Figure - available from: Royal Society Open Science
This content is subject to copyright.
Abdominal tracheal gills in fossil and recent larvae of Ephemeroptera and retention of gills by their subimagoes and imagoes of Plecoptera. (a–d) Photographs of abdomen showing bifid tracheal gills and outlines of laterotergites. (a) Ephemeropsis trisetalis, Hexagenitidae, Ephemeroptera, PIN 3064-3332, Early Cretaceous, Baissa, Russia, larva with seven pairs of bifid abdominal tracheal gills. (b) Misthodotes sharovi, Mistodotidae, PIN 1700-374, Early Permian, Tshekarda, Russia, abdomen of nymph with discernable abdominal tracheal gills. (c,d) Coloburiscus humeralis, Coloburiscidae, Ephemeroptera, larva, TS coll., Cartenbury, New Zealand. (e) Palingenia longicaudata, Palingenidae, subimago, TS coll., Hungary. (f) Neuroperla schedingi, Eustheniidae, Plecoptera, NMP coll., IX. La Araucanía Region, Chile, imago, ventral aspect of abdomen with discernable tracheal gills. (g) Diamphipnoa annulata, Diamphipnoidae, Plecoptera, NMP coll., IX. La Araucanía Region, Chile, imago, ventral aspect of abdomen with discernable tracheal gills. tg, tracheal gills. Scale bars (a) 5 mm; (b–g) 1 mm.
Source publication
The Late Palaeozoic insect superorder Palaeodictyopterida exhibits a remarkable disparity of larval ecomorphotypes, enabling these animals to occupy diverse ecological niches. The widely accepted hypothesis presumed that their immature stages only occupied terrestrial habitats, although authors more than a century ago hypothesized they had speciali...
Similar publications
Broad‐scale patterns of resource utilization and the corresponding morphological evolution is a result of an integral relationship among form and function. In addition, there is also an inherent role of the latter in determining species co‐interaction and assemblage pattern that forms an integral aspect of ecological research. The present study aim...
Citations
... Cicada nymphs can live underground for up to 17 years 17,18 , with their life cycles producing significant effects on forest soils, microbial biomass, nutrient availability, predators, and host plants [21][22][23][24][25] . Immature and imaginal stages of individuals do not equally respond to the same evolutionary forces; therefore, different growth stages are of great significance in revealing different aspects of evolutionary mechanisms [26][27][28] . Consequently, nymphal fossils are necessary to illuminate the complete life cycles of ancient cicadas and their effects on terrestrial ecosystems, both below-and above ground. ...
Extant cicada (Hemiptera: Cicadoidea) includes widely distributed Cicadidae and relictual Tettigarctidae, with fossils ascribed to these two groups based on several distinct, minimally varying morphological differences that define their extant counterparts. However, directly assigning Mesozoic fossils to modern taxa may overlook the role of unique and transitional features provided by fossils in tracking their early evolutionary paths. Here, based on adult and nymphal fossils from mid-Cretaceous Kachin amber of Myanmar, we explore the phylogenetic relationships and morphological disparities of fossil and extant cicadoids. Our results suggest that Cicadidae and Tettigarctidae might have diverged at or by the Middle Jurassic, with morphological evolution possibly shaped by host plant changes. The discovery of tymbal structures and anatomical analysis of adult fossils indicate that mid-Cretaceous cicadas were silent as modern Tettigarctidae or could have produced faint tymbal-related sounds. The discovery of final-instar nymphal and exuviae cicadoid fossils with fossorial forelegs and piercing-sucking mouthparts indicates that they had most likely adopted a subterranean lifestyle by the mid-Cretaceous, occupying the ecological niche of underground feeding on root. Our study traces the morphological, behavioral, and ecological evolution of Cicadoidea from the Mesozoic, emphasizing their adaptive traits and interactions with their living environments.
... The superorder Palaeodictyopterida with specialized piercing and sucking mouthparts in the form of a rostrum is among the first recorded pterygotes and its phylogenetic placement as stem group of Neoptera is resolved 13,14,20 . Specializations for aquatic or semiaquatic lifestyles in larvae of Palaeodictyoptera have been studied for more than a century, but the interpretations differ greatly [21][22][23][24][25] . Caudal appendages of palaeodictyopteran larvae with a presumed respiratory function were recently reported in an early instar of Idoptilus sp. 26 , whereas in all others only cerci are documented 27,28 and exceptionally interpreted as long ovipositors 29 . ...
