Abstract
SUMMARYThe recent Zika virus (ZIKV) and chikungunya virus (CHIKV) epidemics highlight the explosive nature of arthropod-borne (arbo)viruses transmitted by Aedes spp. mosquitoes1,2. Vector competence and the extrinsic incubation period (EIP) are two key entomological parameters used to assess the public health risk posed by arboviruses3. These are typically measured empirically by offering mosquitoes an infectious bloodmeal and temporally sampling mosquitoes to determine infection and transmission status. This approach has been used for the better part of a century; however, it does not accurately capture the biology and behavior of many mosquito vectors which refeed frequently (every 2–3 days)4. Here we demonstrate that acquisition of a second non-infectious bloodmeal significantly shortens the EIP of ZIKV-infected Ae. aegypti by enhancing virus dissemination from the mosquito midgut. Similarly, a second bloodmeal increases the competence of this species for dengue virus and CHIKV as well as Ae. albopictus for ZIKV, suggesting that this phenomenon may be common among other virus-vector pairings and that Ae. albopictus might be a more important vector than once thought. Bloodmeal-induced microperforations in the virus-impenetrable basal lamina which surrounds the midgut provide a mechanism for enhanced virus escape. Modeling of these findings reveals that a shortened EIP would result in a significant increase in the basic reproductive number, R0, estimated from experimental data. This helps explain how Ae. aegypti can sustain explosive epidemics like ZIKV despite relatively poor vector competence in single-feed laboratory trials. Together, these data demonstrate a direct and unrecognized link between mosquito feeding behavior, EIP, and vector competence.
Highlights
Once a mosquito ingests an infected bloodmeal, arboviruses must overcome multiple barriers within the mosquito for transmission to occur[19]
A second bloodmeal increases the competence of this species for dengue virus and chikungunya virus (CHIKV) as well as Ae. albopictus for Zika virus (ZIKV), suggesting that this phenomenon may be common among other virus-vector pairings and that Ae. albopictus might be a more important vector than once thought
Modeling of these findings reveals that a shortened extrinsic incubation period (EIP) would result in a significant increase in the basic reproductive number, R0, estimated from experimental data
Summary
The recent Zika virus (ZIKV) and chikungunya virus (CHIKV) epidemics highlight the explosive nature of arthropod-borne (arbo)viruses transmitted by Aedes spp. mosquitoes[1,2]. Bloodmeal-induced microperforations in the virus-impenetrable basal lamina which surrounds the midgut provide a mechanism for enhanced virus escape Modeling of these findings reveals that a shortened EIP would result in a significant increase in the basic reproductive number, R0, estimated from experimental data. The increased dissemination rates associated with double-feeding resulted in a higher proportion of mosquitoes transmitting CHIKV to mice (Fig. 1h) This demonstrates that the serial feeding behavior of Ae. aegypti enhances transmission of taxonomically diverse arboviruses and suggests that the mechanisms mediating this observation may be applicable to other virus-mosquito pairings. Similar to Ae. aegypti, administration of a second non-infectious bloodmeal increased dissemination rates in Ae. albopictus (Extended Data 3) These findings suggest that under field conditions of frequent feeding, Ae. albopictus are more competent and could have contributed more to transmission during the ZIKV epidemic than previously thought. Past studies may underestimate the risks of arbovirus transmission by measuring vector competence after only a single infectious bloodmeal
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