Abstract
The taste system controls many insect behaviours, yet little is known about how tastants are encoded in mosquitoes or how they regulate critical behaviours. Here we examine how taste stimuli are encoded by Aedes albopictus mosquitoes—a highly invasive disease vector—and how these cues influence biting, feeding and egg laying. We find that neurons of the labellum, the major taste organ of the head, differentially encode a wide variety of human and other cues. We identify three functional classes of taste sensilla with an expansive coding capacity. In addition to excitatory responses, we identify prevalent inhibitory responses, which are predictive of biting behaviour. Certain bitter compounds suppress physiological and behavioural responses to sugar, suggesting their use as potent stop signals against appetitive cues. Complex cues, including human sweat, nectar and egg-laying site water, elicit distinct response profiles from the neuronal repertoire. We identify key tastants on human skin and in sweat that synergistically promote biting behaviours. Transcriptomic profiling identifies taste receptors that could be targeted to disrupt behaviours. Our study sheds light on key features of the taste system that suggest new ways of manipulating chemosensory function and controlling mosquito vectors.
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Data availability
All relevant data associated with this study are available upon request from the corresponding author, in addition to the source data files provided here. For RNA-sequencing analysis, all associated data are available as Supplementary Data 1–3. Raw reads are accessible at the Genbank Sequence Read Archive under BioProject accession PRJNA1048827. The previously published Ae. albopictus genome36 can be accessed on the NCBI website at https://www.ncbi.nlm.nih.gov/assembly/GCA_018104305.1. Source data are provided with this paper.
Code availability
Code used for biteOscope analyses are available at GitHub (https://github.com/felixhol/biteOscope).
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Acknowledgements
The authors thank K. Lizbinski, M. Platt, J. Fauver and members of the Carlson laboratory for discussion and comments on this manuscript; J. Greenwood and T. Sizemore for technical assistance; and K. Kim and P. Sweeney for discussions on floral nectar collection and identification. This work was supported by NIH Grants R01 DC02174, R01 DC04729, and R01 DC11697 (to J.R.C.); F32DC019250 and K99DC021504 (to L.S.B.).
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L.S.B. conceptualized and designed the study, collected, analysed and interpreted the data, and wrote and edited the manuscript. G.J.S.T. curated and analysed the RNA-sequencing data and edited the manuscript. S.G., H.S.P. and T.N.P. collected and analysed data and edited the manuscript. J.E.N. collected and analysed data. F.J.H.H. contributed analytic tools, analysed data and edited the manuscript. J.R.C. conceptualized and designed the study, interpreted the data, and wrote and edited the manuscript.
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Extended data figures and tables
Extended Data Fig. 1 Compound- and dose-dependent inhibitory responses to bitter compounds and amino acids.
a, Schematic of base electrophysiology recording, where the recording electrode and taste stimulus are delivered separately, allowing measurement of neuronal firing before, during, and after the taste stimulus delivery. b, Example traces of S-class sensilla responding to control (paraffin oil; top), 1 mM QUI (bottom) during base recording. c, Peristimulus time histogram of base recording of S-class sensilla responding to 1 mM QUI. d, Spike rates before, during, and after exposure to 1 mM QUI, n = 6 biologically independent experiments. e, Example trace of S-class sensilla responding to 10 mM Serine. f, Peristimulus time histogram of base recording of S-class sensilla responding to 10 mM Serine. g, Spike rates before, during, and after exposure to 10 mM Serine, n = 14 biologically independent experiments. h, Example trace of S-class sensilla responding to 10 mM Lysine. i, Peristimulus time histogram of base recording of S-class sensilla responding to 10 mM Lysine. j, Spike rates before, during, and after exposure to 10 mM Lysine, n = 10 biologically independent experiments. k, Example trace of S-class sensilla responding to 10 mM Cysteine. l, Peristimulus time histogram of base recording of S-class sensilla responding to 10 mM Cysteine. Line indicates mean spike rate, and shaded region indicates ±SEM in c, f, i, and l. m, Spike rates before, during, and after exposure to 10 mM Cysteine, n = 14 biologically independent experiments. Welch’s t test (two-tailed) was used for comparison in panels d, g, j, and m. Asterisks indicate significant difference in mean spike rate, *p < 0.05, **p < 0.01 in all panels. n, Schematic of tip electrophysiology recording, where the recording electrode and taste stimulus simultaneously make contact with the taste sensillum. o-r, Example traces of S-class sensilla responses to control (TCC solvent; top), 0.1 mM (middle), and 1 mM (bottom) concentrations of Denatonium benzoate (DEN)(o), Quinine (QUI)(p), Berberine chloride (BER)(q), and Caffeine (CAF)(r). s-v, Summary of dose-dependent inhibitory responses, in comparison to spontaneous spike rate of each sensillum, for DEN, n = 15–27 (s), QUI, n = 12–27 (t), BER, n = 12–27 (u), and CAF, n = 9–27 biologically independent experiments (v). Control firing rate observed with TCC solvent alone is subtracted from tastant responses of each corresponding sensillum type in s-v. Data are presented as mean values and error bars are ±SEM in all panels.
