Identifying the Molecular Basis of Host-Parasite Coevolution: Merging Models and Mechanisms

Abstract

Mathematical models of the coevolutionary process have uncovered consequences of host-parasite interactions that go well beyond the traditional realm of the Red Queen, potentially explaining several important evolutionary transitions. However, these models also demonstrate that the specific consequences of coevolution are sensitive to the structure of the infection matrix, which is embedded in models to describe the likelihood of infection in encounters between specific host and parasite genotypes. Traditional cross-infection approaches to estimating infection matrices might be unreliable because evolutionary dynamics and experimental sampling lead to missing genotypes. Consequently, our goal is to identify the likely structure of infection matrices by synthesizing molecular mechanisms of host immune defense and parasite counterdefense with coevolutionary models. This synthesis reveals that the molecular mechanisms of immune reactions, although complex and diverse, conform to two basic models commonly used within coevolutionary theory: matching infection and targeted recognition. Our synthesis also overturns conventional wisdom, revealing that the general models are not taxonomically restricted but are applicable to plants, invertebrates, and vertebrates. Finally, our synthesis identifies several important areas for future research that should improve the explanatory power of coevolutionary models. The most important among these include empirical studies to identify the molecular hotspots of genotypic specificity and theoretical studies examining the consequences of matrices that more accurately represent multistep infection processes and quantitative defenses.

Mutations That Determine Resistance Breaking in a Plant RNA Virus Have Pleiotropic Effects on Its Fitness That Depend on the Host Environment and on the Type, Single or Mixed, of Infection

“…In GFG systems there is a hierarchy of infectivity alleles in the pathogen and of resistance alleles in the host so that some pathogen infectivity alleles are intrinsically better than others, conferring the capacity to infect and multiply in a larger set of host genotypes, and, conversely, some host resistance alleles confer the capacity to resist a larger set of pathogen genotypes (14,55). In GFG systems the pathogen is predicted to evolve by successive steps of resistance breaking until it infects and multiplies in all host genotypes (14).…”

Parasite transmission among relatives halts Red Queen dynamics

“…To determine these probabilities, we implement the commonly used matching and inverse matching alleles models (Dybdahl et al. , and references therein, Metzger et al. 2016).…”

Host-Parasite Coevolutionary Dynamics with Generalized Success/Failure Infection Genetics

“…Moreover, as first pointed out by Frank (1996), an inherent problem with this approach is that it relies on the sampling of genotypes from polymorphism currently available in the host and parasite populations under study. This means that genotypes that occur at a low frequency in the population will usually be missed, and wrong conclusions about the overall infection matrix and the expected coevolutionary dynamics may be drawn (see also Dybdahl et al 2014 for a discussion of this problem). One way to reduce this problem would be to extensively sample many genotypes through time and space to achieve convergence to the "real" infection matrix involving all relevant genotypes.…”

“…An alternative approach that has recently been advocated by Dybdahl et al (2014) is to derive plausible infection matrices from experimentally established molecular principles about host immunology and parasite infection. This approach might uncover different types of infection matrices with different underlying host and parasite genes that govern the various stages of the infection process, such as host recognition by a parasite, parasite entry into the host, and detection and eradication of the parasite by the immune system.…”