Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-22T20:31:25.507Z Has data issue: false hasContentIssue false

Chapter Six - Effects of host lifespan on the evolution of age-specific resistance: a case study of anther-smut disease on wild carnations

from Part I - Understanding within-host processes

Published online by Cambridge University Press:  28 October 2019

By
Emily Bruns
Edited by
Kenneth Wilson ,
Andy Fenton  and
Dan Tompkins
Kenneth Wilson
Affiliation:
Lancaster University
Andy Fenton
Affiliation:
University of Liverpool
Dan Tompkins
Affiliation:
Predator Free 2050 Ltd
Get access

Summary

A large class of diseases is dependent on juvenile hosts for transmission because younger hosts are typically more susceptible to disease. Studies have investigated the epidemiological consequences of juvenile susceptibility, but why species retain such high susceptibility in the juvenile stage remains a puzzle. Life-history theory predicts that hosts should evolve to be more resistant as juveniles than as adults because early infection is costlier. Studies of anther-smut on wild carnations show that disease persistence is strongly dependent on the presence of a highly susceptible juvenile class. While there is evidence of genetic variation in juvenile resistance, the majority of plant families are highly susceptible at this stage, so juvenile resistance may be less beneficial than assumed. To understand how the costs and benefits of resistance and life-history traits affect the evolution of age-specific resistance, we developed a general analytical model of age-specific resistance, which shows that if there is genetic variation for the onset of resistance, selection and numerical feedbacks often drive the evolution of adult resistance but maintain juvenile susceptibility. The implications of these results are discussed.

Keywords

resistanceevolutionchildhood diseasejuvenile susceptibilitycost of resistancelifespanage structuresterilisingplant–pathogenanther-smut disease
Type
Chapter
Information
Wildlife Disease Ecology
Linking Theory to Data and Application
 , pp. 161 - 186
Publisher: Cambridge University Press
Print publication year: 2019