Extended Data Fig. 2 Intensity coding of taste cues.
a, Example traces of the increasing responses of labellar taste neurons to 0.1–100 mM concentrations of sucrose (SUC). Spikes are counted during the first 0.5 s of contact. b-e, Mean spike rate responses of each sensillum to increasing doses of sucrose, n = 5–23 biologically independent experiments (b), sodium chloride (NaCl), n = 6–15 biologically independent experiments (c) ammonium chloride (NH4Cl), n = 4–28 biologically independent experiments (d). e, Mean spike rate response of each sensillum to sodium L-Lactate (Na L-Lactate), n = 6–12 biologically independent experiments. Control firing rate observed with TCC solvent alone is subtracted from the tastant responses of each corresponding sensillum type in each panel. Error bars are ±SEM.
Extended Data Fig. 3 Bitter compound suppression of sucrose response.
a, Schematic of two-choice feeding assay. Created with Biorender.com. b, Feeding preference of non-blood-fed females given a choice between 100 mM sucrose alone versus water. Feeding preference index greater than zero indicates preference for sucrose over water. One sample t test (two-tailed) compared to 0. Asterisks indicate significant differences from preference index of 0, n = 7 trials, 20 mosquitoes/trial. ****p = <0.0001. c, % of fed mosquitoes in two-choice feeding assay in Extended Data Fig. 3b. n = 7 trials, 20 mosquitoes/trial. d-g, Mean responses of each sensillum to sucrose is suppressed in a dose-dependent manner by denatonium benzoate (DEN), n = 4–11 biologically independent experiments (d), quinine (QUI), n = 5–19 biologically independent experiments (e), and berberine chloride, n = 6–19 biologically independent experiments (f), but not by caffeine (CAF), n = 6–19 biologically independent experiments (g). Sucrose response in the absence of bitter compound recovers after the exposure to bitter compounds, indicating that the lack of firing is not due to severe toxicity. Each set of bar graphs is in the following order: S1, S2, S3, S4, I1, I2, I3, I4, I5, I6, L1, L2, L3, L4, and L5 sensilla, from left to right. The control firing rate observed with TCC solvent alone is subtracted from the responses in each panel. The sucrose only data plotted in e, f, and g are repeated. h, % of fed mosquitoes in two-choice feeding assay in Main Fig. 3c. None differed from the control value. n = 6–18 trials, 20 mosquitoes/trial. Ordinary one-way ANOVA. Error bars are ±SEM.
Extended Data Fig. 4 Bitter compounds deter egg laying.
a, Schematic of two-choice egg-laying preference assay measuring preference of blood-fed, gravid females to lay eggs in solution of stimulus or in sterile water control. Created with Biorender.com. b, Egg-laying preferences for different tastants. Preference index of zero indicates no preference for either stimulus or water control. Preference index less than zero indicates stronger preference for water control over stimulus. One sample t test (two-tailed) compared to 0; and Welch’s t test for dose comparisons. n = 6-7 trials, 20 mosquitoes/trial. Asterisks indicate significant differences from preference index of zero or between different doses of bitter compound. ns=not significant, *p < 0.05, **p < 0.01, ***p < 0.001, ****p < 0.0001. c, Total number of eggs laid per cage of 20 mosquitoes in two-choice egg-laying preference assay, n = 6-7 independent experiments, using 20 mosquitoes/trial. Cages with high salt (100 mM NaCl) had fewer eggs (***p = 0.0008) than control cages. Ordinary one-way ANOVA. Data are presented as mean values and error bars are ±SEM in all panels.
