The role of ecological feedbacks in the evolution of host defence: what does theory tell us?

Abstract

Hosts have evolved a diverse range of defence mechanisms in response to challenge by infectious organisms (parasites and pathogens). Whether defence is through avoidance of infection, control of the growth of the parasite once infected, clearance of the infection, tolerance to the disease caused by infection or innate and/or acquired immunity, it will have important implications for the population ecology (epidemiology) of the host-parasite interaction. As a consequence, it is important to understand the evolutionary dynamics of defence in the light of the ecological feedbacks that are intrinsic to the interaction. Here, we review the theoretical models that examine how these feedbacks influence the nature and extent of the defence that will evolve. We begin by briefly comparing different evolutionary modelling approaches and discuss in detail the modern game theoretical approach (adaptive dynamics) that allows ecological feedbacks to be taken into account. Next, we discuss a number of models of host defence in detail and, in particular, make a distinction between 'resistance' and 'tolerance'. Finally, we discuss coevolutionary models and the potential use of models that include genetic and game theoretical approaches. Our aim is to review theoretical approaches that investigate the evolution of defence and to explain how the type of defence and the costs associated with its acquisition are important in determining the level of defence that evolves.

Introduction. Ecological immunology

“…Ebert et al 2002;Forde et al 2004;Cooper et al 2005;Morgan et al 2005;Brockhurst et al 2006;Vogwill et al 2008), which in turn implies that they also affect evolution of the immune system. In fact, Boots et al (2009) review a number of theoretical articles which use population genetic models in order to evaluate evolution of different aspects of immune defence (e.g. avoidance, resistance or tolerance).…”

Host persistence or extinction from emerging infectious disease: insights from white-nose syndrome in endemic and invading regions

“…Two mechanisms, reduced host density for pathogens in which transmission is density-dependent, and poor environmental conditions for pathogen survival or replication outside hosts, will result in lower pathogen transmission [7,12]. Similarly, if hosts in the introduced region are inherently resistant to the pathogen or evolve to become resistant, then this will limit transmission [9,13]. By contrast, if hosts are tolerant (or evolve tolerance) then transmission of the pathogen will be maintained at a much higher intensity, with correspondingly large impacts on intolerant, nonresistant species.…”

Evolution of hosts paying manifold costs of defence

“…R. Soc. B 282: 20150065 [30]). Constitutive costs of immunity are those incurred in the development and maintenance of the immune system, whereas facultative costs are those incurred in the deployment of the immune system (or indeed any inducible defence system [36]).…”

“…The generality of the dependence of immunopathology upon recovery rate and/or exploitation [37,45], however, remains to be assessed with suitable data from a wider variety of systems, including those restricted to the urogenital tract. Moreover, the probability of infection will affect optimal investment into defence, via feedback loops between individual and population scales [30]. Clearly, more theoretical and empirical work is needed, to better understand host evolution in a world of costly and complex defensive demands.…”