Machine learning reveals the control mechanics of an insect wing hinge.

Insects constitute the most species-rich radiation of metazoa, a success that is due to the evolution of active flight. Unlike pterosaurs, birds and bats, the wings of insects did not evolve from legs1, but are novel structures that are attached to the body via a biomechanically complex hinge that transforms tiny, high-frequency oscillations of specialized power muscles into the sweeping back-and-forth motion of the wings2. The hinge consists of a system of tiny, hardened structures called sclerites that are interconnected to one another via flexible joints and regulated by the activity of specialized control muscles. Here we imaged the activity of these muscles in a fly using a genetically encoded calcium indicator, while simultaneously tracking the three-dimensional motion of the wings with high-speed cameras. Using machine learning, we created a convolutional neural network3 that accurately predicts wing motion from the activity of the steering muscles, and an encoder-decoder4 that predicts the role of the individual sclerites on wing motion. By replaying patterns of wing motion on a dynamically scaled robotic fly, we quantified the effects of steering muscle activity on aerodynamic forces. A physics-based simulation incorporating our hinge model generates flight manoeuvres that are remarkably similar to those of free-flying flies. This integrative, multi-disciplinary approach reveals the mechanical control logic of the insect wing hinge, arguably among the most sophisticated and evolutionarily important skeletal structures in the natural world.

Hybrid speciation driven by multilocus introgression of ecological traits.

Hybridization allows adaptations to be shared among lineages and may trigger the evolution of new species1,2. However, convincing examples of homoploid hybrid speciation remain rare because it is challenging to demonstrate that hybridization was crucial in generating reproductive isolation3. Here we combine population genomic analysis with quantitative trait locus mapping of species-specific traits to examine a case of hybrid speciation in Heliconius butterflies. We show that Heliconius elevatus is a hybrid species that is sympatric with both parents and has persisted as an independently evolving lineage for at least 180,000 years. This is despite pervasive and ongoing gene flow with one parent, Heliconius pardalinus, which homogenizes 99% of their genomes. The remaining 1% introgressed from the other parent, Heliconius melpomene, and is scattered widely across the H. elevatus genome in islands of divergence from H. pardalinus. These islands contain multiple traits that are under disruptive selection, including colour pattern, wing shape, host plant preference, sex pheromones and mate choice. Collectively, these traits place H. elevatus on its own adaptive peak and permit coexistence with both parents. Our results show that speciation was driven by introgression of ecological traits, and that speciation with gene flow is possible with a multilocus genetic architecture.

Joint extension speed dictates bio-inspired morphing trajectories for optimal longitudinal flight dynamics.

Avian wing morphing allows dynamic, active control of complex flight manoeuvres. Previous linear time-invariant (LTI) models have quantified the effect of varying fixed wing configurations but the time-dependent effects of morphing between different configurations is not well understood. To fill this gap, I implemented a linear parameter-varying (LPV) model for morphing wing gull flight. This approach models the wing joint angles as scheduled parameters and accounts for nonlinear kinematic and gravitational effects while interpolating between LTI models at discrete trim points. With the resulting model, I investigated the longitudinal response associated with various joint extension trajectories. By optimizing the extension trajectory for four independent objectives (speed and pitch angle overshoot, speed rise time and pitch angle settling time), I found that the extension trajectory inherent to the gull wing does not guarantee an optimal response but may provide a sufficient response with a simpler mechanical implementation. Furthermore, the results indicated that gulls likely require extension speed feedback. This morphing LPV model provides insights into underlying control mechanisms, which may allow for avian-like flight in future highly manoeuvrable uncrewed aerial vehicles.

Blind measurements did not confirm effects of forest fragmentation on fluctuating asymmetry of a tropical butterfly Morpho helenor.

Re-evaluation of photographs of the tropical butterfly Morpho helenor from a previous study (Pignataro et al. 2023) revealed that its conclusion regarding increased wing fluctuating asymmetry in forest edge habitats compared to forest interior habitats could not be replicated. This discrepancy likely arises from (i) original measurements not being conducted blindly, (ii) insufficient photograph quality hindering accurate landmark selection, and (iii) a lack of detailed description of the measurement protocol. The likelihood of false positive discoveries within the published data concerning the impacts of environmental stress on the fluctuating asymmetry of plants and animals is probably higher than previously assumed.

Evolutionary change in flight-to-light response in urban moths comes with changes in wing morphology.

