The Drosophila wing consists of a transparent wing membrane supported by a network of wing veins. Previously, we have shown that the wing membrane cuticle is not flat but is organized into ridges that are the equivalent of one wing epithelial cell in width and multiple cells in length. These cuticle ridges have an anteroposterior orientation in the anterior wing and a proximodistal orientation in the posterior wing. The precise topography of the wing membrane is remarkable because it is a fusion of two independent cuticle contributions from the dorsal and ventral wing epithelia. Here, through morphological and genetic studies, we show that it is the dorsal wing epithelium that determines wing membrane topography. Specifically, we find that wing hair location and membrane topography are coordinated on the dorsal, but not ventral, surface of the wing. In addition, we find that altering Frizzled Planar Cell Polarity (i.e., Fz PCP) signaling in the dorsal wing epithelium alone changes the membrane topography of both dorsal and ventral wing surfaces. We also examined the wing morphology of two model Hymenopterans, the honeybee Apis mellifera and the parasitic wasp Nasonia vitripennis. In both cases, wing hair location and wing membrane topography are coordinated on the dorsal, but not ventral, wing surface, suggesting that the dorsal wing epithelium also controls wing topography in these species. Because phylogenomic studies have identified the Hymenotera as basal within the Endopterygota family tree, these findings suggest that this is a primitive insect character.

The appearance of wings in insects, early in their evolution [1], has been one of the more critical innovations contributing to their extraordinary diversity. Despite the conspicuousness and importance of wings, the origin of these structures has been difficult to resolve and represented one of the "abominable mysteries" in evolutionary biology [2]. More than a century of debate has boiled the matter down to two competing alternatives-one of wings representing an extension of the thoracic notum, the other stating that they are appendicular derivations from the lateral body wall. Recently, a dual model has been supported by genomic and developmental data [3-6], representing an amalgamation of elements from both the notal and pleural hypotheses. Here, we reveal crucial information from the wing pad joints of Carboniferous palaeodictyopteran insect nymphs using classical and high-tech techniques. These nymphs had three pairs of wing pads that were medially articulated to the thorax but also broadly contiguous with the notum anteriorly and posteriorly (details unobservable in modern insects), supporting their overall origin from the thoracic notum as well as the expected medial, pleural series of axillary sclerites. Our study provides support for the formation of the insect wing from the thoracic notum as well as the already known pleural elements of the arthropodan leg. These results support the unique, dual model for insect wing origins and the convergent reduction of notal fusion in more derived clades, presumably due to wing rotation during development, and they help to bring resolution to this long-standing debate.

Animal wings deform during flight in ways that can enhance lift, facilitate flight control, and mitigate damage. Monitoring the structural and aerodynamic state of the wing is challenging because deformations are passive, and the flow fields are unsteady; it requires distributed mechanosensors that respond to local airflow and strain on the wing. Without a complete map of the sensor arrays, it is impossible to model control strategies underpinned by them. Here, we present the first systematic characterization of mechanosensors on the dragonfly's wings: morphology, distribution, and wiring. By combining a cross-species survey of sensor distribution with quantitative neuroanatomy and a high-fidelity finite element analysis, we show that the mechanosensors are well placed to perceive features of the wing dynamics relevant to flight. This work describes the wing sensory apparatus in its entirety and advances our understanding of the sensorimotor loop that facilitates exquisite flight control in animals with highly deformable wings.

Thermal plasticity of melanin pigmentation patterns in Drosophila species has been studied as a model to investigate developmental mechanisms of phenotypic plasticity. The developmental process of melanin pigmentation patterns on wings of Drosophila is divided into two parts, prepattern specification during the pupal period and wing vein-dependent transportation of melanin precursors after eclosion. Which part can be affected by thermal changes? To address this question, we used polka-dotted melanin spots on wings of Drosophila guttifera, whose spot areas are specified by wingless morphogen. In this research, we reared D. guttifera at different temperatures to test whether wing spots show thermal plasticity. We found that wing size becomes larger at lower temperature and that different spots have different reaction norms. Furthermore, we changed the rearing temperature in the middle of the pupal period and found that the most sensitive developmental periods for wing size and spot size are different. The results suggest that the size control mechanisms for the thermal plasticity of wing size and spot size are independent. We also found that the most sensitive stage for spot size was part of the pupal period including stages at which wingless is expressed in the polka-dotted pattern. Therefore, it is suggested that temperature change might affect the prepattern specification process and might not affect transportation through wing veins.

