Not all mosquitoes are created equal: incriminating mosquitoes as vectors of arboviruses

Abstract

AbstractThe globalization of mosquito-borne arboviral diseases has placed more than half of the human population at risk. Understanding arbovirus ecology, including the role individual mosquito species play in virus transmission cycles, is critical for limiting disease. Canonical virus-vector groupings, such as Aedes- or Culex-associated flaviviruses, have historically been defined using phylogenetic associations, virus isolation in the field, and mosquito feeding patterns. These associations less frequently rely on vector competence, which quantifies the intrinsic ability of a mosquito to become infected with and transmit a virus during a subsequent blood feed. Herein, we quantitatively synthesize data from 80 laboratory vector competence studies of 115 mosquito-virus pairings of Australian mosquito species and viruses of public health concern to further substantiate existing canonical vector-virus groupings, uncover new associations, and quantify variation within these groupings. Our synthesis reinforces current canonical vector-virus groupings but reveals substantial variation within them. While Aedes species were generally the most competent vectors of canonical “Aedes-associated flaviviruses” (such as dengue, Zika, and yellow fever viruses), there are some notable exceptions; for example, Aedes notoscriptus is an incompetent vector of dengue viruses. Culex spp. were the most competent vectors of many traditionally Culex-associated flaviviruses including West Nile, Japanese encephalitis and Murray Valley encephalitis viruses, although some Aedes spp. are also moderately competent vectors of these viruses. Conversely, many mosquito genera were associated with the transmission of the arthritogenic alphaviruses, Ross River, Barmah Forest, and chikungunya viruses. We also confirm that vector competence is impacted by multiple barriers to infection and transmission within the mesenteron and salivary glands of the mosquito. Although these barriers represent important bottlenecks, species that were susceptible to infection with a virus were often likely to transmit it. Importantly, this synthesis provides essential information on what species need to be targeted in mosquito control programs.Author summaryThere are over 3,500 species of mosquitoes in the world, but only a small proportion are considered important vectors of arboviruses. Vector competence, the physiological ability of a mosquito to become infected with and transmit arboviruses, is used in combination with virus detection in field populations and analysis of vertebrate host feeding patterns to incriminate mosquito species in virus transmission cycles. Here, we quantified the vector competence of Australian mosquitoes for endemic and exotic viruses of public health concern by analyzing 80 laboratory studies of 115 mosquito-virus pairings. We found that Australia has species that could serve as efficient vectors for each virus tested and it is these species that should be targeted in control programs. We also corroborate previously identified virus-mosquito associations at the mosquito genus level but show that there is considerable variation in vector competence between species within a genus. We also confirmed that vector competence is influenced by infection barriers within the mosquito and the experimental protocols employed. The framework we developed could be used to synthesize vector competence experiments in other regions or expanded to a world-wide overview.