Book contents
- Wildlife Disease Ecology
- Ecological Reviews
- Wildlife Disease Ecology
- Copyright page
- Contents
- Contributors
- Preface: Wildlife Disease Ecology
- Glossary of Terms
- Part I Understanding within-host processes
- Chapter one Pollinator diseases: the Bombus–Crithidia system
- Chapter Two Genetic diversity and disease spread: epidemiological models and empirical studies of a snail–trematode system
- Chapter Three Wild rodents as a natural model to study within-host parasite interactions
- Chapter Four From population to individual host scale and back again: testing theories of infection and defence in the Soay sheep of St Kilda
- Chapter Five The causes and consequences of parasite interactions: African buffalo as a case study
- Chapter Six Effects of host lifespan on the evolution of age-specific resistance: a case study of anther-smut disease on wild carnations
- Chapter Seven Sexually transmitted infections in natural populations: what have we learnt from beetles and beyond?
- Part II Understanding between-host processes
- Part III Understanding wildlife disease ecology at the community and landscape level
- Index
- Plate Section (PDF Only)
- References
Chapter Two - Genetic diversity and disease spread: epidemiological models and empirical studies of a snail–trematode system
from Part I - Understanding within-host processes
Published online by Cambridge University Press: 28 October 2019
Book contents
- Wildlife Disease Ecology
- Ecological Reviews
- Wildlife Disease Ecology
- Copyright page
- Contents
- Contributors
- Preface: Wildlife Disease Ecology
- Glossary of Terms
- Part I Understanding within-host processes
- Chapter one Pollinator diseases: the Bombus–Crithidia system
- Chapter Two Genetic diversity and disease spread: epidemiological models and empirical studies of a snail–trematode system
- Chapter Three Wild rodents as a natural model to study within-host parasite interactions
- Chapter Four From population to individual host scale and back again: testing theories of infection and defence in the Soay sheep of St Kilda
- Chapter Five The causes and consequences of parasite interactions: African buffalo as a case study
- Chapter Six Effects of host lifespan on the evolution of age-specific resistance: a case study of anther-smut disease on wild carnations
- Chapter Seven Sexually transmitted infections in natural populations: what have we learnt from beetles and beyond?
- Part II Understanding between-host processes
- Part III Understanding wildlife disease ecology at the community and landscape level
- Index
- Plate Section (PDF Only)
- References
Summary
For simplicity’s sake, standard population genetic models of host–parasite coevolution often exclude ecological and epidemiological detail. In particular, they assume that each host is exposed to a single infectious propagule, regardless of the parasite’s prevalence. On the other hand, standard epidemiological models usually assume that all hosts are equally susceptible to infection. Here, we summarise models in which we relax these simplifying assumptions, thereby allowing for feedbacks between evolution, ecology, and epidemiology. One major result from these models is that, under certain general conditions, a parasite’s potential for disease spread (R0) decreases as genetic diversity for resistance increases in the host population. Moreover, R0 can increase if we allow the parasite population to track common host genotypes. Feedbacks between ecology and evolution mean that as a common genotype comes to dominate the host population, the parasite population adapts to preferentially infect this genotype, increasing the prevalence of infection and the mean number of parasite exposures per host. We further connect these findings to the major evolutionary hypothesis that coevolving parasites can favour sexual reproduction.