The genetic basis of wing development has been well characterised for model insect species, but remains poorly understood in phylogenetically divergent, non-model taxa. Wing-polymorphic insect species potentially provide ideal systems for unravelling the genetic basis of secondary wing reduction. Stoneflies (Plecoptera) represent an anciently derived insect assemblage for which the genetic basis of wing polymorphism remains unclear. We undertake quantitative RNA-seq of sympatric full-winged versus vestigial-winged nymphs of a widespread wing-dimorphic New Zealand stonefly, Zelandoperla fenestrata, to identify genes potentially involved in wing development and secondary wing loss.

In addition to the heart proper, insects possess wing hearts in the thorax to ensure regular hemolymph flow through the narrow wings. In Drosophila, the wing hearts consist of two bilateral muscular pumps of unknown origin. Here, we present the first developmental study on these organs and report that the wing hearts originate from eight embryonic progenitor cells arising in two pairs in parasegments 4 and 5. These progenitors represent a so far undescribed subset of the Even-skipped positive pericardial cells (EPC) and are characterized by the early loss of tinman expression in contrast to the continuously Tinman positive classical EPCs. Ectopic expression of Tinman in the wing heart progenitors omits organ formation, indicating a crucial role for Tinman during progenitor specification. The subsequent postembryonic development is a highly dynamic process, which includes proliferation and two relocation events. Adults lacking wing hearts display a severe wing phenotype and are unable to fly. The phenotype is caused by omitted clearance of the epidermal cells from the wings during maturation, which inhibits the formation of a flexible wing blade. This indicates that wing hearts are required for proper wing morphogenesis and functionality.

The decapentaplegic (dpp) gene plays a variety of roles in diverse cellular and molecular processes of the growth and development. In insects, dpp is mainly required for dorsal-ventral patterning and appendage formation. The brown planthopper (BPH) Nilaparvata lugens, a major pest of rice, possesses two distinct wing morphs described as long-winged (LW) and short-winged (SW) morphs. With our lab-maintained stable strains of LW and SW BPH, RNA interference (RNAi) was used to research the functions of N. lugens dpp (Nldpp) on wing development. Silencing of Nldpp in the SW strain led to the significant lengthening of the forewing, while Nldpp-knockdown in the LW strain resulted in distorted wings. Moreover, knockdown of Nldpp caused the complete absence of wing veins. During the development of wing-pads, the Nldpp abundance in the terga of the SW strain was significantly higher than that of the LW strain. Through controlling the direction of wing morph transformation, we found that the expression level of Nldpp increased in the NlInR1-knockdown BPH (tending to SW) and abundance of Nldpp declined after dsNlInR2 injection (tending to LW). Our results showed that Nldpp is mainly responsible for the formation and development of veins in BPH. Also, Nldpp can be regulated by NlInR1/2 and participate in the wing morph transformation.

The origin and evolution of the novel insect wing remain enigmatic after a century-long discussion. The mechanism of wing development in hemimetabolous insects, in which the first functional wings evolved, is key to understand where and how insect wings evolutionarily originate. This study explored the developmental origin and the postembryonic dramatic growth of wings in the cricket Gryllus bimaculatus. We find that the lateral tergal margin, which is homologous between apterygote and pterygote insects, comprises a growth organizer to expand the body wall to form adult wing blades in Gryllus. We also find that Wnt, Fat-Dachsous, and Hippo pathways are involved in the disproportional growth of Gryllus wings. These data provide insights into where and how insect wings originate. Wings evolved from the pre-existing lateral terga of a wingless insect ancestor, and the reactivation or redeployment of Wnt/Fat-Dachsous/Hippo-mediated feed-forward circuit might have expanded the lateral terga.

Signaling between cells in the anterior (A) and posterior (P) compartments directs Drosophila wing disc development and is dependent on expression of the homeodomain transcription factor Engrailed (En) in P cells. Downstream of en, posteriorly expressed Hedgehog (Hh) protein signals across the A/P border to establish a developmental organizer that directs pattern formation and growth throughout the wing primordium. Here we extend investigations of the processes downstream of en by using expression array analysis to compare A and P cells. A total of 102 candidate genes were identified that express differentially in the A and P compartments; four were characterized: Stubble (Sb) expression is restricted to A cells due to repression by en. CG15905, CG16884; CG10200/hase und igel (hui) are expressed in A cells downstream of Hh signaling; and RNA interference for hui, Stubble, and CG16884 revealed that each is essential to wing development.

