Within-host competitive exclusion among species of the anther smut pathogen

Alexander Gold,Michael E Hood,Tatiana Giraud

doi:10.1186/1472-6785-9-11

Abstract

BackgroundHost individuals represent an arena in which pathogens compete for resources and transmission opportunities, with major implications for the evolution of virulence and the structure of populations. Studies to date have focused on competitive interactions within pathogen species, and the level of antagonism tends to increase with the genetic distance between competitors. Anther-smut fungi, in the genus Microbotryum, have emerged as a tractable model for within-host competition. Here, using two pathogen species that are frequently found in sympatry, we investigated whether the antagonism seen among genotypes of the same species cascades up to influence competition among pathogen species.ResultsSequential inoculation of hosts showed that a resident infection most often excludes a challenging pathogen genotype, which is consistent with prior studies. However, the challenging pathogen was significantly more likely to invade the already-infected host if the resident infection was a conspecific genotype compared to challenges involving a closely related species. Moreover, when inter-specific co-infection occurred, the pathogens were highly segregated within the host, in contrast to intra-specific co-infection.ConclusionWe show evidence that competitive exclusion during infection can be greater among closely related pathogen species than among genotypes within species. This pattern follows from prior studies demonstrating that genetic distance and antagonistic interactions are positively correlated in Microbotryum. Fungal vegetative incompatibility is a likely mechanism of direct competitive interference, and has been shown in some fungi to be effective both within and across species boundaries. For systems where related pathogen species frequently co-occur in the same host populations, these competitive dynamics may substantially impact the spatial segregation of pathogen species.

Highlights

Host individuals represent an arena in which pathogens compete for resources and transmission opportunities, with major implications for the evolution of virulence and the structure of populations
Treatments that sequentially inoculated S. vulgaris plants with combinations of two pathogen genotypes from either of two Microbotryum species resulted in high rates of infection (Table 1)
It is among these diseased plants that the outcome of within-host competition could be assessed by using morphological and genetic markers that discriminate each pathogen genotype used

Summary

Introduction

Host individuals represent an arena in which pathogens compete for resources and transmission opportunities, with major implications for the evolution of virulence and the structure of populations. Studies to date have focused on competitive interactions within pathogen species, and the level of antagonism tends to increase with the genetic distance between competitors. Theoretical studies focus heavily on virulence evolution and the consequence of whether the different pathogen genotypes remain together within the host, i.e. coinfection, or whether one competitively excludes the other, i.e. superinfection [5,6,7,8,9]. As pathogen genetic distance increases, there should be greater evolutionary conflict arising from sharing host resources, and enhanced selection for higher rates of exploitation associated with competition and virulence. Pathogen genetic diversity has been shown to influence both the outcome of competition and whether a particular disease system assumes a coinfection or superinfection model. Research has primarily focused on the intra-specific level of pathogen relatedness [11,13,16,17]

Methods

Results

Discussion

Conclusion