Natural salivary gland barrier curtails Zika virus transmission in Thai Aedes aegypti

Abstract

BackgroundVector competence is a critical determinant of arbovirus transmission dynamics, yet most studies in Thailand have primarily examined Aedes aegypti susceptibility to infection and systemic viral dissemination rather than the mosquitos potential to transmit infectious virions. Given that transmission potential varies among mosquito populations, identifying population-specific transmission barriers is crucial for optimizing vector control strategies especially under budget and resource constrains. Methodology/Principal FindingsThis study assessed the Zika virus (ZIKV) transmission potential of three Ae. aegypti populations from Thailand: two field-derived populations from Chiang Mai (CSP) and Nakhon Sawan (NAK) and a long-established laboratory strain (DMSC). Following oral exposure to a locally circulating ZIKV strain, viral transmission potential was evaluated. CSP mosquitoes demonstrated the earliest and highest ZIKV prevalence in salivary glands at 7 days post-infectious blood meal (dpibm), with DMSC and NAK populations reaching comparable infection levels at later time points. Despite this, NAK mosquitoes exhibited a strong barrier, resulting in significantly lower transmission potential. Genetic crosses revealed that this phenotype is inherited as an autosomal dominant trait and is similarly effective against dengue virus serotype 2 (DENV2), underscoring the broad-spectrum potential of NAK Ae. aegypti for transmission suppression. Furthermore, male NAK mosquitoes exhibited superior mating competitiveness, reinforcing their viability as a tool for vector control by population replacement. Conclusions/SignificanceOur findings highlight significant variability in ZIKV vector competence among Thai Ae. aegypti populations, emphasizing the importance of direct transmission assessments in vector competence studies. The discovery of a naturally occurring, heritable salivary gland escape barrier presents an opportunity for vector control strategies through NAK-based population replacement approaches. With their strong mating capability and broad arbovirus-blocking ability, NAK mosquitoes provide a natural alternative to Wolbachia-based and genetically modified mosquito interventions. Author summaryAedes aegypti is the primary vector of arboviruses such as Zika virus (ZIKV) and dengue virus (DENV), but not all mosquitoes that become infected successfully transmit the virus. While most research in Thailand has focused on mosquito infection and virus dissemination, fewer studies have examined the ability of mosquitoes to transmit infectious virus through their saliva. We discovered a mosquito population from Nakhon Sawan (NAK) that exhibits a natural barrier to virus release from the salivary glands, leading to significant blocking of virus transmission in ZIKV-infected mosquitoes. This salivary gland escape barrier of NAK is a heritable autosomal dominant characteristic that also restricts DENV transmission. Given their high mating competitiveness, NAK mosquitoes present a promising candidate for population replacement strategies aimed at reducing arbovirus transmission. Our findings emphasize the importance of assessing transmission rates rather than relying solely on infection and dissemination rates. Furthermore, the discovery of a naturally occurring mosquito population with reduced transmission potential offers a practical and sustainable vector control approach. The implementation of NAK-based population replacement strategies could serve as an alternative to traditional control methods, such as insecticide application or genetically modified mosquito releases. Future research should focus on field trials to validate the efficacy of this approach in real-world settings and assess its long-term impact on virus transmission dynamics.