Extended Data Fig. 5 Mixture of human host cues promote biting behaviors.
a, Schematic of two-choice Glytube biting preference assay. Created with Biorender.com. b, Female Ae. albopictus unengorged or engorged on red, blue, or both (violet) Glytube artificial blood meals. c-d, % of engorged mosquitoes in Main Fig. 4c (c) and 5d,e (d). There was no significant difference in % of engorged animals. Ordinary one-way ANOVA. n = 6–17 trials, 20 mosquitoes/trial. e, Mean biting preference of non-blood-fed female mosquitoes given a choice to bite on surface treated with stimulus mixture of 50 mM NaCl and L-Lys versus control surface treated with water. Different doses of L-Lys and pHs of mixtures were tested. Biting preference greater than zero indicates stronger preference for stimulus-treated surface over the control surface. One sample t test (two-tailed) comparing biting preference index to 0. Asterisks indicate significant differences from preference index of 0. n = 6–12 independent experiments, using 20 mosquitoes/trial. ns=not significant, *p < 0.05, **p < 0.01, ****p < 0.0001. Data are presented as mean values and error bars are ±SEM. f, % of engorged mosquitoes in Extended Data Fig. 5e. Ordinary one-way ANOVA found no significant differences. n = 6–12 trials, 20 mosquitoes/trial. Error bars are ±SEM. g, Heatmap representing mean responses of taste sensilla to 100.5mM L-Lys, 50 mM NaCl salt, or a combination of both. n = 5–25 per (tastant, sensillum) combination. h-j, Correlation of biting preference index and spike rates of I1 (h), I5 (i), and I6 (j) sensilla in response to taste stimuli. (50 mM NaCl mixed with 100.5mM Gly, Ser, Ala, Ile, Trp, Arg, Cys, or Lys; 100.5mM Lys or Arg; 1 mM NH4Cl; 10 mM, 50 mM, or 100 mM NaCl) in Main Fig. 4. Pearson correlation (two-tailed; *p < 0.05, **p < 0.01). Center line indicates simple linear regression analysis. Shading indicates 95% confidence interval. Control firing rates to TCC solvent alone for each sensillum type are subtracted from all responses of that sensillum type.
Extended Data Fig. 6 Sources of floral nectar and egg-laying site water samples.
a-f, Pictures of floral nectar sources belonging to genus Hemerocallis for nectar A (a), Hemerocallis for nectar B (b), Campsis for nectar C (c), Hosta for nectar D (d), Pentas for nectar E (e), and Lantana for nectar F (f). g-m, Pictures of egg-laying sites, plastic container site A (g), roadside ditch site B (h), glass vase site C (i), plastic trash bin site D (j), tire site E (k), metal base for road sign pole site F (l), and ceramic planter saucer site G (m).
Extended Data Fig. 7 Biting, landing, feeding, and egg-laying behaviors in response to naturally sourced taste cues.
a, Total number of eggs laid per cage of 20 mosquitoes in two-choice egg-laying preference assay, in reference to Main Fig. 5e and Extended Data Fig. 7b. Only cages with water from egg-laying site A had a significantly higher number of eggs (**p < 0.01) than control cages. Ordinary one-way ANOVA. b, Two-choice egg-laying assay measuring preference of blood-fed, gravid females to lay eggs in water incubated with food with/without conspecific larvae versus in sterile water control. An egg-laying preference index of zero indicates no preference. Egg-laying preference index greater than zero indicates preference for egg-laying site water (stimulus), n = 8–10 trials, 20 mosquitoes/trial. Water incubated with conspecific larvae and food had a higher preference index than water incubated with food alone (**p < 0.01). Control data is taken from Main Fig. 5e. One-sample t test (two-tailed) was used to compare preference index to 0; Welch’s t test (two-tailed) was used to compare food alone versus food + larvae conditions. c, Heatmap of mean electrophysiological responses to seven egg-laying site water samples and water incubated with food with/without conspecific larvae, n = 5–16. The control firing rate observed with TCC solvent alone is subtracted from the responses in each panel. The data for the egg-laying sites is taken from Fig. 5c. d, Two-choice feeding preference assay comparing feeding on 100 mM sucrose versus water from egg-laying sites. Schematic created with Biorender.com. Female mosquitoes show significantly higher preference to feed on sucrose over egg-laying site waters. One-sample t test (two-tailed) compared to 0. Control data is taken from Main Fig. 3c. e, Total number of fed mosquitoes in Extended Data Fig. 7d. Mann-Whitney test (two-tailed) compared to control. n = 6–22 trials, 20 mosquitoes/trial. f-j, In reference to main Fig. 5f, n = 5–10 independent experiments, using 20 mosquitoes/trial for panels f-j. f, Schematic of biteOscope biting preference assay. g, Total number of landing events per cage for biteOscope assays. Welch ANOVA test compared to control. Asterisks indicate significant differences from control. h, Average landing preference of non-blood-fed female mosquitoes in biteOscope assay. Landing preference greater than zero indicates stronger preference for sweat-treated (stimulus) biting surface over the untreated control surface. One-sample t test compared to 0. Asterisks indicate significant differences from preference index of 0. i, Number of landing and biting events for biteOscope assays. j, % of landing events that resulted in biting and engorgement. Error bars are ±SEM. ns=not significant, *p < 0.05, **p < 0.01, ***p < 0.001, ****p < 0.0001 in all panels.