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

Alexander, H.M. (1989) An experimental field study of anther-smut disease of Silene alba caused by Ustilago violacea: genotypic variation and disease incidence. Evolution, 43, 835–847.Google Scholar
Alexander, H.M. (1990) Epidemiology of anther-smut infection of Silene alba caused by Ustilago violacea: patterns of spore deposition and disease incidence. Journal of Ecology, 78, 166–179.CrossRefGoogle Scholar
Alexander, H.M. & Antonovics, J. (1988) Disease spread and population dynamics of anther-smut infection of Silene alba caused by the fungus Ustilago violacea. Journal of Ecology, 76, 91–104.CrossRefGoogle Scholar
Alexander, H.M. & Antonovics, J. (1995) Spread of anther-smut disease (Ustilago violacea) and character correlations in a genetically variable experimental population of Silene alba. Journal of Ecology, 83, 783–794.Google Scholar
Alexander, H.M., Antonovics, J. & Kelly, A.W. (1993) Genotypic variation in plant disease resistance–physiological resistance in relation to field disease transmission. Journal of Ecology, 81, 325–333.CrossRefGoogle Scholar
Altizer, S., Davis, A.K., Cook, K.C. & Cherry, J.J. (2004) Age, sex, and season affect the risk of mycoplasmal conjunctivitis in a southeastern house finch population. Canadian Journal of Zoology, 82, 755–763.Google Scholar
Antonovics, A.J., Stratton, D., Thrall, P.H. & Jarosz, A.M. (1996) An anther-smut disease (Ustilago violacea) of Fire-pink (Silene virginica): its biology and relationship to the anther-smut disease of white campion (Silene alba). American Midland Naturalist, 135, 130–143.CrossRefGoogle Scholar
Antonovics, J. (2004) Long-term study of a plant-pathogen metapopulation. In: Ecology, Genetics, and Evolution of Metapopulations (pp. 471–488). Amsterdam: Elsevier.CrossRefGoogle Scholar
Antonovics, J. & Alexander, H.M. (1992) Epidemiology of anther-smut infection of Silene alba (= S. latifolia) caused by Ustilago violacea: patterns of spore deposition in experimental populations. Proceedings of the Royal Society of London B, 250, 157–163.Google Scholar
Antonovics, J., Hood, M.E., Thrall, P.H., Abrams, J.Y. & Duthie, G.M. (2003) Herbarium studies on the distribution of anther-smut fungus (Microbotryum violaceum) and Silene species (Caryophyllaceae) in the eastern United States. American Journal of Botany, 90, 1522–1531.Google Scholar
Antonovics, J. & Thrall, P.H. (1994) The cost of resistance and maintenance of genetic polymorphism in host–pathogen systems. Proceedings of the Royal Society of London B, 257, 105–110.Google Scholar
Armitage, S.A.O., Thompson, J.J.W., Rolff, J. & Siva-Jothy, M.T. (2003) Examining costs of induced and constitutive immune investment in Tenebrio molitor. Journal of Evolutionary Biology, 16, 1038–1044.Google Scholar
Baird, J.K. (1998) Age-dependent characteristics of protection v. susceptibility to Plasmodium falciparum. Annals of Tropical Medicine and Parasitology, 92, 367–390.CrossRefGoogle ScholarPubMed
Barton, K.E. & Koricheva, J. (2010) The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. The American Naturalist, 175, 481–493.CrossRefGoogle ScholarPubMed
Bergelson, J. & Purrington, C.B. (1996) Surveying patterns in the cost of resistance in plants. The American Naturalist, 148, 536–558.CrossRefGoogle Scholar
Bernasconi, G., Antonovics, J., Biere, A., et al. (2009) Silene as a model system in ecology and evolution. Heredity, 103, 5–14.CrossRefGoogle Scholar
Biere, A. & Antonovics, J. (1996) Sex-specific costs of resistance to the fungal pathogen Ustilago violacea (Microbotryum violaceum) in Silene alba. Evolution, 50, 1098–1110.Google Scholar
Boege, K. & Marquis, R.J. (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends in Ecology and Evolution, 20, 441–448.Google Scholar
Boots, M., Donnelly, R. & White, A. (2013) Optimal immune defence in the light of variation in lifespan. Parasite Immunology, 35, 331–338.Google Scholar
Brambell, F.W.R. (1970) The Transmission of Passive Immunity from Mother to Young. Amsterdam: North Holland.Google Scholar
Bruns, E., Hood, M.E. & Antonovics, J. (2015) Rate of resistance evolution and polymorphism in long- and short-lived hosts. Evolution, 69, 551–560.CrossRefGoogle ScholarPubMed
Bruns, E.L., Antonovics, J., Carasso, V. & Hood, M. (2017) Transmission and temporal dynamics of anther-smut disease (Microbotryum) on alpine carnation (Dianthus pavonius). Journal of Ecology, 105, 1413–1424.Google Scholar
Buono, L., López-Villavicencio, M., Shykoff, J.A., Snirc, A. & Giraud, T. (2014) Influence of multiple infection and relatedness on virulence: disease dynamics in an experimental plant population and its castrating parasite. PLoS ONE, 9, e98526.CrossRefGoogle Scholar
