Evolution of insect wings and development – new details from Palaeozoic nymphs

The nymphal stages of Palaeozoic insects differ significantly in morphology from those of their modern counterparts. Morphological details for some previously reported species have recently been called into question. Palaeozoic insect nymphs are important, however – their study could provide key insights into the evolution of wings, and complete metamorphosis. Here we review past work on these topics and juvenile insects in the fossil record, and then present both novel and previously described nymphs, documented using new imaging methods. Our results demonstrate that some Carboniferous nymphs – those of Palaeodictyopteroidea – possessed movable wing pads and appear to have been able to perform simple flapping flight. It remains unclear whether this feature is ancestral for Pterygota or an autapomorphy of Palaeodictyopteroidea. Further characters of nymphal development which were probably in the ground pattern of Pterygota can be reconstructed. Wing development was very gradual (archimetaboly). Wing pads did not protrude from the tergum postero‐laterally as in most modern nymphs, but laterally, and had well‐developed venation. The modern orientation of wing pads and the delay of wing development into later developmental stages (condensation) appears to have evolved several times independently within Pterygota: in Ephemeroptera, Odonatoptera, Eumetabola, and probably several times within Polyneoptera. Selective pressure appears to have favoured a more pronounced metamorphosis between the last nymphal and adult stage, ultimately reducing exploitation competition between the two. We caution, however, that the results presented herein remain preliminary, and the reconstructed evolutionary scenario contains gaps and uncertainties. Additional comparative data need to be collected. The present study is thus seen as a starting point for this enterprise.     

Four characters in a trade-off: dissecting their phenotypic and genetic relations

Phenotypic characters may covary negatively because they are in a trade-off or positively because they contribute to a single function. Genetic correlations can be used to test the validity and generality of these functional relationships by indicating the level of genetic integration and checking the conditions under which they are expressed. Phenotypic correlations indicate that there is a widespread trade-off between flight capability and early fecundity in insects. Different wing morphs (long and short wing) are thought to have a suite of reproductive and flight capability traits. In a half-sib mating experiment, we estimated phenotypic relationships between two flight-capability-related characters (flight muscle condition, wing morph) and two components of early fecundity (number of eggs in the ovaries, number of eggs laid), as well as genetic correlations relating wing morph and both components of fecundity in the wing-dimorphic cricket, Gryllus firmus. The number of eggs in the ovaries and the number of eggs laid were negatively correlated phenotypically and genetically with wing length morph (i.e., long wings associated with low fecundity). Both fecundity characters differed between wing morphs, but only if flight muscle was present and not histolyzed. The phenotypic and genetic correlations between fecundity characters were not significant. This suggests that the phenotypic relationship between ovary development and eggs laid is complex, they are not genetically integrated, and they may evolve independently. However, both early fecundity characters are functionally and genetically integrated within the trade-off to a similar degree. Finally, the trade-off affects early fecundity of both wing morphs suggesting that the functional relationship depends on flight muscle size. Received: 1 December 1998 / Accepted: 20 May 1999     

Time-Varying Wing-Twist Improves Aerodynamic Efficiency of Forward Flight in Butterflies

Insect wings can undergo significant chordwise (camber) as well as spanwise (twist) deformation during flapping flight but the effect of these deformations is not well understood. The shape and size of butterfly wings leads to particularly large wing deformations, making them an ideal test case for investigation of these effects. Here we use computational models derived from experiments on free-flying butterflies to understand the effect of time-varying twist and camber on the aerodynamic performance of these insects. High-speed videogrammetry is used to capture the wing kinematics, including deformation, of a Painted Lady butterfly (Vanessa cardui) in untethered, forward flight. These experimental results are then analyzed computationally using a high-fidelity, three-dimensional, unsteady Navier-Stokes flow solver. For comparison to this case, a set of non-deforming, flat-plate wing (FPW) models of wing motion are synthesized and subjected to the same analysis along with a wing model that matches the time-varying wing-twist observed for the butterfly, but has no deformation in camber. The simulations show that the observed butterfly wing (OBW) outperforms all the flat-plate wings in terms of usable force production as well as the ratio of lift to power by at least 29% and 46%, respectively. This increase in efficiency of lift production is at least three-fold greater than reported for other insects. Interestingly, we also find that the twist-only-wing (TOW) model recovers much of the performance of the OBW, demonstrating that wing-twist, and not camber is key to forward flight in these insects. The implications of this on the design of flapping wing micro-aerial vehicles are discussed.     

