Pathogen and host genotype differently affect pathogen fitness through their effects on different life-history stages

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Abstract

Background

Adaptation of pathogens to their hosts depends critically on factors affecting pathogen reproductive rate. While pathogen reproduction is the end result of an intricate interaction between host and pathogen, the relative contributions of host and pathogen genotype to variation in pathogen life history within the host are not well understood. Untangling these contributions allows us to identify traits with sufficient genetic variation for selection to act and to identify mechanisms of coevolution between pathogens and their hosts. We investigated the effects of pathogen and host genotype on three life-history components of pathogen fitness; infection efficiency, latent period, and sporulation capacity, in the oat crown rust fungus, Puccinia coronata f.sp. avenae, as it infects oats ( Avena sativa).

Results

We show that both pathogen and host genotype significantly affect total spore production but do so through their effects on different life-history stages. Pathogen genotype has the strongest effect on the early stage of infection efficiency, while host genotype most strongly affects the later life-history stages of latent period and sporulation capacity. In addition, host genotype affected the relationship between pathogen density and the later life-history traits of latent period and sporulation capacity. We did not find evidence of pathogen-by-host genotypic (GxG) interactions.

Conclusion

Our results illustrate mechanisms by which variation in host populations will affect the evolution of pathogen life history. Results show that different pathogen life-history stages have the potential to respond differently to selection by host or pathogen genotype and suggest mechanisms of antagonistic coevolution. Pathogen populations may adapt to host genotypes through increased infection efficiency while their plant hosts may adapt by limiting the later stages of pathogen growth and spore production within the host.

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Most cited references 58

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Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection.

Antje D. Ebert, Gareth T. Little, H Carius (2001)

Models of host-parasite coevolution assume the presence of genetic variation for host resistance and parasite infectivity, as well as genotype-specific interactions. We used the freshwater crustacean Daphnia magna and its bacterial microparasite Pasteuria ramosa to study genetic variation for host susceptibility and parasite infectivity within each of two populations. We sought to answer the following questions: Do host clones differ in their susceptibility to parasite isolates? Do parasite isolates differ in their ability to infect different host clones? Are there host clone-parasite isolate interactions? The analysis revealed considerable variation in both host resistance and parasite infectivity. There were significant host clone-parasite isolate interactions, such that there was no single host clone that was superior to all other clones in the resistance to every parasite isolate. Likewise, there was no parasite isolate that was superior to all other isolates in infectivity to every host clone. This form of host clone-parasite isolate interaction indicates the potential for coevolution based on frequency-dependent selection. Infection success of original host clone-parasite isolate combinations (i.e., those combinations that were isolated together) was significantly higher than infection success of novel host clone-parasite isolate combinations (i.e., those combinations that were created in the laboratory). This finding is consistent with the idea that parasites track specific host genotypes under natural conditions. In addition, correspondence analysis revealed that some host clones, although distinguishable with neutral genetic markers, were susceptible to the same set of parasite isolates and thus probably shared resistance genes.

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Evolutionary dynamics of plant R-genes.

J Bergelson, M Kreitman, E Stahl … (2001)

Plant R-genes involved in gene-for-gene interactions with pathogens are expected to undergo coevolutionary arms races in which plant specificity and pathogen virulence continually adapt in response to each other. Lending support to this idea, the solvent-exposed amino acid residues of leucine-rich repeats, a region of R-genes involved in recognizing pathogens, often evolve at unusually fast rates. But within-species polymorphism is also common in R-genes, implying that the adaptive substitution process is not simply one of successive selective sweeps. Here we document these features in available data and discuss them in light of the evolutionary dynamics they likely reflect.

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Evolutionary ecology of plant diseases in natural ecosystems.

Robert G. Gilbert (2001)

Plant pathogens cause mortality and reduce fecundity of individual plants, drive host population dynamics, and affect the structure and composition of natural plant communities. Pathogens are responsible for both numerical changes in host populations and evolutionary changes through selection for resistant genotypes. Linking such ecological and evolutionary dynamics has been the focus of a growing body of literature on the effects of plant diseases in natural ecosystems. A guiding principle is the importance of understanding the spatial and temporal scales at which plants and pathogens interact. This review summarizes the effects of diseases on populations of wild plants, focusing in particular on the mediation of plant competition and succession, the maintenance of plant species diversity, as well as the process of rapid evolutionary changes in host-pathogen symbioses.

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Author and article information

Journal

Journal ID (nlm-ta): BMC Evol Biol

Journal ID (iso-abbrev): BMC Evol. Biol

Title: BMC Evolutionary Biology

Publisher: BioMed Central

ISSN (Electronic): 1471-2148

Publication date Collection: 2012

Publication date (Electronic): 2 August 2012

Volume: 12

Page: 135

Affiliations

[1 ]Department of Ecology Evolution and Behavior, University of Minnesota, Saint Paul, MN, 55108, USA

[2 ]Graduate Program in Ecology, Evolution and Behavior, University of Minnesota, Saint Paul, MN, 55108, USA

[3 ]United States Department of Agriculture – Agriculture Research Service, Cereal Disease Laboratory, University of Minnesota, Saint Paul, 55108, USA

Article

Publisher ID: 1471-2148-12-135

DOI: 10.1186/1471-2148-12-135

PMC ID: 3483255

PubMed ID: 22857005

SO-VID: 8185ceda-66c7-4e44-bbaf-ed70b4c988e8

License:

This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Pathogen and host genotype differently affect pathogen fitness through their effects on different life-history stages

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Abstract

Background

Results

Conclusion

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European Journal of Microbiology and Immunology

Most cited references 58

Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection.

Evolutionary dynamics of plant R-genes.

Evolutionary ecology of plant diseases in natural ecosystems.

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