Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-23T23:49:28.708Z Has data issue: false hasContentIssue false

Plasticity, not genetic variation, drives infection success of a fungal parasite

Published online by Cambridge University Press:  25 February 2015

C. L. SEARLE*
Affiliation:
Department of Biological Sciences, Purdue University, West Lafayette, Indiana 47907, USA
J. H. OCHS
Affiliation:
School of Biology, Georgia Institute of Technology, Atlanta, Georgia 30332, USA
C. E. CÁCERES
Affiliation:
School of Integrative Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, USA
S. L. CHIANG
Affiliation:
Department of Biology, Emory University, Atlanta, Georgia 30322, USA
N. M. GERARDO
Affiliation:
Department of Biology, Emory University, Atlanta, Georgia 30322, USA
S. R. HALL
Affiliation:
Department of Biology, Indiana University, Bloomington, Indiana 47405, USA
M. A. DUFFY
Affiliation:
Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan 48109, USA
*
*Corresponding author. Department of Biological Sciences, Purdue University, 915 W. State Street, West Lafayette, Indiana 47907-2054, USA. E-mail: [email protected]

Summary

Hosts strongly influence parasite fitness. However, it is challenging to disentangle host effects on genetic vs plasticity-driven traits of parasites, since parasites can evolve quickly. It remains especially difficult to determine the causes and magnitude of parasite plasticity. In successive generations, parasites may respond plastically to better infect their current type of host, or hosts may produce generally ‘good’ or ‘bad’ quality parasites. Here, we characterized parasite plasticity by taking advantage of a system in which the parasite (the yeast Metschnikowia bicuspidata, which infects Daphnia) has no detectable heritable variation, preventing rapid evolution. In experimental infection assays, we found an effect of rearing host genotype on parasite infectivity, where host genotypes produced overall high or low quality parasite spores. Additionally, these plastically induced differences were gained or lost in just a single host generation. Together, these results demonstrate phenotypic plasticity in infectivity driven by the within-host rearing environment. Such plasticity is rarely investigated in parasites, but could shape epidemiologically important traits.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2015 

