The order Coleoptera (beetles) is arguably the most speciose group of animals, but the evolutionary history of beetles, including the impacts of plant feeding (herbivory) on beetle diversification, remain poorly understood. We inferred the phylogeny of beetles using 4,818 genes for 146 species, estimated timing and rates of beetle diversification using 89 genes for 521 species representing all major lineages and traced the evolution of beetle genes enabling symbiont-independent digestion of lignocellulose using 154 genomes or transcriptomes. Phylogenomic analyses of these uniquely comprehensive datasets resolved previously controversial beetle relationships, dated the origin of Coleoptera to the Carboniferous, and supported the codiversification of beetles and angiosperms. Moreover, plant cell wall-degrading enzymes (PCWDEs) obtained from bacteria and fungi via horizontal gene transfers may have been key to the Mesozoic diversification of herbivorous beetles—remarkably, both major independent origins of specialized herbivory in beetles coincide with the first appearances of an arsenal of PCWDEs encoded in their genomes. Furthermore, corresponding (Jurassic) diversification rate increases suggest that these novel genes triggered adaptive radiations that resulted in nearly half of all living beetle species. We propose that PCWDEs enabled efficient digestion of plant tissues, including lignocellulose in cell walls, facilitating the evolution of uniquely specialized plant-feeding habits, such as leaf mining and stem and wood boring. Beetle diversity thus appears to have resulted from multiple factors, including low extinction rates over a long evolutionary history, codiversification with angiosperms, and adaptive radiations of specialized herbivorous beetles following convergent horizontal transfers of microbial genes encoding PCWDEs.

Polyneoptera represents one of the major lineages of winged insects, comprising around 40,000 extant species in 10 traditional orders, including grasshoppers, roaches, and stoneflies. Many important aspects of polyneopteran evolution, such as their phylogenetic relationships, changes in their external appearance, their habitat preferences, and social behavior, are unresolved and are a major enigma in entomology. These ambiguities also have direct consequences for our understanding of the evolution of winged insects in general; for example, with respect to the ancestral habitats of adults and juveniles. We addressed these issues with a large-scale phylogenomic analysis and used the reconstructed phylogenetic relationships to trace the evolution of 112 characters associated with the external appearance and the lifestyle of winged insects. Our inferences suggest that the last common ancestors of Polyneoptera and of the winged insects were terrestrial throughout their lives, implying that wings did not evolve in an aquatic environment. The appearance of the first polyneopteran insect was mainly characterized by ancestral traits such as long segmented abdominal appendages and biting mouthparts held below the head capsule. This ancestor lived in association with the ground, which led to various specializations including hardened forewings and unique tarsal attachment structures. However, within Polyneoptera, several groups switched separately to a life on plants. In contrast to a previous hypothesis, we found that social behavior was not part of the polyneopteran ground plan. In other traits, such as the biting mouthparts, Polyneoptera shows a high degree of evolutionary conservatism unique among the major lineages of winged insects.