Burdon, J.J., Oates, J.D. & Marshall, D.R. (1983) Interactions between Avena and Puccinia species. I. The wild hosts: Avena barbata Pott Ex Link, A. fatua L. and A. ludoviciana Durieu. Journal of Applied Ecology, 20, 571–584.CrossRefGoogle Scholar
Cafuir, L., Antonovics, J. & Hood, M.E. (2007) Tissue culture and quantification of individual‐level resistance to anther‐smut disease in Silene vulgaris.International Journal of Plant Sciences, 168, 415–419.Google Scholar
Carlsson-Granér, U. (1997) Anther-smut disease in Silene dioica: variation in susceptibility among genotypes and populations, and patterns of disease within populations. Evolution, 51, 1416–1426.Google ScholarPubMed
Carlsson-Granér, U. (2006) Disease dynamics, host specificity and pathogen persistence in isolated host populations. Oikos, 112, 174–184.Google Scholar
Carlsson-Granér, U. & Thrall, P.H. (2006) The impact of host longevity on disease transmission: host–pathogen dynamics and the evolution of resistance. Evolutionary Ecology Research, 8, 659–675.Google Scholar
Charlesworth, B. (1980) Evolution in Age-structured Populations. Cambridge: Cambridge University Press.Google Scholar
Chen, X. (2013) High-temperature adult-plant resistance, key for sustainable control of stripe rust. American Journal of Plant Science and Biotechnology, 4, 608–627.CrossRefGoogle Scholar
Chung, E., Petit, E., Antonovics, J., Pedersen, A.B. & Hood, M.E. (2012) Variation in resistance to multiple pathogen species: anther smuts of Silene uniflora. Ecology and Evolution, 2, 2304–2314.Google Scholar
Develey-Rivière, M.P. & Galiana, E. (2007) Resistance to pathogens and host developmental stage: a multifaceted relationship within the plant kingdom. New Phytologist, 175, 405–416.Google Scholar
Diamond, J. (1997) Guns, Germs and Steel: The Fates of Human Societies. New York, NY: Norton.Google Scholar
Donnelly, R., White, A. & Boots, M. (2015) The epidemiological feedbacks critical to the evolution of host immunity. Journal of Evolutionary Biology, 28, 2042–2053.CrossRefGoogle Scholar
Fellous, S. & Lazzaro, B.P. (2011) Potential for evolutionary coupling and decoupling of larval and adult immune gene expression. Molecular Ecology, 20, 1558–1567.CrossRefGoogle ScholarPubMed
Flor, H.H. (1956) The complementary genic systems in flax and flax rust. Advances in Genetics, 8, 29–54.Google Scholar
Garbutt, J.S., O’Donoghue, A.J.P., McTaggart, S.J., Wilson, P.J. & Little, T.J. (2014) The development of pathogen resistance in Daphnia magna: implications for disease spread in age-structured populations. The Journal of Experimental Biology, 217, 3929–3934.Google Scholar
Garnier, R., Gandon, S., Harding, K.C. & Boulinier, T. (2014) Length of intervals between epidemics: evaluating the influence of maternal transfer of immunity. Ecology and Evolution, 4, 568–575.Google Scholar
Getz, W.M. & Pickering, J. (1983) Epidemic models: thresholds and population regulation. The American Naturalist, 121, 892–898.Google Scholar
Hanssen, S.A., Hasselquist, D., Folstad, I. & Erikstad, K.E. (2004) Costs of immunity: immune responsiveness reduces survival in a vertebrate. Proceedings of the Royal Society of London B, 271, 925–930.Google Scholar
Härkönen, T., Harding, K., Rasmussen, T.D., Teilmann, J. & Dietz, R. (2007) Age- and sex-specific mortality patterns in an emerging wildlife epidemic: the phocine distemper in European harbour seals. PLoS ONE, 2, e887.CrossRefGoogle Scholar
Hendrix, F.F. & Campbell, W. (1973) Pythiums as plant pathogens. Annual Review of Phytopathology, 11, 77–98.Google Scholar
Hood, M.E., Mena-Alí, J.I., Gibson, A.K., et al. (2010). Distribution of the anther-smut pathogen Microbotryum on species of the Caryophyllaceae. The New Phytologist, 187, 217–229.Google Scholar
Jarosz, A.M. & Burdon, J.J. (1990) Predominance of a single major gene for resistance to Phakopsora pachyrhizi in a population of Glycine argyrea. Heredity, 64, 347–353.Google Scholar
Jayakar, S.D. (1970) A mathematical model for interaction of gene frequencies in a parasite and its host. Theoretical Population Biology, 1, 140–164.Google Scholar
Kallio, E.R., Begon, M., Henttonen, H., et al. (2010) Hantavirus infections in fluctuating host populations: the role of maternal antibodies. Proceedings of the Royal Society of London B, 277, 3783–3791.Google Scholar
Kaltz, O., Gandon, S., Michalakis, Y. & Shykoff, J.A. (1999) Local maladaptation in the anther-smut fungus Microbotryum violaceum to its host plant Silene latifolia: evidence from a cross-inoculation experiment. Evolution, 53, 395–407.Google Scholar