Moths and other insects are attracted by artificial light sources. This flight-to-light behaviour disrupts their general activity focused on finding resources, such as mating partners, and increases predation risk. It thus has substantial fitness costs. In illuminated urban areas, spindle ermine moths Yponomeuta cagnagella were reported to have evolved a reduced flight-to-light response. Yet, the specific mechanism remained unknown, and was hypothesized to involve either changes in visual perception or general flight ability or overall mobility traits. Here, we test whether spindle ermine moths from urban and rural populations-with known differences in flight-to-light responses-differ in flight-related morphological traits. Urban individuals were found to have on average smaller wings than rural moths, which in turn correlated with a lower probability of being attracted to an artificial light source. Our finding supports the reduced mobility hypothesis, which states that reduced mobility in urban areas is associated with specific morphological changes in the flight apparatus.

Morphological and structural characteristics of the elytra reduce impact damage to ladybird beetles.

Beetle elytra act as natural protective covers and effectively shield their flexible abdomens and fragile hindwings from damage. The existing studies have attributed this contribution of the elytra to its honeycomb structures. In this combined experimental and theoretical study, we used the seven-spotted ladybird beetle to demonstrate that both biological morphology and the hollow structure of the dome-like elytra combined to reduce damage during falling. The falling ladybird beetles had a high probability (59.52%) of hitting the ground with the costal edge of the elytra. This strategy could assist with converting the translational energy into rotational kinetic energy, resulting in the reduction of the impulse during falling. In addition, the hollow structures on the elytra could further absorb the residual impact energy. In the future, this biological paradigm could be used as a basis for the development of falling/landing techniques for advanced robots.

Maple samara flight is robust to morphological perturbation and united by a classic drag model.

Winged, autorotating seeds from the genus Acer, have been the subject of study for botanists and aerodynamicists for decades. Despite this attention and the relative simplicity of these winged seeds, there are still considerable gaps in our understanding of how samara dynamics are informed by morphological features. Additionally, questions remain regarding the robustness of their dynamics to morphological alterations such as mass change by moisture or area change by damage. We here challenge the conventional approach of using wing-loading correlations and instead demonstrate the superiority of a classical aerodynamic model. Using allometry, we determine why some species deviate from interspecific aerodynamic behavior. We alter samara mass and wing area and measure corresponding changes to descent velocity, rotation rate, and coning angle, thereby demonstrating their remarkable ability to autorotate despite significant morphological alteration. Samaras endure mass changes greater than 100% while maintaining descent velocity changes of less than 15%, and are thus robust to changes in mass by moisture or damage. Additionally, samaras withstand up to a 40% reduction in wing area before losing their ability to autorotate, with the largest wings more robust to ablation. Thus, samaras are also robust to wing damage in their environment, a fact children joyfully exploit.

Surprise RNA paints colorful patterns on butterfly wings.

Understudied means of regulating genes is likely widespread in butterflies-and perhaps other animals.

Functional constraints on the number and shape of flight feathers.

As a fundamental ecological aspect of most organisms, locomotor function significantly constrains morphology. At the same time, the evolution of novel locomotor abilities has produced dramatic morphological transformations, initiating some of the most significant diversifications in life history. Despite significant new fossil evidence, it remains unclear whether volant locomotion had a single or multiple origins in pennaraptoran dinosaurs and the volant abilities of individual taxa are controversial. The evolution of powered flight in modern birds involved exaptation of feathered surfaces extending off the limbs and tail yet most studies concerning flight potential in pennaraptorans do not account for the structure and morphology of the wing feathers themselves. Analysis of the number and shape of remex and rectrix feathers across a large dataset of extant birds indicates that the number of remiges and rectrices and the degree of primary vane asymmetry strongly correlate with locomotor ability revealing important functional constraints. Among these traits, phenotypic flexibility varies reflected by the different rates at which morphological changes evolve, such that some traits reflect the ancestral condition, whereas others reflect current locomotor function. While Mesozoic birds and Microraptor have remex morphologies consistent with extant volant birds, that of anchiornithines deviate significantly providing strong evidence this clade was not volant. The results of these analyses support a single origin of dinosaurian flight and indicate the early stages of feathered wing evolution are not sampled by the currently available fossil record.

Transposable Element Insertions Are Associated with Batesian Mimicry in the Pantropical Butterfly Hypolimnas misippus.

