Not all mosquitoes are created equal: A synthesis of vector competence experiments reinforces virus associations of Australian mosquitoes

Abstract

The 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 virus detection in field-collected mosquitoes, mosquito feeding patterns, and 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 68 laboratory-based vector competence studies of 111 mosquito-virus pairings of Australian mosquito species and viruses of public health concern to further substantiate existing canonical vector-virus groupings 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 different 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.

A minimum data standard for vector competence experiments

“…Some studies have begun to scale this gap: one study compiled a table of results from several dozen studies of Aedes aegypti and various arboviruses (see Table 6) 27 . More recently, another study compiled a dataset of 68 experimental studies that tested 111 combinations of Australian mosquitoes and arboviruses, and analyzed biological signals in the aggregated data 28 . These types of efforts are painstaking, requiring substantial manual curation of metadata, and hundreds more experiments are reported in the literature, yet remain unsynthesized due to this barrier.…”

Exploring the Mosquito–Arbovirus Network: A Survey of Vector Competence Experiments

“…Finally, our study highlights that a substantial breadth and depth of vector competence data are published every year in the peer-reviewed literature, but currently, the results of these experiments have no standardized home. Other recent studies highlight that synthesis of these data is possible, despite the complexity of metadata required to describe variation in experimental protocols 6 ; however, our study highlights the challenges of recovering "findable" data from the vector competence literature. Limitations we encountered included 1) Web of Science is not a comprehensive record of this research area, and older studies in particular appear to be missing; 2) keywords we used may not have captured all of the relevant studies because of variable terminology; 3) a handful of non-English-language publications-in particular, Spanish and French language publications from Latin America and Africa, respectively-were not captured by our search terms; and 4) not all studies reported reusable experimental results and metadata.…”

“…Experimental studies simplify real-world complexities of transmission and can be used to test not only the basic compatibility of a given virus and arthropod vector species but also vector competence-the relative ability of arthropod vectors to be infected by a virus and then disseminate and transmit it to a susceptible host. 2 Despite arboviruses' evolutionary tendencies toward broad host and vector range, 1,3,4 there are complex genetic underpinnings that govern vector competence, 5 which can manifest as variation in competence between closely related species of the vector 6 or even among populations of the same species. 7 Vector competence experiments are often conducted in response to the emergence of novel pathogens or the emergence of a known pathogen in a new location with previously untested vectors.…”

Land use predicts proportion of West Nile virus vector‐competent mosquitoes

“…Drivers of these shifts may include a reduction in natural breeding habitats or resources that may favor more generalist or disturbance‐tolerant species often adapted to humans and their environment (Thongsripong et al, 2013), a redistribution of host species available for blood feeding (Burkett‐Cadena et al, 2013), and processes that favor greater adaptation of pathogens to common hosts (Burkett‐Cadena et al, 2013). Community shifts matter because many mosquito‐borne pathogens may be transmitted by multiple species (Kain et al, 2022; Turell et al, 2005), and interspecific variations in vector competency within mosquito assemblages can affect pathogen circulation and transmission outcomes (McMillan et al, 2020; Roche et al, 2013). Given the involvement of multiple species in these disease systems, a continued focus on individual vector species is insufficient for understanding and predicting transmission hazard and public health risk.…”