Diversity, Form, and Postembryonic Development of Paleozoic Insects.

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.

The earliest known holometabolous insects.

The Eumetabola (Endopterygota (also known as Holometabola) plus Paraneoptera) have the highest number of species of any clade, and greatly contribute to animal species biodiversity. The palaeoecological circumstances that favoured their emergence and success remain an intriguing question. Recent molecular phylogenetic analyses have suggested a wide range of dates for the initial appearance of the Holometabola, from the Middle Devonian epoch (391 million years (Myr) ago) to the Late Pennsylvanian epoch (311 Myr ago), and Hemiptera (310 Myr ago). Palaeoenvironments greatly changed over these periods, with global cooling and increasing complexity of green forests. The Pennsylvanian-period crown-eumetabolan fossil record remains notably incomplete, particularly as several fossils have been erroneously considered to be stem Holometabola (Supplementary Information); the earliest definitive beetles are from the start of the Permian period. The emergence of the hymenopterids, sister group to other Holometabola, is dated between 350 and 309 Myr ago, incongruent with their current earliest record (Middle Triassic epoch). Here we describe five fossils--a Gzhelian-age stem coleopterid, a holometabolous larva of uncertain ordinal affinity, a stem hymenopterid, and early Hemiptera and Psocodea, all from the Moscovian age--and reveal a notable penecontemporaneous breadth of early eumetabolan insects. These discoveries are more congruent with current hypotheses of clade divergence. Eumetabola experienced episodes of diversification during the Bashkirian-Moscovian and the Kasimovian-Gzhelian ages. This cladogenetic activity is perhaps related to notable episodes of drying resulting from glaciations, leading to the eventual demise in Euramerica of coal-swamp ecosystems, evidenced by floral turnover during this interval. These ancient species were of very small size, living in the shadow of Palaeozoic-era 'giant' insects. Although these discoveries reveal unexpected Pennsylvanian eumetabolan diversity, the lineage radiated more successfully only after the mass extinctions at the end of the Permian period, giving rise to the familiar crown groups of their respective clades.

Redefining the extinct orders Miomoptera and Hypoperlida as stem acercarian insects.

BACKGROUND: The systematic positions of the extinct insect orders Hypoperlida, Miomoptera and Permopsocida were enigmatic and unstable for nearly a century. The recent studies based on new material, especially from the Cenomanian Burmese amber, shed light on evolutionary history of Acercaria resolving Permopsocida as the stem group of Condylognatha. However, the knowledge of the remaining two orders differs significantly. RESULTS: In this study, we describe new specimens and evaluate morphology of various structures with emphasis on the mouthparts and wing venation. Our results are primary based on revisions of the type specimens with a proper delimitation of taxa Hypoperlida and Miomoptera followed by their significance for the evolutionary history of Acercaria. Three new genera as Belmomantis gen. nov., Elmomantis gen. nov., and Mazonopsocus gen. nov. are designated as members of Palaeomanteidae. The Pennsylvanian Mazonopsocus provides a minimum age for calibration, in accordance to the presence of crown acercarians during the late Carboniferous. CONCLUSIONS: This contribution demonstrates that Hypoperlida and Miomoptera are stem groups of Acercaria. The putative clade (Hypoperlida + Miomoptera) is appearing as potential sister group of (Psocodea + (Permopsocida + (Thripida + Hemiptera))).

The structure of wing in the earliest Permopsocida.

Permopsocids are small acercarian insects with mouthparts specialized for sucking. They are closely related to Hemiptera and Thysanoptera. The earliest known representatives are from the Early Permian. Here evidence is presented that the Permopsocida occurred even earlier in Pennsylvanian (Moscovian) deposits in the Piesberg quarry near Osnabrück (Lower Saxony, Germany). This material is assigned to the Permian family Psocidiidae; Carbonopsocus mercuryi gen. et sp. nov., based on the wing venation diagnosed by the unique branching pattern of the main veins, the shape of the areola postica being longer than wide, the angular shape of the pterostigma, the ir crossvein directed proximally mid of pterostigma (apomorphy) and the vannus formed by the three veins of PCu, A1 and A2. The shape of the veins, with a Y-vein formed by the distal fusion of PCu with A1, could be a putative symplesiomorphy of the Psocodea with Permopsocida and Hemiptera. C. mercuryi gen. et sp. nov. is the first appearance date for Permopsocida and roots the Acercaria tree. In addition, another specimen of Dichentomum cf. arroyo (Psocidiidae) from Carrizo Arroyo is presented and figured, confirming the presence of the genus Dichentomum near the Carboniferous-Permian boundary and linking it to the Artinskian species from Elmo in Kansas, USA.