On the sex-specific mechanisms of butterfly flight: flight performance relative to flight morphology, wing kinematics, and sex in Pararge aegeria

Many evolutionary ecological studies have documented sexual dimorphism in morphology or behaviour. However, to what extent a sex-specific morphology is used differently to realize a certain level of behavioural performance is only rarely tested. We experimentally quantified flight performance and wing kinematics (wing beat frequency and wing stroke amplitude) and flight morphology (thorax mass, body mass, forewing aspect ratio, and distance to centre of forewing area) in the butterfly Pararge aegeria (L.) using a tethered tarsal reflex induced flight set-up under laboratory conditions. On average, females showed higher flight performance than males, but frequency and amplitude did not differ. In both sexes, higher flight performance was partly determined by wing beat frequency but not by wing stroke amplitude. Dry body mass, thorax mass, and distance to centre of forewing area were negatively related to wing beat frequency. The relationship between aspect ratio and wing stroke amplitude was sex-specific: females with narrower wings produced higher amplitude whereas males show the opposite pattern. The results are discussed in relation to sexual differences in flight behaviour.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 675–687.     

中国古生代化石昆虫研究回顾

自林启彬先生1978年命名了我国第一个古生代昆虫至今, 中国学者共发表20余篇分类学论著, 描述鉴定我国古生代昆虫共61种, 归属于9目（总目）。这些标本分布于西北、 西南、 华东等9省区, 其中石炭纪47种, 二叠纪14种。本文统计了我国已发现的古生代化石昆虫属种名录以及它们的分布和地质年代, 总结了国内古生代化石昆虫当前的研究状况和发展趋势, 并分析了研究中存在的问题。其中关于化石昆虫普遍存在的脉序差异问题需给予足够的重视, 高级阶元的建立应更加慎重。研究表明我国古生代昆虫已经高度分异, 古翅类、 新翅类均已出现, 且代表着有翅昆虫辐射演化的重要阶段。     

Evolution of flight morphology in a butterfly that has recently expanded its geographic range

Individuals colonizing unoccupied habitats typically possess characters associated with increased dispersal and, in insects, colonization success has been related to flight morphology. The speckled wood butterfly, Pararge aegeria, has undergone recent major expansions in its distribution: in the north of its range, P. aegeria has colonized many areas in north and east England, and in the south, it was first recorded on Madeira in 1976. We examined morphological traits associated with flight and reproduction in the northern subspecies tircis, and in the southern subspecies aegeria, from sites colonized about 20 years ago in northern England and on Madeira, respectively. Investment in flight was measured as relative wing area and thorax mass, and investment in reproduction as relative abdomen mass. All measurements were from individuals reared in a common environment and there were significant family effects in most of the variables measured. Compared with individuals from sites continuously occupied in recent history, colonizing individuals were larger (adult live mass). In the subspecies tircis, colonizing individuals also had relatively larger thoraxes and lower wing aspect ratios indicating that evolutionary changes in flight morphology may be related to colonization. However, sex by site interactions in analyses of thorax mass and abdomen mass suggest different selection pressures on flight morphology between the sexes in relation to colonization. Overall, the subspecies aegeria was smaller (adult live mass) and had a relatively larger thorax and wings, and smaller abdomen than subspecies tircis. Evolutionary changes in flight morphology and dispersal rate may be important determinants of range expansion, and may affect responses to future climate change. Received: 1 March 1999 / Accepted: 30 June 1999     

The costs of being dark: the genetic basis of melanism and its association with fitness‐related traits in the sand cricket

Melanism is an important component of insect cuticle and serves numerous functions that enhance fitness. Despite its importance, there is little information on its genetic basis or its phenotypic and genetic correlation with fitness‐related traits. Here, we examine the heritability of melanism in the wing dimorphic sand cricket and determine its phenotypic and genetic correlation with wing morphology, gonad mass and size of the dorso‐longitudinal muscles (the principle flight muscles). Previously demonstrated trade‐offs among these traits are significant factors in the evolution of life history variation. Using path analysis, we show that melanization is causally related to gonad mass, but not flight muscle mass. Averaged over the sexes, the heritability of melanism was 0.61, the genetic correlation with gonad mass was ?0.36 and with wing morph was 0.51. The path model correctly predicted the ranking of melanization score in lines selected for increased ovary mass, increased flight muscle mass, an index that increased both traits and an unselected control. Our results support the general hypothesis that melanization is costly for insects and negatively impacts investment in early reproduction.     

