Temporal synchrony between human odor rhythms and mosquito olfactory preference shapes host attraction
Lan Lou, Karthikeyan ChandrasegaraniD, Julien DevilliersiD, Austin ComptoniD, Abdulhadi Kobiowu, Emilie Applebach, Adaline Bisese, Richard Rust, Shajaesza Diggs, Sydney Luff, Sneha Sapkota, Nicole E. Wynne, Diane F. EilertsiD, Olivia EvansiD, Joshua B. BenoitiD, Zhijian Jake TuiD, Chloé LahondèreiD, Clément VinaugeriD
Abstract
For anthropophilic mosquitoes such as Aedes aegypti, aligning host-seeking with human availability enhances foraging efficiency and reproductive success. Although time of day modulates mosquito activity and olfactory sensitivity, it remains unknown whether human hosts display rhythmic changes in odor cues and whether mosquitoes adjust their sensory responses accordingly. Here, we combine chemical, behavioral, genetic, and transcriptomic approaches to reveal that both mosquitoes and their human hosts in this interaction are temporally synchronized. Gas chromatography-mass spectrometry showed systematic daily shifts in human body odor composition between morning and evening. Correspondingly, mosquitoes prefer host odors that match their own active phase--a time-specific preference abolished in timeless mutants and under constant darkness. Silencing the timeless gene further induced an aversion for the host scent under light-dark conditions. Transcriptomic analysis of mosquito heads and antennae uncovered rhythmic expression of sensory and neuromodulatory genes, driven by both circadian and light-dark cycles and which peaks during mosquitoes active periods, with rhythmic co-expression networks collapsing in timeless knockouts. Together, these results show that mosquito attraction to humans is temporally tuned by the interplay of host odor rhythms and mosquito sensory rhythms, revealing a previously unrecognized form of interspecific temporal synchronization in vector-host interactions.
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