A Role for Early-Phase Transmission in the Enzootic Maintenance of Plague

Abstract

Yersinia pestis, the bacterial agent of plague, is enzootic in many parts of the world within wild rodent populations and is transmitted by different flea vectors. The ecology of plague is complex, with rodent hosts exhibiting varying susceptibilities to overt disease and their fleas exhibiting varying levels of vector competence. A long-standing question in plague ecology concerns the conditions that lead to occasional epizootics among susceptible rodents. Many factors are involved, but a major one is the transmission efficiency of the flea vector. In this study, using Oropsylla montana (a ground squirrel flea that is a major plague vector in the western United States), we comparatively quantified the efficiency of the two basic modes of flea-borne transmission. Transmission efficiency by the early-phase mechanism was strongly affected by the host blood source. Subsequent biofilm-dependent transmission by blocked fleas was less influenced by host blood and was more efficient. Mathematical modeling predicted that early-phase transmission could drive an epizootic only among highly susceptible rodents with certain blood characteristics, but that transmission by blocked O. montana could do so in more resistant hosts irrespective of their blood characteristics. The models further suggested that for most wild rodents, exposure to sublethal doses of Y. pestis transmitted during the early phase may restrain rapid epizootic spread by increasing the number of immune, resistant individuals in the population. Author summary The ecology of bubonic plague is complex but depends largely on flea-borne transmission. Certain susceptible rodents experience periodic epizootics that can decimate local populations, but the conditions that lead to these episodes are not fully understood. Fleas can transmit Yersinia pestis, the bacterial agent of plague, during two different phases: an early phase within the first few days after their infectious blood meal and again sometime later after the development of a Y. pestis biofilm in the flea foregut. The relative contribution of these two transmission modes to plague ecology has not been systematically examined. Our results indicate that in most ecological contexts early-phase transmission is too inefficient to drive an epizootic, but instead acts to reduce the number of susceptible individuals in a population, thereby favoring a more stable enzootic state.