Incomplete host immunity favors the evolution of virulence in an emergent pathogen

Abstract

Immune memory evolved to protect hosts from reinfection, but incomplete responses that allow future reinfection may inadvertently select for more-harmful pathogens. We present empirical and modeling evidence that incomplete immunity promotes the evolution of higher virulence in a natural host-pathogen system. We performed sequential infections of house finches with strains of various levels of virulence. Virulent bacterial strains generated stronger host protection against reinfection than less virulent strains and thus excluded less virulent strains from infecting previously exposed hosts. In a two-strain model, the resulting fitness advantage selected for an almost twofold increase in pathogen virulence. Thus, the same immune systems that protect hosts from infection can concomitantly drive the evolution of more-harmful pathogens in nature.

Rapid Antagonistic Coevolution in an Emerging Pathogen and Its Vertebrate Host

“…In addition, because non-resistant birds are immuno-suppressed by M. gallisepticum and so cannot mount a protective immune response [17,34,35], any potential maternal effect would require the prior evolution of genetic resistance. Third, we ensured that all birds used in the experiment were captured within 3 months post-fledging and had no prior exposure to the pathogen, meaning that population differences cannot be explained by secondary responses to infection [12,36] (see STAR Methods). Taken together, our results strongly suggest that house finches have evolved genetic resistance in direct response to the pathogen.…”

“…Most notably, our results suggest that apparent evidence for tolerance is likely to be an artifact of inoculation with an early, non-virulent 1994 isolate: inoculation with later-epidemic isolates are required to generate the differences between ancestral and adapted populations predicted under resistance. Second, it has been recently hypothesized that incomplete immunity against M. gallisepticum protects hosts against secondary infections with low virulence isolates, thereby favoring the evolution of increasing virulence [12]. This hypothesis assumes that the selective consequences of secondary infections are sufficiently high to drive the evolution of pathogen virulence.…”

“…Despite this, direct evidence for host-pathogen coevolution is exceptional [5][6][7], particularly in vertebrate hosts. Indeed, although vertebrate hosts have been shown to evolve in response to pathogens or vice versa [8][9][10][11][12], there is little evidence for the necessary reciprocal changes in the success of both antagonists over time [13]. Here, we generate a time-shift experiment to demonstrate adaptive, reciprocal changes in North American house finches (Haemorhous mexicanus) and their emerging bacterial pathogen, Mycoplasma gallisepticum [14][15][16].…”

Virulence‐driven trade‐offs in disease transmission: A meta‐analysis*

“…For instance, a recent study found an important role of incomplete immunity driving the selection of higher virulence (Fleming‐Davies et al. ). As noted by Ebert and Bull (), the trade‐off hypothesis reduces the relationship between variables to two dimensions when multiple variables may interact to influence, for example, the relationship between virulence and transmission rate.…”

Understanding the Evolutionary Ecology of host–pathogen Interactions Provides Insights into the Outcomes of Insect Pest Biocontrol

“…A crucial result obtained by fitting SIR-type models to data on infectious diseases is the discovery that the non-linear relationships between host density and transmission are often better explained by models that incorporate heterogeneity in transmission [44,[71][72][73][74]. Heterogeneity in transmission has been incorporated in these models by including more than one class of hosts (e.g., by assuming that susceptible or infectious individuals are classed in different groups based on age, behaviour or other phenotypic classes [75,76]), or by assuming that the transmission rate is distributed continuously and incorporating a model parameter representing the variation of this distribution (e.g., in humans [43]; fish [77]; and insects [44]).…”