The evolutionary cost of homophily: Social stratification facilitates stable variant coexistence and increased rates of evolution in host-associated pathogens

Coexistence of multiple strains of a pathogen in a host population can present significant challenges to vaccine development or treatment efficacy. Here we discuss a novel mechanism that can increase rates of long-lived strain polymorphism, rooted in the presence of social structure in a host population. We show that social preference of interaction, in conjunction with differences in immunity between host subgroups, can exert varying selection pressure on pathogen strains, creating a balancing mechanism that supports stable viral coexistence, independent of other known mechanisms. We use population genetic models to study rates of pathogen heterozygosity as a function of population size, host population composition, mutant strain fitness differences and host social preferences of interaction. We also show that even small periodic epochs of host population stratification can lead to elevated strain coexistence. These results are robust to varying social preferences of interaction, overall differences in strain fitnesses, and spatial heterogeneity in host population composition. Our results highlight the role of host population social stratification in increasing rates of pathogen strain diversity, with effects that should be considered when designing policies or treatments with a long-term view of curbing pathogen evolution.Author summary: Understanding the mechanisms that shape and protect the maintenance of diversity in a pathogen population is of significant importance to curbing their spread in the population. Here we discuss a new diversity-promoting mechanism where, unlike typical balancing mechanisms, the diversity is not buffered from selection in protected life-stages of the pathogen or distinct spatially separated subpopulations, but instead, variant diversity is protected by the social interaction structure of the host population. In turn, increased diversity in the pathogen population increases the rate of their evolution, incurring the health cost to the host population, which we refer to as the evolutionary cost of homophily. Our model can also be interpreted through the lens of contagious social behaviors and showcases how the social architecture of the population can shape the coexistence of a diverse array of cultural variants. For both cultural or biological pathogens, understanding the evolutionary mechanisms that contribute to transient or stable variant diversity is essential for designing responses and policies that prevent increases in strain repertoire of pathogenic variants in the population.