Keywords
- Type
- Chapter
- Information
- Wildlife Disease EcologyLinking Theory to Data and Application, pp. 32 - 57Publisher: Cambridge University PressPrint publication year: 2019
References
References
Agrawal, A. & Lively, C.M. (2002) Infection genetics: gene-for-gene versus matching-alleles models and all points in between. Evolution Ecology Research, 4, 79–90.Google Scholar
Agrawal, A. & Lively, C.M. (2003) Modelling infection as a two-step process combining gene-for- gene and matching-allele genetics. Proceedings of the Royal Society of London B: Biological Sciences, 270, 323–334.Google Scholar
Engelstädter, J. & Bonhoeffer, S. (2009) Red Queen dynamics with non-standard fitness interactions. PLoS Computational Biology, 5, e1000469.Google Scholar
Fenton, A., Antonovics, J. & Brockhurst, M.A. (2012) Two-step infection processes can lead to coevolution between functionally independent infection and resistance pathways. Evolution, 66, 2030–2041.Google Scholar
Flor, H.H. (1956) The complementary genetic system in flax and flax rust. Advances in Genetics, 8, 29–54.Google Scholar
Frank, S.A. (1992) Models of plant–pathogen coevolution. Trends in Genetics, 8, 213–219.Google Scholar
Frank, S.A. (1993) Specificity versus detectable polymorphism in host–parasite genetics. Proceedings of the Royal Society of London B, 254, 191–197.Google Scholar
Frank, S.A. (1994) Recognition and polymorphism in host–parasite genetics. Philosophical Transactions of the Royal Society of London B, 346, 283–293.Google ScholarPubMed
Frank, S.A. (1996) Statistical properties of polymorphism in host–parasite genetics. Evolutionary Ecology, 10, 307–317.Google Scholar
Grosberg, R. & Hart, M. (2000) Mate selection and the evolution of highly polymorphic self/nonself recognition genes. Science, 289, 2111–2114.Google Scholar
King, K. & Lively, C. (2012) Does genetic diversity limit disease spread in natural host populations? Heredity, 109, 199–203.Google Scholar
Lively, C.M. (2010) The effect of host genetic diversity on disease spread. American Naturalist, 175, E149–E152.Google Scholar
Lively, C.M. (2016) Coevolutionary epidemiology: disease spread, local adaptation, and sex. American Naturalist, 187, E77–E82.Google Scholar
References
Adams, M.W., Ellingboe, A.H. & Rossman, E.C. (1971) Biological uniformity and disease epidemics. BioScience, 21, 1067–1070.Google Scholar
Altermatt, F. & Ebert, D. (2008) Genetic diversity of Daphnia magna populations enhances resistance to parasites. Ecology Letters, 11, 918–928.Google Scholar
Augspurger, C.K. & Kelly, C.K. (1984) Pathogen mortality of tropical tree seedlings: experimental studies of the effects of dispersal distance, seedling density, and light conditions. Oecologia, 61, 211–217.Google Scholar
Bell, T., Freckleton, R.P. & Lewis, O.T. (2006) Plant pathogens drive density-dependent seedling mortality in a tropical tree. Ecology Letters, 9, 569–574.Google Scholar
Bento, G., Routtu, J., Fields, P.D., et al. (2017) The genetic basis of resistance and matching-allele interactions of a host–parasite system: the Daphnia magna–Pasteuria ramosa model. PLoS Genetics, 13, e1006596.Google Scholar
Biggs, B. & Malthus, T. (1982) Macroinvertebrates associated with various aquatic macrophytes in the backwaters and lakes of the upper Clutha Valley, New Zealand. New Zealand Journal of Marine and Freshwater Research, 16, 81–88.Google Scholar
Browning, J.A. & Frey, K.J. (1969) Multiline cultivars as a means of disease control. Annual Review of Phytopathology, 7, 355–382.Google Scholar
Carius, H.J., Little, T.J. & Ebert, D. (2001) Genetic variation in a host–parasite association: potential for coevolution and frequency-dependent selection. Evolution, 55, 1136–1145.Google Scholar
