Resilin in the flight apparatus of Odonata (Insecta)—cap tendons and their biomechanical importance for flight

Abstract

In Odonata, a direct flight mechanism with specialized tendons evolved. One particular adaptation, the implementation of the rubber-like protein resilin in these cap tendons, might be of major importance. Although resilin was first described in one tendon of Odonata, to our knowledge no comprehensive study about the presence of resilin in the thorax exists yet. We investigated various species of Odonata, using mCT, dissection and fluorescence microscopy. Here we show a complete mapping of the odonatan pterothorax, regarding the presence of tendons and their properties. Thus, 20-21 cap tendons in the pterothorax of Odonata show the presence of resilin. While performing outstanding and often-aggressive flight manoeuvres, resilin can provide shock absorption against mechanical damage from strong impacts. It may further improve the wear and fatigue resistance owing to resilin's damping behaviour. Additionally, resilin in tendons can absorb and return kinetic energy to restore muscles to their original shape after contracting and help in maintaining self-oscillation of the flight muscles. Here, the material distribution within the direct flight system of Odonata and the biomechanical importance and possible function of resilin are discussed. These results are an important step towards the understanding of the complex form -material -function interplay of the insect cuticle.

Light and Autofluorescence, Multitasking Features in Living Organisms

“…The bluish autofluorescence of resilin has also allowed its differentiation from the green and red emission respectively from sclerotized and chitinous cuticle, besides confirming its presence in the pterothorax cap tendons. This finding is fully consistent with the role of resilin in supporting and protecting muscles from mechanical shock, by absorbing and bringing them back energy [198]. Autofluorescence detection of resilin and chitin depending on their respective brilliant light blue and yellowish-reddish emission colors has also been proved to discriminate antennal gustatory sensilla in leaf beetles, opening interesting investigation perspectives on the sensing of non-volatile metabolites in herbivorous insect in decoding plant biochemical composition [199].…”

“…Imaging has evidenced the prevalence of reddish-yellowish sclerotized material in the parts of mandibles where a high force is applied by the insect to crush preys, while the bluish emitting resilin is mainly present in elastic membranous structures, confirming the autofluorescence potential for the in situ study of functional organization of complex structures [196]. Even more interestingly, resilin autofluorescence in Odonata has been also exploited to study the biomechanical role of this protein in the mechanism of flight defined as "direct", for the direct connection between musculature and wings by means of cap tendons ensuring unique skills of fly movement [197,198]. The bluish autofluorescence of resilin has also allowed its differentiation from the green and red emission respectively from sclerotized and chitinous cuticle, besides confirming its presence in the pterothorax cap tendons.…”

The Bright Side of the Tiger: Autofluorescence Patterns in Aedes albopictus (Diptera, Culicidae) Male and Female Mosquitoes

“…Several studies have focused on the bluish fluorescing resilin, a protein described as rubber-like due to its distinctive elastic mechanical properties, endowed by its chemical composition. In combination with other proteins or with the sclerotized or chitinous cuticle, fluorescing in the green and red spectral regions, respectively, resilin allows the accomplishment of a variety of mechanical and receptor functions [ 13 , 14 , 15 ]. In this regard, the particular ability of the antennae to play various sensory roles in detecting chemicals, as well as sound vibrations, can account for the frequent occurrence of species- and sex-specific structural variability entailing differences in the compositional material, responding to the adaptation to the different needs of mosquitoes [ 16 , 17 ].…”

Functional morphology of the raptorial forelegs in Mantispa styriaca (Insecta: Neuroptera)

“…Yet, Loxton and Nicholls (1979) indicated differences within the cuticle in Mantodea, due to either heavily sclerotized or thin and flexible cuticle at the base of femoral spines, that needs further investigation. However, the relevance of the material composition in a functional and/or biomechanical context, was shown in a number of studies for a variety of character systems in insects like: mouthparts (Büsse and Gorb 2018), thorax (Bäumler and Büsse 2019) or abdomen (Willkommen et al 2015), but most often for wings (Gorb 1999;Haas et al, 2000;Appel and Gorb 2011;Rajabi et al 2016) and legs (Peisker et al 2013;Jandausch et al 2018;Petersen et al 2018;Büsse et al 2019a, b). The main purpose of the study is therefore, to present a detailed description of the raptorial forelegs of Mantispa styriaca (Poda, 1761), including extrinsic and intrinsic musculature as well as the material composition of their cuticle.…”