Host Resistance, Population Structure and the Long-Term Persistence of Bubonic Plague: Contributions of a Modelling Approach in the Malagasy Focus

Abstract

Although bubonic plague is an endemic zoonosis in many countries around the world, the factors responsible for the persistence of this highly virulent disease remain poorly known. Classically, the endemic persistence of plague is suspected to be due to the coexistence of plague resistant and plague susceptible rodents in natural foci, and/or to a metapopulation structure of reservoirs. Here, we test separately the effect of each of these factors on the long-term persistence of plague. We analyse the dynamics and equilibria of a model of plague propagation, consistent with plague ecology in Madagascar, a major focus where this disease is endemic since the 1920s in central highlands. By combining deterministic and stochastic analyses of this model, and including sensitivity analyses, we show that (i) endemicity is favoured by intermediate host population sizes, (ii) in large host populations, the presence of resistant rats is sufficient to explain long-term persistence of plague, and (iii) the metapopulation structure of susceptible host populations alone can also account for plague endemicity, thanks to both subdivision and the subsequent reduction in the size of subpopulations, and extinction-recolonization dynamics of the disease. In the light of these results, we suggest scenarios to explain the localized presence of plague in Madagascar.

Climatic and evolutionary drivers of phase shifts in the plague epidemics of colonial India

“…In the western United States, prairie dogs show no resistance to plague, despite longstanding prevalence of the disease and its devastating impact on their populations (31,94). Our modeling supports theoretical insights (56)(57)(58) as well as historical (42) and contemporary evidence (95) that disease-mediated selection rapidly alters the distribution of susceptibility of rats, thereby impacting epidemic dynamics. In addition to improving our understanding of the mechanism of innate resistance, characterizing the genetic basis of this trait may afford novel tools for animal-based plague surveillance.…”

“…We explored the contributions of climatically forced vector mortality and selection for host resistance using a trait-based mathematical model coupling bubonic plague transmission with phenotypic evolution of a rat host population. The model was informed by previous models of rat and flea population dynamics contributing to the transmission of the disease (56)(57)(58), but tailored to address climatic determinants of transmission, to include explicit evolutionary mechanisms, and to incorporate the fitness consequences (59) associated with host selection (Fig. 1).…”

The Asian house shrew Suncus murinus as a reservoir and source of human outbreaks of plague in Madagascar

“…In rural areas of the Central Highlands in Madagascar, where most human cases occur, the epidemiology of plague is relatively well understood, primarily involving the black rat Rattus rattus and two flea vectors Xenopsylla cheopis and Synopsyllus fonquerniei [ 11 , 12 ]. Black rats in these areas have acquired resistance [ 13 , 14 ] and this may play an important role in persistence as the co-existence of resistant and susceptible hosts is often thought to play an essential role in the maintenance of plague [ 15 ].…”

Zoonoses As Ecological Entities: A Case Review of Plague

“…Yet, the authors warn that the separation between enzootic and epizootic events is often dubious, as both are density-dependent phenomena, and events regarded as epizootic could be simply cases of higher mortality among enzootic hosts or a more efficient detection of the natural die-off during the enzootic phase. Such exercise is important to comprehend the nature of reservoir systems, as in some foci a single species is held accountable for maintaining the infection, such as Rattus rattus in a Malagasy focus [ 21 ] and Necromys lasiurus ( Zygodontomys lasiurus pixuma ) in Brazil [ 22 ].…”