Hierarchical Dragonfly Wing: Microstructure-Biomechanical Behavior Relations

The dragonfly wing,which consists of veins and membrane,is of biological hierarchical material.We observed the cross-sections of longitudinal veins and membrane using Environmental Scanning Electron Microscopy (ESEM).Based on the experiments and previous studies,we described the longitudinal vein and the membrane in terms of two hierarchical levels of organization of composite materials at the micro- and nano-scales.The longitudinal vein of dragonfly wing has a complex sandwich structure with two chitinous shells and a protein layer,and it is considered as the first hierarchical level of the vein.Moreover,the chitinous shells are concentric multilayered structures.Clusters of nano-fibrils grow along the circumferential orientation embedded into the protein layer.It is considered as the second level of the hierarchy.Similarly,the upper and lower epidermises of membrane constitute the first hierarchical level of organization in micro scale.Similar to the vein shell,the membrane epidermises were found to be a paralleled multilayered structure,defined as the second hierarchical level of the membrane.Combining with the mechanical behavior analysis of the dragonfly wing,we concluded that the growth orientation of the hierarchical structure of the longitudinal vein and membrane is relevant to its biomechanical behavior.     

Effects of Dragonfly Wing Structure on the Dynamic Performances

The configurations of dragonfly wings, including the corrugations of the chordwise cross-section, the microstructure of the longitudinal veins and membrane, were comprehensively investigated using the Environmental Scanning Electron Microscopy (ESEM). Based on the experimental results reported previously, the multi-scale and multi-dimensional models with different structural features of dragonfly wing were created, and the biological dynamic behaviors of wing models were discussed through the Finite Element Method (FEM). The results demonstrate that the effects of different structural features on dynamic behaviors of dragonfly wing such as natural frequency/modal, bending/torsional deformation, reaction force/torque are very significant. The corrugations of dragonfly wing along the chordwise can observably improve the flapping frequency because of the greater structural stiffness of wings. In updated model, the novel sandwich microstructure of the longitudinal veins remarkably improves the torsional deformation of dragonfly wing while it has a little effect on the flapping frequency and bending deformation. These integrated structural features can adjust the deformation of wing oneself, therefore the flow field around the wings can be controlled adaptively. The fact is that the flights of dragonfly wing with sandwich microstructure of longitudinal veins are more efficient and intelligent.     

The Role of Soft Vein Joints in Dragonfly Flight

Dragonflies are excellent flyers among insects and their flight ability is closely related to the architecture and material properties of their wings.The veins are main structure components of a dragonfly wing,which are found to be connected by resilin with high elasticity at some joints.A three-dimensional (3D) finite element model of dragonfly wing considering the soft vein joints is developed,with some simplifications.Passive deformation under aerodynamic loads and active flapping motion of the wing are both studied.The functions of soft vein joints in dragonfly flight are concluded.In passive deformation,the chordwise flexibility is improved by soft vein joints and the wing is cambered under loads,increasing the action area with air.In active flapping,the wing rigidity in spanwise direction is maintained to achieve the required amplitude.As a result,both the passive deformation and the active control of flapping work well in dragonfly flight.The present study may also inspire the design of biomimetic Flapping Micro Air Vehicles (FMAVs).     

The Wettability and Mechanism of Geometric Non-Smooth Structure of Dragonfly Wing Surface

Scanning electron microscope and optical contact angle measuring instruments were used to investigate the microstructure and wettability of geometric non-smooth structure of dragonfly wing surface. Results show that the geometric non-smooth structure of dragonfly wing surface is one part of epicuticle, some organic solvents can effectively dissolve the main ingredient of non-smooth structure. The hydrophobicity of dragonfly wing surface is induced by the co-coupling of the non-smooth structure and the waxy layer covering.     