Distributed power and control actuation in the thoracic mechanics of a robotic insect

Recent advances in the understanding of biological flight have inspired roboticists to create flapping-wing vehicles on the scale of insects and small birds. While our understanding of the wing kinematics, flight musculature and neuromotor control systems of insects has expanded, in practice it has proven quite difficult to construct an at-scale mechanical device capable of similar flight performance. One of the key challenges is the development of an effective and efficient transmission mechanism to control wing motions. Here we present multiple insect-scale robotic thorax designs capable of producing asymmetric wing kinematics similar to those observed in nature and utilized by dipteran insects to maneuver. Inspired by the thoracic mechanics of dipteran insects, which entail a morphological separation of power and control muscles, these designs show that such distributed actuation can also modulate wing motion in a robotic design.     

Lateral Flight Stability of Two Hovering Model Insects

The longitudinal disturbance motion of different insects at hovering flight has the same modal structure. Here, we consider the case of lateral motion. The lateral dynamic flight stability of two model insects, hoverfly and honeybee, at hovering flight is studied. The method of computational fluid dynamics is applied to compute the stability derivatives. The techniques of eigenvalue and eigenvector analysis are used to solve the equations of motion. Results show that the lateral disturbance motion of the hoverfly has three natural modes of motion： an unstable divergence mode, a stable oscillatory mode and a stable subsidence mode, and the flight is unstable; while the honeybee has a different modal structure （a stable slow subsidence mode, a stable fast subsidence mode, and a nearly neutrally stable oscillatory mode） and the flight is nearly neutrally stable. The change in modal structure between the two insects is due to their roll-moment/side-velocity derivative having different sign, and the sign difference is because that the hoverfly has a relatively small, but the honeybee has a relatively large, distance between the wing roots and the center of mass. Thus, unlike the case of longitudinal motion, for lateral motion, some insects have different modal structures and stability properties from others.     

THE FLYING ABILITY OF ARCHAEOPTERYX

Estimates for the wing span, mass and wing area of Archaeopteryx lithographica are provided, and these are used to derive certain of the flight parameters. From the data available on the lengths of skeletal components, amplified by examination of casts of the specimens and full-size enlargements of photographs, the wing span is estimated at 58–59 cm and the wing area as 479 cm2. To judge from animals of similar size, the mass was probably about 200 g. These figures give an estimated minimum flying speed of 7-6 m/sec and a wing loading of 0–42 gf/cm2. These figures are, and must be from their method of derivation, comparable with those of similar sized modern birds, These data are used to reconsider the possibility of flapping flight in this bird. It is suggested that the primitive anatomy of the pectoral skeleton has been somewhat over-emphasized, and it is shown that the pectoral crest on the humerus was relatively very large compared with modern birds. The power required to fly would require muscular physiology outside the range of mammalian (at least, human) capability, but well within the modern avian range. It is felt that Archaeopteryx was capable of flapping flight, but that it was probably not long sustained.     

A nondestructive method of calculating the wing area of insects

Most insects engage in winged flight. Wing loading, that is, the ratio of body mass to total wing area, has been demonstrated to reflect flight maneuverability. High maneuverability is an important survival trait, allowing insects to escape natural enemies and to compete for mates. In some ecological field experiments, there is a need to calculate the wing area of insects without killing them. However, fast, nondestructive estimation of wing area for insects is not available based on past work. The Montgomery equation (ME), which assumes a proportional relationship between leaf area and the product of leaf length and width, is frequently used to calculate leaf area of plants, in crops with entire linear, lanceolate leaves. Recently, the ME was proved to apply to leaves with more complex shapes from plants that do not have any needle leaves. Given that the wings of insects are similar in shape to broad leaves, we tested the validity of the ME approach in calculating the wing area of insects using three species of cicadas common in eastern China. We compared the actual area of the cicadas’ wings with the estimates provided by six potential models used for wing area calculation, and we found that the ME performed best, based on the trade‐off between model structure and goodness of fit. At the species level, the estimates for the proportionality coefficients of ME for three cicada species were 0.686, 0.693, and 0.715, respectively. There was a significant difference in the proportionality coefficients between any two species. Our method provides a simple and powerful approach for the nondestructive estimation of insect wing area, which is also valuable in quantifying wing morphological features of insects. The present study provides a nondestructive approach to estimating the wing area of insects, allowing them to be used in mark and recapture experiments.     

