Elimination of vision-guided target attraction in Aedes aegypti using CRISPR

Abstract

Blood-feeding insects, such as the mosquito, Aedes (Ae.) aegypti, use multiple senses to seek out and bite humans. 1 McMeniman C.J. Corfas R.A. Matthews B.J. Ritchie S.A. Vosshall L.B. Multimodal integration of carbon dioxide and other sensory cues drives mosquito attraction to humans. Cell. 2014; 156: 1060-1071 Abstract Full Text Full Text PDF PubMed Scopus (226) Google Scholar ,2 Montell C. Zwiebel L.J. Mosquito sensory systems. in: Advances in Insect Physiology. Volume 51. Academic Press, 2016: 294-328 Google Scholar Upon exposure to the odor of CO2, the attention of female mosquitoes to potential targets is greatly increased. Female mosquitoes are attracted to high-contrast visual cues and use skin olfactory cues to assist them in homing in on targets several meters away. 3 van Breugel F. Riffell J. Fairhall A. Dickinson M.H. Mosquitoes use vision to associate odor plumes with thermal targets. Curr. Biol. 2015; 25: 2123-2129 Abstract Full Text Full Text PDF PubMed Scopus (147) Google Scholar , 4 Day J.F. Host-seeking strategies of mosquito disease vectors. J. Am. Mosq. Control Assoc. 2005; 21: 17-22 Crossref PubMed Google Scholar , 5 Kawada H. Takemura S.Y. Arikawa K. Takagi M. Comparative study on nocturnal behavior of Aedes aegypti and Aedes albopictus. J. Med. Entomol. 2005; 42: 312-318 Crossref PubMed Scopus (37) Google Scholar , 6 Dekker T. Cardé R.T. Moment-to-moment flight manoeuvres of the female yellow fever mosquito (Aedes aegypti L.) in response to plumes of carbon dioxide and human skin odour. J. Exp. Biol. 2011; 214: 3480-3494 Crossref PubMed Scopus (62) Google Scholar , 7 Vinauger C. Van Breugel F. Locke L.T. Tobin K.K.S. Dickinson M.H. Fairhall A.L. Akbari O.S. Riffell J.A. Visual-olfactory integration in the human disease vector mosquito Aedes aegypti. Curr. Biol. 2019; 29: 2509-2516.e5 Abstract Full Text Full Text PDF PubMed Scopus (28) Google Scholar , 8 Liu M.Z. Vosshall L.B. General visual and contingent thermal cues interact to elicit attraction in female Aedes aegypti mosquitoes. Curr. Biol. 2019; 29: 2250-2257.e4 Abstract Full Text Full Text PDF PubMed Scopus (25) Google Scholar , 9 Bidlingmayer W.L. Hem D.G. The range of visual attraction and the effect of competitive visual attractants upon mosquito (Diptera: Culicidae) flight. Bull. Entomol. Res. 1980; 70: 321-342 Crossref Scopus (38) Google Scholar Within close range, convective heat from skin and additional skin odors further assist the mosquitoes’ evaluation as to whether the object of interest might be a host. 10 Khan A.A. Maibach H.I. A study of the probing response of Aedes aegypti. 4. Effect of dry and moist heat on probing. J. Econ. Entomol. 1971; 64: 442-443 Crossref PubMed Scopus (5) Google Scholar ,11 Acree Jr., F. Turner R.B. Gouck H.K. Beroza M. Smith N. L-Lactic acid: a mosquito attractant isolated from humans. Science. 1968; 161: 1346-1347 Crossref PubMed Scopus (161) Google Scholar Here, using CRISPR-Cas9, we mutated the gene encoding Op1, which is the most abundant of the five rhodopsins expressed in the eyes of Ae. aegypti. Using cage and wind-tunnel assays, we found that elimination of op1 did not impair CO2-induced target seeking. We then mutated op2, which encodes the rhodopsin most similar to Op1, and also found that there was no impact on this behavior. Rather, mutation of both op1 and op2 was required for abolishing vision-guided target attraction. In contrast, the double mutants exhibited normal phototaxis and odor-tracking responses. By measuring the walking optomotor response, we found that the double mutants still perceived optic flow. In further support of the conclusion that the double mutant is not blind, the animals retained an electrophysiological response to light, although it was diminished. This represents the first genetic perturbation of vision in mosquitoes and indicates that vision-guided target attraction by Ae. aegypti depends on two highly related rhodopsins.

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