Mode of transmission and the evolution of arbovirus virulence in mosquito vectors

Abstract

The traditional assumption that vector-borne pathogens should evolve towards a benign relationship with their arthropod vectors has been challenged on theoretical grounds and empirical evidence. However, in the case of arboviruses (arthropod-borne viruses), although a number of investigators have reported experimental evidence for virus-induced vector mortality, others have failed to detect any significant impact. Whether this variation in the observed level of arbovirus virulence depends on biological traits or experimental design is unclear. Here, we perform a meta-analysis of studies across a range of mosquito–virus systems to show that, overall, arboviruses do reduce the survival of their mosquito vectors, but that the magnitude of the effect depends on the vector/virus taxonomic groups and the mode of virus transmission. Alphaviruses were associated with highest virulence levels in mosquitoes. Horizontal transmission (intrathoracic inoculation or oral infection) was correlated with significant virus-induced mortality, whereas a lack of adverse effect was found for Aedes mosquitoes infected transovarially by bunyaviruses—a group of viruses characterized by high natural rates of vertical transmission in their enzootic vectors. Our findings are consistent with the general prediction that vertically transmitted pathogens should be less virulent than those transmitted horizontally. We conclude that varying degrees of virulence observed among vector–virus systems probably reflect different selective pressures imposed on arboviruses that are primarily transmitted horizontally versus vertically.