... nov. can be attributed to the order Palaeodictyoptera based on the form and structure of the wing pads as well as characteristic abdominal outgrowths, although the distinctive haustellate mouthparts are not preserved on any specimen (Prokop et al. 25 ). Palaeodictyopteran larvae are recognizable by large keel in the costal area on the forewings and markedly pleated venation with well-developed convex precursor of vein MA 27,32 . ...
... It remains questionable how widespread the aquatic lifestyle was within Palaeodictyoptera as the fossils of their larvae are extremely rare. Further support for an aquatic lifestyle is the retention of vestigial gill like structures in adults, which are also recorded in other lineages of Palaeodictyopterida, such as Megasecoptera 25 . Hence, it could represent the ancestral state within this clade. ...
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.
... While beaklike mouthparts are well known in hemipterans, these are usually not forward-projecting and are often less tightly connected to the head, providing them a certain movability (especially in heteropterans) and may only serve for a rather distant comparison. The rather short length of the beak and the more continuous connection to the head resembles the beak-like mouthparts of palaeodictyopteroideans (immatures and adults; Prokop et al., 2019). Unfortunately, we do not know a lot of the feeding habits of these Paleozoic, long extinct animals. ...
The group Neuropteriformia (beetles, lacewings, etc.) is today very species-rich, but also has a good fossil record in the Mesozoic. Amber provides not only adults, but also fossil larvae; some of these fossil neuropteriformian larvae have very unusual morphologies not seen in the modern fauna. We here report an unusual new fossil neuropteriformian larva. The mouthparts form a beak. Fossil larvae with similar mouthparts are known, and it seems that this new larva is a representative of the species ?Partisaniferus edjarzembowskii. The new larva, unlike the already known ones, has a large and inflated trunk. Based on comparison with extant larvae, such an inflated trunk should be considered physogastric. The new larva is only the second case of physogastry in fossil holometabolan larvae. Also early larvae of this species are known. The strong difference between the different larval stages give reason to interpret the ontogeny hypermetamorphic. Also this phenomenon is in fact very rare in the fossil record; most earlier candidates remain assumptions without further substantiation. Physogastry in larvae is often coupled to a mode of live in confined spaces, for a fossil preserved in amber this may mean living inside wood. Feeding mode might have been predatory, but could also have been feeding on fungi.
... The larvae of palaeodictyopterids are known only for Palaeodictyoptera and Megasecoptera. They show a remarkable morphological disparity reflecting various ecomorphological strategies, from the trilobite-like onisciform larvae of some Palaeodictyoptera to elongate forms with spined thoraces in Megasecoptera (116) (Figure 4l-p). While an exclusively aquatic lifestyle was suggested by early scholars, most authors during the twentieth century concluded that they were terrestrial due to a lack of distinctive aquatic specializations (22,177). ...
... These were modified caudal appendages made up of paired paraprocts and epiproct that are formed as tracheal gills in Zygoptera (123). Thus, the latest hypothesis is that some species were amphibious or aquatic in early instars, possibly transitioning to a semiaquatic mode in more mature larvae (much like in petalurid dragonflies) and even an amphibious lifestyle in some adults where rudimentary or even functional lateral abdominal tracheal gills were seemingly retained (116). However, it cannot be assumed that such biology was fixed across all orders given the extreme morphological variety, and it is likely that both terrestrial and aquatic lineages of Palaeodictyopterida coexisted. ...
... Several marked differences can be observed between the larvae of Palaeodictyoptera and those of Megasecoptera (Figure 4l-p). The costal area in the forewings of Palaeodictyoptera have a noticeably broad keel, usually as a continuation of the enlarged prothoracic winglets, while the larvae of Megasecoptera lack such an extension, and their wing pads are usually more expanded along the body axis (22,116). The prothorax of Palaeodictyoptera often has prominent prothoracic lobes (what some authors call winglets), while some species of Megasecoptera had long, laterally protruding spines, most likely serving a protective function. ...
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.
... Both exuviae and whole insects were found, generally in isolation, in fine claystone. Palaeodictyoptera were highly diverse during the Carboniferous where they made up one of the first hyper-diverse insect herbivore groups 66 , and seem to have progressively decreased in diversity throughout the Permian. Of the nymphs collected, one form strongly resembles the spilapterid Bizarrea obscura 67 from the Upper Carboniferous Mazon Creek Formation in North America. ...
... The abundance of Palaeodictoptera preserved in this lacustrine setting is particularly interesting, as the group was previously thought to be have been exclusively terrestrial. Only recently has an amphibious or aquatic lifestyle been considered for some Palaeodictoptera species 66,67 . A detailed examination of the exceptionally wellpreserved Onder Karoo nymphs will contribute key insights into the lifestyle and ecology of the group. ...
Continental ecosystems of the middle Permian Period (273–259 million years ago) are poorly understood. In South Africa, the vertebrate fossil record is well documented for this time interval, but the plants and insects are virtually unknown, and are rare globally. This scarcity of data has hampered studies of the evolution and diversification of life, and has precluded detailed reconstructions and analyses of ecosystems of this critical period in Earth’s history. Here we introduce a new locality in the southern Karoo Basin that is producing exceptionally well-preserved and abundant fossils of novel freshwater and terrestrial insects, arachnids, and plants. Within a robust regional geochronological, geological and biostratigraphic context, this Konservat- and Konzentrat-Lagerstätte offers a unique opportunity for the study and reconstruction of a southern Gondwanan deltaic ecosystem that thrived 266–268 million years ago, and will serve as a high-resolution ecological baseline towards a better understanding of Permian extinction events.
... This group is among the earliest Pterygota, with their oldest record from the early Late Carboniferous, approximately 325 million years ago, and with an astonishing diversity and morphological disparity of larvae and adults flourishing across Pangea until the Late Permian. 16,17 Palaeodictyoptera, with their close relatives Megasecoptera, Diaphanopterodea, and Dicliptera, shared a synapomorphy of a unique type of beak-like mouthparts supposedly for feeding on ferns and early gymnosperms, 18 and despite their successful diversification they vanished before or during the end Permian mass extinction. 19 The members of Palaeodictyoptera had wings permanently outstretched, and often developed wing-like lobes on the prothoracic segment in some species. ...
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, 4, 5, 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.
... Grimaldi and Engel 2005;Prokop et al., 2016). Yet, newer findings indicate possible aquatic immatures also in this lineage (Prokop et al., 2019). ...
... Many immatures of Palaedictyopteroidea possessed prominent lateral protrusions on the abdominal segments (Kukalová -Peck 1978;Garwood et al., 2012;Haug et al., 2016;Kiesmü ller et al., 2019;Prokop et al. 2016Prokop et al. , 2019). Yet, we largely lack a clear indication of these structures bearing/covering gills, or functioning in this way (Prokop et al., 2016) and in most cases, the protrusions appear to be simple lateral extensions of the tergites. ...
... Only one adult specimen preserves structures laterally on the abdomen that are reminiscent of gills (Prokop et al., 2019, their Figure 4;Figures 2D and 2G). This was interpreted as retention of larval features into the adult phase, as known in quite a number of extant species (Prokop et al., 2019, their Figure 5). Despite the uncertainty for the (few) fossil immatures of Palaeodictyopteroidea, we have at least an indirect indication of the presence of gills as lateral protrusions on the abdominal segments in such larvae ( Figure 3B). ...
Aquatic larvae are known in three early branches of Pterygota: Ephemeroptera (mayflies), Plecoptera (stoneflies), and Odonata (dragonflies, damselflies). A common origin of these larvae has been suggested, yet also counterarguments have been put forward, for example, the different position of larval gills: laterally on the abdomen in Ephemeroptera, terminally in Odonata, variably in Plecoptera. We discuss recent fossil findings and report a new dragonfly-type larva from Kachin amber (Myanmar), which possesses ancestral characters such as a terminal filum, maintained in ephemeropterans, but lost in modern odonatan larvae. The new larva possesses lateral protrusions on the abdominal segments where in other lineages gills occur. Together with other fossils, such as a plecopteran retaining lateral gills on the abdomen, this indicates that lateral protrusions on the abdomen might have well been an ancestral feature, removing one important argument against the idea of an aquatic larva in the ground pattern of Pterygota.
... While these fossils are often preserved as complete specimens they are usually not well preserved in terms of the less sclerotized body structures. Later, some material including nymphs of Mischopteridae and adults of Protohymenidae were described from siderite nodules from Mazon Creek Konservat-Lagerst€ atte (USA, Carboniferous, Moscovian), which were preserved in three dimensions (Carpenter and Richardson, 1968;Pecharov a and Prokop, 2018;Prokop et al., 2017Prokop et al., , 2019. A highly diverse fauna of megasecopterans was discovered at the Early Permian locality at Tshekarda in the Russian Federation (Martynov, 1940;. ...
... However, in the case of Corydaloides scudderi Brongniart, 1885a the lateral abdominal structures are distinctly bifid and emerge from between segments. These most presumably represent either rudimentary or functional tracheal gills (Brongniart, 1885b;Prokop et al., 2019). ...