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

Altizer, S., Harvell, D. and Friedle, E. (2003). Rapid evolutionary dynamics and disease threats to biodiversity. Trends in Ecology and Evolution 18, 589596.CrossRefGoogle Scholar
Auld, S. K. J. R., Hall, S. R. and Duffy, M. A. (2012). Epidemiology of a Daphnia-multiparasite system and its implications for the Red Queen. PLoS ONE 7, e39564.CrossRefGoogle ScholarPubMed
Auld, S. K. J. R., Penczykowski, R. M., Ochs, J. H., Grippi, D. C., Hall, S. R. and Duffy, M. A. (2013). Variation in costs of parasite resistance among natural host populations. Journal of Evolutionary Biology 26, 24792486.CrossRefGoogle ScholarPubMed
Auld, S. K. J. R., Hall, S. R., Ochs, J. H., Sebastian, M. and Duffy, M. A. (2014). Predators and patterns of within-host growth can mediate both among-host competition and the evolution of transmission potential of parasites. The American Naturalist 184, S77S90.CrossRefGoogle ScholarPubMed
Bakker, T. C. M., Mazzi, D. and Zala, S. (1997). Parasite-induced changes in behavior and color make Gammarus pulex more prone to fish predation. Ecology 78, 10981104.CrossRefGoogle Scholar
Begon, M., Hazel, S. M., Baxby, D., Bown, K., Cavanagh, R., Chantrey, J., Jones, T. and Bennett, M. (1999). Transmission dynamics of a zoonotic pathogen within and between wildlife host species. Proceedings of the Royal Society B: Biological Sciences 266, 19391945.CrossRefGoogle ScholarPubMed
Berdoy, M., Webster, J. P. and Macdonald, D. W. (2000). Fatal attraction in rates infected with Toxoplasma gondii. Proceedings of the Royal Society B: Biological Sciences 267, 15911594.CrossRefGoogle Scholar
Berger, L., Marantelli, G., Skerratt, L. F. and Speare, R. (2005). Virulence of the amphibian chytrid fungus Batrachochytrium dendrobatidis varies with the strain. Diseases of Aquatic Organisms 68, 4750.CrossRefGoogle ScholarPubMed
Boots, M., Best, A., Miller, M. R. and White, A. (2009). The role of ecological feedbacks in the evolution of host defense: what does theory tell us? Philosophical Transactions of the Royal Society B 364, 2736.CrossRefGoogle ScholarPubMed
Cáceres, C. E. and Tessier, A. J. (2004). To sink or swim: variable diapause strategies among Daphnia species. Limnology and Oceanography 49, 13331340.CrossRefGoogle Scholar
Cáceres, C. E., Hall, S. R., Duffy, M. A., Tessier, A. J., Helmle, C. and MacIntyre, S. (2006). Physical structure of lakes constrains epidemics in Daphnia populations. Ecology 87, 14381444.CrossRefGoogle ScholarPubMed
Cameron, A., Reece, S. E., Drew, D. R., Haydon, D. T. and Yates, A. J. (2013). Plasticity in transmission strategies of the malaria parasite, Plasmodium chabaudi: environmental and genetic effects. Evolutionary Applications 6, 365376.CrossRefGoogle ScholarPubMed
Carius, H. J., Little, T. J. and Ebert, D. (2001). Genetic variation in a host–parasite association: potential for coevolution and frequency-dependent selection. Evolution 55, 11361145.Google Scholar
Cornet, S., Bichet, C., Larcombe, S., Faivre, B. and Sorci, G. (2014). Impact of host nutritional status on infection dynamics and parasite virulence in a bird-malaria system. Journal of Animal Ecology 83, 256265.CrossRefGoogle Scholar
Craft, M. E., Hawthorne, P. L., Packer, C. and Dobson, A. P. (2008). Dynamics of a multihost pathogen in a carnivore community. Journal of Animal Ecology 77, 12571264.CrossRefGoogle Scholar
Dlugosch, K. M. and Parker, I. M. (2008). Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple invasions. Molecular Ecology 17, 431449.CrossRefGoogle Scholar
Duffy, M. A. and Hall, S. R. (2008). Selective predation and rapid evolution can jointly dampen effects of virulent parasites on Daphnia populations. The American Naturalist 171, 499510.CrossRefGoogle ScholarPubMed
Duffy, M. A. and Forde, S. E. (2009). Ecological feedbacks and the evolution of resistance. Journal of Animal Ecology 78, 11061112.CrossRefGoogle ScholarPubMed
Duffy, M. A. and Sivars-Becker, L. (2007). Rapid evolution and ecological host-parasite dynamics. Ecology Letters 10, 4453.CrossRefGoogle ScholarPubMed
Duffy, M. A., Cáceres, C. E., Hall, S. R., Tessier, A. J. and Ives, A. R. (2010). Temporal, spatial and between-host comparisons of patterns of parasitism in lake zooplankton. Ecology 91, 33223331.CrossRefGoogle ScholarPubMed
