origin of insect wings
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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.
- Klíčová slova
- Carboniferous, Insecta, Late Paleozoic, Palaeodictyoptera, Pterygota, origin of insect wings, wing pad articulation, wing pad postembryonic development, wing pad tracheation,
- MeSH
- biologická evoluce * MeSH
- hmyz anatomie a histologie růst a vývoj MeSH
- křídla zvířecí anatomie a histologie MeSH
- nymfa anatomie a histologie MeSH
- zkameněliny * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
The Late Paleozoic acquisition of wings in insects represents one of the key steps in arthropod evolution. While the origin of wings has been a contentious matter for nearly two centuries, recent evolutionary developmental studies suggest either the participation of both tergal and pleural tissues in the formation of wings1 or wings originated from exites of the most proximal leg podite incorporated into the insect body wall.2 The so-called "dual hypothesis" for wing origins finds support from studies of embryology, evo-devo, and genomics, although the degree of the presumed contribution from tergal and pleural tissues differ.3-6 Ohde et al.,7 confirmed a major role for tergal tissue in the formation of the cricket wing and suggested that "wings evolved from the pre-existing lateral terga of a wingless insect ancestor." Additional work has focused on identifying partial serially homologous structures of wings on the prothorax8,9 and abdominal segments.10 Thus, several studies have suggested that the prothoracic horns in scarab beetles,9 gin traps of tenebrionid and scarab beetle pupae,11,12 or abdominal tracheal gills of mayfly larvae1,13 evolved from serial homologues of wings. Here, we present critical information from abdominal lateral outgrowths (flaps) of Paleozoic palaeodictyopteran larvae, which show comparable structure to thoracic wings, consisting of cordate lateral outgrowths antero-basally hinged by muscle attachments. These flaps therefore most likely represent wing serial homologues. The presence of these paired outgrowths on abdominal segments I-IX in early diverging Pterygota likely corresponds to crustacean epipods14,15 and resembles a hypothesized ancestral body plan of a "protopterygote" model.
- Klíčová slova
- Insecta, Palaeodictyoptera, Palaeodictyopterida, Protopterygote model, Pterygota, evolutionary origin, larva, respiratory organs, tracheal gills, wing serial homology,
- MeSH
- biologická evoluce MeSH
- brouci * MeSH
- Ephemeroptera * MeSH
- hmyz MeSH
- křídla zvířecí MeSH
- larva MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Metamorphosis endowed the insects with properties that enabled them to conquer the Earth. It is a hormonally controlled morphogenetic process that transforms the larva into the adult. Metamorphosis appeared with the origin of wings and flight. The sesquiterpenoid juvenile hormone (JH) suppresses wing morphogenesis and ensures that metamorphosis takes place at the right ontogenetic time. This review explores the origin of insect metamorphosis and the ancestral function of JH. Fossil record shows that the first Paleozoic winged insects had (hemimetabolous) metamorphosis, and their larvae were likely aquatic. In the primitive wingless silverfish that lacks metamorphosis, JH is essential for late embryogenesis and reproduction. JH production after the embryo dorsal closure promotes hatching and terminal tissue maturation.
- MeSH
- biologická evoluce * MeSH
- biologická proměna MeSH
- hmyz * růst a vývoj fyziologie MeSH
- juvenilní hormony MeSH
- larva růst a vývoj fyziologie MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
- Názvy látek
- juvenilní hormony MeSH
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.