Phylogenetic clustering of wingbeat frequency and flight‐associated morphometrics across insect orders

Wingbeat frequency in insects is an important variable in aerodynamic and energetic analyses of insect flight and often is studied on a family‐ or species‐level basis. Meta‐analyses of these studies report order‐level patterns suggesting that flight strategy is moderately well conserved phylogenetically. Studies incorporated into these meta‐analyses, however, use variable methodologies across different temperatures, which may confound results and phylogenetic patterns. In the present study, a high‐speed camera is used to measure wingbeat frequency in a wide variety of species (n = 102) under controlled conditions aiming (i) to determine the validity of previous meta‐analyses showing phylogenetic clustering of flight strategy and (ii) to identify new evolutionary patterns between wingbeat frequency, body mass, wing area, wing length and wing loading at the order level. All flight‐associated morphometrics significantly affect wingbeat frequency. Linear models show that wing area explains the most amount of variation in wingbeat frequency (r² = 0.59, P ≤ 0.001), whereas body mass explains the least (r² = 0.09, P ≤ 0.01). A multiple regression model incorporating both body mass and wing area is the best overall predictor of wingbeat frequency (r² = 0.84, P ≤ 0.001). Order‐level phylogenetic patterns across relationships are consistent with previous studies. Thus, the present study provides experimental validation of previous meta‐analyses and provides new insights into phylogenetically conserved flight strategies across insect orders.     

Avian wing proportions and flight styles: first step towards predicting the flight modes of mesozoic birds

We investigated the relationship between wing element proportions and flight mode in a dataset of living avian species to provide a framework for making basic estimates of the range of flight styles evolved by Mesozoic birds. Our results show that feather length (f(prim)) and total arm length (ta) (sum of the humerus, ulna and manus length) ratios differ significantly between four flight style groups defined and widely used for living birds and as a result are predictive for fossils. This was confirmed using multivariate ordination analyses, with four wing elements (humerus, ulna/radius, manus, primary feathers), that discriminate the four broad flight styles within living birds. Among the variables tested, manus length is closely correlated with wing size, yet is the poorest predictor for flight style, suggesting that the shape of the bones in the hand wing is most important in determining flight style. Wing bone thickness (shape) must vary with wing beat strength, with weaker forces requiring less bone. Finally, we show that by incorporating data from Mesozoic birds, multivariate ordination analyses can be used to predict the flight styles of fossils.     

Flight style in bats as predicted from wing morphometry: the effects of specimen preservation

An as yet unconsidered potential error in studies that predict flight style from morphological measurements of bats is the effect of the specimen type employed. On the basis of the finding that morphological measurements taken from fluid-preserved bat specimens may not yield values equivalent to those taken from the live animal, we compared the values of several variables (lifting surface area, wingspan, mass, aspect ratio, wing loading and minimum power speed) for live and fluid-preserved little brown bats ( Myotis lucifugus ) with the accepted standards for this species given by Norberg & Rayner (1987). Significant differences were detected for lifting surface area, wingspan, mass, aspect ratio and wing loading values taken from live bats and their respective values reported by Norberg & Rayner. Differences between preserved bats and Norberg & Rayner's numbers were limited to lifting surface area and wingspan (extended wing positions only), aspect ratio (all wing positions), and mass (both 70% ethanol- and 45% isopropyl alcohol-preserved specimens). Thus, Norberg & Rayner's values correspond most closely to values obtained from preserved museum specimens, a fact reflecting the source of their data in this instance. This and other limitations involved in attempting to predict the flight style of bats from a few morphological characters are discussed.     

The kinematics of Heteroptera in free flight

The kinematics of six species of Heteroptera in free flight are analysed and compared.

• (1) 

  Using nested analysis of variance techniques, statistically significant variation was detected between species for several of the flight parameters measured: mean angular velocity; pronation/supination ratio; upstroke/downstroke ratio; and wing beat frequency. In each case this is discussed in terms of variation in flight behaviour.
• (2) 

  Beneficial aerodynamic forces are generated during the upstroke and the downstroke, in both fast forward and rising flight.
• (3). 

  When the insects change from level, forward flight to near vertical, rising flight, the following parameters are altered in most of the sequences analysed:

• (a). 

  the stroke plane angle becomes steeply, negatively inclined, associated with an increase in body angle;
• (b). 

  the stroke amplitude is reduced;
• (c). 

  wing beat frequency is lowered, associated with a drop in mean angular velocity;
• (d). 

  the speed of stroke reversal (rotational velocity) is increased. This may be associated with increased wing torsion and tip flexion which in turn could improve any beneficial unsteady aerodynamic effects generated at stroke reversal.

