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, 9 (1), 9699

Age-dependent Regulation of Host Seeking in Anopheles Coluzzii

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Age-dependent Regulation of Host Seeking in Anopheles Coluzzii

A B Omondi et al. Sci Rep.

Abstract

Behavioural attraction of the malaria vector Anopheles coluzzii to human host odour increases during adult maturation. We have previously demonstrated that the onset of host seeking in An. coluzzii coincides with an increased sensitivity of the CO2-sensitive neurons and abundance of chemosensory receptor gene transcripts in the maxillary palp. In this study, we extend our analysis to the antenna. Functional characterisation of the near-complete repertoire of odorant receptors (Ors) expressed in this tissue, to fractioned human odour, reveals a subset of salient human odorants to be detected by Ors at physiological relevant concentrations. When presented as a blend in their ratio of natural emission, these odorants elicit attraction by host-seeking mosquitoes, emphasising that Ors alone can mediate this behaviour. However, the same blend inhibits attraction in teneral mosquitoes. This switch in behavioural response indicates a change in valence during adult maturation. Quantitative analysis of Or transcript abundance and in vivo electrophysiological analysis reveal that the olfactory system of female An. coluzzii undergoes concerted changes that correlate with the onset of host seeking. We conclude that changes in Or abundance modulate peripheral olfactory coding, resulting in ecologically relevant behavioural effects.

Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
Select Ors of Anopheles coluzzii respond to human odorants, which when combined elicit differential behavioural responses in teneral and host-seeking female mosquitoes. (A) Schematic of the combined gas chromatography-coupled single sensillum recording (GC–SSR) setup. FID, flame ionization detector. (B) Sample GC-SSR trace, with the SSR trace at the top showing the response of the Or39-expressing neuron (large amplitude neuron) and the FID chromatogram showing the elution of human odorants. (C) Heat map displaying the threshold of response of the Ors responding to human odorants. (D) Release rate of the human odorants. (E) Y-tube olfactometer design (synthetic human odour with CO2 versus CO2). (F) Behavioural responses of teneral (1 day post-eclosion (1 dpe)) (green) and host-seeking (4 dpe) (red) mosquitoes to the full synthetic human odour blend + CO2 versus CO2 (top), and to CO2 versus CO2 (bottom). Statistical significance was tested using nominal logistic regression. Error bars represent standard errors of the mean. *p < 0.05, **p < 0.01, ns: not significant.
Figure 2
Figure 2
Changes in Or transcript abundance and sensitivity of OSNs to salient human odorants in teneral and host-seeking Anopheles coluzzii. (A) Relative transcription levels of genes encoding Ors tuned to human odorants in teneral (1 day post-eclosion (1 dpe)) (green) and host-seeking (4 dpe) (red) females. Statistical significance was tested using a two-tailed paired Student’s t-test. Error bars represent standard errors of the mean. *p < 0.05, **p < 0.01, ns: not significant. nd: not detected. (B) Responses of the TE-B neuron to increasing doses of phenol in teneral (left) and host-seeking (right) mosquitoes. (C) Physiological response of OSNs in TD, TE and capitate peg sensilla, in teneral (green) and host-seeking (red) mosquitoes, to increasing doses of human volatiles. Statistical significance was tested using a repeated measures ANOVA. Error bars represent standard errors of the mean. *p < 0.05, **p < 0.01, ns: not significant.
Figure 3
Figure 3
Behavioural responses of teneral and host-seeking Anopheles coluzzii to subtractive blends of the synthetic human odour. Removal of odorants from the full synthetic human odour blend, as indicated by the absence of grey bars, elicit differential behavioural responses in teneral (1 day post-eclosion (1 dpe); green) and host-seeking (4 dpe; red) mosquitoes. A total of four subtractive blends (I–IV) were evaluated. Statistical significance was tested using nominal logistic regression. Error bars represent standard errors of the mean. *p < 0.05, **p < 0.01, ***p < 0,001, ns: not significant.

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