Fluctuation in the diversity of mayflies (Insecta, Ephemerida) as documented in the fossil record.

Due to their aquatic larvae, the evolution of mayflies is intricately tied to environmental changes affecting lakes and rivers. Despite a rich fossil record, little is known about the factors shaping the pattern of diversification of mayflies in deep time. We assemble an unprecedented dataset encompassing all fossil occurrences of mayflies and perform a Bayesian analysis to identify periods of increased origination or extinction. We provide strong evidence for a major extinction of mayflies in the mid-Cretaceous. This extinction and subsequent faunal turnover were probably connected with the rise of angiosperms. Their dominance caused increased nutrient input and changed the chemistry of the freshwater environments, a trend detrimental mainly to lacustrine insects. Mayflies underwent a habitat shift from hypotrophic lakes to running waters, where most of their diversity has been concentrated from the Late Cretaceous to the present.

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.

Abdominal serial homologues of wings in Paleozoic insects.

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.

The earliest beetle with mouthparts specialized for feeding on nectar is a parasitoid of mid-Cretaceous Hymenoptera.

BACKGROUND: During the Mesozoic, there were many insects in several holometabolous orders (Neuroptera, Mecoptera and Diptera) with elongated mouthparts adapted for feeding on nectar. The evolutionary history of the megadiverse order Coleptera, which has a great diversity of mouthparts and feeding strategies, is well documented since early Permian with a significant peak in diversity in the Triassic. Currently, however, there is no evidence that in the Mesozoic these beetles fed on nectar despite the recorded specializations for pollination of flowering plants in several families since the mid-Cretaceous. RESULTS: Here we describe a new wedge-shaped beetle Melanosiagon serraticornis gen. et sp. nov. from mid-Cretaceous Burmese amber attributed to Macrosiagonini (Ripiphoridae: Ripiphorinae), which has elongated galea comparable to that in the extant parasitoid genus Macrosiagon, and a well known example of adaptation for nectar feeding in Coleoptera. Furthermore, Salignacicola gen. nov. is established for Macrosiagon ebboi Perrichot, Nel et Néraudeau, 2004, based on the holotype found in mid-Cretaceous amber from France. Systematic positions of both newly established genera are discussed. A list of potential wasp and bee hosts of Ripiphorinae from the Mesozoic is provided. CONCLUSIONS: This study presents evidence of the earliest occurrence of specialized nectar feeding mouthparts in Coleoptera. Melanosiagon serraticornis is closely related to extant Macrosiagonini. In all genera belonging to subfamily Ripiphorinae the primary larvae are adapted for parasitism on aculeate Hymenoptera (bees and wasps) and adults are associated with blossoms of flowering plants, in terms of their specialized morphology. Adults of Macrosiagon visit blossoms of flowering plants to obtain nectar and lay eggs from which the hatching larvae attack visiting wasps and bees. An association with flowers of some tropical trees is already corroborated in some extant species. Interestingly the larvae of Ripiphorinae are also found in Burmese amber. Thus, both life stages of the mid-Cretaceous Ripiphorinae indicate a close association of this lineage with flowering trees.

Evidence for wing development in the Late Palaeozoic Palaeodictyoptera revisited.

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.

The complete life cycle of a Cretaceous beetle parasitoid.

Life cycles of parasites, particularly those with complex life histories and developmental pathways, are rarely preserved as fossils in total.1 The evidence is almost universally biased toward incomplete perspectives derived from a single sex or life stage.2,3 Here, we report a piece of Cretaceous Burmese amber that contains 28 males, a larviform female, and two longipede larvae of the wedge-shaped beetle Paleoripiphorus, and its potential cockroach host. Collectively, this fossil represents the complete series of free-living stages (except of the last larval instar) for a 99-million-year-old parasitoid insect from Myanmar (Figure 1 and Supplemental Information). The wedge-shaped beetles (Ripiphoridae) are of special interest among parasitoids because of their obligatory, protelean development in larvae of cockroaches, beetles, bees and wasps.4.

Life history, systematics and flight ability of the Early Permian stem-mayflies in the genus Misthodotes Sellards, 1909 (Insecta, Ephemerida, Permoplectoptera).