The reasons for this change in flight performance and the deviations from that seen in other insects are discussed.
It is shown that Heteroptera may make use of wing drag in flight, particularly during rising flight.     

Tomographic Reconstruction of Neopterous Carboniferous Insect Nymphs

Two new polyneopteran insect nymphs from the Montceau-les-Mines Lagerstätte of France are presented. Both are preserved in three dimensions, and are imaged with the aid of X-ray micro-tomography, allowing their morphology to be recovered in unprecedented detail. One–Anebos phrixos gen. et sp. nov.–is of uncertain affinities, and preserves portions of the antennae and eyes, coupled with a heavily spined habitus. The other is a roachoid with long antennae and chewing mouthparts very similar in form to the most generalized mandibulate mouthparts of extant orthopteroid insects. Computer reconstructions reveal limbs in both specimens, allowing identification of the segments and annulation in the tarsus, while poorly developed thoracic wing pads suggest both are young instars. This work describes the morphologically best-known Palaeozoic insect nymphs, allowing a better understanding of the juveniles’ palaeobiology and palaeoecology. We also consider the validity of evidence from Palaeozoic juvenile insects in wing origin theories. The study of juvenile Palaeozoic insects is currently a neglected field, yet these fossils provide direct evidence on the evolution of insect development. It is hoped this study will stimulate a renewed interest in such work.     

A dual layer hair array of the brown lacewing: repelling water at different length scales

Additional weight due to contamination (water and/or contaminating particles) can potentially have a detrimental effect on the flight capabilities of large winged insects such as butterflies and dragonflies. Insects where the wing surface area-body mass ratio is very high will be even more susceptible to these effects. Water droplets tend to move spontaneously off the wing surface of these insects. In the case of the brown lacewing, the drops effectively encounter a dual bed of hair springs with a topographical structure which aids in the hairs resisting penetration into water bodies. In this article, we demonstrate experimentally how this protective defense system employed by the brown lacewing (Micromus tasmaniae) aids in resisting contamination from water and how the micro- and nanostructures found on these hairs are responsible for quickly shedding water from the wing which demonstrates an active liquid-repelling surface.     

Aerial Contests, Sexual Selection and Flight Morphology in Solitary Pompilid Wasps

Aerial contest competition has proven to be a challenging phenomenon to interpret in many territorial insects. Because the duels often consist of elaborate and/or high speed ascending maneuvers, the hypothesis that they are settled due to asymmetries in flight performance is intuitively appealing. We evaluated this hypothesis by contrasting differences in known morphological determinants of flight performance between (1) residents vs. non-residents of the territorial wasp, Hemipepsis ustulata and between (2) H. ustulata vs. a non-territorial relative, Pepsis thisbe . In the first contrast, resident male H. ustulata were seen to be larger, and had a tendency for reduced wing loading, but they did not possess greater flight musculature or wing aspect ratios (i.e., more elongated wings) than their non-resident counterparts. In the second contrast, male H. ustulata exhibited clearly greater flight musculature and greater sexual dimorphism in this parameter (males more muscular), and also exhibited a slight tendency for greater wing loading and smaller aspect ratios than males of the patrolling species P. thisbe . Interestingly, although size is linked with territorial success in H. ustulata , males of this species were not larger than male P. thisbe , nor did the former species exhibit greater sexual size dimorphism. These results do not support the hypothesis that the repeated ascending contests of H. ustulata require, and select for, a high acceleration design. However, the observed intraspecific patterns of flight musculature suggest that high acceleration is favored in males of the perching species, perhaps for the ability to intercept passing receptive females.     

Peculiarities of structural-functional organization of the motor neuropil in the dragonfly thoracic ganglia

The study considers structural-functional relations in motor neuropil of the thoracic ganglia in dragonflies-insects capable of performing very complex and fast maneuvering in flight. The motor neuropil in dragonflies was shown to be more differentiated than in less mobile insects, while its motor nuclei are more outlined and approached to each other. There were revealed dendrites of the leg muscle motoneurons (intermediate nucleus), running to the anterior and posterior nuclei that contain dendrites of the wing muscle motoneurons. A possible role of such a dendrite approaching is discussed for close functional cooperation of wing and leg muscles essential for dragonflies to catch a large prey in flight by using their legs. Peculiarities of structural organization of the wing muscle motoneurons in dragonflies and locusts are considered to suggest the greater functional capabilities of motoneurons in the dragonfly motor apparatus.