Extended Data Fig. 8 Chemosensory genes with multiple isoforms.
(a, c, e, g) Integrative Genomics Viewer (IGV) browser view of regions that include a chemosensory gene encoding multiple isoforms. Orientation of each gene (arrow) and annotation of each isoform (boxes = exons, lines = introns) are shown below the coverage. The number of reads is indicated. The scale of the y-axis differs among panels. (b, d, f, h) Each isoform was named based on its similarity to Ae. aegypti gustatory receptors; cluster analysis of the predicted protein sequences are shown on the right, for genes Gr19 (a, b); Gr20 (c, d); Gr39 (e, f); and Gr60 (g, h). In the labellum, the following isoforms were detected ( ≥ 1 TPM), ranked by their abundance: Gr19a, Gr19c, and Gr19b; Gr20d-2, Gr20a, Gr20m, Gr20j, Gr20i-1, and Gr20g; Gr39b, Gr39d, Gr39h, Gr39a, Gr39f, and Gr39g-P (a pseudogene); Gr60d, Gr60a, Gr60b-2, Gr60b-1, Gr60b-3.
Extended Data Fig. 9 The expansion of Ir41 and Ir7 clades in Ae. albopictus, and a putative sugar- or amino acid-sensing Gr encoded in Ae. albopictus but not in Ae. aegypti.
a-b, Cluster analysis of the protein sequences of Irs annotated in the Ae. albopictus genome (AalbF3, [Boyle et al.36, Insects]) and Drosophila melanogaster, for the Ir41 clade (a), and Ir7 clade (b). Dots indicate transcripts that are detected in the labellum ( ≥ 1 TPM). Drosophila transcript expression data from [Wang et al.37, eLife]. Three genes (Ir41g-1, ir41m, and Ir41p) were not included in this analysis due to incomplete open reading frame in the current genome. c, Cluster analysis of the protein sequences of all Grs annotated in the Ae. albopictus genome (AalbF3, [Boyle et al.36, Insects]). The Ae. albopictus Gr82 (boxed) shares most similarity with Gr13. Gr44 was not included in this analysis due to its incomplete open reading frame in the current genome. Dots indicate transcripts that are detected in the labellum ( ≥ 1 TPM). d, Gene annotation of orthologous region that includes AAEL000033, a gene predicted to encode the integrator complex subunit 10 that is near a gustatory receptor gene; and Grs from Ae. albopictus (top) and Ae. aegypti (bottom). Ae. albopictus locus encodes an additional gustatory receptor, Gr82, relative to Ae. aegypti.
Extended Data Fig. 10
Chemosensory gene expression in the labellum of non-blood-fed females belonging to gene families, a-d, Transient receptor potential (Trp)(a), Rhodopsin (Rh)(b), Odorant binding protein (Obp)(c), and Odorant receptor (Or)(d). Genes are listed in decreasing order by transcripts per million +1 (TPM). n = 3 biological replicates, each prepared from the distal end of proboscis dissected from ~900 animals/replicate. Error bars are ±SEM. e-g, Scanning electron micrographs (SEM) of the Ae. albopictus labellum with arrow and dotted circle indicating olfactory sensillum (e), and single olfactory sensillum (f and g). Scale bars, 10μm for e and 0.5μm for f and g.
Supplementary information
Supplementary Data 1
Curated gene annotations. We curated and expanded the set of Ae. albopictus taste receptor gene annotations, including all of their isoforms, genes that had been missing in the genome (18 genes), or present in the genome but unannotated or labelled as uncharacterized genes (37 genes).
Supplementary Data 2
Transcripts per million (TPM) counts. RNA-sequencing reads mapping to a curated annotation were counted using HTseq (v. 0.13.5) and normalized by length and read depth. This data file lists the transcripts per million (TPM) counts from this analysis.
Supplementary Data 3
HTSeq raw counts. RNA-sequencing reads mapping to a curated annotation were counted using HTseq (v. 0.13.5). This data file lists the raw counts from this analysis.
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Baik, L.S., Talross, G.J.S., Gray, S. et al. Mosquito taste responses to human and floral cues guide biting and feeding. Nature 635, 639–646 (2024). https://doi.org/10.1038/s41586-024-08047-y
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DOI: https://doi.org/10.1038/s41586-024-08047-y