Human impact on biodiversity usually is measured by reduction in species abundance or richness. Just as important, but much more difficult to discern, is the anthropogenic elimination of ecological interactions. Here we report on the persistence of a long ecological interaction chain linking diverse food webs and habitats in the near-pristine portions of a remote Pacific atoll. Using biogeochemical assays, animal tracking, and field surveys we show that seabirds roosting on native trees fertilize soils, increasing coastal nutrients and the abundance of plankton, thus attracting manta rays to native forest coastlines. Partnered observations conducted in regions of this atoll where native trees have been replaced by human propagated palms reveal that this complex interaction chain linking trees to mantas readily breaks down. Taken together these findings provide a compelling example of how anthropogenic disturbance may be contributing to widespread reductions in ecological interaction chain length, thereby isolating and simplifying ecosystems.

Bats have large, thin wings that are particularly susceptible to tearing. Anatomical specializations, such as fiber reinforcement, strengthen the wing and increase its resistance to puncture, and an extensive vasculature system across the wing also promotes healing. We investigated whether tear positioning is associated with anatomy in common pipistrelles (Pipistrellus pipistrellus). Wing anatomy was described using histological techniques, imaging, and material testing. Tear information, including type, position, time in rehabilitation, and possible causes, was collected from rehabilitators of injured bats across the United Kingdom. Results suggest that the position of the plagiopatagium (the most proximal wing section to the body), rather than its anatomy, influenced the number, location, and orientation of wing tears. While material testing did not identify the plagiopatagium as being significantly weaker than the chiropatagium (the more distal sections of the wing), the plagiopatagium tended to have the most tears. The position of the tears, close to the body and toward the trailing edge, suggests that they are caused by predator attacks, such as from a cat (Felis catus), rather than collisions. Consistent with this, 38% of P. pipistrellus individuals had confirmed wing tears caused by cats, with an additional 38% identified by rehabilitators as due to suspected cat attacks. The plagiopatagium had the lowest number of blood vessels and highest amounts of elastin fibers, suggesting that healing may take longer in this section. Further investigations into the causes of tears, and their effect on flight capabilities, will help to improve bat rehabilitation.

Wings are probably the most advanced evolutionary novelty in insects. In the fruit fly Drosophila melanogaster, proper development of wings requires the activity of so-called wing hearts located in the scutellum of the thorax. Immediately after the imaginal ecdysis, these accessory circulatory organs remove hemolymph and apoptotic epidermal cells from the premature wings through their pumping action. This clearing process is essential for the formation of functional wing blades. Mutant flies that lack intact wing hearts are flightless and display malformed wings. The embryonic wing heart progenitors originate from two adjacent parasegments corresponding to the later second and third thoracic segments. However, adult dipterian flies harbor only one pair of wings and only one pair of associated wing hearts in the second thoracic segment. Here we show that the specification of WHPs depends on the regulatory activity of the Hox gene Ultrabithorax. Furthermore, we analyzed the development of wing hearts in the famous four-winged Ultrabithorax (Ubx) mutant, which was first discovered by Ed Lewis in the 1970s. In these flies, the third thoracic segment is homeotically transformed into a second thoracic segment resulting in a second pair of wings instead of the club-shaped halteres. We show that a second pair of functional wing hearts is formed in the transformed third thoracic segment and that all wing hearts originate from the wild-type population of wing heart progenitor cells.

Regeneration is the ability of an organism to rebuild a body part that has been damaged or amputated, and can be studied at the molecular level using model organisms. Drosophila imaginal discs, which are the larval primordia of adult cuticular structures, are capable of undergoing regenerative growth after transplantation and in vivo culture into the adult abdomen.

