Bluetongue virus spread in Europe is a consequence of climatic, landscape and vertebrate host factors as revealed by phylogeographic inference

Maude Jacquot,Kyriaki Nomikou,Massimo Palmarini,Peter Mertens,Roman Biek

doi:10.1098/rspb.2017.0919

Abstract

Spatio-temporal patterns of the spread of infectious diseases are commonly driven by environmental and ecological factors. This is particularly true for vector-borne diseases because vector populations can be strongly affected by host distribution as well as by climatic and landscape variables. Here, we aim to identify environmental drivers for bluetongue virus (BTV), the causative agent of a major vector-borne disease of ruminants that has emerged multiple times in Europe in recent decades. In order to determine the importance of climatic, landscape and host-related factors affecting BTV diffusion across Europe, we fitted different phylogeographic models to a dataset of 113 time-stamped and geo-referenced BTV genomes, representing multiple strains and serotypes. Diffusion models using continuous space revealed that terrestrial habitat below 300 m altitude, wind direction and higher livestock densities were associated with faster BTV movement. Results of discrete phylogeographic analysis involving generalized linear models broadly supported these findings, but varied considerably with the level of spatial partitioning. Contrary to common perception, we found no evidence for average temperature having a positive effect on BTV diffusion, though both methodological and biological reasons could be responsible for this result. Our study provides important insights into the drivers of BTV transmission at the landscape scale that could inform predictive models of viral spread and have implications for designing control strategies.

Highlights

Vector-borne pathogens threaten human and animal health in many parts of the world and are responsible for a high proportion of disease emergence events [1,2]
We investigated the potential of each raster variable to be a predictor of Bluetongue virus (BTV) diffusion, when it was treated either as a conductance or resistance factor, using the SERAPHIM library in R [47]
Summarizing across the different analytical approaches used, our analyses revealed consistent support for BTV diffusion being positively affected by higher livestock densities and low altitude terrestrial habitat as conductors and by the direction of winds

Summary

Introduction

Vector-borne pathogens threaten human and animal health in many parts of the world and are responsible for a high proportion of disease emergence events [1,2]. Theses emergences often involve ecological and environmental drivers, because vector populations are able to respond rapidly to such cues, including shifts in host distribution and climatic as well as landscape characteristics [3]. Understanding the specific environmental factors that drive the emergence and spread of vector-borne pathogens is, critical for the development of improved control and prevention measures and to reduce disease impacts on human and animal health as well as economic losses. Bluetongue virus (BTV), an arbovirus, with a segmented double-stranded RNA genome, is the causative agent of ‘bluetongue’, a major disease of ruminants.

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Conclusion