Search

Summary: Multiple sensory cues emanating from humans are thought to guide blood-feeding female mosquitoes to a host. To determine the relative contribution of carbon dioxide (CO2) detection to mosquito host-seeking behavior, we mutated the AaegGr3 gene, a subunit of the heteromeric CO2 receptor in Aedes aegypti mosquitoes. Gr3 mutants lack electrophysiological and behavioral responses to CO2. These mutants also fail to show CO2-evoked responses to heat and lactic acid, a human-derived attractant, suggesting that CO2 can gate responses to other sensory stimuli. Whereas attraction of Gr3 mutants to live humans in a large semi-field environment was only slightly impaired, responses to an animal host were greatly reduced in a spatial-scale-dependent manner. Synergistic integration of heat and odor cues likely drive host-seeking behavior in the absence of CO2 detection. We reveal a networked series of interactions by which multimodal integration of CO2, human odor, and heat orchestrates mosquito attraction to humans. [ABSTRACT FROM AUTHOR]

The African malaria mosquito Anopheles gambiae exhibits a strong innate drive to seek out humans in its sensory environment, classically entering homes to land on human skin in the hours flanking midnight. To gain insight into the role that olfactory cues emanating from the human body play in generating this epidemiologically important behavior, we developed a large-scale multi-choice preference assay in Zambia with infrared motion vision under semi-field conditions. We determined that An. gambiae prefers to land on arrayed visual targets warmed to human skin temperature during the nighttime when they are baited with carbon dioxide (CO 2) emissions reflective of a large human over background air, body odor from one human over CO 2 , and the scent of one sleeping human over another. Applying integrative whole body volatilomics to multiple humans tested simultaneously in competition in a six-choice assay, we reveal high attractiveness is associated with whole body odor profiles from humans with increased relative abundances of the volatile carboxylic acids butyric acid, isobutryic acid, and isovaleric acid, and the skin microbe-generated methyl ketone acetoin. Conversely, those least preferred had whole body odor that was depleted of carboxylic acids among other compounds and enriched with the monoterpenoid eucalyptol. Across expansive spatial scales, heated targets without CO 2 or whole body odor were minimally or not attractive at all to An. gambiae. These results indicate that human scent acts critically to guide thermotaxis and host selection by this prolific malaria vector as it navigates towards humans, yielding intrinsic heterogeneity in human biting risk. [Display omitted] • Development of an expansive and naturalistic multi-choice smell test for mosquitoes • CO 2 and other components of human scent guide Anopheles gambiae thermotaxis • Anopheles gambiae exhibits olfactory preferences for some humans versus others • Carboxylic acids are associated with human attractiveness to Anopheles gambiae Giraldo et al. develop an expansive semi-field system for multi-choice assays of mosquito olfactory preference. They find human scent draws malaria mosquitoes to warmed targets mimicking human skin to guide mosquito thermotaxis behavior and host selection, with levels of certain air-borne carboxylic acids associated with attractiveness. [ABSTRACT FROM AUTHOR]

Summary Female Aedes aegypti mosquitoes typically mate only once with one male in their lifetime, a behavior known as “monandry” [ 1 ]. This single mating event provisions the female with sufficient sperm to fertilize the >500 eggs she will produce during her ∼4- to 6-week lifespan in the laboratory [ 2 ]. Successful mating induces lifetime refractoriness to subsequent insemination by other males, enforcing the paternity of the first male [ 3–5 ]. Ae. aegypti mate in flight near human hosts [ 6 ], and females become refractory to remating within seconds [ 1, 3, 4 ], suggesting the existence of a rapid mechanism to prevent female remating. In this study, we implicate HP-I, an Aedes - and male-specific peptide transferred to females [ 7 ], and its cognate receptor in the female, NPYLR1 [ 8 ], in rapid enforcement of paternity. HP-I mutant males were ineffective in enforcing paternity when a second male was given access to the female within 1 hr. NPYLR1 mutant females produced mixed paternity offspring at high frequency, indicating acceptance of multiple mates. Synthetic HP-I injected into wild-type, but not NPYLR1 mutant, virgins reduced successful matings. Asian tiger mosquito ( Ae. albopictus ) HP-I peptides potently activated Ae. aegypti NPYLR1. Invasive Ae. albopictus males are known to copulate with and effectively sterilize Ae. aegypti females by causing them to reject future mates [ 9 ]. Cross-species transfer of sperm and active seminal fluid proteins including HP-I may contribute to this phenomenon. This signaling system promotes rapid paternity enforcement within Ae. aegypti but may promote local extinction in areas where they compete with Ae. albopictus . [ABSTRACT FROM AUTHOR]