Hypolimnas misippus is a Batesian mimic of the toxic African Queen butterfly (Danaus chrysippus). Female H. misippus butterflies use two major wing patterning loci (M and A) to imitate three color morphs of D. chrysippus found in different regions of Africa. In this study, we examine the evolution of the M locus and identify it as an example of adaptive atavism. This phenomenon involves a morphological reversion to an ancestral character that results in an adaptive phenotype. We show that H. misippus has re-evolved an ancestral wing pattern present in other Hypolimnas species, repurposing it for Batesian mimicry of a D. chrysippus morph. Using haplotagging, a linked-read sequencing technology, and our new analytical tool, Wrath, we discover two large transposable element insertions located at the M locus and establish that these insertions are present in the dominant allele responsible for producing mimetic phenotype. By conducting a comparative analysis involving additional Hypolimnas species, we demonstrate that the dominant allele is derived. This suggests that, in the derived allele, the transposable elements disrupt a cis-regulatory element, leading to the reversion to an ancestral phenotype that is then utilized for Batesian mimicry of a distinct model, a different morph of D. chrysippus. Our findings present a compelling instance of convergent evolution and adaptive atavism, in which the same pattern element has independently evolved multiple times in Hypolimnas butterflies, repeatedly playing a role in Batesian mimicry of diverse model species.

Got milkweed? Genetic assimilation as potential source for the evolution of nonmigratory monarch butterfly wing shape.

Monarch butterflies (Danaus plexippus) are well studied for their annual long-distance migration from as far north as Canada to their overwintering grounds in Central Mexico. At the end of the cold season, monarchs start to repopulate North America through short-distance migration over the course of multiple generations. Interestingly, some populations in various tropical and subtropical islands do not migrate and exhibit heritable differences in wing shape and size, most likely an adaptation to island life. Less is known about forewing differences between long- and short-distance migrants in relation to island populations. Given their different migratory behaviors, we hypothesized that these differences would be reflected in wing morphology. To test this, we analyzed forewing shape and size of three different groups: nonmigratory, lesser migratory (migrate short-distances), and migratory (migrate long-distances) individuals. Significant differences in shape appear in all groups using geometric morphometrics. As variation found between migratory and lesser migrants has been shown to be caused by phenotypic plasticity, and lesser migrants develop intermediate forewing shapes between migratory and nonmigratory individuals, we suggest that genetic assimilation might be an important mechanism to explain the heritable variation found between migratory and nonmigratory populations. Additionally, our research confirms previous studies which show that forewing size is significantly smaller in nonmigratory populations when compared to both migratory phenotypes. Finally, we found sexual dimorphism in forewing shape in all three groups, but for size in nonmigratory populations only. This might have been caused by reduced constraints on forewing size in nonmigratory populations.

Wing pattern diversity in Eunica butterflies (Nymphalidae: Biblidinae): phylogenetic analysis implies decoupled adaptive trends in dorsal sexual dimorphism and ventral eyespot evolution.

Butterfly eyespots are wing patterns reminiscent of vertebrate eyes, formed by concentric rings of contrastingly coloured scales. Eyespots are usually located close to the wing margin and often regarded as the single most conspicuous pattern element of butterfly wing colour displays. Recent efforts to understand the processes involved in the formation of eyespots have been driven mainly by evo-devo approaches focused on model species. However, patterns of change implied by phylogenetic relationships can also inform hypotheses about the underlying developmental mechanisms associated with the formation or disappearance of eyespots, and the limits of phenotypic diversity occurring in nature. Here we present a combined evidence phylogenetic hypothesis for the genus Eunica, a prominent member of diverse Neotropical butterfly communities, that features notable variation among species in eyespot patterns on the ventral hind wing surface. The data matrix consists of one mitochondrial gene region (COI), four nuclear gene regions (GAPDH, RPS5, EF1a and Wingless) and 68 morphological characters. A combined cladistic analysis with all the characters concatenated produced a single most parsimonious tree that, although fully resolved, includes many nodes with modest branch support. The phylogenetic hypothesis presented corroborates a previously proposed morphological trend leading to the loss of eyespots, together with an increase in the size of the conserved eyespots, relative to outgroup taxa. Furthermore, wing colour pattern dimorphism and the presence of androconia suggest that the most remarkable instances of sexual dimorphism are present in the species of Eunica with the most derived eyespot patterns, and are in most cases accompanied by autapomorphic combinations of scent scales and "hair pencils". We discuss natural and sexual selection as potential adaptive explanations for dorsal and ventral wing patterns.

Thoracic and abdominal outgrowths in early pterygotes: a clue to the common ancestor of winged insects?

