Romain Garrouste

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.

A complete insect from the Late Devonian period

After terrestrialization, the diversification of arthropods and vertebrates is thought to have occurred in two distinct phases, the first between the Silurian and the Frasnian stages (Late Devonian period) (425–385 million years (Myr) ago), and the second characterized by the emergence of numerous new major taxa, during the Late Carboniferous period (after 345 Myr ago). These two diversification periods bracket the depauperate vertebrate Romer’s gap (360–345 Myr ago) and arthropod gap (385–325 Myr ago), which could be due to preservational artefact. Although a recent molecular dating has given an age of 390 Myr for the Holometabola, the record of hexapods during the Early–Middle Devonian (411.5–391 Myr ago, Pragian to Givetian stages) is exceptionally sparse and based on fragmentary remains, which hinders the timing of this diversification. Indeed, although Devonian Archaeognatha are problematic, the Pragian of Scotland has given some Collembola and the incomplete insect Rhyniognatha, with its diagnostic dicondylic, metapterygotan mandibles. The oldest, definitively winged insects are from the Serpukhovian stage (latest Early Carboniferous period). Here we report the first complete Late Devonian insect, which was probably a terrestrial species. Its ‘orthopteroid’ mandibles are of an omnivorous type, clearly not modified for a solely carnivorous diet. This discovery narrows the 45-Myr gap in the fossil record of Hexapoda, and demonstrates further a first Devonian phase of diversification for the Hexapoda, as in vertebrates, and suggests that the Pterygota diversified before and during Romer’s gap.

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.

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

The first ant-termite syninclusion in amber with CT-scan analysis of taphonomy.

We describe here a co-occurrence (i.e. a syninclusion) of ants and termites in a piece of Mexican amber (Totolapa deposit, Chiapas), whose importance is two-fold. First, this finding suggests at least a middle Miocene antiquity for the modern, though poorly documented, relationship between Azteca ants and Nasutitermes termites. Second, the presence of a Neivamyrmex army ant documents an in situ raiding behaviour of the same age and within the same community, confirmed by the fact that the army ant is holding one of the termite worker between its mandibles and by the presence of a termite with bitten abdomen. In addition, we present how CT-scan imaging can be an efficient tool to describe the topology of resin flows within amber pieces, and to point out the different states of preservation of the embedded insects. This can help achieving a better understanding of taphonomical processes, and tests ethological and ecological hypotheses in such complex syninclusions.

Two new biting midges of the modern type from Santonian amber of France (Diptera: Ceratopogonidae)

The second Mesozoic representative of the (Dasyheleinae & Forcipomyiinae) clade of Ceratopogonidae, Devalquia brisaci gen. et sp. n., as well as the first Mesozoic Ceratopogoninae Heteromyiini Metahelea roggeroi sp. n., are the first arthropods described from the Santonian amber outcrop of Piolenc (Vaucluse, France). Both confirm the great morphological stability through time within the Ceratopogonidae. They also suggest that the other ceratopogonine clades were also present by at least the Upper Cretaceous.

Garrouste et al. reply

replying to T. Hörnschemeyer et al. Nature 494, 10.1038/nature11887 (2013)Since the nineteenth century, Devonian insects have repeatedly proven to be something else, the sole exception being Rhyniognatha. Recently the Devonian insect Strudiella devonica has been denied by Hörnschemeyer et al., who could not “confirm the presence of a mandible or of mandibular teeth”.

First semi-aquatic bugs Mesoveliidae and Hebridae (Hemiptera: Heteroptera: Gerromorpha) in Miocene Dominican amber

Two new semiaquatic bugs of the families Mesoveliidae and Gerridae are described from the Middle Miocene Dominican amber, Mesovelia dominicana sp.n. and Miohebrus anderseni gen.n., sp.n. The former is the first fossil record of the extant genus Mesovelia and the second described fossil of the family Mesoveliidae (the first mesoveliid fossil record was from undescribed fossils in French Cretaceous amber). The latter is the second described fossil Hebridae.

Exceptionally preserved insect fossils in the Late Jurassic lagoon of Orbagnoux (Rhône Valley, France)

The Late Kimmeridgian marine limestones of the area around Orbagnoux (Rhône, France) are well known for their fish fauna and terrestrial flora. Here we record the first insects and their activities (mines on leaves and trails in sediments) from these layers, including the oldest record of the gerromorphan bugs, as a new genus and species Gallomesovelia grioti, attributed to the most basal family Mesoveliidae and subfamily Madeoveliinae. These new fossils suggest the presence of a complex terrestrial palaeoecosystem on emerged lands near the lagoon where the limestones were deposited. The exquisite state of preservation of these fossils also suggests that these outcrops can potentially become an important Konservat-Lagerstätte for the Late Jurassic of Western Europe.

La première observation in natura de l’entomophagie de Panstrongylus geniculatus (Latreille 1811) hématophage vecteur de la maladie de Chagas (Hemiptera: Reduviidae)

Résumé Le comportement entomophage de Panstrongylus geniculatus (Latreille 1811), vecteur de la maladie de Chagas, est observé pour la première fois dans la nature, sur un Lépidoptère (Eacles sp., Lepidoptera: Saturniidae) au cours d’une chasse à la lumière dans une forêt de Guyane française.