Duffy, M. A., Ochs, J. H., Penczykowski, R. M., Cáceres, C. E. and Hall, S. R. (2011). Unhealthy herds: indirect effects of predators enhance two drivers of disease spread. Functional Ecology 25, 945953.CrossRefGoogle Scholar
Duffy, M. A., Ochs, J. H., Penczykowski, R. M., Civitello, D. J., Klausmeier, C. A. and Hall, S. R. (2012). Ecological context influences epidemic size and parasite-mediated selection. Science 335, 16361638.CrossRefGoogle Scholar
Ebert, D. (1998). Experimental evolution of parasites. Science 282, 14321435.CrossRefGoogle ScholarPubMed
Ebert, D., Zschokke-Rohringer, C. D. and Carius, H. J. (1998). Within- and between-population variation for resistance of Daphnia magna to the bacterial endoparasite Pasteuria ramosa . Proceedings of the Royal Society B: Biological Sciences 265, 21272134.CrossRefGoogle Scholar
Ebert, D., Lipsitch, M. and Mangin, K. L. (2000). The effect of parasites on host population density and extinction: experimental epidemiology with Daphnia and six microparasites. The American Naturalist 156, 459477.CrossRefGoogle ScholarPubMed
Ellner, S. P., Geber, M. A. and Hairston, N. G. (2011). Does rapid evolution matter? Measuring the rate of contemporary evolution and its impacts on ecological dynamics. Ecology Letters 14, 603614.CrossRefGoogle ScholarPubMed
England, P. R., Osler, G. H. R., Woodworth, L. M., Montgomery, M. E., Briscoe, D. A. and Frankham, R. (2003). Effects of intense versus diffuse population bottlenecks on microsatellite genetic diversity and evolutionary potential. Conservation Genetics 4, 595604.CrossRefGoogle Scholar
Godfrey, S. S., Bull, C. M., James, R. and Murray, K. (2009). Network structure and parasite transmission in a group of living lizard, the gidgee skink, Egernia stokesii . Behavioral Ecology and Sociobiology 67, 10451056.CrossRefGoogle Scholar
Green, J. (1974). Parasites and epibionts of Cladocera. Transactions of the Zoological Society of London 32, 417515.CrossRefGoogle Scholar
Greischar, M. A. and Koskella, B. (2007). A synthesis of experimental work on parasite local adaptation. Ecology Letters 10, 418434.CrossRefGoogle ScholarPubMed
Hall, S. R., Simonis, J. L., Nisbet, R. M., Tessier, A. J. and Cáceres, C. E. (2009). Resource ecology of virulence in a planktonic host–parasite system: an explanation using dynamic energy budgets. The American Naturalist 174, 149162.CrossRefGoogle Scholar
Hall, S. R., Becker, C. R., Duffy, M. A. and Cáceres, C. E. (2010 a). Variation in resource acquisition and use among host clones creates key epidemiological trade-offs. The American Naturalist 176, 557565.CrossRefGoogle ScholarPubMed
Hall, S. R., Smyth, R., Becker, C. R., Duffy, M. A., Knight, C. J., MacIntyre, S., Tessier, A. J. and Cáceres, C. E. (2010 b). Why are Daphnia in some lakes sicker? Disease ecology, habitat structure, and the plankton. Bioscience 60, 363375.CrossRefGoogle Scholar
Hall, S. R., Becker, C. R., Duffy, M. A. and Cáceres, C. E. (2012). A power-efficiency trade-off in resource use alters epidemiological relationships. Ecology 93, 645656.CrossRefGoogle ScholarPubMed
Hebert, P. D. N. (1995). The Daphnia of North America: an Illustrated Fauna. CyberNatural Software, University of Guelph, Guelph, Canada.Google Scholar
Kaltz, O. and Shykoff, J. A. (1998). Local adaptation in host–parasite systems. Heredity 81, 361370.CrossRefGoogle Scholar
Kaltz, O., Gandon, S., Michalakis, Y. and 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, 395407.Google ScholarPubMed
Kluttgen, B., Dulmer, U., Engels, M. and Ratte, H. T. (1994). ADaM, an artificial freshwater for the culture of zooplankton. Water Resources. 28, 743746.Google Scholar
Leggett, H. C., Benmayor, R., Hodgson, D. J. and Buckling, A. (2013). Experimental evolution of adaptive phenotypic plasticity in a parasite. Current Biology 23, 139142.CrossRefGoogle Scholar
Lively, C. M. (1989). Adaptation by a parasitic trematode to local populations of its snail host. Evolution 43, 16631671.CrossRefGoogle ScholarPubMed
Lively, C. M. and Dybdahl, M. F. (2000). Parasites adaptation to locally common host genotypes. Nature 405, 679681.CrossRefGoogle ScholarPubMed
