Natural Aedes-Borne Virus Infection Detected in Male Adult Aedes aegypti (Diptera: Culicidae) Collected From Urban Settings in Mérida, Yucatán, México

Abstract

Aedes-borne viruses (ABVs) such as dengue (DENV), chikungunya (CHIKV), and Zika (ZIKV) contribute significantly to the global burden of infectious diseases, disproportionately affecting disadvantaged populations from tropical and subtropical urban areas. ABVs can be transmitted from female mosquitoes to their progeny by vertical transmission via transovarial and/or trans-egg vertical transmission and contribute to the maintenance of infected-mosquito populations year-round in endemic regions. This study describes the natural infection rate of DENV, CHIKV, and ZIKV in field-caught male Aedes (Sergentomyia) aegypti (Linnaeus) mosquitoes from Mérida, Yucatán, México, as a proxy for the occurrence of vertical virus transmission. We used indoor sequential sampling with Prokopack aspirators to collect all mosquitoes inside houses from ABV hotspots areas. Collections were performed in a DENV and CHIKV post-epidemic phase and during a period of active ZIKV transmission. We individually RT-qPCR tested all indoor collected Ae. aegypti males (1,278) followed by Sanger sequencing analysis for final confirmation. A total of 6.7% male mosquitoes were positive for ABV (CHIKV = 5.7%; DENV = 0.9%; ZIKV = 0.1%) and came from 21.0% (30/143) houses infested with males. Most ABV-positive male mosquitoes were positive for CHIKV (84.8%). The distribution of ABV-positive Ae. aegypti males was aggregated in a few households, with two houses having 11 ABV-positive males each. We found a positive association between ABV-positive males and females per house. These findings suggested the occurrence of vertical arbovirus transmission within the mosquito populations in an ABV-endemic area and, a mechanism contributing to viral maintenance and virus re-emergence among humans in post-epidemic periods.

Keywords: Aedes; density; infection; male; transmission.

Graphical Abstract

Fig. 1.

Potential transmission routes for Aedes-borne viruses: Horizontal (HT) when a female mosquito vector acquires the virus through blood-feeding on an infected vertebrate host (vector-borne transmission) is the most common and efficient route. Another type of HT includes the passage of the virus during mating (venereal transmission, HVT). Vertical transmission (TV), also called hereditary, occurs when an infected female mosquito transmits the virus to its progeny. VT can occur when germinal tissues of the female mosquitoes are infected (transovarial transmission, TOT) or during oviposition (trans-egg transmission, TET).

Fig. 2.

Distribution of the number of male Ae. aegypti positive for CHIKV, DENV, and ZIKV detected per house in Mérida, Yucatán, México during 2016–2017.

Fig. 3.

Percentage of houses infested with CHIKV, DENV, and/or ZIKV-positive male Ae. aegypti from low-density (<10 total male mosquitos collected per house, N = 101) and high-density (>10 total male mosquitoes collected per house, N = 42) premises in Yucatán, México. The variable co-occurrence contains percentages of houses where mosquitoes were positive for two viruses within the same house.

Fig. 4.

Relationship between infected female Ae. aegypti and positive males at house level.

Fig. 5.

Predicted probability of ABV infection in male Ae. aegypti as a function of the number of infected females detected in the same house. The solid line represents the mean prediction from a binomial generalized linear model (GLM) and gray band the 95% CI of the prediction. The dots indicate the binomial data, with dark dots showing multiple (overlapping) observations.