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 mosquitovirus 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.

The role of the ratio of vector and host densities in the evolution of transmission modes in vector-borne diseases. The example of sylvatic Trypanosoma cruzi

“…[1]) and empirical studies (e.g. [2,3,4]) suggest that pathogen virulence is responsible for a trade-off between horizontal (i.e., via contacts between infected and uninfected hosts) and vertical (i.e., from infected mother to offspring) transmission modes. Indeed, increased levels of virulence would translate into high parasite loads in the organism (i.e., parasitemia) and thus favor pathogen horizontal transmission, but impair host fitness and consequently the likeliness of vertical transmission [1].…”

Vector biology prospects in dengue research

“…Across different vector-virus systems, the effect of arboviral infection on mosquito survival is modest, but significantly negative (Lambrechts & Scott 2009). In a striking example, Ae.…”

“…Presumably, the negative effect of viral replication on vector survival does not result from a direct pathogenic effect, but rather from an indirect effect due to metabolism disturbance. Although reduced vector survival negatively impacts the probability of virus transmission, evolutionary theory predicts that the overall outcome can be advantageous to the virus if increased virulence (the reduction of host fitness due to infection) also confers enhanced horizontal transmission (Lambrechts & Scott 2009). For instance, increased frequency of vector-host contacts resulting from the manipulation of blood feeding behaviour in heavily infected mosquitoes may counterbalance the negative effects on survival.…”

Rapid selection against arbovirus-induced apoptosis during infection of a mosquito vector

“…Arbovirus infection often leads to apoptosis in vertebrate cells, but mosquito cells usually undergo nonlytic, persistent arbovirus infections (16)(17)(18)(19)(20), even though A. aegypti cells have a functional apoptosis pathway that largely resembles that of Drosophila melanogaster (21)(22)(23). Pathological effects resulting from arbovirus infection in mosquitoes have been reported in a few cases (24)(25)(26)(27), but arbovirus infections are generally thought to have a minimal effect on mosquito vectors, although that assumption has been challenged (28). However, there have been a small handful of reports of apoptosis correlating with resistance of mosquitoes to infection by arboviruses.…”