Megasecoptera is a late Paleozoic order of herbivorous insects with rostrum-like mouthparts and slender homonomous outstretched wings. Our knowledge of their morphology is mainly based on wings while other body parts are scarcely documented. Here we focus on the families Bardohymenidae and Aspidothoracidae. A new well preserved specimen of Sylvohymen cf. sibiricus is described and illustrated, particularly the structures of the external male genitalia previously unknown for Bardohymenidae. Sylvohymen marginatus sp. nov. is described from the early Permian of Tshekarda based on unique traits in the wing venation. The genera Paleohymen and Taigahymen are both removed from Bardohymenidae and the latter is transferred to Vorkutiidae. Alexahymen aestatis (Brauckmann, 1991) comb. nov. from Pennsylvanian at Piesberg is transferred from Aspidothoracidae to Bardohymenidae. Piesbergbrodia gen. nov. is designated for Piesbergbrodia tristrata (Brauckmann and Herd, 2003) comb. nov. as a member of Brodiidae and the first known record of this family from Piesberg quarry. The placement of Sylvohymen peckae in the Bardohymenidae is considered doubtful due to lack of significant characters in its venation. Furthermore, our study is focused on the form of the apical cell and the pattern of wing pigmentation. Peculiarities of the integumental outgrowths and external genitalia of representatives of Aspidothoracidae and Bardohymenidae, and other close relatives, are highlighted.
... Fossils are preserved in sphero-sideritic concretions with 3D relief and include various groups of arthropods, molluscs, vertebrates and most commonly plant remains (Krawczyński et al. 2001, Stworzewicz et al. 2009, Pacyna and Zdebská 2010. The entomofauna consists predominantly of paoliids, palaeodictyopteran nymphs and their exuvia, followed by sparsely recorded other groups like Archaeognatha and Archaeorthoptera (Prokop et al. 2012(Prokop et al. , 2014(Prokop et al. , 2017(Prokop et al. , 2019. ...
Archaeorthoptera is a high rank insect taxon comprising Orthoptera as well as the extinct orders Titanoptera and Caloneurodea, and several other late Paleozoic groups formerly assigned to polyphyletic Protorthoptera. Synapomorphies defining Archaeorthoptera and some fossil subordinate taxa are exclusively based on wing venation. This study presents
a detailed description of two new archaeorthopteran genera and three new species from the Pennsylvanian of the Upper Silesian Coal Basin in Poland. These new taxa provide new insights into the wing venation disparity of this remarkable and insufficiently studied insect group. Omaliella polonica sp. nov. is based on a well preserved forewing, including
the wing base, which allows a thorough discussion and comparison with other archaeorthopterans. Surprisingly, it is the first complete wing for this group of related genera (Omaliella, Omalia, Coselia and Paleomastax). Owadpteron dareki gen. et sp. nov. has an unusual arrangement of cubital veins. The marked resemblance of the venation of Owadpteron to that of some members of the gerarid line, such as Nacekomia, supports its placement within the family Geraridae (stemgroup Orthoptera). Finally, the venation of Parapalaeomastax dariuszi gen. et sp. nov. strikingly resembles that of the genus Palaeomastax, differing only in the distally branched media. Discovery of these three new archaeorthopterans from the Upper Silesian Coal Basin fits well with that of closely related taxa known from other deposits in Euramerica, such as Mazon Creek Lagerstätte, Avion in Pas-de-Calais Basin and others. Furthermore, a new re-examination of the
earliest archaeorthopteran from the Upper Silesian Coal Basin confirms doubtful assignment of this fragmentary fossil to Archaeorthoptera or even to Pterygota.
The first winged insects evolved from a wingless ancestor, but details of the transition to a fully-winged morphology remain unclear. Studying extant pterygotes with partial wings, such as the stick insects (order Phasmatodea), may help us to understand such a transition. Here, we address how a series of flight-related morphological parameters may correlate with flight evolution by studying different phasmids representing a volancy continuum ranging from miniaturized to full-sized wings. Variation in phasmid wing shape, venation, wing mass and the mass of flight muscle can be described by specific scaling laws referenced to wing length and wing loading. Also, the mass distribution of the body-leg system is conserved in spite of a wide range of variation in body shape. With reduced wing size and increased wing loading, the longitudinal position of the wing-bearing thoracic segments is shifted closer to the insects’ centre of body mass. These results demonstrate complex reconfiguration of the flight system during wing morphological transitions in phasmids, with various anatomical features potentially correlated with reduced flight performance attained with partial wings. Although these data represent phasmid-specific features of the flight apparatus and body plan, the associated scaling relationships can provide insight into the functionality of intermediate conditions between wingless and fully-winged insects more generally.
