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

Gold, Alexander S.; Giraud, Tatiana; Hood, Michael E.

doi:10.1186/1472-6785-9-11

Cited by 27 publications

(38 citation statements)

References 54 publications

(86 reference statements)

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“…We provide evidence here that annual species become diseased at a significantly higher rate than perennial species under artificial inoculation. As verification of the artificial inoculation protocol used here, we find that infection rates on perennial species are comparable to those measured in prior studies using similar techniques (Biere and Honders 1996; Antonovics et al 2002; Hood 2003; Gold et al 2009). Moreover, the variation in infection rates observed between species is unlikely to be a technical artifact, as previous greenhouse and field experiments have shown that it represents heritable variation in physiological resistance (Alexander et al 1993; Biere and Honders 1996).…”

Section: Discussionsupporting

confidence: 86%

Life‐history strategy defends against disease and may select against physiological resistance

Gibson

Petit

Mena‐Alí

et al. 2013

Ecology and Evolution

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Host ecological traits may limit exposure to infectious disease, thereby generating the wide variation in disease incidence observed between host populations or species. The exclusion of disease by ecological traits may then allow selection to act against physiological defenses when they are costly to maintain in the absence of disease. This study investigates ecological resistance in the Silene-Microbotryum pathosystem. An estimated 80% of perennial Silene species host the anther-smut disease while no annuals harbor the disease in nature. Artificial inoculations of annual and perennial Silene plants, obtained from both natural and horticultural populations, demonstrate that the absence of disease in annuals is not explained by elevated physiological resistance. The annual habit is thus a powerful form of ecological defense against anther smut. Moreover, the higher susceptibility of annual species to anther smut relative to perennials supports the hypothesis of a loss of costly physiological resistance under ecological protection. The observation in annuals that physiological susceptibility is correlated with lower rates of flowering (i.e., lower fitness) suggests that variation in physiological resistance is costly in the absence of disease, even in a naїve Silene species. The absence of disease in natural populations of annuals combined with their high physiological susceptibility attest to the strength of host ecology in shaping the distribution of disease and to the dynamic nature of disease resistance.

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Section: Discussionsupporting

confidence: 86%

Life‐history strategy defends against disease and may select against physiological resistance

Gibson

Petit

Mena‐Alí

et al. 2013

Ecology and Evolution

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“…As with many diseases, the anther‐smut life history plays a role in shaping where the pathogen is found in nature. Anther‐smut fungi in the genus Microbotryum are obligate, biotrophic pathogens of perennial plants mainly in the Caryophyllaceae (Hood et al, ; Thrall, Biere, & Antonovics, ), where infections cause host sterility, are systemic and persistent, and have the potential to competitively exclude subsequent invasion by other Microbotryum pathogens (Gold et al, ; Hood, ; López‐Villavicencio et al, ). There are many host species for anther smut with broad and overlapping geographic distributions (Hitchcock & Maguire, ; Hood et al, ), and disease incidence can be remarkably high in some host species.…”

Section: Methodsmentioning

confidence: 99%

“…Anther‐smut disease, caused by fungi in the genus Microbotryum , is one of the most studied host–pathogen associations in natural systems (Figure ). This disease has been used as a model for pathogen speciation, pollinator‐mediated dispersal, multiple infection, biological invasion, and competition (Abbate & Antonovics, ; Bruns, Antonovics, & Hood, ; Fontaine, Gladieux, Hood, & Giraud, ; Giraud, Gladieux, & Gavrilets, ; Gold, Giraud, & Hood, ; Kemler et al, ; Le Gac, Hood, Fournier, & Giraud, ; Vercken et al, ). Research has shown that the fungi formerly grouped under the Microbotryum violaceum epithet represent a large species complex, consisting of many independent lineages, each specific (i.e., endemic) to only one or a very small number of host species (Kemler et al, ; Le Gac et al, ; Lutz et al, ; Piątek, Lutz, & Kemler, ; de Vienne, Hood, & Giraud, ).…”

