One health - an ecological and evolutionary framework for tackling Neglected Zoonotic Diseases

Abstract

Understanding the complex population biology and transmission ecology of multihost parasites has been declared as one of the major challenges of biomedical sciences for the 21st century and the Neglected Zoonotic Diseases (NZDs) are perhaps the most neglected of all the Neglected Tropical Diseases (NTDs). Here we consider how multihost parasite transmission and evolutionary dynamics may affect the success of human and animal disease control programmes, particularly neglected diseases of the developing world. We review the different types of zoonotic interactions that occur, both ecological and evolutionary, their potential relevance for current human control activities, and make suggestions for the development of an empirical evidence base and theoretical framework to better understand and predict the outcome of such interactions. In particular, we consider whether preventive chemotherapy, the current mainstay of NTD control, can be successful without a One Health approach. Transmission within and between animal reservoirs and humans can have important ecological and evolutionary consequences, driving the evolution and establishment of drug resistance, as well as providing selective pressures for spill-over, host switching, hybridizations and introgressions between animal and human parasites. Our aim here is to highlight the importance of both elucidating disease ecology, including identifying key hosts and tailoring control effort accordingly, and understanding parasite evolution, such as precisely how infectious agents may respond and adapt to anthropogenic change. Both elements are essential if we are to alleviate disease risks from NZDs in humans, domestic animals and wildlife.

Keywords: NTDs; NZDs; disease control; ecology; evolution; key hosts; preventive chemotherapy; zoonoses.

Figure 1

Schematic representation of a general multihost – multiparasite scenario. Parasite species 1 is the focal parasite of interest, and is a generalist (see Box 1 glossary) able to infect both host species A and B. However, host species B is the key host species for this parasite, dominating transmission. In the extreme, if host species B is a maintenance host and species A is not then, in the absence of any evolutionary response by the parasite, treating host species B will result in elimination of parasite species 1. However, parasite 1 may be able to evolve in response to that treatment, either by evolving resistance to the treatment, or undergoing a host shift to be maintained on host species A. In the scenario shown this would then expose it to possible co‐infections with parasite species 2. Parasite species 2 could act to facilitate or suppress the likelihood of species 1 establishing in the new host and, if the two parasite species are sufficiently related, could result in hybridization and/or introgression between them.