Effects of corrugation of the dragonfly wing on gliding performance

We investigate the aerodynamic performance of the dragonfly wing, which has cross-sectional corrugation, via a static 2-dimensional unsteady simulation. Computational conditions are Re=150, 1400, and 10,000 with angles of attack ranging from 0° to 40°. From the computational results, lift coefficients are increased by the wing corrugation at all Reynolds number. However, the corrugation has little influence on the drag coefficients. The flows such as vortex in the valley of corrugation and near the edge of the corrugation are locally different from those of an elliptic wing. However, such local flows have little influence on the time averaged wing performance. From the numerical experiment presented in this study, it is determined that suction side corrugations of the wing have very little influence on increase of the lift coefficient at a positive angle of attack.     

Morphology of hindwing veins in the shield bug Graphosoma italicum (Heteroptera: Pentatomidae)

Light, fluorescence, and electron microscopy were applied to cross sections and -breakage and whole-mount preparations of the anterior hindwing vein of the shield bug Graphosoma italicum. These analyses were complemented by investigations of the basal part of the forewing Corium and Clavus. The integration of structural, histological, and fluorescence data revealed a complex arrangement of both rigid and elastic structures in the wall of wing veins and provided insights into the constitution of transition zones between rigid and elastic regions. Beneath the exocuticular layers, which are continuous with the dorsal and ventral cuticle of the wing membrane, the lumen of the veins is encompassed by a mesocuticular layer, an internal circular exocuticular layer, and an internal longitudinal endocuticular layer. Separate parallel lumina within the anterior longitudinal vein of the hindwing, arranged side-by-side rostro-caudally, suggest that several veins have fused in the phylogenetic context of vein reduction in the pentatomid hindwing. Gradual structural transition zones and resilin enrichment between sclerotized layers of the vein wall and along the edges of the claval furrow are interpreted as mechanical adaptations to enhance the reliability and durability of the mechanically stressed wing veins.     

现存蜉蝣翅基纵脉走向及愈合模式(昆虫纲：蜉蝣目)

有翅昆虫翅基纵脉的走向及愈合模式在系统发育重建中占有重要地位。然而,现存蜉蝣翅基纵脉的走向及愈合状况在大部分种类变化极大,无法推测其原始状况,只在极少数种类保留有部分可见残迹。中国拟短丝蜉Siphluriscus chinensis的翅基保留有独立的亚前缘脉弓、部分中脉M和肘脉Cu主干以及前中脉MA及径分脉Rs的走向痕迹。据此并结合红斑蜉Ephemera rufomaculata 和大网脉蜉Chromarcys magnifica翅基的相关特征,本文提出了蜉蝣目主要纵脉基部走向及愈合的基本模式,其要点有：中脉主干在基部与径脉主干独自发出后先接近或愈合后又分离、它们各自分成两支后的前中脉及径分脉又先愈合再分离、肘脉始终独立。这种中脉与径脉先接近或愈合后分离的模式非常接近新翅类的情况而与蜻蜓很不相同(在蜻蜓,中脉与肘脉在基部愈合) 。亚前缘脉弓的作用相信是加强了因翅基骨板发达而相互远离的纵脉间的连结作用。这个假说也可以来解释蜻蜓复杂脉相的形成原因。     

brinker and optomotor-blind act coordinately to initiate development of the L5 wing vein primordium in Drosophila

The stereotyped pattern of Drosophila wing veins is determined by the action of two morphogens, Hedgehog (Hh) and Decapentaplegic (Dpp), which act sequentially to organize growth and patterning along the anterior-posterior axis of the wing primordium. An important unresolved question is how positional information established by these morphogen gradients is translated into localized development of morphological structures such as wing veins in precise locations. In the current study, we examine the mechanism by which two broadly expressed Dpp signaling target genes, optomotor-blind (omb) and brinker (brk), collaborate to initiate formation of the fifth longitudinal (L5) wing vein. omb is broadly expressed at the center of the wing disc in a pattern complementary to that of brk, which is expressed in the lateral regions of the disc and represses omb expression. We show that a border between omb and brk expression domains is necessary and sufficient for inducing L5 development in the posterior regions. Mosaic analysis indicates that brk-expressing cells produce a short-range signal that can induce vein formation in adjacent omb-expressing cells. This induction of the L5 primordium is mediated by abrupt, which is expressed in a narrow stripe of cells along the brk/omb border and plays a key role in organizing gene expression in the L5 primordium. Similarly, in the anterior region of the wing, brk helps define the position of the L2 vein in combination with another Dpp target gene, spalt. The similar mechanisms responsible for the induction of L5 and L2 development reveal how boundaries set by dosage-sensitive responses to a long-range morphogen specify distinct vein fates at precise locations.     

