Parasite evolution in response to sex‐based host heterogeneity in resistance and tolerance

Abstract

Heterogenity between sexes in terms of both the level and the type of immune response to infection is documented in many species, but its role on parasite evolution is only beginning to be explored. We adopt an evolutionary epidemiology approach to study how the ability of a host to respond to infection through active immunity (resistance) or through minimizing deleterious effects of a given parasite load (tolerance) affects the evolution of parasite virulence. Consistently with earlier models, we find that increases in host resistance and tolerance both favour more virulent parasite strains. However, we show that qualitatively different results can be obtained if dimorphism between the sexes occurs through resistance or through tolerance depending on the contact pattern between the sexes. Finally, we find that variations in host sex ratio can amplify the consequences of heterogeneity for parasite evolution. These results are analysed in the light of several examples from the literature to illustrate the prevalence of sexually dimorphic immune responses and the potential for further study of the role of sexual dimorphism on parasite evolution. Such studies are likely to be highly relevant for improving treatment of chronic infections and control of infectious diseases, and understanding the role of sex in immune function.

The impact of host sex on the outcome of co-infection

“…In birds and mammals, for example, males are often more susceptible to infection and develop higher parasite loads than females 4,5 , whereas the reverse pattern is often observed in invertebrates 6–8 . When combined with the diversity of sex ratios, sex biases in dispersal, and general behavioural difference between males and females 1,9,10 , there is ample opportunity for dimorphism between the sexes to influence many aspects of disease epidemiology and evolution 3,8,11 .…”

The evolution of sex-specific virulence in infectious diseases

“…Epidemiological models of pathogens that are only horizontally or vertically transmitted do not consider pathogens that may exhibit different virulence in men and women (but see ref. 29 for sex-specific virulence as a result of different resistance of male and female hosts).…”

Host sexual dimorphism affects the outcome of within‐host pathogen competition

“…; Sheridan et al. ; Zuk ; Cousineau and Alizon ). The sexes may also represent hosts of varying exploitative potential due to differences in lifespan, energy acquisition, reproductive investment, or simply body or organ size (Christe et al.…”

“…; Gipson and Hall ). Together, this heterogeneity between the sexes is increasingly being linked to the performance of a single pathogen genotype within a male or female host and its subsequent transmission between susceptible hosts (e.g., Cousineau and Alizon ; Úbeda and Jansen ; Hall and Mideo ). Yet, it remains largely unexplored how each sex can influence the relationship between within‐host pathogen competition and virulence (but see Thompson et al.…”