Research Article: Morphological and mechanical properties of flexible resilin joints on damselfly wings (Rhinocypha spp.)

Date Published: March 7, 2018

Publisher: Public Library of Science

Author(s): Kenjiro Yazawa, Keiji Numata, Y. Norma-Rashid, Sharon Swartz.

http://doi.org/10.1371/journal.pone.0193147

Abstract

Resilin functions as an elastic spring that demonstrates extraordinary extensibility and elasticity. Here we use combined techniques, laser scanning confocal microscopy (LSCM) and scanning electron microscopy (SEM) to illuminate the structure and study the function of wing flexibility in damselflies, focusing on the genus Rhinocypha. Morphological studies using LSCM and SEM revealed that resilin patches and cuticular spikes were widespread along the longitudinal veins on both dorsal and ventral wing surfaces. Nanoindentation was performed by using atomic force microscopy (AFM), where the wing samples were divided into three sections (membrane of the wing, mobile and immobile joints). The resulting topographic images revealed the presence of various sizes of nanostructures for all sample sections. The elasticity range values were: membrane (0.04 to 0.16 GPa), mobile joint (1.1 to 2.0 GPa) and immobile joint (1.8 to 6.0 GPa). The elastomeric and glycine-rich biopolymer, resilin was shown to be an important protein responsible for the elasticity and wing flexibility.

Partial Text

Insects were among the first animals that have been recognised to have unique structures of elastic proteins that assist in movements [1]. Insect wings, including those of dragonflies are complex mechanical structures. A study reported a venous system for dragonfly wings, mainly composed of veins and membranes, possessing both stiff and flexible materials [2]. Wang et al [3] further reported the wing veins of complex sandwich structure of chitinous shells and a protein layer containing fibrils that further enhance the capability to absorb mechanical energy [4]. This hierarchical composite structure is said to be common in biological materials [5, 6]. While the deformations of the wing in Odonata are known to be contributed by a one-way hinge that allows the free movements in the upstroke and restrains the displacements in the downstroke [7], it is influenced by a number of criterion over the wing, one of the most effective elements are vein micro joints in contrast to others [8, 9, 10].

The initial scanning by SEM on the wings of Rhinocypha spp. had confirmed that there are two main types of joints; mobile and immobile joints as suggested by previous study [15]. According to Newman [39], there were more than six different types of cross veins. The presence of the blue-fluorescing material in the vein-joints, which was revealed by the LSCM, are known as resilin. Here, in the three species, distinct patches of resilin were found within the nodus dorsally and ventrally that are consistent with the results reported previously by Donoughe et al [17]. These unique structures are renowned to have roles in the wing torsion [21]. Moreover, resilin was found mostly in the mobile joints where cross veins meet longitudinal veins which provided elasticity and not flexibility for the twisting movements of the wing [15].

While previous studies were on dragonflies, such as [19, 35, 41, 53, 60], this work presents the first comprehensive investigation on the structure and mechanical properties of the damselfly (Rhinocypha spp.) wings, combining three microscopy techniques; LSCM, SEM and AFM, together with the protein analysis. The structural analysis revealed that the flexibility of the wings varied from one area to another, and the resilin distribution pattern was the mechanism that controlled the characteristics of the wing. Furthermore, this study confirms the presence of spikes at most parts of the longitudinal veins in damselflies (Suborder: Zygoptera) which were reported to be rare in dragonflies (Suborder: Anisoptera). Additionally, the AFM images revealed resilin nanostructures of varied sizes and enabled the calculation of elasticity values at each section of the wing; membrane, mobile and immobile joints in Rhinocypha spp. Here we report for the first time glycine (instead of proline, as commonly described elsewhere), played a more prominent role in wing flexibility. Approaches that combine structural and mechanical studies on resilin would offer more convincing evidences for the relationship of proline -glycine structural function. While studies on silks and elastin received a lot of attention in the past decade, this has now change to focus on recombinant resilin; structure-mechanical properties of the resilin with potentially greater application in a variety of fields.

 

Source:

http://doi.org/10.1371/journal.pone.0193147

 

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