Collier, K., Ilcock, R. & Meredith, A. (1997) Influence of substrate type and physico-chemical conditions on macroinvertebrate faunas and biotic indices of some lowland Waikato, New Zealand, streams. New Zealand Journal of Marine and Freshwater Research, 32, 1–19.CrossRefGoogle Scholar
Decaestecker, E., Gaba, S., Raeymaekers, J.A.M., et al. (2007) Host–parasite ‘Red Queen’ dynamics archived in pond sediment. Nature, 450, 870–873.Google Scholar
Duffy, M.A. & Sivars-Becker, L. (2007) Rapid evolution and ecological host–parasite dynamics. Ecology Letters, 10, 44–53.Google Scholar
Duneau, D., Luijckx, P., Ben-Ami, F., Laforsch, C. & Ebert, D. (2011) Resolving the infection process reveals striking differences in the contribution of environment, genetics and phylogeny to host–parasite interactions. BMC Biology, 9, 11.Google Scholar
Dybdahl, M.F., Jokela, J., Delph, L.F., Koskella, B. & Lively, C.M. (2008) Hybrid fitness in a locally adapted parasite. American Naturalist, 172, 772–782.Google Scholar
Dybdahl, M.F. & Krist, A.C. (2004) Genotypic vs. condition effects on parasite-driven rare advantage. Journal of Evolutionary Biology, 17, 967–973.Google Scholar
Dybdahl, M.F. & Lively, C.M. (1995) Diverse endemic and polyphyletic clones in mixed populations of the freshwater snail, Potamopyrgus antipodarum. Journal of Evolutionary Biology, 8, 385–398.CrossRefGoogle Scholar
Dybdahl, M.F. & Lively, C.M. (1996) The geography of coevolution: comparative population structures for a snail and its trematode parasite. Evolution, 50, 2264–2275.Google Scholar
Dybdahl, M.F. & Lively, C.M. (1998) Host–parasite coevolution: evidence for rare advantage and time-lagged selection in a natural population. Evolution, 52, 1057–1066.Google Scholar
Fontcuberta Garcia-Cuenca, A., Dumas, Z. & Schwander, T. (2016) Extreme genetic diversity in asexual grass thrips populations. Journal of Evolutionary Biology, 29, 887–899.Google Scholar
Forsyth, D. & McCallum, I. (1981) Benthic macroinvertebrates of Lake Taupo. New Zealand Journal of Marine and Freshwater Research, 15, 41–46.Google Scholar
Fox, J., Dybdahl, M.F., Jokela, J. & Lively, C.M. (1996) Genetic structure of coexisting sexual and clonal subpopulations in a freshwater snail (Potamopyrgus antipodarum). Evolution, 50, 1541–1548.Google Scholar
Gandon, S. (2002) Local adaptation and the geometry of host–parasite coevolution. Ecology Letters, 5, 246–256.Google Scholar
Gandon, S., Capowiez, Y., Dubois, Y., Michalakis, Y. & Olivieri, I. (1996) Local adaptation and gene-for-gene coevolution in a metapopulation model. Proceedings of the Royal Society of London B, 263, 1003–1009.Google Scholar
Gandon, S. & Michalakis, Y. (2002) Local adaptation, evolutionary potential and host–parasite coevolution: interactions between migration, mutation, population size and generation time. Journal of Evolutionary Biology, 15, 451–462.Google Scholar
Gandon, S. & Nuismer, S.L. (2009) Interactions between genetic drift, gene flow, and selection mosaics drive parasite local adaptation. American Naturalist, 173, 212–224.Google Scholar
Ganz, H.H. & Ebert, D. (2010) Benefits of host genetic diversity for resistance to infection depend on parasite diversity. Ecology, 91, 1263–1268.CrossRefGoogle ScholarPubMed
Garrett, K.A. & Mundt, C.C. (1999) Epidemiology in mixed host populations. Phytopathology, 89, 984–990.Google Scholar
Gibson, A.K., Jokela, J. & Lively, C.M. (2016) Fine-scale spatial covariation between infection prevalence and susceptibility in a natural population. American Naturalist, 188, 1–14.Google Scholar
Gibson, A.K., Xu, J.Y. & Lively, C.M. (2016) Within-population covariation between sexual reproduction and susceptibility to local parasites. Evolution, 70, 2049–2060.Google Scholar