One of the fundamental questions in insect evolution is the origin of their wings and primary function of ancestral wing precursors. Recent phylogenomic and comparative morphological studies broadly support a terrestrial ancestor of pterygotes, but an aquatic or semiaquatic ancestor cannot be ruled out. Here new features of the branchial system of palaeodictyopteran larvae of several different instars of Katosaxoniapteron brauneri gen. et sp. nov. (Eugereonoidea) from the late Carboniferous collected at Piesberg (Germany) are described, which consist of delicate dorsolateral and lamellate caudal abdominal gills that support an aquatic or at least semiaquatic lifestyle for these insects. Moreover, the similar form and surface microstructures on the lateral abdominal outgrowths and thoracic wing pads indicate that paired serial outgrowths on segments of both tagmata presumably functioned as ancestral type of gills resembling a protopterygote model. This is consistent with the hypothesis that the wing sheaths of later stage damselfly larvae in hypoxic conditions have a respiratory role similar to abdominal tracheal gills. Hence, the primary function and driving force for the evolution of the precursors of wing pads and their abdominal homologues could be respiration.

Morphological evolution of bird wings follows a mechanical sensitivity gradient determined by the aerodynamics of flapping flight.

The physical principles that govern the function of biological structures also mediate their evolution, but the evolutionary drivers of morphological traits within complex structures can be difficult to predict. Here, we use morphological traits measured from 1096 3-dimensional bird wing scans from 178 species to test the interaction of two frameworks for relating morphology to evolution. We examine whether the evolutionary rate (σ2) and mode is dominated by the modular organization of the wing into handwing and armwing regions, and/or the relationship between trait morphology and functional output (i.e. mechanical sensitivity, driven here by flapping flight aerodynamics). Our results support discretization of the armwing and handwing as morphological modules, but morphological disparity and σ2 varied continuously with the mechanical sensitivity gradient and were not modular. Thus, mechanical sensitivity should be considered an independent and fundamental driver of evolutionary dynamics in biomechanical traits, distinct from morphological modularity.

The function of wing bullae in mayflies (Insecta: Ephemeroptera) reveals new insights into the early evolution of Pterygota.

BACKGROUND: Mayflies are basal winged insects of crucial importance for the understanding of the early evolution of Pterygota. Unlike all other insects, they have two successive winged stages, the subimago and the imago. Their forewings feature so-called bullae, which are desclerotized spots in the anterior main veins. Up to now, they have been considered to play a major role in wing bending during flight. RESULTS: We investigated bullae by multiple methods to reveal their structure and arrangement and to gain new information on the evolution of insect flight. Bullae are mostly present in the anterior negative wing veins, disrupting the otherwise rigid veins. High-speed videography reveals that mayfly wings do not bend during flight. Likewise, different arrangements of bullae in different species do not correlate with different modes of flying. Observations on the moulting of subimagines unravel that they are essential for wing bending during the extraction of the imaginal wing from the subimaginal cuticle. Bullae define predetermined bending lines, which, together with a highly flexible wing membrane enriched with resilin, permit wing bending during subimaginal moulting. Bullae are only absent in those species that remain in the subimaginal stage or that use modified modes of moulting. Bullae are also visible in fossil mayflies and can be traced back to stemgroup mayflies of the Early Permian, the 270 million years old Protereismatidae, which most probably had bullae in both fore- and hind wings. CONCLUSIONS: Bullae in mayfly wings do not play a role in flight as previously thought, but are crucial for wing bending during subimaginal moulting. Thus, the presence of bullae is a reliable morphological marker for a subimaginal life stage, confirming the existence of the subimago already in Permian Protereismatidae. A thorough search for bullae in fossils of other pterygote lineages may reveal wheather they also had subimagines and at what point in evolution this life stage was lost. In mayflies, however, the subimago may have been retained due to selective advantages in connection with the transition from aquatic to terrestrial life or due to morphological requirements for a specialized mating flight.

Early origin and diverse phenotypic implementation of iridescent UV patterns for sexual signaling in pierid butterflies.

Iridescent ultraviolet (IUV) patterns on pierid butterfly wings are phenotypic adaptations commonly used as sexual signals, generated by scales with ultrastructural modifications. Pierid IUV patterns are sexually dichromatic, with reduced size in females, where conspicuous sexual signaling balances courtship against ecological predation. There have been no phylogenetic reconstructions of IUV within Pieridae and little morphological characterization of phenotypic diversity. Our genus-wide characterization of IUV revealed the uniform similarity of stacked lamellar ridges on the dorsal surface of cover scales. We tested a hypothesis of single versus multiple origins by reconstructing a phylogeny of 534 species (~43.2% described species), with all genera represented, and a trait matrix of 734 species (~59.4%) screened for IUV. A single, early dimorphic origin of IUV followed by several losses and gains received strong support, concluding that IUV patterns and structural coloration are old traits. Collectively, these results support the homology of IUV scales and patterns that diversified within several lineages, suggesting an interplay between female-mediated sexual selection and ecological predatory selection.

Independent wing reductions and losses among stick and leaf insects (Phasmatodea), supported by new Cretaceous fossils in amber.

