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. 2022 Nov;283(11):1390-1410.
doi: 10.1002/jmor.21510. Epub 2022 Sep 16.

Evolutionary functional morphology of the proboscis and feeding apparatus of hawk moths (Sphingidae: Lepidoptera)

Affiliations

Affiliation

  • 1 Department of Evolutionary Biology, University of Vienna, Vienna, Austria.

Evolutionary functional morphology of the proboscis and feeding apparatus of hawk moths (Sphingidae: Lepidoptera)

Caroline Reinwald et al. J Morphol. 2022 Nov.
. 2022 Nov;283(11):1390-1410.
doi: 10.1002/jmor.21510. Epub 2022 Sep 16.

Affiliation

  • 1 Department of Evolutionary Biology, University of Vienna, Vienna, Austria.

Abstract

The morphology of the proboscis and associated feeding organs was studied in several nectar-feeding hawk moths, as well as a specialized honey-feeder and two supposedly nonfeeding species. The proboscis lengths ranged from a few millimeters to more than 200 mm. Despite the variation in proboscis length and feeding strategy, the principle external and internal composition of the galeae, the stipes pump, and the suction pump were similar across all species. The morphology of the smooth and slender proboscis is highly conserved among all lineages of nectar-feeding Sphingidae. Remarkably, they share a typical arrangement of the sensilla at the tip. The number and length of sensilla styloconica are independent from proboscis length. A unique proboscis morphology was found in the honey-feeding species Acherontia atropos. Here, the distinctly pointed apex displays a large subterminal opening of the food canal, and thus characterizes a novel type of piercing proboscis in Lepidoptera. In the probably nonfeeding species, the rudimentary galeae are not interlocked and the apex lacks sensilla styloconica; galeal muscles, however, are present. All studied species demonstrate an identical anatomy of the stipes, and suction pump, regardless of proboscis length and diet. Even supposedly nonfeeding Sphingidae possess all organs of the feeding apparatus, suggesting that their proboscis rudiments might still be functional. The morphometric analyses indicate significant positive correlations between galea lumen volume and stipes muscle volume as well as the volume of the food canal and the muscular volume of the suction pump. Size correlations of these functionally connected organs reflect morphological fine-tuning in the evolution of proboscis length and function.

Keywords: insects; mouthparts; sensilla; suction pump.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1

Figure 1

Head and coiled proboscis of…

Figure 1

Head and coiled proboscis of three Sphingidae, left labial palpus removed (LM photos).…

Figure 1
Head and coiled proboscis of three Sphingidae, left labial palpus removed (LM photos). (a) Nectar‐feeding Xylophanes pyrrhus; proboscis (45.2 mm long) coiled in about 5 coils; (b) Honey‐feeding Acherontia atropos, stout proboscis (12.4 mm long) coiled in approximately 1 coil; (c) Probably nonfeeding Mimas tiliae; galeae not interlocked throughout the entire length; rudimentary proboscis (4 mm long), coiled in 1.5 coils. ce, complex eye; ga, galea; lp, labial palpus; pi, piliferes.
Figure 2

Figure 2

Proboscis of various Sphingidae (SEM).…

Figure 2

Proboscis of various Sphingidae (SEM). (a) Nectar‐feeding Deilephila elpenor ; the galeal surface…

Figure 2
Proboscis of various Sphingidae (SEM). (a) Nectar‐feeding Deilephila elpenor; the galeal surface of the long slender proboscis displays cuticle ribs. Sensilla of various types in great distance to each other, drinking region with drinking slits; (b–d) Robust proboscis of the honey‐feeding Acherontia atropos; (b) proximal region of the galea covered with long bristle‐shaped sensilla filiformia; sensilla of the piliferes are in contact with the galeal base; (c) wide opening of the food canal on the dorsal side of the tip; (d) distal half of the proboscis (lateral view); distinct decrease of thickness forms pointed tip; (e) rudimentary galea of Smerinthus ocellata (lateral view). cr, cuticle rib; dl, dorsal legulae; ds, drinking slits; pi, pilifer; sc, sensillum chaeticum; SEM, scanning electron microscopy; sf, sensilla filiformia; sst, sensillum styoconicum; vl, ventral legulae.
Figure 3

Figure 3

Proboscis sensilla in various Sphingidae…

Figure 3

Proboscis sensilla in various Sphingidae (SEM). (a) Galea tip of Sphinx pinastri ;…

Figure 3
Proboscis sensilla in various Sphingidae (SEM). (a) Galea tip of Sphinx pinastri; nectar‐feeding species; (b) galea tip of Acherontia atropos; honey‐feeding species (c) Smerinthus ocellata; apex with a sensillum chaeticum and a sensillum basiconicum (d) Protambulyx strigilis; food canal in drinking region; (e) Deilephila elpenor; sensillum basiconica located in depression of the cuticle (f) P. strigilis; sensillum basiconicum in the food canal; (g) A. atropos; sensillum coeloconicum close to the apex. dl, dorsal legulae; fc, food canal; sb, sensillum basiconicum; sc, sensillum chaeticum; SEM, scanning electron microscopy; sst, sensillum styloconicum; vl, ventral legulae.
Figure 4

Figure 4

Cross sections of proboscises of…

Figure 4

Cross sections of proboscises of three Sphingidae (semithin sections; all sections at the…

Figure 4
Cross sections of proboscises of three Sphingidae (semithin sections; all sections at the same scale); despite various sizes, the same principle composition can be found; proximal proboscis region in the first row, distal proboscis region in the second row, drinking region in the third row, (a–c) Nectar‐feeding Agrius convolvuli; one galea magnified, (d–f) honey‐feeding Acherontia atropos; (g–i) nonfeeding Mimas tiliae; galeae not connected; one galea magnified; lim and mim could not be separated. fc, food canal; lim, lateral intrinsic muscles; mim, median intrinsic muscles; ne, nerve; tr, trachea.
Figure 5

Figure 5

Head, muscles of the proboscis…

Figure 5

Head, muscles of the proboscis base, and the stipes pump of three Sphingidae;…

Figure 5
Head, muscles of the proboscis base, and the stipes pump of three Sphingidae; reconstruction from microCT images (all species at same scale); (a) nectar‐feeding Agrius convolvuli, frontal view; (b) A. convolvuli, lateral view; (c) honey‐feeding Acherontia atropos, frontal view; (d) A. atropos, lateral view; (e) Mimas tiliae, proboscis rudimentary, frontal view; (f) M. tiliae lateral view. External stipes muscles (esm) in purple; internal stipes muscles (ism) in green; basal galeal muscles (bgm) in yellow.
Figure 6

Figure 6

Volumes of functionally connected organs…

Figure 6

Volumes of functionally connected organs of the feeding apparatus correlate significantly. Spearman's rank…

Figure 6
Volumes of functionally connected organs of the feeding apparatus correlate significantly. Spearman's rank correlation of morphometrical variables was measured in 10 sphingids with varying proboscis length. Each data point represents a measurement obtained from one individual of a species. Black‐filled dots indicate species with a proboscis longer than the body, and white‐filled dots indicate species with a proboscis shorter than the body (see Table 4). Values are given in mm³. (a) Galeal lumen and external stipes musculature of the hemolymph pump (ρ(8) = 0.96, p = 2.2 × 10−16). (b) Galeal lumen and internal stipes musculature of the hemolymph pump (ρ(8) = 0.88, p = 9.1 × 10−4). (c) Suction pump dilator musculature and food canal (ρ(8) = 0.69, p = 0.04). (d) Suction pump compressor musculature and food canal (ρ(8) = 0.65, p = 0.05).
Figure 7

Figure 7

Suction pumps of three Sphingidae;…

Figure 7

Suction pumps of three Sphingidae; reconstructions from microCT images (all species at same…

Figure 7
Suction pumps of three Sphingidae; reconstructions from microCT images (all species at same scale); (a) nectar‐feeding Agrius convolvuli, frontal view; (b) A. convolvuli, lateral view; (c) honey‐feeding Acherontia atropos, frontal view; (d) A. atropos, lateral view (e) nonfeeding Mimas tiliae, frontal view; (f) M. tiliae, lateral view. Dilator muscles (dil), which expand the suction pump lumen (lum), in red; compressor muscles (com), which decrease the suction pump lumen, in the dark blue; lumen in light blue.

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