Dpp/BMP transport mechanism is required for wing venation in the sawfly Athalia rosae

The pattern of wing venation varies considerably among different groups of insects and has been used as a means of species-specific identification. However, little is known about how wing venation is established and diversified among insects. The decapentaplegic (Dpp)/bone morphogenetic protein (BMP) signaling pathway plays a critical role in wing vein formation during the pupal stages in Drosophila melanogaster. A key mechanism is BMP transport from the longitudinal veins (LVs) to the posterior crossvein (PCV) by the BMP-binding proteins, short gastrulation (Sog) and twisted gastrulation2/crossveinless (Tsg2/Cv). To investigate whether the BMP transport mechanism is utilized to specify insect wing vein patterns in other than Drosophila, we used the sawfly Athalia rosae as a model, which has distinct venation patterns in the fore- and hindwings. Here, we show that Ar-dpp is ubiquitously expressed in both the fore- and hindwings, but is required for localized BMP signaling that reflects distinct wing vein patterns between the fore- and hindwings. By isolating Ar-tsg/cv in the sawfly, we found that Ar-Tsg/Cv is also required for BMP signaling in wing vein formation and retains the ability to transport Dpp. These data suggest that the BMP transport system is widely used to redistribute Dpp to specify wing venation and may be a basal mechanism underlying diversified wing vein patterns among insects.     

Origin and evolution of insect wings and their relation to metamorphosis,as documented by the fossil record

In contemporary entomology the morphological characters of insects are not always treated according to their phylogenetic rank. Fossil evidence often gives clues for different interpretations. All primitive Paleozoic pterygote nymphs are now known to have had articulated, freely movable wings reinforced by tubular veins. This suggests that the wings of early Pterygota were engaged in flapping movements, that the immobilized, fixed, veinless wing pads of Recent nymphs have resulted from a later adaptation affecting only juveniles, and that the paranotal theory of wing origin is not valid. The wings of Paleozoic nymphs were curved backwards in Paleoptera and were flexed backwards at will in Neoptera, in both to reduce resistance during forward movement. Therefore, the fixed oblique-backwards position of wing pads in all modern nymphs is secondary and is not homologous in Paleoptera and Neoptera. Primitive Paleozoic nymphs had articulated and movable prothoracic wings which became in some modern insects transformed into prothoracic lobes and shields. The nine pairs of abdominal gillplates of Paleozoic mayfly nymphs have a venation pattern, position, and development comparable to that in thoracic wings, to which they are serially homologous. Vestigial equivalents of wings and legs were present in the abdomen of all primitive Paleoptera and primitive Neoptera. The ontogenetic development of Paleozoic nymphs was confluent, with many nymphal and subimaginal instars, and the metamorphic instar was missing. The metamorphic instar originated by the merging together of several instars of old nymphs; it occurred in most orders only after the Paleozoic, separately and in parallel in all modern major lineages (at least twice in Paleoptera, in Ephemeroptera and Odonata; separately in hemipteroid, blattoid, orthopteroid, and plecopteroid lineages of exopterygote Neoptera; and once only in Endopterygota). Endopterygota evolved from ametabolous, not from hemimetabolous, exopterygote Neoptera. The full primitive wing venation consists of six symmetrical pairs of veins; in each pair, the first branch is always convex and the second always concave; therefore costa, subcosta, radius, media, cubitus, and anal are all primitively composed of two separate branches. Each pair arises from a single veinal base formed from a sclerotized blood sinus. In the most primitive wings the circulatory system was as follows: the costa did not encircle the wing, the axillary cord was missing, and the blood pulsed in and out of each of the six primary, convex-concave vein pair systems through the six basal blood sinuses. This type of circulation is found as an archaic feature in modern mayflies. Wing corrugation first appeared in preflight wings, and hence is considered primitive for early (paleopterous) Pterygota. Somewhat leveled corrugation of the central wing veins is primitive for Neoptera. Leveled corrugation in some modern Ephemeroptera, as well as accentuated corrugation in higher Neoptera, are both derived characters. The wing tracheation of Recent Ephemeroptera is not fully homologous to that of other insects and represents a more primitive, segmental stage of tracheal system. Morphology of an ancient articular region in Palaeodictyoptera shows that the primitive pterygote wing hinge in its simplest form was straight and composed of two separate but adjoining morphological units: the tergal, formed by the tegula and axillaries; and the alar, formed by six sclerotized blood sinuses, the basivenales. The tergal sclerites were derived from the tergum as follows: the lateral part of the tergum became incised into five lobes; the prealare, suralare, median lobe, postmedian lobe and posterior notal wing process. From the tips of these lobes, five slanted tergal sclerites separated along the deep paranotal sulcus: the tegula, first axillary, second axillary, median sclerite, and third axillary. Primitively, all pteralia were arranged in two parallel series on both sides of the hinge. In Paleoptera, the series stayed more or less straight; in Neoptera, the series became V-shaped. Pteralia in Paleoptera and Neoptera have been homologized on the basis of the fossil record. A differential diagnosis between Paleoptera and Neoptera is given. Fossil evidence indicates that the major steps in evolution, which led to the origin first of Pterygota, then of Neoptera and Endopterygota, were triggered by the origin and the diversification of flight apparatus. It is believed here that all above mentioned major events in pterygote evolution occurred first in the immature stages.     

