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Intraspecific Variation in the Placement of Campaniform Sensilla on the Wings of the Hawkmoth Manduca Sexta - PubMed Skip to main page content
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. 2024 Mar 13;6(1):obae007.
doi: 10.1093/iob/obae007. eCollection 2024.

Intraspecific Variation in the Placement of Campaniform Sensilla on the Wings of the Hawkmoth Manduca Sexta

K E Stanchak  1 , T Deora  2 , A I Weber  1 , M K Hickner  3 , A Moalin  1 , L Abdalla  1 , T L Daniel  1 , B W Brunton  1
Affiliations

Intraspecific Variation in the Placement of Campaniform Sensilla on the Wings of the Hawkmoth Manduca Sexta

K E Stanchak et al. Integr Org Biol. .

Abstract

Flight control requires active sensory feedback, and insects have many sensors that help them estimate their current locomotor state, including campaniform sensilla (CS), which are mechanoreceptors that sense strain resulting from deformation of the cuticle. CS on the wing detect bending and torsional forces encountered during flight, providing input to the flight feedback control system. During flight, wings experience complex spatio-temporal strain patterns. Because CS detect only local strain, their placement on the wing is presumably critical for determining the overall representation of wing deformation; however, how these sensilla are distributed across wings is largely unknown. Here, we test the hypothesis that CS are found in stereotyped locations across individuals of Manduca sexta, a hawkmoth. We found that although CS are consistently found on the same veins or in the same regions of the wings, their total number and distribution can vary extensively. This suggests that there is some robustness to variation in sensory feedback in the insect flight control system. The regions where CS are consistently found provide clues to their functional roles, although some patterns might be reflective of developmental processes. Collectively, our results on intraspecific variation in CS placement on insect wings will help reshape our thinking on the utility of mechanosensory feedback for insect flight control and guide further experimental and comparative studies.

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Conflict of interest statement

The authors have no conflicts of interest to declare.

Figures

Fig. 1
Fig. 1
Campaniform sensilla (CS) on Manduca sexta wings are visible in brightfield (A) and are even more apparent under low-wavelength illumination (B), which makes the cap and collar readily visible due to autofluorescence of the wing cuticle. CS can be found on the top of the veins (A and B) or on the sides of veins (C and D), such that they are oriented to face either the leading or trailing edge of the wing rather than face orthogonally to the plane of the wing (as in A and B). Scale bars are 50 µm.
Fig. 2
Fig. 2
Campaniform sensilla (CS) are generally found on the same dorsal veins of Manduca sexta wings across individuals, although the distribution of sensilla along those veins varies. Wing schematics show locations of dorsal CS on one example individual. The veins around the central cell are dark grey, while the veins that correspond to the line diagrams are in gold. The line diagrams next to each wing image demonstrate the distribution of CS on M1, M3, and CU1 for different individuals (9 forewings, 10 hindwings). The gray-scale heatmaps below each line diagram for each vein demonstrate where CS are found along the length of the vein, split into 10 bins. Black indicates the location with the most CS (for that particular vein), while white indicates no CS.
Fig. 3
Fig. 3
Like the dorsal campaniform sensilla (CS), ventral CS are generally found on the same veins of Manduca sexta wings across individuals, although their distribution varies. Wing schematics show locations of CS on one example individual. The veins around the central cell are dark grey, while the veins that correspond to the line diagrams are in gold. The line diagrams next to each wing image demonstrate the distribution of CS on M1, M3, and CU1 for different moth individuals (9 forewings, 10 hindwings). The ventral surface of the wing has many CS that are located on the sides of veins (indicated by green triangle), such that their dome points roughly toward the leading or trailing edge of the wing (direction indicated by triangle). Below each set of distribution plots are heatmaps of CS locations along that particular vein, where the length of the vein is split into 10 bins. Black indicates the location with the most CS (for that particular vein), while white indicates no CS.
Fig. 4
Fig. 4
There are many campaniform sensilla (CS) distributed across the leading edge of the ventral forewing. This is a representative distribution from one wing, with magnified views of three CS within this distribution taken under low-wavelength light. Scale bars are 50 µm. In the distribution diagram, each CS is noted with a single dot regardless of where it is located on the vein (top or side). In the microscope images, the CS are indicated with arrows.
Fig. 5
Fig. 5
Campaniform sensilla (CS) at the distal tip of the ventral longitudinal veins are most often found in pairs, but they also occur singly. Barplots show the number of individual wings with a single or a paired CS on the tips of the longitudinal veins, ordered from leading-to-trailing edge of the wing, for the forewing (A) and the hindwing (B). Some sample wings were damaged at one or more vein tips such that we could not confirm the number of CS; thus not all bars sum to the total sample of wings. Images of CS are of a single sensillum at a vein tip (C), a paired set aligned with the axis of the vein (D), and a paired set aligned off-axis of the vein (E). The dashed line in (C–E) roughly follows the longitudinal axis of the vein. Scale bars are 50 µm.
Fig. 6
Fig. 6
We found one feature resembling a campaniform sensillum that was located on the wing membrane in-between veins, rather than on a vein itself (A). A closer image of the sensillum-like structure is in (B). Scale bars are 100 µm.
Fig. 7
Fig. 7
An insect wing vein under loading can be thought of as a beam under bending. The color scale represents the x-x normal strain due to the stresses caused by bending due to an applied force at the distal (right) end of the beam, which is fixed at the left end. The top of the cylinder experiences the most strain due to tension, while the bottom of the cylinder experiences the most strain due to compression. The transition from tension to compression occurs at what is known as the “neutral axis,” where the strain is zero. The wireframe indicates the at-rest position of the cantilevered cylinder. The cross-sectional size and shape of the beam also affects the strain gradient along the beam. For instance, under the same applied loading condition, the location of the greatest strain varies in tapered beam from the cylindrical (constant cross-section) condition.
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