Lloyd-Smith, J. O., Schreiber, S. J., Kopp, P. E. and Getz, W. M. (2005). Superspreading and the effect of individual variation on disease emergence. Nature 438, 355359.CrossRefGoogle ScholarPubMed
Louhi, K. R., Karvonen, A., Rellstab, C. and Jokela, J. (2013). Genotypic and phenotypic variation in transmission traits of a complex life cycle parasite. Ecology and Evolution 3, 21162127.CrossRefGoogle ScholarPubMed
LoVerde, P. T., DeWald, J., Minchella, D. J., Bosshardt, S. C. and Damian, R. T. (1985). Evidence for host-induced selection in Schistosoma mansoni . Journal of Parasitology 71, 297301.CrossRefGoogle ScholarPubMed
Lynch, M. and Ennis, R. (1983). Resource availability, maternal effects, and longevity. Experimental Gerontology 18, 147165.CrossRefGoogle ScholarPubMed
Mideo, N. and Reece, S. E. (2012). Plasticity in parasite phenotypes: evolutionary and ecological implications for disease. Future Microbiology 7, 1724.CrossRefGoogle ScholarPubMed
Peay, K. F., Kennedy, P. G. and Bruns, T. D. (2008). Fungal community ecology: a hybrid beast with a molecular master. BioScience 58, 799810.CrossRefGoogle Scholar
Penczykowski, R. M., Hall, S. R., Civitello, D. J. and Duffy, M. A. (2014 a). Habitat structure and ecological drivers of disease. Limnology and Oceanography 59, 340348.CrossRefGoogle Scholar
Penczykowski, R. M., Lemanski, B. C. P., Sieg, R. D., Hall, S. R., Ochs, J. H., Kubanek, J. and Duffy, M. A. (2014 b). Poor resource quality lowers transmission potential by changing foraging behaviour. Functional Ecology 28, 12451255.CrossRefGoogle Scholar
Pulkkinen, K. and Ebert, D. (2004). Host starvation decreases parasite load and mean host size in experimental populations. Ecology 85, 823833.CrossRefGoogle Scholar
R Core Development Team (2012). R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/.Google Scholar
Reece, S. E., Ramiro, R. S. and Nussey, D. H. (2009). Plastic parasites: sophisticated strategies for survival and reproduction? Evolutionary Applications 2, 1123.CrossRefGoogle ScholarPubMed
Searle, C. L., Gervasi, S. S., Hua, J., Hammond, J. I., Relyea, R. A., Olson, D. H. and Blaustein, A. R. (2011). Differential host susceptibility to Batrachochytrium dendrobatidis, an emerging amphibian pathogen. Conservation Biology 25, 965974.CrossRefGoogle ScholarPubMed
Sicard, D., Pennings, P. S., Grandcement, C., Acosta, J., Kaltz, O. and Shykoff, J. A. (2007). Specialization and local adaptation of a fungal parasite on two host plant species as revealed by two fitness traits. Evolution 61, 2741.CrossRefGoogle ScholarPubMed
Tessier, A. J. and Woodruff, P. (2002). Cryptic trophic cascade along a gradient of lake size. Ecology 83, 12631270.CrossRefGoogle Scholar
Thrall, P. H. and Burdon, J. J. (2003). Evolution of virulence in a plant host–pathogen metapopulation. Science 299, 17351737.CrossRefGoogle Scholar
Tschirren, B., Bischoff, L. L., Saladin, V. and Richner, H. (2007). Host condition and host immunity affect parasite fitness in a bird-ectoparasite system. Functional Ecology 21, 372378.CrossRefGoogle Scholar
Tsutsui, N. D., Suarez, A. V., Holway, D. A. and Case, T. J. (2000). Reduced genetic variation and the success of an invasive species. Proceedings of the National Academy of the Sciences, USA 97, 59485953.CrossRefGoogle ScholarPubMed
Wolinska, J., Giessler, S. and Koerner, H. (2009). Molecular identification and hidden diversity of novel Daphnia parasites from European lakes. Applied and Environmental Microbiology 75, 70517059.CrossRefGoogle ScholarPubMed
Woolhouse, M. E., Dye, C., Etard, J. F., Smith, T., Charlwood, J. D., Garnett, G. P., Hagan, P., Hii, J. L., 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 the Sciences, USA 94, 338342.CrossRefGoogle ScholarPubMed
Wootton, J. C., Feng, X., Ferdig, M. T., Cooper, R. A., Mu, J., Baruch, D. I., Magill, A. J. and Xu, X. (2002). Genetic diversity and chloroquine selective sweeps in Plasmodium falciparum . Nature 418, 320323.CrossRefGoogle ScholarPubMed
Zuur, A., Ieno, E. N., Walker, N., Saveliev, A. A. and Smith, G. M. (2009). Mixed Effects Models and Extensions in Ecology with R, 1st Edn. Springer, New York, NY.CrossRefGoogle Scholar
Supplementary material: File

Searle supplementary material

Tables S1-S2 and Figure S1

Download Searle supplementary material(File)
File 154.4 KB