Gibson, A.K., Delph, L.F. & Lively, C.M. (2017) The two-fold cost of sex: experimental evidence from a natural system. Evolution Letters, 1, 6–15.CrossRefGoogle ScholarPubMed
Gibson, A.K., Vergara, D., Delph, L.F. & Lively, C.M. (2018) Periodic parasite-mediated selection for and against sex. American Naturalist, 192, 537–551.Google Scholar
Hamilton, W.D., Axelrod, R. & Tanese, R. (1990) Sexual reproduction as an adaptation to resist parasites (a review). Proceedings of the National Academy of Sciences of the United States of America, 87, 3566–3573.Google Scholar
Hechinger, R.F. (2012) Faunal survey and identification key for the trematodes (Platyhelminthes: Digenea) infecting Potamopyrgus antipodarum (Gastropoda: Hydrobiidae) as first intermediate host. Zootaxa, 3418, 1–27.Google Scholar
Howard, R.S. & Lively, C.M. (1994) Parasitism, mutation accumulation and the maintenance of sex. Nature, 367, 554–557.CrossRefGoogle ScholarPubMed
Howard, R.S. & Lively, C.M. (1998) The maintenance of sex by parasitism and mutation accumulation under epistatic fitness functions. Evolution, 52, 604–610.Google Scholar
Jensen, N.F. (1952) Intra-varietal diversification in oat breeding. Agronomy Journal, 44, 30–34.Google Scholar
Jokela, J., Dybdahl, M.F. & Lively, C.M. (2009) The maintenance of sex, clonal dynamics, and host–parasite coevolution in a mixed population of sexual and asexual snails. American Naturalist, 174, S43–S53.CrossRefGoogle Scholar
Jokela, J., Lively, C.M., Dybdahl, M.F. & Fox, J. (2003) Genetic variation in sexual and clonal lineages of a freshwater snail. Biological Journal of the Linnean Society, 79, 165–181.Google Scholar
King, K.C., Delph, L.F., Jokela, J. & Lively, C.M. (2009) The geographic mosaic of sex and the Red Queen. Current Biology, 19, 1438–1441.Google Scholar
King, K.C., Delph, L.F., Jokela, J. & Lively, C.M. (2011) Coevolutionary hotspots and coldspots for host sex and parasite local adaptation in a snail–trematode interaction. Oikos, 120, 1335–1340.Google Scholar
King, K.C. & Lively, C.M. (2012) Does genetic diversity limit disease spread in natural host populations? Heredity, 109, 199–203.Google Scholar
Koskella, B. & Lively, C.M. (2007) Advice of the rose: experimental coevolution of a trematode parasite and its snail host. Evolution, 61, 152–159.Google Scholar
Koskella, B. & Lively, C.M. (2009) Evidence for negative frequency-dependent selection during experimental coevolution of a freshwater snail and a sterilizing trematode. Evolution, 63, 2213–2221.Google Scholar
Koskella, B., Vergara, D. & Lively, C.M. (2011) Experimental evolution of sexual host populations in response to sterilizing parasites. Evolutionary Ecology Research, 13, 315–322.Google Scholar
Laine, A.L., Burdon, J.J., Dodds, P.N. & Thrall, P.H. (2011) Spatial variation in disease resistance: from molecules to metapopulations. Journal of Ecology, 99, 96–112.CrossRefGoogle ScholarPubMed
Lively, C.M. (1987) Evidence from a New Zealand snail for the maintenance of sex by parasitism. Nature, 328, 519–521.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. (1992) Parthenogenesis in a freshwater snail: reproductive assurance versus parasitic release. Evolution, 46, 907–913.Google Scholar
Lively, C.M. (1999) Migration, virulence, and the geographic mosaic of adaptation by parasites. American Naturalist, 153, S34–S47.Google Scholar
Lively, C.M. (2009) The maintenance of sex: host–parasite coevolution with density-dependent virulence. Journal of Evolutionary Biology, 22, 2086–2093.Google Scholar
Lively, C.M. (2010a) Antagonistic coevolution and sex. Evolution: Education and Outreach, 3, 19–25.Google Scholar
Lively, C.M. (2010b) The effect of host genetic diversity on disease spread. American Naturalist, 175, E149–E152.Google Scholar
