Multiple infections by the anther smut pathogen are frequent and involve related strains.

Population models of host-parasite interactions predict that when different parasite genotypes compete within a host for limited resources, those that exploit the host faster will be selected, leading to an increase in parasite virulence. When parasites sharing a host are related, however, kin selec...

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Main Authors: Manuela López-Villavicencio, Odile Jonot, Amélie Coantic, Michael E Hood, Jérôme Enjalbert, Tatiana Giraud
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2007-11-01
Series:PLoS Pathogens
Online Access:https://doi.org/10.1371/journal.ppat.0030176
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spelling doaj-3a876582696b4c46ac79ad11e6d65fb52021-04-21T17:20:36ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742007-11-01311e17610.1371/journal.ppat.0030176Multiple infections by the anther smut pathogen are frequent and involve related strains.Manuela López-VillavicencioOdile JonotAmélie CoanticMichael E HoodJérôme EnjalbertTatiana GiraudPopulation models of host-parasite interactions predict that when different parasite genotypes compete within a host for limited resources, those that exploit the host faster will be selected, leading to an increase in parasite virulence. When parasites sharing a host are related, however, kin selection should lead to more cooperative host exploitation that may involve slower rates of parasite reproduction. Despite their potential importance, studies that assess the prevalence of multiple genotype infections in natural populations remain rare, and studies quantifying the relatedness of parasites occurring together as natural multiple infections are particularly scarce. We investigated multiple infections in natural populations of the systemic fungal plant parasite Microbotryum violaceum, the anther smut of Caryophyllaceae, on its host, Silene latifolia. We found that multiple infections can be extremely frequent, with different fungal genotypes found in different stems of single plants. Multiple infections involved parasite genotypes more closely related than would be expected based upon their genetic diversity or due to spatial substructuring within the parasite populations. Together with previous sequential inoculation experiments, our results suggest that M. violaceum actively excludes divergent competitors while tolerating closely related genotypes. Such an exclusion mechanism might explain why multiple infections were less frequent in populations with the highest genetic diversity, which is at odds with intuitive expectations. Thus, these results demonstrate that genetic diversity can influence the prevalence of multiple infections in nature, which will have important consequences for their optimal levels of virulence. Measuring the occurrence of multiple infections and the relatedness among parasites within hosts in natural populations may be important for understanding the evolutionary dynamics of disease, the consequences of vaccine use, and forces driving the population genetic structure of parasites.https://doi.org/10.1371/journal.ppat.0030176
collection DOAJ
language English
format Article
sources DOAJ
author Manuela López-Villavicencio
Odile Jonot
Amélie Coantic
Michael E Hood
Jérôme Enjalbert
Tatiana Giraud
spellingShingle Manuela López-Villavicencio
Odile Jonot
Amélie Coantic
Michael E Hood
Jérôme Enjalbert
Tatiana Giraud
Multiple infections by the anther smut pathogen are frequent and involve related strains.
PLoS Pathogens
author_facet Manuela López-Villavicencio
Odile Jonot
Amélie Coantic
Michael E Hood
Jérôme Enjalbert
Tatiana Giraud
author_sort Manuela López-Villavicencio
title Multiple infections by the anther smut pathogen are frequent and involve related strains.
title_short Multiple infections by the anther smut pathogen are frequent and involve related strains.
title_full Multiple infections by the anther smut pathogen are frequent and involve related strains.
title_fullStr Multiple infections by the anther smut pathogen are frequent and involve related strains.
title_full_unstemmed Multiple infections by the anther smut pathogen are frequent and involve related strains.
title_sort multiple infections by the anther smut pathogen are frequent and involve related strains.
publisher Public Library of Science (PLoS)
series PLoS Pathogens
issn 1553-7366
1553-7374
publishDate 2007-11-01
description Population models of host-parasite interactions predict that when different parasite genotypes compete within a host for limited resources, those that exploit the host faster will be selected, leading to an increase in parasite virulence. When parasites sharing a host are related, however, kin selection should lead to more cooperative host exploitation that may involve slower rates of parasite reproduction. Despite their potential importance, studies that assess the prevalence of multiple genotype infections in natural populations remain rare, and studies quantifying the relatedness of parasites occurring together as natural multiple infections are particularly scarce. We investigated multiple infections in natural populations of the systemic fungal plant parasite Microbotryum violaceum, the anther smut of Caryophyllaceae, on its host, Silene latifolia. We found that multiple infections can be extremely frequent, with different fungal genotypes found in different stems of single plants. Multiple infections involved parasite genotypes more closely related than would be expected based upon their genetic diversity or due to spatial substructuring within the parasite populations. Together with previous sequential inoculation experiments, our results suggest that M. violaceum actively excludes divergent competitors while tolerating closely related genotypes. Such an exclusion mechanism might explain why multiple infections were less frequent in populations with the highest genetic diversity, which is at odds with intuitive expectations. Thus, these results demonstrate that genetic diversity can influence the prevalence of multiple infections in nature, which will have important consequences for their optimal levels of virulence. Measuring the occurrence of multiple infections and the relatedness among parasites within hosts in natural populations may be important for understanding the evolutionary dynamics of disease, the consequences of vaccine use, and forces driving the population genetic structure of parasites.
url https://doi.org/10.1371/journal.ppat.0030176
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