lai, Z., Kraft, C. L., Abril, J. F., Anthouard, V., Arensburger, P., Atkinson, P. W., Baden, H., de Berardinis, V., Baldwin, D., Benes, Vl., Biedler, J., Blass, C., Bolanos, R., Boscus, D., Barnstead, M., Cai, S., Center, A., Chatuverdi, K., Christophides, G. K., Chrystal, M. A., Clamp, M., Cravchik, A., Curwen, V., Dana, A., Delcher, A., Dew, I., Evans, C. A., Flanigan, M., Grundschober-Freimoser, A., Friedli, L., Gu, Z., Guan, P., Guigo, R., Hillenmeyer, M. E., Hladun, S. L., Hogan, J. R., Hong, Y. S., Hoover, J., Jaillon, O., Ke, Z., Kodira, C., Kokoza, E., Koutsos, A., Letunic, I., Levitsky, A., Liang, Y., Lin, J., Lobo, N. F., Lopez, J. R., Malek, J. A., McIntosh, T. C., Meister, S., Miller, J., Mobarry, C., Mongin, E., Murphy, S. D., O'Brochta, D. A., Pfannkoch, C., Qi, R., Regier, M. A., Remington, K., Shao, H., Sharakhova, M. V., Sitter, C. D., Shetty, J., Smith, T. J., Strong, R., Sun, J., Thomasova, D., Ton, L. Q., Topalis, P., Tu, Z., Unger, M. F., Walenz, B., Wang, A., Wang, J., Wang, M., Wang, X., Woodford, K. J., Wortman, J. R., Wu, M., Yao, A., Zdobnov, E. M., Zhang, H., Zhao, Q., Zhao, S., Zhu, S. C., Zhimulev, I., Coluzzi, M., della Torre, A., Roth, C. W., Louis, C., Kalush, F., Mural, R. J., Myers, E. W., Adams, M. D., Smith, H. O., Broder, S., Gardner, M. J., Fraser, C. M., Birney, E., Bork, P., Brey, P. T., Venter, J. C., Weissenbach, J., Kafatos, F. C., Collins, F. H. and Hoffman, S. L. (2002). The genome of the malaria mosquito Anopheles gambiae . Science 4, 129–149. doi: 10.1126/science.1076181.CrossRefGoogle Scholar
Jager, I. and Schjorring, S. (2006). Multiple infections: relatedness and time between infections affect the establishment and growth of the cestode Schistocephalus solidus in its stickleback host. Evolution 60, 616–622. doi: 10.1111/j.0014-3820.2006.tb01141.x.Google Scholar
Jankowski, M. D., Williams, C. J., Fair, J. M. and Owen, J. C. (2013). Birds shed RNA-viruses according to the Pareto Principle. PLoS One 8. doi: 10.1371/journal.pone.0072611.Google Scholar
Johnson, P. T. J. and McKenzie, V. J. (2009). Effects of environmental change on helminth infections in amphibians: exploring the emergence of Ribeiroia and Echinostoma infections in North America. In The Biology of Echinostomes from the Molecule to the Community (ed. Toledo, R. and Fried, B.), pp. 1–32. Springer, New York, NY, USA.Google Scholar
Jones-Nelson, O., Thiele, E. A. and Minchella, D. J. (2011). Transmission dynamics of two strains of Schistosoma mansoni utilizing novel intermediate and definitive hosts. Parasitology Research 109, 675–687. doi: 10.1007/s00436-011-2299-2.Google Scholar
Jovani, R. and Tella, J. L. (2006). Parasite prevalence and sample size: misconceptions and solutions. Trends in Parasitology 22, 214–218. doi: 10.1016/j.pt.2006.02.011.Google Scholar
Kaltz, O. and Shykoff, J. (1998). Local adaptation in host-parasite systems. Heredity 81, 361–370. doi: 10.1046/j.1365-2540.1998.00435.x.Google Scholar
Karvonen, A., Rellstab, C., Louhi, K. and Jokela, J. (2011). Synchronous attack is advantageous: mixed genotype infections lead to higher infection success in trematode parasites. Proceedings of the Royal Society B: Biological Sciences 279, 171–176. doi: 10.1098/rspb.2011.0879.Google Scholar