Changing spatial patterns of DNA replication in the developing wing of Drosophila

Using an antibody against bromodeoxyuridine we have analyzed the distribution of S-phase nuclei in the wing disc of Drosophila as the larval disc transforms into the adult wing during metamorphosis. On the basis of the timing of replication three cell populations can be distinguished: the cells of the presumptive wing margin, the precursor cells of the longitudinal veins, and those of the intervein regions. In each of these populations the cell cycle is first arrested and later resumes at a specific time, so that at each developmental time point a characteristic spatial pattern of S-phase nuclei is seen. An interpretation of these changing patterns in terms of vein formation, compartments, and neural development is offered.     

Insights into the molecular mechanisms underlying diversified wing venation among insects

Insect wings are great resources for studying morphological diversities in nature as well as in fossil records. Among them, variation in wing venation is one of the most characteristic features of insect species. Venation is therefore, undeniably a key factor of species-specific functional traits of the wings; however, the mechanism underlying wing vein formation among insects largely remains unexplored. Our knowledge of the genetic basis of wing development is solely restricted to Drosophila melanogaster. A critical step in wing vein development in Drosophila is the activation of the decapentaplegic (Dpp)/bone morphogenetic protein (BMP) signalling pathway during pupal stages. A key mechanism is the directional transport of Dpp from the longitudinal veins into the posterior crossvein by BMP-binding proteins, resulting in redistribution of Dpp that reflects wing vein patterns. Recent works on the sawfly Athalia rosae, of the order Hymenoptera, also suggested that the Dpp transport system is required to specify fore- and hindwing vein patterns. Given that Dpp redistribution via transport is likely to be a key mechanism for establishing wing vein patterns, this raises the interesting possibility that distinct wing vein patterns are generated, based on where Dpp is transported. Experimental evidence in Drosophila suggests that the direction of Dpp transport is regulated by prepatterned positional information. These observations lead to the postulation that Dpp generates diversified insect wing vein patterns through species-specific positional information of its directional transport. Extension of these observations in some winged insects will provide further insights into the mechanisms underlying diversified wing venation among insects.     

