The Dominance of Coinfecting Parasites' Indirect Genetic Effects on Host Traits

AbstractIndirect genetic effects (IGEs) exist when there is heritable variation in one organism's ability to alter a second organism's traits. For example, parasites have antigens that can induce a host immune response, as well as disparate strategies to evade or suppress host immunity; among-parasite genetic variation in these antigens generates among-host variation in immune traits. Here, we experimentally show that the cestode parasite Schistocephalus solidus exerts an IGE on an immune trait (peritoneal fibrosis) in its threespine stickleback host: stickleback developed strong fibrosis after exposure to some parasite genotypes but not others. A complication arises during coinfection, when two or more parasite genotypes may impose conflicting IGEs on the same host trait. What parasite-controlled trait will the host express? Will the host trait reflect the more immune-stimulatory parasite genotype or the more immune-evasive genotype? These alternatives can be quantified by estimating the dominance coefficient, as if a coinfected host were a heterozygote. We experimentally estimated the dominance of S. solidus IGEs by coinjecting antigens from different parasite genotypes. Contrary to our a priori hypotheses, coinjected antigens induced an overdominant effect, stronger than either parasite's antigens alone. We present a mathematical model showing that the value of this IGE dominance is biologically important, affecting the evolutionary dynamics of parasites in a density- and frequency-dependent manner. The model indicates that overdominance would be detrimental to immigrants when resident prevalence is high. This combination of experimental data and modeling provides an example of a parasite IGE on host traits and the evolutionary significance of IGE dominance.