Associating with kin selects against disease tolerance

Abstract

Behavioural and physiological immunity are key to slowing epidemic spread. Here, we explore the evolutionary and epidemic consequences of their different costs for the evolution of tolerance vs. resistance: behavioural resistance affects social cohesion, with associated group-level costs, while physiological resistance costs should accrue to the individual. Further, the transmission-reduction benefits of resistance accrue differently to susceptible hosts and those already infected; infected hosts only benefit indirectly, by reducing transmission to kin. We therefore model the coevolution of transmission-reducing defences expressed in susceptible hosts with those expressed in infected hosts, as a function of kin association, and analyse the effect on population-level outcomes. Using parameter values for guppies, Poecilia reticulata, and their gyrodactylid parasites, we find that: 1) either susceptible or infected hosts should invest heavily in preventing infection, but not both; 2) kin association drives investment in physiological resistance more strongly than in behavioural resistance; 3) even weak levels of kin association can favour altruistic infected hosts that invest heavily in resistance (vs. selfish tolerance), eliminating the disease. Overall, our finding that weak kin association affects the coevolution of infected and susceptible investment in both behavioural and physiological immunity suggests that kin selection may affect disease dynamics across systems.