The Evolutionary Consequences of Stepwise Infection Processes

Molecular and cellular studies reveal that the resistance of hosts to parasites and pathogens is a cascade-like process with multiple steps required to be passed for successful infection. By contrast, much of evolutionary reasoning is based on strongly simplified, one- or two-step infection processes with simple genetics or on resistance being a quantitative trait. Here we attempt a conceptual unification of these two perspectives with the aim of cross-fostering research and filling some of the gaps in our concepts of the ecology and evolution of disease. This conceptual unification has a profound impact on the way we understand the genetics and evolution of host resistance, ecological immunity, evolution of virulence, defence portfolios, and host-pathogen coevolution. Many biological traits are determined by the progression of stepwise events. Dissecting host-parasite interactions into steps offers great potential for understanding infectious disease biology and evolution.The steps of infection are typically governed by unequal contributions of genetic (G), environmental (E), and G. ×. E effects, allowing unique evolutionary trajectories at each step.Variation at each step has different consequences for hosts and pathogens. A pathogen must pass through all steps until transmission starts or else its fitness is zero. For the host, the profitability of resistance at a given step declines with increasing virulence experienced by the host.Red Queen coevolution driven by negative frequency-dependent selection can occur only at steps with host genotype-pathogen genotype interactions. By contrast, selective sweeps may occur at any step.