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.2015 Oct 29:6:306.
doi: 10.3389/fphys.2015.00306. eCollection 2015.

Multitasking roles of mosquito labrum in oviposition and blood feeding

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Multitasking roles of mosquito labrum in oviposition and blood feeding

Young-Moo Choo et al. Front Physiol..

Abstract

Reception of odorants by two main head appendages, antennae and maxillary palps, is essential for insects' survival and reproduction. There is growing evidence in the literature suggesting that the proboscis is also an olfactory appendage and its function as an additional "antenna" has been previously proposed. We surmised that movements of the labrum toward a blood vessel might be chemically oriented and, if so, there should be odorant receptors expressed in the labrum. To test this hypothesis, we first compared by quantitative PCR expression of odorant receptors (OR) from the Southern house mosquito, Culex quinquefasciatus in antennae and proboscis and, subsequently compared OR expression in various proboscis parts. Our data suggested that a receptor for the oviposition attractant, skatole, CquiOR21, was not expressed in proboscis, whereas a receptor for another oviposition attractant, 4EP (4-ethylphenol), CquiOR99, and a receptorf for the insect repellent DEET, CquiOR136, were expressed in the stylet of the proboscis, particularly in the tip of the labrum. In a dual-choice olfactometer, mosquitoes having the stylet coated with nail polish were attracted to 4EP in the same manner as the untreated mosquitoes. By contrast, in an oviposition assay, the stylet-treated mosquitoes did not discriminate 4EP from control oviposition cups, whereas the untreated mosquitoes (as well as mosquitoes having the labella coated) laid significantly more egg rafts in cups treated with 4EP. Ablation experiments confirmed that 4EP was sensed by the labrum where CquiOR99 is highly expressed. Stylet-coated, labella-coated, and untreated mosquitoes laid significantly more egg rafts in skatole-treated cups than in control cups. Likewise, coating of proboscis structures with nail polish had no effect on DEET-mediated oviposition deterrence. In a behavioral arena designed to mimic a human arm, mosquitoes showed significantly reduced probing time when blood was impregnated with 4EP, i.e., they engaged more rapidly in continuous blood feeding as compared to untreated blood. The time of engagement for feeding in skatole-containing blood vs. untreated blood did not differ significantly. Taken together, these data suggest that 4EP reception by the labrum is important not only for oviposition decisions, but also for reducing probing and initiation of blood feeding.

Keywords: 4-ethylphenol; CquiOR99; olfaction; oviposition attractant; proboscis.

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Figures

Figure 1
Figure 1
Illustration of head appendages from the Southern house mosquito. In this computer reconstruction, the two main olfactory appendages, the antennae and the maxillary palps, were de-emphasized in light gray. For clarity, the proboscis is depicted with the stylet removed from the labium, and the six fascicles forming the stylet separated and displayed in color. During blood feeding, the labium (in gray) bends and remains outside with the two lobes on the tip (labella) making direct contact with the host's skin. All six fascicles of the stylet are inserted in the host's skin, i.e., a pair of maxillae (Mx, cayenne), a pair of mandibles (M, fern), the hypopharynx (H, clover), and the labrum (blueberry).
Figure 2
Figure 2
Diagram and photographs of the dual-choice olfactometer. (A) Diagrammatic representation of the olfactometer highlighting the suction system and the direction of the plume.(B) Bird-view of the olfactomer and photos illustrating(C) the suction system and release chamber and(D) the sample compartments at the upwind end of olfactometer.
Figure 3
Figure 3
Differential expression of odorant receptors in antennae and proboscis. These qPCR data showed that, as expected, most receptors are more expressed in antennae than in proboscis. However, transcripts of multipleORs were detected at high levels in proboscis, whereas twoOR genes,CquiOR21 andCquiOR125, appeared below an arbitrary threshold of 15%, which is depicted by a horizontal dashed line.
Figure 4
Figure 4
qPCR data comparing expression of ORs in stylet and labium. Transcript levels for most of the receptors tested were much higher in the stylet than in labium, expect forCquiOR1 andCquiOR95. Of note, a DEET receptor, CquiOR136, and a receptor for the oviposition attractant, 4EP, CquiOR99, were predominantly expressed in the stylet.
Figure 5
Figure 5
Differential expression ofCulex ORs in labrum vs. the remainder of the stylet. As expected, transcript levels for most ORs were mainly detected in the labrum, with a notable exception ofCquiOR1.
Figure 6
Figure 6
Distribution of ORs within the labrum. In agreement with the existence of apical and subapical sensory organs in the labrum, qPCR data suggest that the tested receptors are expressed not only on the tip, but also in the remainder of the labrum.
Figure 7
Figure 7
Behavioral responses of gravid female mosquitoes to 4EP. (A) In a dual-choice olfactometer, both females having their stylets coated with nail polish and untreated females were more significantly attracted to the arm of the olfactometer with 4EP (untreated,P = 0.016,n = 5; stylet-coated,P = 0.002,n = 8).(B) In oviposition bioassays, untreated female mosquitoes laid significantly more egg rafts in 4EP-treated cups (P = 0.002,n = 21), whereas the same treated females (stylet-coated with nail polish) used in olfactometer, showed no oviposition preference (P = 0.396) for 4EP.*p ≤ 0.05.
Figure 8
Figure 8
Effect of microsurgery on 4EP-mediated oviposition. While labella-ablated mosquitoes laid significantly more egg rafts in 4EP-treated cups (P = 0.002), labrum-ablated mosquitoes laid eggs indiscriminately in 4EP-treated and control cups (P = 0.25). (n = 27 in both experiments).*p ≤ 0.05.
Figure 9
Figure 9
Effect of coating on skatole-mediated oviposition. Mosquitoes with the stylet coated with nail polish laid significantly more eggs rafts in skatole-treated cups (P = 0.0001;n = 11), as did untreated mosquitoes (P < 0.0001,n = 16). Mosquitoes with the labella coated with nail polish also showed preference for skatole-treated cups (P = 0.039,n = 8).*p ≤ 0.05;**p ≤ 0.01.
Figure 10
Figure 10
Effect of coating on oviposition deterrence by DEET. Untreated, stylet-coated, and labella-coated mosquitoes laid significantly more eggs in control cups than in cups treated with DEET (P = 0.0001,n = 10;P = 0.0038,n = 8;P = 0.0002,n = 6, respectively).*p ≤ 0.05;**p ≤ 0.01.
Figure 11
Figure 11
Chemical-mediated shortening of engagement time. In an arena designed to mimic a human arm, blood-seeking mosquitoes were given physical and chemical stimuli, and a choice to feed either on blood treated with an additional chemical signal (4EP or skatole) or untreated blood.(A) The duration of probing before continuous blood-feeding started, i.e., the “time of engagement” was significantly reduced with blood was treated with 0.01, 0.001, and 0.0001% of 4EP (P = 0.02;n = 31–40;P = 0.04;n = 17–19;P = 0.02,n = 15–16, respectively).(B) By contrast, skatole at the same concentrations did not affect the time of engagement (P = 0.14,n = 21–28;P = 0.63,n = 11–14;P = 0.15;n = 29–46, respectively).*p ≤ 0.05.
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