Physiology and ecology combine to determine host and vector importance for Ross River virus.

Morgan P Kain,Erin A Mordecai,Andrew F Van Den Hurk,Eloise B Skinner,Hamish Mccallum

doi:10.7554/elife.67018

Abstract

Identifying the key vector and host species that drive the transmission of zoonotic pathogens is notoriously difficult but critical for disease control. We present a nested approach for quantifying the importance of host and vectors that integrates species' physiological competence with their ecological traits. We apply this framework to a medically important arbovirus, Ross River virus (RRV), in Brisbane, Australia. We find that vertebrate hosts with high physiological competence are not the most important for community transmission; interactions between hosts and vectors largely underpin the importance of host species. For vectors, physiological competence is highly important. Our results identify primary and secondary vectors of RRV and suggest two potential transmission cycles in Brisbane: an enzootic cycle involving birds and an urban cycle involving humans. The framework accounts for uncertainty from each fitted statistical model in estimates of species' contributions to transmission and has has direct application to other zoonotic pathogens.

Highlights

More than 60% of existing infectious diseases of humans are multi-host pathogens and approximately 75% of emerging and re-emerging infectious dis16 eases affecting humans have a non-human origin (Taylor et al, 2001, van Doorn, 2014)
41 Here, we present a general framework (Box 1) that: 1) quantifies host and vector species’ relative im42 portance across a complete transmission cycle of zoonotic arboviruses (Figure 1), using Ross River virus (RRV) as the model virus—a system for which we have data for many host and vector species for nearly all components of the transmission process; 2) identifies which of the many interacting physiological and ecological processes have the largest control over the importance of each species; and 3) helps to reveal 46 where the largest sources of uncertainty occur in order to identify which datasets require additional collec47 tion for more robust predictions (Restif et al, 2012)
We focus on Ross River virus (RRV), an alphavirus that causes a disease syndrome 57 characterized by polyarthritis, which is responsible for the greatest number of mosquito-borne human dis58 ease notifications in Australia, with approximately 5,000 cases notified annually

Summary

Introduction

More than 60% of existing infectious diseases of humans are multi-host pathogens (i.e., moving between 15 non-human and human populations) and approximately 75% of emerging and re-emerging infectious dis eases affecting humans have a non-human origin (Taylor et al, 2001, van Doorn, 2014). Studies characteris ing zoonotic arbovirus transmission often focus on pairwise transmission between non-human hosts and vectors, or vectors and humans (for example work in West Nile virus: Kilpatrick et al 2006, Ross River Virus: Koolhof and Carver 2017, Stephenson et al 2018, leishmaniasis: Stephens et al 2016, Chagas disease: Gurtler and Cardinal 2015, Jansen et al 2018) These and other proposed approaches (Appendix 1-Table 1) that capture only a portion of a pathogen’s transmission cycle cannot completely quantify a species’ contribution to transmission within a community. Understanding the ecological importance of host and vector species for transmission requires modeling the complete transmission cycle (host-vector host or vector-host-vector transmission), “closing the loop” by estimating the number of new infections in the generation This is needed to quantify each species’ contribution to R0, defined as the number of new infections arising from a single case in an otherwise susceptible population. Even for systems with limited data, a framework that integrates the entire transmission cycle can be useful for hypothesis testing and for guiding data collection by identifying the processes that most contribute to uncertainty in competence (i.e., model-guided fieldwork, sensu Restif et al, 2012)

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