BACKGROUND: The stem-group of Ephemeroptera is phylogenetically important for understanding key steps in evolutionary history of early pterygote insects. However, these taxa have been mostly studied from the taxonomy point of view focused on the pattern of wing venation and often using only classical optical microscopy devices. In-depth studies on detailed morphology of the different body structures are scarcely performed, although the results are critical for elucidation of life history traits and their evolutionary pattern among the basal pterygotes. RESULTS: New information is presented on the morphology of two species of Misthodotes, which are stem-mayflies from the Early Permian. Based on new results obtained from a re-examination of the type specimens and supplementary material, we infer the life history traits of both the adult and larval stages of these Palaeozoic insects and reconsider previous interpretations. For the first time, we report the structure of the thoracic pleura and the articulation at the base of the wing in a stem-group of Ephemeroptera and compare them with those of extant mayflies. We also provide additional support for the systematic placement of investigated taxa and an amended diagnosis of the genus Misthodotes. CONCLUSIONS: Adult Misthodotes sharovi and Misthodotes zalesskyi had chewing mouthparts, which enabled them to scavenge or feed on plants. The wing apparatus was adapted for slow powered flapping flight and gliding, using long caudal filaments for steering. The wing base does not have rows of articulary sclerites as previously hypothesized for some Palaeozoic taxa but inflexible axilla similar to that found in modern mayflies. The structure of the thoracic pleura is also similar to that in the crown group of Ephemeroptera, while differences in the course of sutures may be explained by an evolutionary trend towards more powerful dorsoventral flying musculature and forewing-based flight (anteromotorism) in modern taxa. There is no evidence for swarming behaviour and mating in the air as occurs in modern mayflies as they had none of the associated morphological adaptations. Putative larvae of Misthodotes can not be unambiguously associated with the adults. They also exhibit some morphological specializations of Protereismatidae like 9 pairs of abdominal tracheal gills supporting their benthic lifestyle with legs adapted to burrowing.

Female calling, life cycle, and microstructures of the parasitic beetle Ripidius quadriceps Abeille de Perrin.

The precopulatory behaviour of the larviform females of Ripidius quadriceps Abeille de Perrin, 1872 is described. The calling posture of virgin females is documented. The cephalic morphology and microstructures are visualised using scanning electron microscopy, in particular the secretory pores in the cuticle of inflatable maxillary palps. An exhaustive overview of relevant publications revealed that the location of secretory pores on the head of females is unique within the order Coleoptera. Compared to other beetles with sedentary calling females, the calling phase of the short-lived and non-feeding female of Ripidius is exceptionally short. For bioassays, various traps using virgin females of Ripidius were tested. It is likely that the sedentary behaviour of the short-lived female combined with a unique morphology and priority for investing in reproduction is compensated for by the actively flying males with remarkably flabellate antennae. The life cycle of this species, including some of the exceptions recorded at the individual level, is discussed. Perspectives for a biological and morphological survey of this rarely collected western Palaearctic species are outlined. In addition, the calling behaviour, secretory sites and location of pheromone glands in females of Coleoptera producing long range pheromones is reviewed.

On the morphology of the Late Paleozoic insect families Bardohymenidae and Aspidothoracidae (Palaeodictyopterida: Megasecoptera).

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 marginatussp. 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. Piesbergbrodiagen. 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.

Male postabdomen reveals ancestral traits of Megasecoptera among winged insects.

External male genitalia of insects are greatly diverse in form and frequently used in evolutionary context and taxonomy. Therefore, our proper recognition of homologous structures among various groups from Paleozoic and extant insect taxa is of crucial interest, allowing to understand the key steps in insect evolution. Here, we reveal structural details of two Late Carboniferous representatives of Megasecoptera (families Bardohymenidae and Brodiopteridae), such as the presence of separated coxal plates VIII and ventral expansions of coxal lobes IX. Together with the confirmed presence of abdominal styli in some other members of Palaeodictyopterida (Diaphanopterodea) this suggests that early pterygotes may have had traits more archaic than expected. Whether or not these traits point to a stem-group relationship of Palaeodictyopterida to all other Pterygota as suspected by earlier authors remains unclear at this stage. Furthermore, the present study provides an updated comparison of male postabdomen morphology among extant species of wingless Archaeognatha and representatives of early diverging groups of Pterygota from the Late Carboniferous and Early Permian, the Megasecoptera (Palaeodictyopterida), Permoplectoptera (Ephemeroptera) and Meganisoptera (Odonatoptera).

Palaeodictyopterida.

Jakub Prokop and Michael Engel introduce palaeodictyopterids, a very diverse extinct lineage of insects.