Section: Introductionmentioning

confidence: 99%

Sympatry and interference of divergent Microbotryum pathogen species

Hood

Antonovics

Wolf

et al. 2019

Ecology and Evolution

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The impact of infectious diseases in natural ecosystems is strongly influenced by the degree of pathogen specialization and by the local assemblies of potential host species. This study investigated anther‐smut disease, caused by fungi in the genus Microbotryum , among natural populations of plants in the Caryophyllaceae. A broad geographic survey focused on sites of the disease on multiple host species in sympatry. Analysis of molecular identities for the pathogens revealed that sympatric disease was most often due to co‐occurrence of distinct, host‐specific anther‐smut fungi, rather than localized cross‐species disease transmission. Flowers from sympatric populations showed that the Microbotryum spores were frequently moved between host species. Experimental inoculations to simulate cross‐species exposure to the pathogens in these plant communities showed that the anther‐smut pathogen was less able to cause disease on its regular host when following exposure of the plants to incompatible pathogens from another host species. These results indicate that multi‐host/multi‐pathogen communities are common in this system and they involve a previously hidden mechanism of interference between Microbotryum fungi, which likely affects both pathogen and host distributions.

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“…DNA was extracted, using the Chelex (Bio‐Rad) method (Bucheli et al 2001), from one to two anthers from a single flower derived from each diseased sample. Artificial inoculation at the single meristem stage of seedlings largely prevents coexistence of multiple infections, resulting in systemic infection by the single pathogen genotype that persists in subsequently derived meristems (Hood 2003; Gold et al 2009). Anthers from a single flower were therefore considered accurate for genetic typing of an infection under our inoculation protocol.…”

Section: Methodsmentioning

confidence: 99%

“…Anthers from a single flower were therefore considered accurate for genetic typing of an infection under our inoculation protocol. Even in the unlikely event of multiple infections, they would segregate in different stems (Hood 2003; Gold et al 2009; López‐Villavicencio et al 2011), and our genotyped strains would represent an unbiased sample of the infecting strains.…”

Section: Methodsmentioning

confidence: 99%

Sibling Competition Arena: Selfing and a Competition Arena Can Combine to Constitute a Barrier to Gene Flow in Sympatry

2012

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Closely related species coexisting in sympatry provide critical insight into the mechanisms underlying speciation and the maintenance of genetic divergence. Selfing may promote reproductive isolation by facilitating local adaptation, causing reduced hybrid fitness in parental environments. Here, we propose a novel mechanism by which selfing can further impair interspecific gene flow: selfing may act to ensure that nonhybrid progeny systematically co-occur whenever hybrid genotypes are produced. Under a competition arena, the fitness differentials between nonhybrid and hybrid progeny are then magnified, preventing development of interspecific hybrids. We investigate whether this "sibling competition arena" can explain the coexistence in sympatry of closely related species of the plant fungal pathogens (Microbotryum) causing anther-smut disease. The probabilities of intrapromycelial mating (automixis), outcrossing, and sibling competition were manipulated in artificial inoculations to evaluate their contribution to reproductive isolation. We report that both intrapromycelial selfing and sibling competition significantly reduced rates of hybrid infection beyond that expected based solely upon selfing rates and noncompetitive fitness differentials between hybrid and nonhybrid progeny. Our results thus suggest that selfing and a sibling competition arena can combine to constitute a barrier to gene flow and diminish selection for additional barriers to gene flow in sympatry. K E Y W O R D S :Assortative mating, fungi, hybridization, prezygotic isolating mechanism, postzygotic reproductive isolation, selection arena, Silene, speciation.

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

Cited by 27 publications

References 54 publications

Life‐history strategy defends against disease and may select against physiological resistance

Life‐history strategy defends against disease and may select against physiological resistance

Sympatry and interference of divergent Microbotryum pathogen species

Sibling Competition Arena: Selfing and a Competition Arena Can Combine to Constitute a Barrier to Gene Flow in Sympatry

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