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Coleopterida (Coleoptera + Strepsiptera) has been established as the sister group of Neuropterida (Megaloptera + Neuroptera + Raphidioptera) based on recent phylogenetic analyses of DNA sequence data obtained from genomes and transcriptomes. However, within the resulting clade (Neuropteroidea) the proposed sister-group relationship between the highly specialized endoparasitic Strepsiptera and the megadiverse Coleoptera still lacks convincing morphological support. Furthermore, relationships among the four suborders of Coleoptera remain controversial, with morphological characters strongly conflicting with results suggested by molecular evidence. A large morphological dataset comprising external and internal features of adults and immature stages is presented here and analysed phylogenetically. Our study is focused on deep splits in Coleopterida and on reconstructing character evolution on the phenotypic level. Parsimony analyses clearly support a sister-group relationship between Strepsiptera and monophyletic Coleoptera. Presumptive synapomorphies are characters linked with posteromotorism, but also features of the head and prothorax. We recover Archostemata as sister group of the remaining extant Coleoptera, and Polyphaga as sister group of the species-poor suborder Myxophaga. The most important character complex of Coleoptera is heavy sclerotization without exposed membranes and a simplification of the thoracic muscle apparatus. Non-archostematan beetles are characterized by further simplifications of the thoracic locomotor apparatus. This trend reaches its peak in Myxophaga and Polyphaga, and these suborders also share apomorphies of the larval legs. A pattern with Polyphaga as sister to all other suborders and a clade Myxophaga + Archostemata (as in recent molecular phylogenetic studies) requires ten additional steps with our dataset. This scenario implies that various simplifications of the thoracic exoskeleton and musculature have taken place several times independently, and also that a complex feeding apparatus suitable for saprophagy and sporophagy was ancestral in Coleoptera, with secondary reduction (or modification) in Archostemata and Adephaga. The coleopteran subordinal relationships remain a challenge, with morphological and molecular data suggesting distinctly different patterns. The earliest evolution of Coleopterida is not documented in the fossil record. The exploration of potential stem-group fossils is a high priority, as is the study of species from the Permian-Triassic transition zone, which are apparently important in the context of evaluating the relationships among beetle suborders.

Insects use different parts of their body to cling to mating partners, to catch prey, or to defend themselves, in most cases the mouthparts or the legs. However, in 400 million years of evolution [1, 2], specialized devices were independently acquired in several groups to adopt these tasks, as for instance modified legs in mantids, assassin bugs or stick insects [3-5], or clasping antennae of the globular springtails [6]. So far, no known species used the neck region between the head and thorax in one of these functional contexts. Here we describe females of †Caputoraptor elegans, a very unusual, presumably predacious insect discovered in approximately 100-million-year-old [7] Burmese amber. Based on several morphological features, we conclude that this species lived in the foliage of trees or bushes. A unique feature of the new taxon is a scissor-like mechanism formed by wing-like extensions on the posterior head and corresponding serrated edges of the dorsal sclerite of the first thoracic segment. Based on the specific structure of the apparatus, we conclude that it was probably used by females to hold on to males during copulation. A defensive or prey-catching function appears less likely. A similar mechanism did not evolve in any other known known group of extant or extinct insects.

The Coleoptera provides an excellent example of the value of fossils for understanding the evolutionary patterns of recent lineages. We reevaluate the morphology of the Early Permian †Tshekardocoleidae to test alternative phylogenetic hypotheses relating to the Palaeozoic evolution of the order. We discuss prior interpretations and revise an earlier data matrix. Both Bayesian and parsimony analyses support the monophyly of Coleoptera excluding †Tshekardocoleidae (= Mesocoleoptera), and of Coleoptera excluding †Tshekardocoleidae and †Permocupedidae (= Metacoleoptera). Plesiomorphies preserved in †Tshekardocoleidae are elytra, which rest over the body in a loose tent-like manner, with flat lateral flanges, projecting beyond the abdominal apex, and abdomens that are flexible and nearly cylindrical. Apomorphies of Mesocoleoptera include shortening of the elytra and a closer fit with the flattened and probably more rigid abdomen. A crucial synapomorphy of Metacoleoptera is the tightly sealed subelytral space, which may have been advantageous during the Permian aridification. Taxon exclusion experiments show that †Tshekardocoleidae is crucial for understanding the early evolution of Coleoptera and that its omission strongly affects ancestral state polarities as well as topology, including crown-group taxa.By constraining the relationships of extant taxa to match those supported by phylogenomic analysis, we demonstrate that features shared by Archostemata with Permian stem groups are most reasonably supported as plesiomorphic and that the smooth and simplified body forms of Polyphaga, Adephaga, Myxophaga, and Micromalthidae were derived in parallel.Our study highlights the reciprocal illumination of molecular, morphological, and paleontological data, and paves the way for tip-dating analysis across the order.

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