Keeney, D. B., Waters, J. M. and Poulin, R. (2007). Clonal diversity of the marine trematode Maritrema novaezealandensis within intermediate hosts: the molecular ecology of parasite life cycles. Molecular Ecology 16, 431–439. doi: 10.111/j.1365-294X.2006.03143.x.Google Scholar
Keeney, D. B., Bryan-Walker, K., Khan, N., King, T. M. and Poulin, R. (2009 a). The influence of clonal diversity and intensity-dependence on trematode infections in an amphipod. Parasitology 136, 339–348. doi: 10.1017/S0031182008005416.Google Scholar
Keeney, D. B., King, T. M., Rowe, D. L. and Poulin, R. (2009 b). Contrasting mtDNA diversity and population structure in a direct developing marine gastropod and its trematode parasites. Molecular Ecology 18, 4591–4603. doi: 10.1111/j.1365-294X.2009.04388.x.Google Scholar
Kempf, F., De Meeus, T., Vaumourin, E., Noel, V., Taragel'ova, V., Plantard, O., Heylen, D. J. A., Eraud, C., Chevillon, C. and McCoy, K. D. (2011). Host races in Ixodes ricinus, the European vector of Lyme borreliosis. Infection, Genetics, and Evolution 11, 2043–2048. doi: 10.1016/j.meegid.2011.09.016.Google Scholar
Kerr, B., Neuhauser, C., Bohannan, B. J. M. and Dean, A. M. (2006). Local migration promotes competitive restraint in a host-pathogen ‘tragedy of the commons’. Nature 442, 75–78. doi: 10.1038/nature04864.Google Scholar
King, K. C. and Lively, C. M. (2012). Does genetic diversity limit disease spread in natural host populations? Heredity 109, 199–203. doi: 10.1038/hdy.2012.33.Google Scholar
Koskella, B., Lin, D. M., Buckling, A. and Thompson, J. N. (2012). The costs of evolving resistance in heterogeneous parasite environments. Proceedings of the Royal Society B: Biological Sciences 279, 1896–1903. doi: 10.1098/rspb.2011.2259.Google Scholar
Kuhls, K., Keilonat, L., Ochsenreither, S., Schaar, M., Schweynoch, C., Presber, W. and Schönian, G. (2007). Multilocus microsatellite typing (MLMT) reveals genetically isolated populations between and within the main endemic regions of visceral leishmaniasis. Microbes and Infection 9, 334–343. doi: 10.1016/j.micinf.2006.12.009.Google Scholar
Labbe, P., Vale, P. F. and Little, T. J. (2010). Successfully resisting a pathogen is rarely costly in Daphnia magna . BMC Evolutionary Biology 10, 355. doi: 10.1186/1471–2148-10-355.Google Scholar
Laine, A.-L., Burdon, J. J., Dodds, P. N. and Thrall, P. H. (2011). Spatial variation in disease resistance: from molecules to metapopulations. Journal of Ecology 99, 96–112. doi: 10.1111/j.1365-2745.2010.01738.x.Google Scholar
Langlois, J. P., Fahrig, L., Merriam, G. and Artsob, H. (2001). Landscape structure influences continental distribution of hantavirus in deer mice. Landscape Ecology 16, 225–266. doi: 10.1023/A:1011148316537.Google Scholar
Lambrechts, L., Halbert, J., Durand, P., Gouagna, L. C. and Koella, J. C. (2005). Host genotype by parasite genotype interactions underlying the resistance of anopheline mosquitoes to Plasmodium falciparum . Malaria Journal 4, 3. doi: 10.1186/1475–2875-4-3.Google Scholar
Lambrechts, L., Fellous, S. and Koella, J. C. (2006). Coevolutionary interactions between host and parasite genotypes. Trends in Parasitology 22, 12–16. doi: 10.1016/j.pt.2005.11.008.Google Scholar
Lefevre, T., Williams, A. J. and de Roode, J. C. (2011). Genetic variation in resistance, but not tolerance, to a protozoan parasite in the monarch butterfly. Proceedings of the Royal Society B: Biological Sciences 278, 751–759. doi: 10.1098/rspb.2010.1479.Google Scholar