New dustywings (Neuroptera, Coniopterygidae) from mid-Cretaceous amber of Myanmar reveal spectacular diversity.

Two new genera and species of Coniopterygidae (Neuroptera) are described and illustrated from mid Cretaceous (Cenomanian) amber of Myanmar. Mulleroconishyalina gen. n. et sp. n., attributed to the Coniopteryginae, bears a unique combination of venation characters and an abdomen without plicatures. The second new genus, attributed to the Aleuropteryginae, i.e. Palaeoconisazari gen. n. et sp. n., displays a unique pattern of crossveins 1m-cua and 2mp2-cua, with the latter crossing the pigmented spot. A check-list of all fossil genera and species of Coniopterygidae is provided.

†Bittacopsocus-a new bizarre genus of †Permopsocida (Insecta) from Burmese Cretaceous amber.

A new insect species (†Bittacopsocus megacephalus Beutel, Prokop, Müller et Pohl gen. et sp. nov.) is described, based on a single small male (ca. 2.5 mm) embedded in mid Cretaceous Burmese amber. The species shows some resemblance with the mecopteran family Bittacidae, mainly due to strongly elongated and thin legs. However, the structural affinities are apparently due to convergency. Different features, but especially the mouthparts and the pattern of wing venation, indicate that the species belongs to the extinct order †Permopsocida (?Archipsyllidae). However, it differs markedly from all species previously described in this extinct group. The very thin and strongly elongated legs are probably autapomorphic. A very unusual feature is the antenna with only seven segments and extremely elongated flagellomeres. The two pairs of wings are unusually narrow. M and CuA are basally fused. Proximal rows of spines, two series of closed cells, and a distinctly increased number of terminal branches of M are present in the forewings, in contrast to other archipsyllid genera. It is conceivable that Bittacopsocus megacephalus used its long legs to rest suspended in the vegetation like Bittacus. The head structures tentatively suggest predatory behavior but the feeding habits are unclarified yet.

Ecomorphological diversification of the Late Palaeozoic Palaeodictyopterida reveals different larval strategies and amphibious lifestyle in adults.

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 specializations for amphibious or even aquatic life histories. Here, we show that different species had a disparity of semiaquatic or aquatic specializations in larvae and even the supposed retention of abdominal tracheal gills by some adults. While a majority of mature larvae in Palaeodictyoptera lack unambiguous lateral tracheal gills, some recently discovered early instars had terminal appendages with prominent lateral lamellae like in living damselflies, allowing support in locomotion along with respiratory function. These results demonstrate that some species of Palaeodictyopterida had aquatic or semiaquatic larvae during at least a brief period of their post-embryonic development. The retention of functional gills or gill sockets by adults indicates their amphibious lifestyle and habitats tightly connected with a water environment as is analogously known for some modern Ephemeroptera or Plecoptera. Our study refutes an entirely terrestrial lifestyle for all representatives of the early diverging pterygote group of Palaeodictyopterida, a greatly varied and diverse lineage which probably encompassed many different biologies and life histories.

The morphology of mouthparts, wings and genitalia of Paleozoic insect families Protohymenidae and Scytohymenidae reveals new details and supposed function.

Megasecoptera is an extinct group of insects with specialized rostrum-like mouthparts, which is a synapomorphy shared with all members of the Late Paleozoic Palaeodictyopterida, and markedly slender wings that are unable to flex backwards. Here we describe the close up morphology of Protohymenidae and Scytohymenidae and uncover new aspects of the endoskeleton (tentorium) of the head, structure of the mouthparts with discernible proximal part of stylets controlled by muscles, surface of compound eyes that consist of a hexagonal pattern of large facets, structure and microstructures on the wings and reconstruct male and female external genitalia using ESEM and light stereomicroscopy. Furthermore, we describe Protohymen novokshonovi sp. n. based on an exceptionally well preserved fossil from the early Permian at Tshekarda in Russia, which shows crucial details, and the earliest species of Protohymenidae, Carbohymen testai gen. et sp. n. from a late Carboniferous siderite nodule at Mazon Creek in Illinois, USA. Our comparative study confirmed a set of structural and microstructural details on their wings, such as the composite anterior wing margin, development of an apical cell and the previously unknown external genitalia. Based on the results and comparison of homologous structures known primarily for extant relatives, such as mayflies and dragonflies, we outline for the first time the function of the mouthparts, in particular, the stylets, structure of the tentorium, vision provided by large hexagonal ommatidia and male copulatory structures bearing curved claspers for holding a female during copulation and penial lobes with seminal grooves.