Resilin-bearing wing vein joints in the dragonfly Epiophlebia superstes

In this study, we compared the dorsal and ventral patterns of three vein joint types and three types of resilin patches in the wings of the dragonfly Epiophlebia superstes. The joint types were classified according to their general structure and the resilin patch types according to their arrangement at joints and in the adjacent wing membrane. Resilin patches are found in both dorsal and ventral pleat valleys of the corrugated wings of E. superstes, which results in different patterns of resilin distribution on the dorsal and ventral sides of the wing. In addition to its probable function in conferring flexibility to stressed joints, resilin may also have a damping function. Our results suggest that resilin patches in the leading edge may be loaded in compression, whereas in the trailing area, they may be involved in angle widening and thus loaded in tension. Possible adaptations to the deformability of different areas of the wing, e.g. during the process of camber formation, are discussed.     

Postsurgical changes of the opening angle of canine autogenous vein graft.

The opening angles of 30 canine autogenous vein grafts were measured to determine the postsurgical change of residual strain in the vein graft. Canine femoral veins were grafted to femoral arteries in the end-to-end anastomosis fashion. When harvested, the vein grafts were cut into short segments and the segments were cut open radially. The opened-up configurations were taken as the zero-stress states of the vessels. Opening angle, defined as the angle between the two lines from the middle point to the tips of the inner wall, was used to describe the zero-stress states. Results show that the opening angles (mean +/- SD) are 63.0 +/- 30.6 deg for normal femoral veins, and -0.4 +/- 4.6, 6.1 +/- 19.4, 25.4 +/- 20.1, and 47.8 +/- 11.4 deg for vein grafts at 1 day, 1 week, 4 and 12 weeks postsurgery, respectively. The postsurgical changes in opening angle reveal nonuniform transmural tissue remodeling in the vascular wall. The relations between the changes in opening angle and the changes in the morphology of the vein grafts are discussed. Intimal hyperplasia is correlated to the opening angle and is suggested to be the main factor for the postsurgical increase in opening angle. The longitudinal strain in the vein graft is found to decrease postsurgically.     

Homology and function in the wings of Heteroptera

Abstract. The homology of veins and other wing characters in Heteroptera is reviewed in the light of palaeontology and new functional studies. A cladogram is given for the higher taxa of Hemiptera. It is probable that the vannus is an autapomorphy of Auchenorrhyncha+Heteropteroidea; that the leading edge vein of heteropteran fore- and hindwings is C+Sc; that Rs cannot be distinguished from R; that the hamus is part of M; that the glochis is a secondary structure. The difficulty of defining a vein is stressed. The functional significance of the hemielytron, cuneal fracture and longitudinal flexion lines is discussed. A preliminary ground-plan for Heteroptera wings is presented.     

Resilin in dragonfly and damselfly wings and its implications for wing flexibility

Although there is mounting evidence that passive mechanical dynamics of insect wings play an integral role in insect flight, our understanding of the structural details underlying insect wing flexibility remains incomplete. Here, we use comparative morphological and mechanical techniques to illuminate the function and diversity of two mechanisms within Odonata wings presumed to affect dynamic wing deformations: flexible resilin vein‐joints and cuticular spikes. Mechanical tests show that joints with more resilin have lower rotational stiffness and deform more in response to a load applied to an intact wing. Morphological studies of 12 species of Odonata reveal that resilin joints and cuticular spikes are widespread taxonomically, yet both traits display a striking degree of morphological and functional diversity that follows taxonomically distinct patterns. Interestingly, damselfly wings (suborder Zygoptera) are mainly characterized by vein‐joints that are double‐sided (containing resilin both dorsally and ventrally), whereas dragonfly wings (suborder Epiprocta) are largely characterized by single‐sided vein‐joints (containing resilin either ventrally or dorsally, but not both). The functional significance and diversity of resilin joints and cuticular spikes could yield insight into the evolutionary relationship between form and function of wings, as well as revealing basic principles of insect wing mechanical design. J. Morphol., 2011. © 2011 Wiley‐Liss, Inc.