Leggett, H. C., Buckling, A., Long, G. H. and Boots, M. (2013). Generalism and the evolution of parasite virulence. Trends in Ecology and Evolution 28, 592–596. doi: http://dx.doi.org/10.1016/j.tree.2013.07.002.Google Scholar
Leung, T. L. F., Poulin, R. and Keeney, D. B. (2009). Accumulation of diverse parasite genotypes within the bivalve second intermediate host of the digenean Gymnophalus sp. International Journal for Parasitology 39, 327–331. doi: 10.1016/j.ijpara.2008.07.003.Google Scholar
Lion, S. and Boots, M. (2010). Are parasites ‘prudent’ in space? Ecology Letters 13, 1245–1255. doi: 10.1111/j.1461-0248.2010.01516x.Google Scholar
Lively, C. M. (1989). Adaptation by a parasitic trematode to local populations of its snail host. Evolution 43, 1663–1671.Google Scholar
Lively, C. M. (1999). Migration, virulence, and the geographic mosaic of adaptation by parasites. American Naturalist 153, S34–S47. doi: 10.1086/303210.Google Scholar
Longley, R., Smith, C., Fortin, A., Berghout, J., McMorran, B., Burgio, G., Foote, S. and Gros, P. (2011). Host resistance to malaria: using mouse models to explore the host response. Mammalian Genome 22, 32–34. doi: 10.1007/s00335-010-9302-6.Google Scholar
Lopez-Villavicencio, M., Courjol, F., Gibson, A. K., Hood, M. E., Jonot, O., Shykoff, J. A. and Giraud, T. (2010). Competition, cooperation among kin, and virulence in multiple infections. Evolution 65, 1357–1366. doi: 10.1111/j.1558-5646.2010.01207.x.Google Scholar
Luquet, E., Garner, T. W. J., Lena, J., Bruel, C., Joly, P., Lengagne, T., Grolet, O. and Plenet, S. (2012). Genetic erosion in wild populations makes resistance to a pathogen more costly. Evolution 66, 1942–1952. doi: 10.1111/j.1558-5646.2011.01570.x.Google Scholar
Mackinnon, M. J. and Marsh, K. (2010). The selection landscape of malaria parasites. Science 328, 866–871. doi: 10.1126/science.1185410.Google Scholar
Matthews, L., Low, J. C., Gally, D. L., Pearce, M. C., Mellor, D. J., Heesterbeek, J. A. P., Chase-Topping, M., Naylor, S. W., Shaw, D. J., Reid, S. W. J., Gunn, G. J. and Woolhouse, M. E. J. (2006). Heterogeneous shedding of Escherichia coli O157 in cattle and its implications for control. Proceedings of the National Academy of Sciences USA 103, 547–552. doi: 10.1073/pnas.0503776103.Google Scholar
Mbora, D. N. M. and McPeek, M. A. (2009). Host density and human activities mediate increased parasite prevalence and richness in primates threatened by habitat loss and fragmentation. Journal of Animal Ecology 78, 210–218. doi: 10.1111/j.1365-2656.2008.01481.x.Google Scholar
McCoy, K. D., Boulinier, T., Tirard, C. and Michalakis, Y. (2003). Host-dependent genetic structure of parasite populations: differential dispersal of seabird tick host races. Evolution 57, 288–296.Google Scholar
McCoy, K. D., Boulinier, T. and Tirard, C. (2005). Comparative host-parasite population structures: disentangling prospecting and dispersal in the black-legged kittiwake Rissa tridactyla . Molecular Ecology 14, 2825–2838. doi: 10.1111/j.1365-294X.2005.02631.x.Google Scholar
Minchella, D. J. (1985). Host life-history variation in response to parasitism. Parasitology 90, 205–516. doi: http://dx.doi.org/10.1017/S0031182000049143.Google Scholar
Minchella, D. J., Sollenberger, K. M. and Pereira De Souza, C. (1995). Distribution of schistosome genetic diversity within molluscan intermediate hosts. Parasitology 111, 217–220. doi: http://dx.doi.org/10.1017/S0031182000064970.Google Scholar