Kaltz, O. & Shykoff, J.A. (2001) Male and female Silene latifolia plants differ in per-contact risk of infection by a sexually transmitted disease. Journal of Ecology, 89, 99–109.Google Scholar
Kubi, C., Van Den Abbeele, J., De Deken, R., et al. (2006) The effect of starvation on the susceptibility of teneral and non-teneral tsetse flies to trypanosome infection. Medical and Veterinary Entomology, 20, 388–392.CrossRefGoogle ScholarPubMed
Kurtis, J.D., Onyango, F.K. & Duffy, P.E. (2001) Human resistance to Plasmodium falciparum increases during puberty and is predicted by dehyroepiandrosterone sulfate levels. Infection and Immunity, 69, 123–128.Google Scholar
le Gac, M., Hood, M.E., Fournier, E. & Giraud, T. (2007) Phylogenetic evidence of host-specific cryptic species in the anther smut fungus. Evolution, 61, 15–26.Google Scholar
Line, R.F. & Chen, X. (1995) Successes in breeding for and managing durable resistance to wheat rusts. Plant Breeding, 79, 1254–1255.Google Scholar
Lochmiller, R.L. & Deerenberg, C. (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos, 88, 87–98.Google Scholar
Marr, D.L. & Delph, L.F. (2005) Spatial and temporal pattern of a pollinator-transmitted pathogen in a long-lived perennial, Silene acaulis. Evolutionary Ecology Research, 7, 335–352.Google Scholar
McDade, T.W. (2003) Life history theory and the immune system: steps toward a human ecological immunology. American Journal of Physical Anthropology, 122(Suppl. 46), 100–125.Google Scholar
McNeill, W.H. (1976) Plagues and Peoples. New York, NY: Anchor Books.Google Scholar
Miller, M.R., White, A. & Boots, M. (2007) Host life span and the evolution of resistance characteristics. Evolution, 61, 2–14.Google Scholar
Morris, W. & Doak, D. (1998) Life history of the long-lived gynodioecious cushion plant Silene acaulis (Caryophyllaceae), inferred from size-based population projection matrices. American Journal of Botany, 85, 784–793.Google Scholar
Müller-Graf, C., Collins, D., Packer, C. & Woolhouse, M. (1997) Schistosoma mansoni infection in a natural population of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania. Parasitology, 115, 621–627.Google Scholar
Nunn, C. & Altizer, S. (2006) Infectious Diseases in Primates. Oxford: Oxford University Press.Google Scholar
Oppelt, C., Starkloff, A., Rausch, P., Von Holst, D. & Rodel, H. (2010) Major histocompatibility complex variation and age-specific endoparasite load in subadult European rabbits.Molecular Ecology, 19, 4155–4167.Google Scholar
Packer, A. & Clay, K. (2000) Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature, 404, 278–281.Google Scholar
Panter, S. & Jones, D.A. (2002) Age-related resistance to plant pathogens. Advances in Botanical Research, 38, 251–280.CrossRefGoogle Scholar
Parker, M.A. (1988) Polymorphism for disease resistance in the annual legume Amphicarpaea bracteata. Heredity, 60, 27–31.Google Scholar
Petit, E., Silver, C., Cornille, A., et al. (2017) Co-occurrence and hybridization of anther-smut pathogens specialized on Dianthus hosts. Molecular Ecology, 26, 1877–1890.Google Scholar
Poland, J.A., Balint-Kurti, P.J., Wisser, R.J., Pratt, R.C. & Nelson, R.J. (2009) Shades of gray: the world of quantitative disease resistance. Trends in Plant Science, 14, 21–29.Google Scholar
Raberg, L., Nilsson, J.A., Ilmonen, P., Stjernman, M. & Hasselquist, D. (2000) The cost of an immune response: vaccination reduces parental effort. Ecology Letters, 3, 382–386.Google Scholar
Rosengaus, R.B. & Traniello, J.F.A. (2001) Disease susceptibility and the adaptive nature of colony demography in the dampwood termite Zootermopsis angusticollis. Behavioral Ecology and Sociobiology, 50, 546–556.Google Scholar
Sait, S., Begon, M. & Thompson, D.J. (1994) The influence of larval age on the response of Plodia interpunctella to a granulosis virus. Journal of Invertebrate Pathology, 63, 107–110.CrossRefGoogle Scholar
Schäfer, A.M., Kemler, M., Bauer, R. & Begerow, D. (2010) The illustrated life cycle of Microbotryum on the host plant Silene latifolia. Botany, 88, 875–885.CrossRefGoogle Scholar
Susi, H. & Laine, A.-L. (2015) The effectiveness and costs of pathogen resistance strategies in a perennial plant. Journal of Ecology, 103, 303–315.Google Scholar
Thrall, P.H., Biere, A. & Antonovics, J. (1993) Plant life-history and disease susceptibility – the occurrence of Ustilago violacea on different species within the Caryophyllaceae. Journal of Ecology, 81, 489–498.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×