Lively, C.M. (2010c) An epidemiological model of host–parasite coevolution and sex. Journal of Evolutionary Biology, 23, 1490–1497.CrossRefGoogle ScholarPubMed
Lively, C.M. (2016) Coevolutionary epidemiology: disease spread, local adaptation, and sex. American Naturalist, 187, E77–E82.Google Scholar
Lively, C.M. & Dybdahl, M.F. (2000) Parasite adaptation to locally common host genotypes. Nature, 405, 679–681.Google Scholar
Lively, C.M., Dybdahl, M.F., Jokela, J., Osnas, E.E. & Delph, L.F. (2004) Host sex and local adaptation by parasites in a snail–trematode interaction. American Naturalist, 164, S6–S18.CrossRefGoogle Scholar
Lively, C.M., Johnson, S.G., Delph, L.F. & Clay, K. (1995) Thinning reduces the effect of rust infection on jewelweed (Impatiens capensis). Ecology, 76, 1859–1862.Google Scholar
Lively, C.M. & Jokela, J. (2002) Temporal and spatial distributions of parasites and sex in a freshwater snail. Evolutionary Ecology Research, 4, 219–226.Google Scholar
Luijckx, P., Ben-Ami, F., Mouton, L., Du Pasquier, L. & Ebert, D. (2011) Cloning of the unculturable parasite Pasteuria ramosa and its Daphnia host reveals extreme genotype–genotype interactions. Ecology Letters, 14, 125–131.Google Scholar
Luijckx, P., Fienberg, H., Duneau, D. & Ebert, D. (2012) Resistance to a bacterial parasite in the crustacean Daphnia magna shows Mendelian segregation with dominance. Heredity, 108, 547–551.Google Scholar
Luijckx, P., Fienberg, H., Duneau, D. & Ebert, D. (2013) A matching-allele model explains host resistance to parasites. Current Biology, 23, 1085–1088.Google Scholar
May, R.M. & Anderson, R.M. (1983) Epidemiology and genetics in the coevolution of parasites and hosts. Proceedings of the Royal Society of London B, 219, 281–313.Google Scholar
Maynard Smith, J. (1971) The origin and maintenance of sex. In: Williams, G.C. (ed.), Group Selection (pp. 163–175). Chicago, IL: Aldine Atherton.Google Scholar
McKone, M., Gibson, A.K., Cook, D., et al. (2016) Fine-scale association between parasites and sex in Potamopyrgus antipodarum within a New Zealand lake. New Zealand Journal of Ecology, 40, 1.Google Scholar
Meagher, S. (1999) Genetic diversity and Capillaria hepatica (Nematoda) prevalence in Michigan deer mouse populations. Evolution, 53, 1318–1324.Google Scholar
Metzger, C.M.J.A., Luijckx, P., Bento, G., Mariadassou, M. & Ebert, D. (2016) The Red Queen lives: epistasis between linked resistance loci. Evolution, 70, 480–487.Google Scholar
Mundt, C. (2002) Use of multiline cultivars and cultivar mixtures for disease management. Annual Review of Phytopathology, 40, 381–410.Google Scholar
Neiman, M., Jokela, J. & Lively, C.M. (2005) Variation in asexual lineage age in Potamopyrgus antipodarum, a New Zealand snail. Evolution, 59, 1945–1952.Google Scholar
Newton, W.L. (1953) The inheritance of susceptibility to infection with Schistosoma mansoni in Australorbis glabratus. Experimental Parasitology, 2, 242–257.Google Scholar
Osnas, E.E. & Lively, C.M. (2004) Parasite dose, prevalence of infection and local adaptation in a host–parasite system. Parasitology, 128, 223–228.Google Scholar
Osnas, E.E. & Lively, C.M. (2005) Immune response to sympatric and allopatric parasites in a snail–trematode interaction. Frontiers in Zoology, 2, 8.Google Scholar
Osnas, E.E. & Lively, C.M. (2006) Host ploidy, parasitism and immune defence in a coevolutionary snail–trematode system. Journal of Evolutionary Biology, 19, 42–48.CrossRefGoogle Scholar
Otto, S.P. & Nuismer, S.L. (2004) Species interactions and the evolution of sex. Science, 304, 1018–1020.Google Scholar