BACKGROUND: Phasmatodea (stick and leaf insects) play a central role on the debate regarding wing reduction and loss, and its wings are putative reacquisition from secondarily wingless ancestors based solely on extant species. A pivotal taxon in this respect is the species-poor Timematodea, consisting of approximately 21 wingless extant species, which form the sister group of all remaining winged or wingless stick and leaf insects, the Euphasmatodea. RESULTS: Herein, the new fossils of Timematodea from mid-Cretaceous Kachin amber are reported, with winged and wingless species co-occurring. The palaeogeographic distributions of all fossils of Holophasmatodea are summarized, showing their wide paleo-distributions. The phylogenetic analysis based on morphological characters confirms the earliest-diverging lineage of winged Breviala cretacea gen. et sp. nov. in Timematodea, and the possible relationships among all families of Holophasmatodea. These are critical for the reconstruction of patterns of wing evolution in early Phasmatodea. CONCLUSIONS: The new fossils suggest that Timematodea once had wings, at least during the mid-Cretaceous. The palaeogeographic occurrences imply that Timematodea probably have been widely distributed since at least the Jurassic. The phylogenetic analysis with the ancestral-state reconstruction of wings indicates that the common ancestors of Holophasmatodea were winged, the reductions and losses of wings among Timematodea and Euphasmatodea have occurred independently since at least the Cretaceous, and the reduction or loss of the forewing earlier than the hind wings.

Fluid-structure interactions of bristled wings: the trade-off between weight and drag.

The smallest flying insects often have bristled wings resembling feathers or combs. We combined experiments and three-dimensional numerical simulations to investigate the trade-off between wing weight and drag generation. In experiments of bristled strips, a reduced physical model of the bristled wing, we found that the elasto-viscous number indicates when reconfiguration occurs in the bristles. Analysis of existing biological data suggested that bristled wings of miniature insects lie below the reconfiguration threshold, thus avoiding drag reduction. Numerical simulations of bristled strips showed that there exist optimal numbers of bristles that maximize the weighted drag when the additional volume due to the bristles is taken into account. We found a scaling relationship between the rescaled optimal numbers and the dimensionless bristle length. This result agrees qualitatively with and provides an upper bound for the bristled wing morphological data analysed in this study.

A Year at the Forefront of Gliding Locomotion.

This review highlights the largely understudied behavior of gliding locomotion, which is exhibited by a diverse range of animals spanning vertebrates and invertebrates, in air and in water. The insights in the literature gained from January 2022 to December 2022 continue to challenge the previously held notion of gliding as a relatively simple form of locomotion. Using advances in field/lab data collection and computation, the highlighted studies cover gliding in animals including seabirds, flying lizards, flying snakes, geckos, dragonflies, damselflies, and dolphins. Altogether, these studies present gliding as a sophisticated behavior resulting from the interdependent aspects of morphology, sensing, environment, and likely selective pressures. This review uses these insights as inspiration to encourage researchers to revisit gliding locomotion, both in the animal's natural habitat and in the laboratory, and to investigate questions spanning gliding biomechanics, ecology, sensing, and the evolution of animal flight.

Incipient wing flapping enhances aerial performance of a robotic paravian model.

The functional origins of bird flight remain unresolved despite a diversity of hypothesized selective factors. Fossil taxa phylogenetically intermediate between typical theropod dinosaurs and modern birds exhibit dense aggregations of feathers on their forelimbs, and the evolving morphologies and kinematic activational patterns of these structures could have progressively enhanced aerodynamic force production over time. However, biomechanical functionality of flapping in such transitional structures is unknown. We evaluated a robot inspired by paravian morphology to model the effects of incremental increases in wing length, wingbeat frequency, and stroke amplitude on aerial performance. From a launch height of 2.8 m, wing elongation most strongly influenced distance travelled and time aloft for all frequency-amplitude combinations, although increased frequency and amplitude also enhanced performance. Furthermore, we found interaction effects among these three parameters such that when the wings were long, higher values of either wingbeat frequency or stroke amplitude synergistically improved performance. For launches from a height of 5.0 m, the effects of these flapping parameters appear to diminish such that only flapping at the highest frequency (5.7 Hz) and amplitude (60°) significantly increased performance. Our results suggest that a gliding animal at the physical scale relevant to bird flight origins, and with transitional wings, can improve aerodynamic performance via rudimentary wing flapping at relatively low frequencies and amplitudes. Such gains in horizontal translation and time aloft, as those found in this study, are likely to be advantageous for any taxon that engages in aerial behavior for purposes of transit or escape. This study thus demonstrates aerodynamic benefits of transition from a gliding stage to full-scale wing flapping in paravian taxa.