Pathogen evolution under host avoidance plasticity

Abstract

Host resistance consists of defences that limit pathogen burden, and can be classified as either adaptations targeting recovery from infection or those focused upon infection avoidance. Conventional theory treats avoidance as a fixed strategy which does not vary from one interaction to the next. However, there is increasing empirical evidence that many avoidance strategies are triggered by external stimuli, and thus should be treated as phenotypically plastic responses. Here, we consider the implications of avoidance plasticity for host-pathogen coevolution. We uncover a number of predictions challenging current theory. First, in the absence of pathogen trade-offs, plasticity can restrain pathogen evolution; moreover, the pathogen exploits conditions in which the host would otherwise invest less in resistance, causing resistance escalation. Second, when transmission trades off with pathogen-induced mortality, plasticity encourages avirulence, resulting in a superior fitness outcome for both host and pathogen. Third, plasticity ensures the sterilizing effect of pathogens has consequences for pathogen evolution. When pathogens castrate hosts, selection forces them to minimize mortality virulence; moreover, when transmission trades off with sterility alone, resistance plasticity is sufficient to prevent pathogens from evolving to fully castrate.

Trade-offs between host tolerances to different pathogens in plant-virus interactions

“…On the other hand, Arabidopsis could not optimize at the same time tolerances to viruses displaying different virulence levels (negative association between these tolerances), with LS-CMV and JPN1-TuMV (lower virulence) inducing different and mutually exclusive life-history modifications than UK1-TuMV (higher virulence). A number of experimental works reported that pathogen-driven changes in host life-history traits can be either genetically determined or the consequence of phenotypic plasticity ( Michalakis & Hochberg, 1994; Schlichting & Pigliucci, 1998; McLeod & Day, 2015 ). Thus, it could be hypothesized that one or both of these two types of determinisms may be involved in the observed tolerance-tolerance trade-offs.…”

Why is sterility virulence most common in sexually transmitted infections? Examining the role of epidemiology

“…We wish to use (3) to understand how selection, stochasticity, and epidemiology interact to shape the evolution of sterility virulence. To do so, we adopt the approach we used elsewhere (McLeod and Day 2019), and ask what is the likelihood of observing the stochastic process in a particular state? If we are more likely to observe the process in a state in which strain i is most frequent, then we will say strain i is favored.…”

“…Instead these previous studies have focused upon how spatial structure (O'Keefe and Antonovics ; Lion and Gandon ) or host coevolution (Best et al. ; Ashby and Boots ; McLeod and Day ) can limit the evolution of sterility virulence, without considering why sterility virulence is more common for STIs than directly transmitted pathogens.…”

“…Although the form of transmission has clear epidemiological consequences (Getz and Pickering 1983;de Castro and Bolker 2005), in deterministic models with large (ideally infinite) population sizes, if sterility virulence causes any increase in transmissibility, sterilizing pathogens are favored, irrespective of the form of transmission (Jaenike 1996;O'Keefe and Antonovics 2002;O'Keefe 2005). Indeed, evolutionary theory on sterility virulence has focused almost exclusively upon such models (Jaenike 1996;O'Keefe and Antonovics 2002;Best et al 2010;Ashby and Boots 2015;Lion and Gandon 2015;McLeod and Day 2015), ignoring the evolutionary consequences of epidemiology in finite populations. Instead these previous studies have focused upon how spatial structure (O'Keefe and Antonovics 2002;Lion and Gandon 2015) or host coevolution (Best et al 2010;Ashby and Boots 2015;McLeod and Day 2015) can limit the evolution of sterility virulence, without considering why sterility virulence is more common for STIs than directly transmitted pathogens.…”

“…Indeed, evolutionary theory on sterility virulence has focused almost exclusively upon such models (Jaenike 1996;O'Keefe and Antonovics 2002;Best et al 2010;Ashby and Boots 2015;Lion and Gandon 2015;McLeod and Day 2015), ignoring the evolutionary consequences of epidemiology in finite populations. Instead these previous studies have focused upon how spatial structure (O'Keefe and Antonovics 2002;Lion and Gandon 2015) or host coevolution (Best et al 2010;Ashby and Boots 2015;McLeod and Day 2015) can limit the evolution of sterility virulence, without considering why sterility virulence is more common for STIs than directly transmitted pathogens.…”