Mulvey, M., Aho, J., Lydeard, C. and Smith, M. H. (1991). Comparative population genetic structure of a parasite (Fascioles magna) in its definitive host. Evolution 45, 1628–1640.Google Scholar
Nadler, S. (1995). Microevolution and the genetic structure of parasite populations. Journal of Parasitology 81, 395–403.CrossRefGoogle ScholarPubMed
Nunn, C. L., Altizer, S., Jones, K. E. and Sechrest, W. (2003). Comparative tests of the parasite species richness in primates. American Naturalist 162, 597–614. doi: 10.1086/378721.Google Scholar
Nkhoma, S. C., Nair, S., Al-Saai, S., Ashley, E., McGready, R., Phyo, A. P., Nosten, F. and Anderson, T. J. C. (2013). Population genetic correlates of declining transmission in a human pathogen. Molecular Ecology 22, 273–285. doi: 10.1111/mec.12099.Google Scholar
Opdam, P. (1991). Metapopulation theory and habitat fragmentation: a review of Holarctic breeding bird studies. Landscape Ecology 5, 93–106. doi: 10.1007/BF00124663.Google Scholar
Paull, S. H., Song, S., McClure, K. M., Sackett, L. C., Kilpatrick, A. M. and Johnson, P. T. (2011). From superspreaders to disease hotspots: linking transmission across hosts and space. Frontiers in Ecology and the Environment 10, 75–82. doi: 10.1890/110111.Google Scholar
Poulin, R. (2003). The decay of similarity with geographical distance in parasite communities of vertebrate hosts. Journal of Biogeography 30, 1609–1615. doi: 10.1046/j.1365-2699.2003.00949.x.Google Scholar
Prugnolle, F., Liu, H., de Meeus, T. and Balloux, F. (2005). Population genetics of complex life-cycle parasites: an illustration with trematodes. International Journal for Parasitology 35, 255–263. doi: 10.1016/j.ijpara.2004.10.027.Google Scholar
Puustinen, S., Koskela, T. and Mutikainen, P. (2004). Relatedness affects competitive performance of a parasitic plant (Cuscuta europea) in multiple infections. Journal of Evolutionary Biology 17, 897–903. doi: 10.1111/j.1420-9101.2004.00728.x.Google Scholar
Qiu, W.-G., Dykhuizen, D. E., Acosta, M. S. and Luft, B. J. (2002). Geographic uniformity of the Lyme disease spirochete (Borrelia burgdorferi) and its shared history with tick vector (Ixodes scapularis) in the Northeastern United States. Genetics 3, 833–849.Google Scholar
Reece, S. E., Drew, D. R. and Gardner, A. (2008). Sex ratio adjustment and kin discrimination in malaria parasites. Nature 453, 609–614. doi: 10.1038/nature06954.CrossRefGoogle ScholarPubMed
Richards, C. (1975). Genetic studies on variation in infectivity of Schistosoma mansoni . Journal of Parasitology 61, 233–236.Google Scholar
Richards, C. S. and Shade, P. C. (1987). The genetic variation of compatibility in Biomphalaria glabrata and Schistosoma mansoni . Journal of Parasitology 73, 1146–1151.Google Scholar
Ridout, C. J., Skamnioti, P., Porritt, O., Sacristan, S., Jones, J. D. G. and Brown, J. K. M. (2006). Multiple avirulence paralogues in cereal powdery mildew fungi may contribute to parasite fitness and defeat of plant resistance. Plant Cell 18, 2402–2414. doi: http://dx.doi.org/10.1105/tpc.106.043307.Google Scholar
Rolstad, J. (1991). Consequences of forest fragmentation for the dynamics of bird populations: conceptual issues and the evidence. Biological Journal of the Linnean Society 42, 149–163. doi: 10.1111/j.1095-8312.1991.tb00557.x.Google Scholar
