Resistance Correlations Influence Infection by Foreign Pathogens

Abstract

AbstractReciprocal selection promotes the specificity of host-pathogen associations and resistance polymorphisms in response to disease. However, plants and animals also vary in response to pathogen species not previously encountered in nature, with potential effects on new disease emergence. Using anther smut disease, we show that resistance (measured as infection rates) to foreign pathogens can be correlated with standing variation in resistance to an endemic pathogen. In Silene vulgaris, genetic variation in resistance to its endemic anther smut pathogen correlated positively with resistance variation to an anther smut pathogen from another host, but the relationship was negative between anther smut and a necrotrophic pathogen. We present models describing the genetic basis for assessing resistance relationships between endemic and foreign pathogens and for quantifying infection probabilities on foreign pathogen introduction. We show that even when the foreign pathogen has a lower average infection ability than the endemic pathogen, infection outcomes are determined by the sign and strength of the regression of the host's genetic variation in infection rates by a foreign pathogen on variation in infection rates by an endemic pathogen as well as by resistance allele frequencies. Given that preinvasion equilibria of resistance are determined by factors including resistance costs, we show that protection against foreign pathogens afforded by positively correlated resistances can be lessened or even result in elevated infection risk at the population level, depending on local dynamics. Therefore, a pathogen's emergence potential could be influenced not only by its average infection rate but also by resistance variation resulting from prior selection imposed by endemic diseases.

Keywords: Microbotryum; disease emergence; disease resistance; host shift.

Figure 1.

Relationship of family-level variation in infection rates in Silene vulgaris following inoculation with the endemic pathogen Microbotryum silenes-inflatae and (A) infection rate by the foreign pathogen Microbotryum lychnidis-dioicae or (B) lesion size following infection by the foliar leaf spot pathogen Stemphylium solani. Circle diameters reflect sample size for families, depending upon seedling survival. Black circles indicate statistical outliers from the overall correlation of resistances (see main text). Lines represent total least squares regression with (dashed) and without (solid) outlier families.

Figure 2.

Representation of the possible rates of infection of two host genotypes (A₂ more resistant than A₁) by an endemic (blue, solid) and a foreign pathogen (red, dotted). Infection rates are represented by the transmission coefficients β_ij for pathogen type j on host type i. (A) Infection rates to the endemic and foreign pathogens represented as ‘reaction norms’ of the two genotypes. $\widehat{S}$ and ${\widehat{S}}^{\prime }$ are the average infection rates for the endemic and foreign pathogens, respectively. (B) Graph showing the result of genetic regression of infection rates by a foreign pathogen on infection rates by an endemic pathogen with two host genotypes. The dashed regression line has a slope T (i.e. “transitivity slope”). The boundary of the shaded grey area is the diagonal one-to-one line showing unit slope and zero y-intercept. $\widehat{S}-{\widehat{S}}^{\prime }$ is the reduction in the average foreign pathogen infection rate relative to the endemic pathogen infection rate.

Figure 3.

Resistance transitivity and infection probabilities by a foreign pathogen for a model of the anther-smut disease. (A) Depiction of the range of transitivity slopes investigated with average infection rate of the foreign pathogen reduced by $\widehat{S}-{\widehat{S}}^{\prime }=0.1$. The axes are comparable to Fig 1A or 2B above. The boundary of the shaded grey area shows the one-to-one line of unit slope (T = 1) and no reduction in average infection rate of the foreign pathogen ($\widehat{S}-{\widehat{S}}^{\prime }=0$) . (B) Probability that the foreign pathogen will infect a random healthy host (p_h β₁₂ + (1 – p_h) β₂₂) in a population at equilibrium and with the endemic pathogen present over the range of resistance costs leading to stable polymorphism for the resistance allele A₂. The thin solid grey line shows the frequency of the resistant allele at equilibrium. (C) As above, but the probability that the foreign pathogen will infect a random healthy host is plotted as a function of the resistance allele frequencies (1 – p_h) at equilibrium generated by the range of resistance costs. For reference, points above the grey shaded area show where infection rate for the foreign pathogen is greater than for the endemic pathogen. Model parameters are $\widehat{S}-{\widehat{S}}^{\prime }=0.1$, β₁₁ = 0.8 and β₂₁ = 0.2, μ = 0.1, γ = 0.01, b₁ = 1, and with cost of resistance, C, varying from 0.2 to 0.8.