The evolution of age-specific resistance to infectious disease

Abstract

Innate, infection-preventing resistance often varies between host life-stages. Juveniles are more resistant than adults in some species, whereas the converse pattern is true in others. This variation cannot always be explained by prior exposure or physiological constraints and so it has been hypothesised that trade-offs with other life-history traits may be involved. However, little is known about how trade-offs between various life-history traits and resistance at different life-stages affect the evolution of age-specific resistance. Here, we use a mathematical model to explore how trade-offs with natural mortality, reproduction and maturation combine to affect the evolution of resistance at different life-stages. Our results show that certain combinations of trade-offs have substantial effects on whether adults or juveniles are more resistant, with trade-offs between juvenile resistance and adult reproduction inherently more costly than trade-offs involving maturation or mortality (all else being equal), resulting in consistent evolution of lower resistance at the juvenile stage even when infection causes a lifelong fecundity reduction. Our model demonstrates how the differences between patterns of age-structured resistance seen in nature may be explained by variation in the trade-offs involved and our results suggest conditions under which trade-offs tend to select for lower resistance in juveniles than adults.

The evolution of the age of onset of resistance to infectious disease

“…Recent theory has shown how trade-offs and life-history traits combine to shape the evolution of age-specific resistance (Ashby and Bruns 2018;Buckingham et al 2022) When the rate of onset of resistance diversifies, it results in a fully (or almost fully) susceptible subpopulation coexisting with a fully resistant subpopulation. Such dimorphic populations, where some individuals are effectively resistant throughout their lives and others are always (or almost always) susceptible, are often seen in real, biological systems (Parker 1988;Jarosz and Burdon 1990;Wayne et al 1996;Turkington et al 2019).…”

“…Recent theory has shown how trade-offs and life-history traits combine to shape the evolution of age-specific resistance (Ashby and Bruns 2018; Buckingham et al 2022). Here, we have shown how the average age at which hosts become resistant (1/ ζ ) evolves, depending on how and when costs of resistance are paid (costs only paid before or after the onset of resistance, or throughout the host’s lifetime).…”

“…The life-stage at which trade-offs occur has a significant effect on the evolution of the rate of onset of resistance. It is well established that the magnitude and shape of trade-offs, as well as the life-history traits involved, are critical to the evolution of various traits, including resistance (Kisdi 2006; Ashby and Bruns 2018; Buckingham et al 2022). We have shown that the life-stage at which trade-offs act also drastically alters the evolutionary outcome for the rate of onset of resistance.…”

“…(Antonovics and Thrall 1994; Boots and Haraguchi 1999; Carlsson-Graner and Thrall 2006; Miller et al 2007; Donnelly et al 2015)) but, in contrast, the evolution of age-structured resistance has received relatively little attention. However, recent theory has explored the evolution of age-specific resistance in juveniles and adults, showing that differences in resistance between life stages are most pronounced for particularly long- or short-lived hosts (Ashby and Bruns 2018) and that adult resistance often evolves to exceed juvenile resistance, depending on which traits trade off with resistance (Buckingham et al 2022). Here, we investigate a different characteristic of age-specific resistance, namely the timing of the onset of resistance.…”