To block or not to block: the adaptive manipulation of plague transmission

Abstract

The ability of the agent of plague, Yersinia pestis, to form a biofilm blocking the gut of the flea has been considered to be a key evolutionary step in maintaining flea-borne transmission. However, blockage decreases dramatically the life expectancy of fleas, challenging the adaptive nature of blockage. Here we develop an epidemiological model of plague that accounts for its different transmission routes, as well as the within-host competition taking place between bacteria within the flea vector. We use this theoretical framework to identify the environmental conditions promoting the evolution of blockage. We also show that blockage is favored at the onset of an epidemic, and that the frequencies of bacterial strains exhibiting different strategies of blockage can fluctuate in seasonal environments. This analysis quantifies the contribution of different transmission routes in plague and makes testable predictions on the adaptive nature of blockage.\n\nSignificance statementPlague transmission relies on the ability of infected fleas to inoculate Y. pestis bacteria to vertebrate hosts. The production of a biofilm by the bacteria blocks the forgut of the flea and increases infectivity. But the adaptive nature of blockage remains controversial because it has a massive survival cost on the infected fleas and reduces dramatically the length of the infection: an extreme form of the classical virulence-transmission tradeoff. Here we develop a comprehensive model of the multiple routes of plague transmission, we determine when blockage can be viewed as an adaptive manipulation of its flea vector and we generate several testable predictions on the evolution of plague in both endemic and epidemic situations.