Metazoan development involves a myriad of dynamic cellular processes that require cytoskeletal function. Nonmuscle myosin II plays essential roles in embryonic development; however, knowledge of its role in post-embryonic development, even in model organisms such as Drosophila melanogaster, is only recently being revealed. In this study, truncation alleles were generated and enable the conditional perturbation, in a graded fashion, of nonmuscle myosin II function. During wing development they demonstrate novel roles for nonmuscle myosin II, including in adhesion between the dorsal and ventral wing epithelial sheets; in the formation of a single actin-based wing hair from the distal vertex of each cell; in forming unbranched wing hairs; and in the correct positioning of veins and crossveins. Many of these phenotypes overlap with those observed when clonal mosaic analysis was performed in the wing using loss of function alleles. Additional requirements for nonmuscle myosin II are in the correct formation of other actin-based cellular protrusions (microchaetae and macrochaetae). We confirm and extend genetic interaction studies to show that nonmuscle myosin II and an unconventional myosin, encoded by crinkled (ck/MyoVIIA), act antagonistically in multiple processes necessary for wing development. Lastly, we demonstrate that truncation alleles can perturb nonmuscle myosin II function via two distinct mechanisms--by titrating light chains away from endogenous heavy chains or by recruiting endogenous heavy chains into intracellular aggregates. By allowing myosin II function to be perturbed in a controlled manner, these novel tools enable the elucidation of post-embryonic roles for nonmuscle myosin II during targeted stages of fly development.

The first purpose of this study was to reveal the distribution of the angel wing (AW) of geese. Our data showed that the total incidence of AW was 6.67% in 150-day-old White Zhedong (ZD) geese, the occurrence of AW in left wing is higher than that in right wing and bilateral wing than unilateral wing (both P < 0.01). In 70-day-old Hybrid-Wanxi (HW) geese, the total incidence of AW was 8.86%, with similar incidence rate between unilateral and bilateral. The sex has not apparently affected the incidence of AW in both ZD and HW geese. To explore the potential relationship between wing type with body weight, organ index, bone characteristic, or blood biochemical parameters in 70-day-old HW geese. We found that the body weight and organ index were similar between normal wing (NW) and AW geese. The length for the humerus, metacarpal and phalanx, and the phalanx weights, as well as the angle between the humerus and the radial ulna (HRU) in NW geese were pronounced greater than that in AW geese (P < 0.05). Furthermore, the angel wing was strongly associated with lower platelet size indicators. Collectively, AW affected the wing bone length, phalanx weight, and HRU, and the occurrence of AW may be related with dysfunctional platelet activation in geese.

Polyphenism is a successful strategy adopted by organisms to adapt to environmental changes. Brown planthoppers (BPH, Nilaparvata lugens) develop two wing phenotypes, including long-winged (LW) and short-winged (SW) morphs. Though insulin receptor (InR) and juvenile hormone (JH) have been known to regulate wing polyphenism in BPH, the interaction between these regulators remains largely elusive. Here, we discovered that a conserved microRNA, miR-34, modulates a positive autoregulatory feedback loop of JH and insulin/IGF signaling (IIS) pathway to control wing polyphenism in BPH. Nlu-miR-34 is abundant in SW BPHs and suppresses NlInR1 by targeting at two binding sites in the 3'UTR of NlInR1. Overexpressing miR-34 in LW BPHs by injecting agomir-34 induces the development towards SW BPHs, whereas knocking down miR-34 in SW BPHs by injecting antagomir-34 induces more LW BPHs when another NlInR1 suppressor, NlInR2, is also suppressed simultaneously. A cis-response element of Broad Complex (Br-C) is found in the promoter region of Nlu-miR-34, suggesting that 20-hydroxyecdysone (20E) might be involved in wing polyphenism regulation. Topic application of 20E downregulates miR-34 expression but does not change wing morphs. On the other hand, JH application upregulates miR-34 expression and induces more SW BPHs. Moreover, knocking down genes in IIS pathway changes JH titers and miR-34 abundance. In all, we showed that miRNA mediates the cross talk between JH, 20E and IIS pathway by forming a positive feedback loop, uncovering a comprehensive regulation mechanism which integrates almost all known regulators controlling wing polyphenism in insects.

