Pathogen Relatedness Affects the Prevalence of within-Host Competition

Abstract

Although the evolutionary consequences of within-host competition among pathogens have been examined extensively, there exists a critical gap in our understanding of factors determining the prevalence of multiple infections. Here we examine the effects of relatedness among strains of the anther-smut pathogen Microbotryum violaceum on the probability of multiple infection in its host, Silene latifolia, after sequential inoculations. We found a significantly higher probability of multiple infection when interacting strains were more closely related, suggesting mechanisms of competitive exclusion that are conditional on genotypic characteristics of the strains involved. Pathogen relatedness therefore determines the prevalence of multiple infection in addition to its outcome, with important consequences for our understanding of virulence evolution and pathogen population structure and diversity.

Variation in Breeding System Traits within and among Populations ofMicrobotryum violaceumonSilene dioica

“…Being able to mate with oneself via selfing and intrapromycelial mating also provides reproductive assurance when an outcrossing partner is missing, for example, at low population density (Kaltz and Shykoff 1999), and makes it possible for a single teliospore to establish a new population (Charlesworth and Pannell 2001). Conjugation within the promycelium is also the most rapid way to produce an infectious dikaryon, which, in a systemic disease, could be crucial for successful infection when teliospores are delivered to flowers with short life spans, for example, the male flowers of dioecious caryophyllaceous species (Kaltz and Shykoff 2001), or where the first infecting pathogen genotype has the ability to exclude subsequent challenging infections (Hood 2003;Koskella et al 2006). However, rapid conjugation among the earliest products of meiosis is thought to reduce the production of sporidia, which limits the number of infectious dikaryons that can be produced by a teliospore (Thomas et al 2003;Giraud et al 2006).…”

Reciprocal Interaction Matrix Reveals Complex Genetic and Dose-Dependent Specificity among Coinfecting Parasites

“…Since hosts represent the parasites' primary environment, a potentially important environmental factor modifying their fitness is the presence of coinfecting parasites. In fact, individual hosts are often simultaneously infected by multiple parasite species (e.g., Holmes and Price 1986;Valtonen et al 2001) and genotypes (reviewed by Read and Taylor 2001) that interact (e.g., Lello et al 2004;de Roode et al 2005;Koskella et al 2006;Staves and Knell 2010;Laine 2011). Furthermore, because the genetic composition of the coinfecting parasite community is typically variable across multiply infected host individuals (i.e., dif-ferent hosts are infected by different parasite species and genotypes), we propose that the outcomes of interactions among parasites could show high variation, potentially contributing to the maintenance of genetic variation.…”

Bacterial cooperation controlled by mobile elements: kin selection versus infectivity

“…We do not deny that altruism among pathogens could evolve by kin selection and there are examples (Koskella et al, 2006;Buckling et al, 2007;Lopez-Villavicencio et al, 2007, 2011. It may well even be that infectivity evolves via kin selection in toxin-producing bacteria, but we contend that the lines of evidence brought in the paper of Rankin et al (2010) and Nogueira et al (2009) are far from sufficient to be conclusive.…”