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

Abstract

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.

Experimental hybridization and backcrossing reveal forces of reproductive isolation in Microbotryum

“…All Microbotryum genotypes produced by hybrid backcrossing caused anther-smut disease following inoculation of the natural host S. latifolia and the artificial host S. colorata [33], allowing assessment of the influence of native versus novel host environment (extrinsic factors) and mating type region (intrinsic factors). In total, 585 S. latifolia plants flowered and the mean infection rate across different gamete types were 0.83 (SE = 0.07), while on S. colorata the flowering individuals (414 in total) were diseased at the rate of 0.59 (SE = 0.05) (Table 2, Figure 2).…”

Host resistance and pathogen infectivity in host populations with varying connectivity

“…Resistance in this host–pathogen system can be mediated both by active physiological and passive morphological mechanisms, that is host floral traits such as flowering time, size and number of flowers, and stigma length that have the potential to alter the probability of visits by pollinators carrying spores of M. violaceum or the number of spores deposited on the flowers (Elmqvist et al ; Alexander et al ; Carlsson‐Granér ; Giles et al ; Gibson et al ). In this study we assessed variation in physiological resistance, which is the prevention of disease following exposure to the pathogen.…”

Genomic and transcriptomic analyses of Microbotryum lychnidis-dioicae provide insights into the biology of a fascinating fungal phytopathogen.

“…All of these could be some degree of disease presentation, since uninfected plants almost never displayed similar symptoms. Such symptoms had previously been observed and reported anecdotally (Fujita et al, 2012;Gibson et al, 2013). Various phenotypic changes were also observed with infection by M. lychnidis-dioicae in which the infection percentage was rather low (Shykoff & Kaltz, 1998).…”

“…Therefore, difficulty with achieving infection may not be uncommon; on the other hand, an acceptable infection rate is usually more than 60% (Gibson et al, 2013).…”

“…lychnidis-dioicae system. We hypothesize that the unusual plant symptoms we observed may be part of the plant's physiological defense strategy against the fungus (Gibson et al, 2013) or possible incompatibility between the host and pathogen . By suppressing bolting (remaining as a rosette), flowering (non-flowering bolts) or blooming (pre-mature death of buds), the host would present an environment where the fungus would be unable to propagate and complete its sexual life cycle through teliosporogenesis in the anthers.…”