The insect wing is a key evolutionary innovation that was essential for insect diversification. Yet despite its importance, there is still debate about its evolutionary origins. Two main hypotheses have been proposed: the paranotal hypothesis, which suggests that wings evolved as an extension of the dorsal thorax, and the gill-exite hypothesis, which proposes that wings were derived from a modification of a pre-existing branch at the dorsal base (subcoxa) of the leg. Here, we address this question by studying how wing fates are initially specified during Drosophila embryogenesis, by characterizing a cis-regulatory module (CRM) from the snail (sna) gene, sna-DP (for dorsal primordia). sna-DP specifically marks the early primordia for both the wing and haltere, collectively referred to as the DP. We found that the inputs that activate sna-DP are distinct from those that activate Distalless, a marker for leg fates. Further, in genetic backgrounds in which the leg primordia are absent, the DP are still partially specified. However, lineage-tracing experiments demonstrate that cells from the early leg primordia contribute to both ventral and dorsal appendage fates. Together, these results suggest that the wings of Drosophila have a dual developmental origin: two groups of cells, one ventral and one more dorsal, give rise to the mature wing. We suggest that the dual developmental origins of the wing may be a molecular remnant of the evolutionary history of this appendage, in which cells of the subcoxa of the leg coalesced with dorsal outgrowths to evolve a dorsal appendage with motor control.

Huanglongbing (HLB) causes considerable economic losses to citrus industries worldwide. Its management depends on controlling of the Asian citrus Psyllid (ACP), the vector of the bacterium, Candidatus Liberibacter asiaticus (CLas), the causal agent of HLB. Silencing genes by RNA interference (RNAi) is a promising tool to explore gene functions as well as control pests. In the current study, abnormal wing disc (awd) gene associated with wing development in insects is used to interfere with the flight of psyllids. Our study showed that transcription of awd is development-dependent and the highest level was found in the last instar (5(th)) of the nymphal stage. Micro-application (topical application) of dsRNA to 5(th) instar of nymphs caused significant nymphal mortality and adult wing-malformation. These adverse effects in ACP were positively correlated with the amounts of dsRNA used. A qRT-PCR analysis confirmed the dsRNA-mediated transcriptional down-regulation of the awd gene. Significant down-regulation was required to induce a wing-malformed phenotype. No effect was found when dsRNA-gfp was used, indicating the specific effect of dsRNA-awd. Our findings suggest a role for awd in ACP wing development and metamorphosis. awd could serve as a potential target for insect management either via direct application of dsRNA or by producing transgenic plants expressing dsRNA-awd. These strategies will help to mitigate HLB by controlling ACP.

Wing patterns are key taxonomic characters that have long been used in descriptions of Lepidoptera; however, wing pattern homologies are not understood among different moth lineages. Here, we examine the relationship between wing venation and wing pattern in the genus Micropterix, among the most basal extant Lepidoptera, in order to evaluate the two existing predictive models that have the potential to establish wing pattern element homologies for the order. The location of wing pattern elements along the costal margin of the wing in Micropterix is consistent with the predictions of the model proposed for Tortricidae by Brown and Powell in 1991, later modified by Baixeras in 2002. The predictive power of this model for such distantly related taxa suggests that the model may hold across various superfamilies within Lepidoptera, and supports the long-held notion that fasciae, not spots, are the most likely primitive wing pattern elements for the order. In addition, the location of wing pattern elements suggests that the wing vein commonly termed Sc1 may in fact be a different vein, which Comstock identified in Trichoptera and referred to as "a."

The blackcap Sylvia atricapilla shows a complex migratory pattern and is a suitable species for the studies of morphological migratory syndrome, including adaptations of wing shape to different migratory performance. Obligate migrants of this species that breed in northern, central, and Eastern Europe differ by migration distance and some cover shorter distance to the wintering grounds in the southern part of Europe/North Africa or the British Isles, although others migrate to sub-Saharan Africa. Based on ˃40 years of ringing data on blackcaps captured during autumn migration in the Southern Baltic region, we studied age- and sex-related correlations in wing pointedness and wing length of obligate blackcap migrants to understand the differences in migratory behavior of this species. Even though the recoveries of blackcaps were scarce, we reported some evidence that individuals which differ in migration distance differed also in wing length. We found that wing pointedness significantly increased with an increasing wing length of migrating birds, and adults had longer and more pointed wings than juvenile birds. This indicates stronger antipredator adaptation in juvenile blackcaps than selection on flight efficiency, which is particularly important during migration. Moreover, we documented more pronounced differences in wing length between adult and juvenile males and females. Such differences in wing length may enhance a faster speed of adult male blackcaps along the spring migration route and may be adaptive when taking into account climatic effects, which favor earlier arrival from migration to the breeding grounds.