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      The olfactory gating of visual preferences to human skin and visible spectra in mosquitoes

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          Abstract

          Mosquitoes track odors, locate hosts, and find mates visually. The color of a food resource, such as a flower or warm-blooded host, can be dominated by long wavelengths of the visible light spectrum (green to red for humans) and is likely important for object recognition and localization. However, little is known about the hues that attract mosquitoes or how odor affects mosquito visual search behaviors. We use a real-time 3D tracking system and wind tunnel that allows careful control of the olfactory and visual environment to quantify the behavior of more than 1.3 million mosquito trajectories. We find that CO 2 induces a strong attraction to specific spectral bands, including those that humans perceive as cyan, orange, and red. Sensitivity to orange and red correlates with mosquitoes’ strong attraction to the color spectrum of human skin, which is dominated by these wavelengths. The attraction is eliminated by filtering the orange and red bands from the skin color spectrum and by introducing mutations targeting specific long-wavelength opsins or CO 2 detection. Collectively, our results show that odor is critical for mosquitoes’ wavelength preferences and that the mosquito visual system is a promising target for inhibiting their attraction to human hosts.

          Abstract

          Vision in mosquitoes plays a critical but understudied role in their attraction to hosts. Here, the authors show that encounter with an attractive odor gates the mosquito attraction to specific colors, especially the long wavelengths reflected from human skin. Filtering the long wavelengths reflected from the human skin or knocking-out the ability for the mosquito to detect the wavelengths, suppressed their attraction. This work transforms our understanding of mosquito vision from the conventional view that vision does little in mediating mosquito-host interactions, to the recognition that vision plays a critical role.

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          Most cited references40

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          Fitting Linear Mixed-Effects Models Using lme4

          Maximum likelihood or restricted maximum likelihood (REML) estimates of the parameters in linear mixed-effects models can be determined using the lmer function in the lme4 package for R. As for most model-fitting functions in R, the model is described in an lmer call by a formula, in this case including both fixed- and random-effects terms. The formula and data together determine a numerical representation of the model from which the profiled deviance or the profiled REML criterion can be evaluated as a function of some of the model parameters. The appropriate criterion is optimized, using one of the constrained optimization functions in R, to provide the parameter estimates. We describe the structure of the model, the steps in evaluating the profiled deviance or REML criterion, and the structure of classes or types that represents such a model. Sufficient detail is included to allow specialization of these structures by users who wish to write functions to fit specialized linear mixed models, such as models incorporating pedigrees or smoothing splines, that are not easily expressible in the formula language used by lmer. Journal of Statistical Software, 67 (1) ISSN:1548-7660
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            The evolution of color vision in insects.

            We review the physiological, molecular, and neural mechanisms of insect color vision. Phylogenetic and molecular analyses reveal that the basic bauplan, UV-blue-green-trichromacy, appears to date back to the Devonian ancestor of all pterygote insects. There are variations on this theme, however. These concern the number of color receptor types, their differential expression across the retina, and their fine tuning along the wavelength scale. In a few cases (but not in many others), these differences can be linked to visual ecology. Other insects have virtually identical sets of color receptors despite strong differences in lifestyle. Instead of the adaptionism that has dominated visual ecology in the past, we propose that chance evolutionary processes, history, and constraints should be considered. In addition to phylogenetic analyses designed to explore these factors, we suggest quantifying variance between individuals and populations and using fitness measurements to test the adaptive value of traits identified in insect color vision systems.
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              Multimodal integration of carbon dioxide and other sensory cues drives mosquito attraction to humans.

              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. Copyright © 2014 Elsevier Inc. All rights reserved.
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                Author and article information

                Contributors
                jriffell@uw.edu
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                4 February 2022
                4 February 2022
                2022
                : 13
                : 555
                Affiliations
                [1 ]GRID grid.34477.33, ISNI 0000000122986657, Department of Biology, , University of Washington, ; Seattle, WA 98195 USA
                [2 ]GRID grid.133342.4, ISNI 0000 0004 1936 9676, University of California, Santa Barbara, ; Santa Barbara, CA 93106 USA
                [3 ]GRID grid.5963.9, Institute of Biology I & Bernstein Center Freibug, Albert-Ludwigs-Univesität Freiburg, ; Freiburg im Breisgau, Germany
                Author information
                http://orcid.org/0000-0002-7645-5779
                Article
                28195
                10.1038/s41467-022-28195-x
                8816903
                35121739
                6366e3fe-7792-4eb9-931e-bbc9f90462f9
                © The Author(s) 2022

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 27 July 2021
                : 5 January 2022
                Funding
                Funded by: FundRef https://doi.org/10.13039/100000181, United States Department of Defense | United States Air Force | AFMC | Air Force Office of Scientific Research (AF Office of Scientific Research);
                Award ID: FA9550-20-1-0422
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/100006492, Division of Intramural Research, National Institute of Allergy and Infectious Diseases (Division of Intramural Research of the NIAID);
                Award ID: R01-AI148300
                Award ID: R21-AI137947
                Award Recipient :
                Categories
                Article
                Custom metadata
                © The Author(s) 2022

                Uncategorized
                colour vision,animal behaviour,visual system
                Uncategorized
                colour vision, animal behaviour, visual system

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