- MeSH
- biologická evoluce * MeSH
- fylogeneze MeSH
- hmyz genetika MeSH
- křídla zvířecí * anatomie a histologie MeSH
- larva genetika MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Insects are the only arthropod group to achieve powered flight, which facilitated their explosive radiation on land. It remains a significant challenge to understand the evolutionary transition from nonflying (apterygote) to flying (pterygote) insects due to the large gap in the fossil record. Under such a situation, ontogenic information has historically been used to compensate for fossil evidence. Recent evo-devo studies support and refine a paleontology-based classical hypothesis that an ancestral exite incorporated into the body wall contributed to the origin of insect wings. The modern hypothesis locates an ancestral precoxa leg segment with an exite within the hexapod lateral tergum, reframing the long-standing debate on the insect wing origin. A current focus is on the contributions of the incorporated exite homolog and surrounding tissues, such as the pleuron and the medial bona fide tergum, to wing evolution. In parallel, recent analyses of Paleozoic fossils have confirmed thoracic and abdominal lateral body outgrowths as transitional wing precursors and suggested their possible role as respiratory organs in aquatic or semiaquatic environments. These recent studies have revised our understanding of the transition to flying insects. This review highlights recent progress in both evo-devo and paleontology, and discusses future challenges, including the evolution of metamorphic development.
The numerous fossil specimens described as consecutive series of different larval stages of two species, Tchirkovaea guttata and Paimbia fenestrata (Palaeodictyoptera: Tchirkovaeidae), were reinvestigated with emphasis on comparing the development and growth of their wings with that of the wings of a recent mayfly, Cloeon dipterum. This unique fossil material was for a long time considered as undisputed evidence for an unusual type of wing development in Palaeozoic insects. The original idea was that the larvae of Palaeodictyopterida had wings, which were articulated and fully movable in their early stages of postembryonic development and that these gradually enlarging wings changed their position from longitudinal to perpendicular to the body axis. Moreover, the development of wings was supposed to include two or more subimaginal instars, implying that the fully winged instars moulted several times during their postembryonic development. The results of the present study revealed that there is no evidence that this series of nymphal, subimaginal and imaginal wings provide support for the original idea of wing development in Palaeozoic insects. On the contrary, our results indicate, that the supposed palaeodictyopteran larval wings are in fact wing pads with a wing developing inside the cuticular sheath as in recent hemimetabolous insects. Moreover, this study newly reinterpreted the wing pad base of Parathesoneura carpenteri and confirmed the presence of nygma like structures on wings and wing pads of palaeodictyopteran Tchirkovaeidae.
- Klíčová slova
- Ephemeroptera, Insecta, Palaeodictyopterida, Palaeoptera, Postembryonic development, Wing tracheae and lacunae,
- MeSH
- Ephemeroptera * MeSH
- hmyz MeSH
- křídla zvířecí * MeSH
- nymfa MeSH
- zkameněliny MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
While Mesozoic, Paleogene, and Neogene insect faunas greatly resemble the modern one, the Paleozoic fauna provides unique insights into key innovations in insect evolution, such as the origin of wings and modifications of postembryonic development including holometaboly. Deep-divergence estimates suggest that the majority of contemporary insect orders originated in the Late Paleozoic, but these estimates reflect divergences between stem groups of each lineage rather than the later appearance of the crown groups. The fossil record shows the initial radiations of the extant hyperdiverse clades during the Early Permian, as well as the specialized fauna present before the End Permian mass extinction. This review summarizes the recent discoveries related to the documented diversity of Paleozoic hexapods, as well as current knowledge about what has actually been verified from fossil evidence as it relates to postembryonic development and the morphology of different body parts.