Sandland, G. J. and Minchella, D. J. (2003). Cost of immune defense: an enigma wrapped in an environmental cloak? Trends in Parasitology 19, 571–574. doi: 10.1016/j.pt.2003.10.006.Google Scholar
Schonian, G., Kuhls, K. and Mauricio, I. L. (2011). Molecular approaches for a better understanding of the epidemiology and population genetics of Leishmania . Parasitology 138, 405–425. doi: 10.1017/S0031182010001538.Google Scholar
Simard, F., Ayala, D., Kamden, G. C., Pombi, M., Etouna, J., Ose, K., Fotsing, J., Fontenille, D., Besansky, N. J. and Costantini, C. (2009). Ecological niche partitioning between Anopheles gambiae molecular forms in Cameroon: the ecological side of speciation. BMC Ecology 9, 17. doi: 10.1186/1472-6785-9-17.Google Scholar
Sire, C., Durand, P., Pointier, J-P. and Theron, A. (1999). Genetic diversity and recruitment pattern of Schistosoma mansoni in a Biomphalaria glabrata snail population: a field study using random-amplified polymorphic DNA markers. Journal of Parasitology 85, 436–441.Google Scholar
Standley, C., Kabatereine, N., Lange, C., Lwambo, N. J. S. and Stothard, J. R. (2010). Molecular epidemiology and phylogeography of Schistosoma mansoni around Lake Victoria. Parasitology 137, 1937–1949. doi: http://dx.doi.org/10.1017/S0031182010000788.Google Scholar
Staves, P. A. and Knell, R. J. (2010). Virulence and competitiveness: the relationship during inter- and intraspecific mixed infections. Evolution 64, 2643–2652. doi: 10.1111/j.1558-5646.2010.00999.x.Google Scholar
Steinauer, M. L., Hanelt, B., Agola, L. E., Mkoji, G. M. and Loker, E. S. (2009). Genetic structure of Schistosoma mansoni in western Kenya: the effects of geography and host sharing. International Journal for Parasitology 39, 1353–1362. doi: 10.1016/j.ijpara.2009.04.010.Google Scholar
Stohler, R., Curtis, J. and Minchella, D. J. (2004). A comparison of microsatellite polymorphism and heterozygosity among field and laboratory populations of Schistosoma mansoni . International Journal for Parasitology 34, 595–601. doi: 10.1016/j.ijpara.2003.11.026.Google Scholar
Tack, A. J. M., Thrall, P. H., Barrett, L. G., Burdon, J. J. and Laine, A.-L. (2012). Variation in infectivity and aggressiveness in space and time in wild host-pathogen systems: causes and consequences. Journal of Evolutionary Biology 25, 1918–1936. doi: 10.1111/j.1420-9101.2012.02588.x.Google Scholar
Taylor, L. H., Mackinnon, M. J. and Read, A. F. (1998). Virulence of mixed-clone and single-clone infections of the rodent malaria Plasmodium chabaudi . Evolution 52, 583–591.Google Scholar
Theron, A., Sire, C., Rognon, A., Prugnolle, F. and Durand, P. (2004). Molecular ecology of Schistosoma mansoni transmission inferred from the genetic composition of larval and adult infrapopulations within intermediate and definitive hosts. Parasitology 129, 571–585. doi: 10.1017/S0031182004005943.Google Scholar
Thiele, E. A., Sorensen, R. E., Gazzinelli, A. and Minchella, D. J. (2008). Genetic diversity and population structuring of Schistosoma mansoni in a Brazilian village. International Journal of Parasitology 38, 389–399. doi: 10.1016/j.ijpara.2007.07.011.CrossRefGoogle Scholar
Thiele, E. A., Correa-Oliveira, G., Gazzinelli, A. and Minchella, D. J. (2013). Elucidating the temporal and spatial dynamics of Biomphalaria glabrata genetic diversity in three Brazilian villages. Tropical Medicine and International Health 18, 1164–1173. doi: 10.1111/tmi.12164.Google Scholar
Thompson, R. C. A., Lymbery, A. J. and Smith, A. (2010). Parasites, emerging disease, and wildlife conservation. International Journal of Parasitology 40, 1163–1170. doi: 10.1016/j.ijpara.2010.04.009.Google Scholar
Tognazzo, M., Schmid-Hempel, R. and Schmid-Hempel, P. (2012). Probing mixed-genotype infections II: High multiplicity in natural infections of the trypanosomatid, Crithidia bombi, in its host, Bombus spp. PLoS One 7. doi: 10.1371/journal.pone.0049137.Google Scholar
Vale, P. F. (2013). Killing them softly: managing pathogen polymorphism and virulence in spatially variable environments. Trends in Parasitology 29, 417–422.Google Scholar
Vojvodic, S., Boomsma, J. J., Eilenberg, J. and Jensen, A. B. (2012). Virulence of mixed fungal infections in honey bee brood. Frontiers in Zoology 9, 5.Google Scholar
Wang, T. P., Shrivastava, J., Johansen, M. V., Zhang, S. Q., Wang, F. F. and Webster, J. P. (2006). Does multiple hosts mean multiple parasites? Population genetic structure of Schistosoma japonicum between definitive host species. International Journal for Parasitology 36, 1317–1325. doi: 10.1016/j.ijpara.2006.06.011.Google Scholar
Webster, J. P. and Woolhouse, M. E. J. (1998). Selection and strain specificity of compatibility between snail intermediate hosts and their parasitic schistosomes. Evolution 52, 1627–1634.Google Scholar
Webster, J. P. and Woolhouse, M. E. J. (1999). Cost of resistance: relationship between reduced fertility and increased resistance in a snail-schistosome host-parasite system. Proceedings of the Royal Society London, Series B 266, 391–396. doi: 10.1098/rspb.1999.0650.Google Scholar
Webster, J. P., Gower, C. M. and Blair, L. (2004). Do hosts and parasites coevolve? Empirical support from the Schistosoma system. American Naturalist 164, 33–35. doi: 10.1086/424607.Google Scholar
Webster, J. P., Shrivastava, J., Johnson, P. J. and Blair, L. (2007). Is host-schistosome coevolution going anywhere? BMC Evolutionary Biology 7, 91. doi: 10.1186/1471–2148-7-91.Google Scholar
Wesolowski, A., Eagle, N., Tatem, A. J., Smith, D. L., Noor, A. M., Snow, R. W. and Buckee, C. O. (2012). Quantifying the impact of human mobility on malaria. Science 338, 267–270. doi: 10.1126/science.1223467.Google Scholar
Widen, P. (1989). The hunting habits of Goshawk Accipiter gentilis in boreal forests in central Sweden. Ibis 131, 205–213. doi: 10.1111/j.1474-919X.1989.tb02763.x.Google Scholar
Wild, G., Gardner, A. and West, S. A. (2009). Adaptation and the evolution of parasite virulence in a connected world. Nature 459, 983–986. doi: 10.1038/nature08071.Google Scholar
Woolhouse, M. E., Dye, C., Etard, J.-F., Smith, T., Charlwood, J. D., Garnett, G. P., Hagan, P., Hii, J. L. K., Ndhlovu, P. D., Quinnell, R. J., Watts, C. H., Chandiwana, S. K. and Anderson, R. M. (1997). Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proceedings of the National Academy of Sciences USA 94, 338–342. doi: 10.1073/pnas.94.1.338.Google Scholar
Zhang, P., Sandland, G. J., Feng, Z., Xu, D. and Minchella, D. J. (2007). Evolutionary implications for interactions between multiple strains of host and parasite. Journal of Theoretical Biology 248, 225–240. doi: 10.1016/j.jtbi.2007.05.011.Google Scholar