Experimental evidence for stabilizing selection on virulence in a bacterial pathogen

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Abstract

The virulence-transmission trade-off hypothesis has provided a dominant theoretical basis for predicting pathogen virulence evolution, but empirical tests are rare, particularly at pathogen emergence. The central prediction of this hypothesis is that pathogen fitness is maximized at intermediate virulence due to a trade-off between infection duration and transmission rate. However, obtaining sufficient numbers of pathogen isolates of contrasting virulence to test the shape of relationships between key pathogen traits, and doing so without the confounds of evolved host protective immunity (as expected at emergence), is challenging. Here, we inoculated 55 isolates of the bacterial pathogen, Mycoplasma gallisepticum, into non-resistant house finches (Haemorhous mexicanus) from populations that have never been exposed to the disease. Isolates were collected over a 20-year period from outbreak in disease-exposed populations of house finches and vary markedly in virulence. We found a positive linear relationship between pathogen virulence and transmission rate to an uninfected sentinel, supporting the core assumption of the trade-off hypothesis. Further, in support of the key prediction, there was no evidence for directional selection on a quantitative proxy of pathogen virulence and, instead, isolates of intermediate virulence were fittest. Surprisingly, however, the positive relationship between virulence and transmission rate was not underpinned by variation in pathogen load or replication rate as is commonly assumed. Our results indicate that selection favors pathogens of intermediate virulence at disease emergence in a novel host species, even when virulence and transmission are not linked to pathogen load.

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