- Klíčová slova
- Hexapoda, Insecta, deep divergences, evolution, functional morphology, metamorphosis,
- MeSH
- biologická evoluce * MeSH
- extinkce biologická MeSH
- fylogeneze MeSH
- hmyz * anatomie a histologie MeSH
- křídla zvířecí anatomie a histologie MeSH
- zkameněliny MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
Plastoceridae Crowson, 1972, Drilidae Blanchard, 1845 and Omalisidae Lacordaire, 1857 (Elateroidea) are families of the Coleoptera with obscure phylogenetic relationships and modified morphology showing neotenic traits such as soft bodies, reduced wing cases and larviform females. We shotgun sequenced genomes of Plastocerus, Drilus and Omalisus and incorporated them into data matrices of 66 and 4202 single-copy nuclear genes representing Elateroidea. Phylogenetic analyses indicate their terminal positions within the broadly defined well-sclerotized and fully metamorphosed Elateridae and thus Omalisidae should now be considered as Omalisinae stat. nov. in Elateridae Leach, 1815. The results support multiple independent origins of incomplete metamorphosis in Elateridae and indicate the parallel evolution of morphological and ecological traits. Unlike other neotenic elateroids derived from the supposedly pre-adapted aposematically coloured and unpalatable soft-bodied elateroids, such as fireflies (Lampyridae) and net-winged beetles (Lycidae), omalisids and drilids evolved from well-sclerotized click beetles. These findings suggest sudden morphological shifts through incomplete metamorphosis, with important implications for macroevolution, including reduced speciation rate and high extinction risk in unstable habitats. Precise phylogenetic placement is necessary for studies of the molecular mechanisms of ontogenetic shifts leading to profoundly changed morphology.
- MeSH
- anotace sekvence MeSH
- brouci klasifikace genetika MeSH
- fylogeneze MeSH
- genom hmyzu * MeSH
- hmyzí proteiny genetika MeSH
- křídla zvířecí anatomie a histologie metabolismus MeSH
- regulace genové exprese * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- hmyzí proteiny MeSH
Twisted winged insects (Strepsiptera) are a highly specialized small order of parasitic insects. Whether parasitism developed at an early or late stage in the evolution of the group was unknown. Here we record and describe the first definite Mesozoic strepsipteran primary larva embedded in Burmese amber (∼99 million years ago). This extends the origin of parasitism back by at least ∼50 million years, and reveals that this specialized life style has evolved in the Mesozoic or even earlier in the group. The extremely small first instar displays all diagnostic characters of strepsipteran immatures of this stage and is nearly identical with those of Mengenillidae, one of the most "ancestral" extant strepsipteran taxa. This demonstrates a remarkable evolutionary stasis over 100 million years. The new finding strongly weakens the case of small larvae embedded in Cretaceous amber interpreted as strepsipteran immatures. They differ in many structural features from extant strepsipteran primary larvae and are very likely parasitic beetle larvae.
- Klíčová slova
- Burmite, Cretaceous, Evolutionary stasis, Larva, Strepsiptera,
- Publikační typ
- časopisecké články MeSH
Deformed wing virus (DWV) transmitted by the parasitic mite Varroa destructor is one of the most significant factors contributing to massive losses of managed colonies of western honey bee (Apis mellifera) subspecies of European origin reported worldwide in recent decades. Despite this fact, no antiviral treatment against honey bee viruses is currently available for practical applications and the level of viral infection can only be controlled indirectly by reducing the number of Varroa mites in honey bee colonies. In this study, we investigated the antiviral potential of the gypsy mushroom (Cortinarius caperatus) to reduce DWV infection in honey bees. Our results indicate that the alcohol extract of C. caperatus prevented the development of DWV infection in cage experiments as well as after direct application to honey bee colonies in a field experiment. The applied doses did not shorten the lifespan of honey bees. The reduced levels of DWV in C. caperatus-treated honey bees in cage experiments were accompanied by significant changes in the gene expression of Tep7, Bap1, and Vago. The C. caperatus treatment was not effective against the trypanosomatid Lotmaria passim. No residues of C.caperatus were found in honey harvested in the spring from colonies supplemented with the mushroom extract for their winter feeding. These findings suggest that C. caperatus alcohol extract could be a potential natural remedy to treat DWV infection in honey bees.
- Klíčová slova
- Antiviral treatment, Apis mellifera carnica, Cortinarius caperatus, Deformed wing virus, Honey bees,
- MeSH
- Agaricales * MeSH
- Cortinarius MeSH
- lidé MeSH
- RNA-viry * genetika MeSH
- Romové * MeSH
- Varroidae * MeSH
- včely MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH