Jakub Prokop

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.

Traits and evolution of wing venation pattern in paraneopteran insects

Two different patterns of wing venation are currently supposed to be present in each of the three orders of Paraneoptera. This is unlikely compared with the situation in other insects where only one pattern exists per order. We propose for all Paraneoptera a new and unique interpretation of wing venation pattern, assuming that the convex cubitus anterior gets fused with the common stem of median and radial veins at or very near to wing base, after separation from concave cubitus posterior, and re‐emerges more distally from R + M stem. Thereafter, the vein between concave cubitus posterior and CuA is a specialized crossvein called “cua‐cup,” proximally concave and distally convex. We show that despite some variations, that is, cua‐cup can vary from absent to hypertrophic; CuA can re‐emerge together with M or not, or even completely disappear, this new interpretation explains all situations among all fossil and recent paraneopteran lineages. We propose that the characters “CuA fused in a common stem with R and M”and “presence of specialized crossvein cua‐cup” are venation apomorphies that support the monophyly of the Paraneoptera. In the light of these characters, we reinterpret several Palaeozoic and early Mesozoic fossils that were ascribed to Paraneoptera, and confirm the attribution of several to this superorder as well as possible attribution of Zygopsocidae (Zygopsocus permianus Tillyard, 1935) as oldest Psocodea. We discuss the situation in extinct Hypoperlida and Miomoptera, suggesting that both orders could well be polyphyletic, with taxa related to Archaeorthoptera, Paraneoptera, or even Holometabola. The Carboniferous Protoprosbolidae is resurrected and retransferred into the Paraneoptera. The genus Lithoscytina is restored. The miomopteran Eodelopterum priscum Schmidt, 1962 is newly revised and considered as a fern pinnule. In addition, the new paraneopteran Bruayaphis oudardi gen. nov. et sp. nov. is described fromthe Upper Carboniferous of France (see Supporting Information). J. Morphol., 2012.

The earliest holometabolous insect from the Carboniferous: a “crucial” innovation with delayed success (Insecta Protomeropina Protomeropidae)

Abstract Insects dominate Earth by their diversity, and the most are Holometabola. Therefore, the holometabolous development characterised by a pupal stage between larvae and adult seems to be linked with the extensive radiation of insects. Holometaboly is suspected to appear in the carboniferous period, however until now fossils have not brought univocal evidence. The discovery in the Carboniferous (Early Langsettian, circa 310 mya, Bashkirian Stage) of France of the earliest Holometabola attributed to the Permian amphiesmenopteran or antliophoran family Protomeropidae brings the first irrefutable evidence that holometaboly existed in the Carboniferous. Given the climatic data of France at this period, this discovery contradicts the traditional scenarii of a relation between the acquisition of endopterygote pupal stage and climatic global cooling during Late Carboniferous and Early Permian. This example illustrates the hypothesis that a new, apparently more efficient, biological innovation is not always sufficient to guarantee the ‘evolutionary success’ of the concerned clade. Ecological opportunities have to be considered as well for this innovation success.

New fossil insect order Permopsocida elucidates major radiation and evolution of suction feeding in hemimetabolous insects (Hexapoda: Acercaria)

With nearly 100,000 species, the Acercaria (lice, plant lices, thrips, bugs) including number of economically important species is one of the most successful insect lineages. However, its phylogeny and evolution of mouthparts among other issues remain debatable. Here new methods of preparation permitted the comprehensive anatomical description of insect inclusions from mid-Cretaceous Burmese amber in astonishing detail. These “missing links” fossils, attributed to a new order Permopsocida, provide crucial evidence for reconstructing the phylogenetic relationships in the Acercaria, supporting its monophyly, and questioning the position of Psocodea as sister group of holometabolans in the most recent phylogenomic study. Permopsocida resolves as sister group of Thripida + Hemiptera and represents an evolutionary link documenting the transition from chewing to piercing mouthparts in relation to suction feeding. Identification of gut contents as angiosperm pollen documents an ecological role of Permopsocida as early pollen feeders with relatively unspecialized mouthparts. This group existed for 185 million years, but has never been diverse and was superseded by new pollenivorous pollinators during the Cretaceous co-evolution of insects and flowers. The key innovation of suction feeding with piercing mouthparts is identified as main event that triggered the huge post-Carboniferous radiation of hemipterans, and facilitated the spreading of pathogenic vectors.

From Carboniferous to Recent: wing venation enlightens evolution of thysanopteran lineage

Recent Thysanoptera are characterized by two pairs of slender wings fringed by long hairs and with reduced venation. Fossils presenting more complete venation have been used in earlier studies to link Thysanoptera to ‘Zoropsocinae’, which form with ‘Lophioneurinae’ the ‘Lophioneuridae’, an extinct family of the superorder Thripida. On the basis of one new Carboniferous fossil described herein, Westphalothripides oudardi sp. nov. (Westphalothripidesidae fam. nov.), as well as new Cretaceous fossils, we revise the current interpretation of venation in Thripida and propose new cladistic analyses, which divide this superorder into three clades: Panthysanoptera nov. (including ‘Zoropsocidae’ stat. rest. and Thysanoptera), Lophioneurida (including ‘Lophioneurinae’ and Moundthripidae), and Westphalothripidesidae. We confirm that the Thysanoptera belong to the superorder Thripida but show that ‘Lophioneuridae’ are paraphyletic. Thanks to the venation observed in fossils, we describe a new character of the wing in some Recent species which allows them to be integrated in phylogenetic studies. Results show two clades inside Thysanoptera: Aeolothripidae + Melanthripidae + Merothripidae, and Thripidae + Stenurothripidae + Fauriellidae. Phlaeothripidae could not be studied due to the absence of the diagnostic wing veins in this family. We discuss the appearance of Thripida within Paraneoptera and particularly the importance of one apomorphy, the reduction of the right mandible as a putative adaptation to spore and pollen piercing.

Evolution of the elytral venation and structural adaptations in the oldest Palaeozoic beetles (Insecta: Coleoptera: Tshekardocoleidae)

The oldest definitive beetle, Coleopsis archaica gen. et sp. nov., is described from the earliest Permian (Asselian or early Sakmarian) of Germany (Grügelborn/Saarland). Its elytral venation is typical of the Early Permian Tshekardocoleidae. The elytral venation pattern of the type of Moravocoleus permianus Kukalová, 1969 is reconsidered in order to clarify structural peculiarities of the type genus of Moravocoleidae Kukalová-Peck & Beutel, 2011, herein regarded as a junior synonym of Tshekardocoleidae. The new discovery allows reinterpretation of the elytral venation, abdominal laterosternites, and other structures, making it possible to identify a ‘subelytral space’. Tshekardocoleoidea and Labradorocolidae are confirmed as Coleoptera, while Umenocoleidae sensu nov. and Umenocoleoidea are restored to Holometabola as a potential sister group of all Coleoptera. The holotype of Umenocoleus sinuatus Chen & T’an, 1973 needs to be revised in more detail. ‘Moravocoleus’ perditus Kukalová, 1969, regarded by Ponomarenko as a member of the genus Avocoleus, is excluded from Tshekardocoleidae and preliminarily considered as Archostemata incertae sedis. Oborocoleidae is considered as a taxon of more dubious position (order uncertain for Oborocoleus Kukalová, 1969, while Liberocoleus Kukalová, 1969 probably belongs to Archostemata (family uncertain)). Protocoleoptera and Paracoleoptera are considered as synonyms of Protelytroptera, while Archecoleoptera is dismissed as a paraphyletic group. Adiphlebia lacoana Scudder, 1885, previously proposed as the oldest beetle, is not a member of Coleoptera, as confirmed by Kukalová-Peck & Beutel (2012). The composition of beetle suborders and the origin of the order, which probably took place concurrently with the initial diversification of other holometabolan insects, are briefly discussed. http://zoobank.org/urn:lsid:zoobank.org:pub:2044EEFE-B88B-4552-B1F9-983E6F7A583D

Phylogeny and the fossil record of the Helophoridae reveal Jurassic origin of extant hydrophiloid lineages (Coleoptera: Polyphaga)

We performed a phylogenetic analysis focused on the hydrophiloid family Helophoridae (Coleoptera: Polyphaga) in order to test the phylogenetic position of selected Mesozoic fossils assigned to the Hydrophiloidea. The analysis is based on 92 characters of larvae and adults, and includes all extant subgenera of Helophorus and representatives of all other extant hydrophiloid families. Based on this analysis, we provide additional evidence for the monophyly of the helophorid lineage containing the families Helophoridae, Georissidae and Epimetopidae, as well as the first hypothesis on the phylogenetic relationships within Helophorus, revealing three main clades: Lihelophorus, Rhopalohelophorus and the clade of sculptured small subgenera; the subgenera Helophorus s.str., Gephelophorus, Trichohelophorus and Transithelophorus are recognized as paraphyletic or polyphyletic. Inclusion of fossil species in the analysis reveals the Mesozoic genera Hydrophilopsia Ponomarenko, Laetopsia Fikáček et al. (adult forms) and Cretotaenia Ponomarenko (larval form) as basal extinct clades of the helophorid lineage, the former genus Mesosperchus Ponomarenko as containing probable stem taxa of Helophorus and the former genus Mesohelophorus Ponomarenko as a member of the Helophorus clade containing extant sculptured subgenera. The extant subgenus Thaumhelophorussyn.nov. is synonymized with Rhopalohelophorus. Our results show that the family Helophoridae may be dated back to the late Jurassic (c. 150 Ma) and the extant clades of Helophorus back to the Early Cretaceous (c. 136 Ma). The basal groups of Helophorus and the supposed basal extinct lineages of the helophorid lineages are shown to be aquatic as adults. A single origin of trichobothria and ventral hydrophobic pubescence in the common ancestor of the Hydrophiloidea is hypothesized, indicating ancestral aquatic habits in the adult stage for the whole Hydrophiloidea.

New early griffenfly, Sinomeganeura huangheensis from the Late Carboniferous of northern China (Meganisoptera: Meganeuridae)

New griffenfly Sinomeganeura huangheensis gen. n., sp. n. (Meganeuridae) is described from Upper Carboniferous (Namurian) of the Tupo Formation in northern China (Ningxia Hui Autonomous Region). This taxon exhibits unique structure of the wing venation pattern. It is highly interesting in reference to the Namurian age known for the occurrence of two meganeurids until present (Namurotypus Brauckmann & Zessin, 1989 and Shenzhousia Zhang & Hong, 2006) as well as the palaeogeographical position of the locality far from all sites in Laurussia. We demonstrate that meganeurids with relatively small wings already co-existed with large species in the Namurian, as for the Stephanian and the Late Permian. Thus, Sinomeganeura demonstrates that the meganeurid diversity and wing venation disparity were comparable during the Namurian and the Stephanian, suggesting that this group already had a long history in the Early Carboniferous. Odonatoptera were probably the main, if not unique predators of the flying insects during the Late Paleozoic.

Insect Wings: The Evolutionary Development of Nature’s First Flyers

Powered flight is one of the more spectacular evolutionary novelties to have come about during the 4-billion-year history of life on Earth. Flight bestows upon the flyer another dimension in which to experience life. Suddenly, new avenues are available for dispersal, escape and avoidance, locating a suitable mate, and reaching once unobtainable resources. Moreover, wings can be so much more than merely a means to fly. Properly adapted the wings themselves may play a role in courtship, camouflage and mimicry, thermoregulation, and protection and defence. Despite the profound significance of flight, it is a challenging feat to achieve and control. Powered flight has evolved independently at least four times, three of which occur among the Amniota, while the last is far flung across the branches of the animal tree of life. It is this last lineage that was also the first to evolve this singularly successful means of locomotion, rivalling in numbers of species all other forms of life combined.

Late Palaeozoic Paoliida is the sister group of Dictyoptera (Insecta: Neoptera)

Paoliida is an insect group of highly controversial composition and equally controversial affinities. Based on comprehensive reinvestigations we propose a new delimitation of the insect order Paoliida sensu nov. associating the families Paoliidae and Blattinopsidae on the basis of the following main wing venation characters: veins CuA convex and CuP concave separating from a rather long basal stem Cu; a short, more or less distinct, but generally convex arculus brace (crossvein) between M and CuA (more distinct in forewing than in hind wing), and a broad area containing veinlets, between CuP and CuA, with a general course of CuA making a double curve (autapomorphy); CuP straight or sigmoidal. The Paoliida is considered as a neopteran clade and potential sister group of the Dictyoptera on the basis of the presence of well-defined anterior branches of CuA, with the same convexity as the median vein and more concave than the posterior branches of the same vein (synapomorphy). The polarities of the other characters shared by these clades are discussed. New diagnoses of the order Paoliida and the family Paoliidae are provided after re-examination of the type material. We attribute Herbstiala herbsti to Paoliidae and consider Herbstialidae as a junior synonym of this family. The grylloblattid family Ideliidae is considered as a junior synonym of Paoliidae, transferring genera Stenaropodites, Aenigmidelia, Archidelia, Sojanidelia, Micaidelia, Acropermula and Mongoloidelia to this family. Kochopteron hoffmannorum and Protoblattina bouvieri are newly included in Paoliidae. Protoblattinopsis stubblefieldi is reinterpreted as a hind wing having highly specialized cubito-anal structures functionally analogous to the anal loop structure of the hind wing of the Mesozoic Isophlebioidea (Odonatoptera). We attribute Protoblattinopsis to Paoliida and consider Protoblattinidae as a junior synonym of Paoliidae. Furthermore, a new Paoliidae, Silesiapteron jarmilae gen. et sp. nov. is described from Upper Carboniferous sphaerosiderite concretion of Poland. http://zoobank.org/urn:lsid:zoobank.org:pub:296A17BD-2A84-4C1F-B19E-737DDFE7E17C