Paczesniak, D., Adolfsson, S., Liljeroos, K., et al. (2014) Faster clonal turnover in high-infection habitats provides evidence for parasite-mediated selection. Journal of Evolutionary Biology, 27, 417–428.Google Scholar
Parker, M.A. (1985) Local population differentiation for compatibility in an annual legume and its host-specific fungal pathogen. Evolution, 39, 713–723.Google Scholar
Pielou, E.C. (1969) An Introduction to Mathematical Ecology. New York, NY: John Wiley & Sons.Google Scholar
Pilet, F., Chacon, G., Forbes, G.A. & Andrivon, D. (2006) Protection of susceptible potato cultivars against late blight in mixtures increases with decreasing disease pressure. Phytopathology, 96, 777–783.Google Scholar
Richards, C.S. (1975) Genetic factors in susceptibility of Biomphalaria glabrata for different strains of Schistosoma mansoni. Parasitology, 70, 231–241.Google Scholar
Richards, C.S. & Merritt, J.W. (1972) Genetic factors in the susceptibility of juvenile Biomphalaria glabrata to Schistosoma mansoni infection. American Journal of Tropical Medicine and Hygiene, 21, 425–434.Google Scholar
Schmid, B. (1994) Effects of genetic diversity in experimental stands of Solidago altissima: evidence for the potential role of pathogens as selective agents in plant populations. Journal of Ecology, 82, 165–175.Google Scholar
Talbot, J. & Ward, J. (1987) Macroinvertebrates associated with aquatic macrophyties in Lake Alexandrina, New Zealand. New Zealand Journal of Marine and Freshwater Research, 21, 199–213.Google Scholar
Thrall, P.H. & Burdon, J.J. (2000) Effect of resistance variation in a natural plant host–pathogen metapopulation on disease dynamics. Plant Pathology, 49, 767–773.Google Scholar
Thrall, P.H., Burdon, J.J. & Young, A. (2001) Variation in resistance and virulence among demes of a plant host–pathogen metapopulation. Journal of Ecology, 89, 736–748.Google Scholar
Tseng, M. (2004) Sex–specific response of a mosquito to parasites and crowding. Proceedings of the Royal Society of London B, 271, S186–S188.CrossRefGoogle ScholarPubMed
Vergara, D., Jokela, J. & Lively, C.M. (2014) Infection dynamics in coexisting sexual and asexual host populations: support for the Red Queen Hypothesis. American Naturalist, 184, S22–S30.Google Scholar
Vergara, D., Lively, C.M., King, K.C. & Jokela, J. (2013) The geographic mosaic of sex and infection in lake populations of a New Zealand snail at multiple spatial scales. American Naturalist, 182, 484–493.Google Scholar
Wallace, C. (1992) Parthenogenesis, sex and chromosomes in Potamopyrgus antipodarum. Journal of Molluscan Studies, 58, 93–107.Google Scholar
Webster, J., Shrivastava, J., Johnson, P. & Blair, L. (2007) Is host–schistosome coevolution going anywhere? BMC Evolutionary Biology, 7, 91.Google Scholar
Webster, J. & Woolhouse, M. (1998) Selection and strain specificity of compatibility between snail intermediate hosts and their parasitic schistosomes. Evolution, 52, 1627–1634.Google Scholar
Webster, J.P. & Davies, C.M. (2001) Coevolution and compatibility in the snail–schistosome system. Parasitology, 123, 41–56.Google Scholar
Webster, J.P., Gower, C.M. & Blair, L. (2004) Do hosts and parasites coevolve? Empirical support from the Schistosoma system. American Naturalist, 164, S33–S51.Google Scholar
Winterbourn, M. (1970) Population studies on the New Zealand freshwater gastropod, Potamopyrgus antipodarum. Proceedings of the Malacological Society of London, 39, 139–149.Google Scholar
Wolfe, M. (1985) The current status and prospects of multiline cultivars and variety mixtures for disease resistance. Annual Review of Phytopathology, 23, 251–273.Google Scholar
Zhu, Y., Chen, H., Fan, J., et al. (2000) Genetic diversity and disease control in rice. Nature, 406, 718–722.Google Scholar
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