A winged relative of ice-crawlers in amber bridges the cryptic extant Xenonomia and a rich fossil record.

Until the advent of phylogenomics, the atypical morphology of extant representatives of the insect orders Grylloblattodea (ice-crawlers) and Mantophasmatodea (gladiators) had confounding effects on efforts to resolve their placement within Polyneoptera. This recent research has unequivocally shown that these species-poor groups are closely related and form the clade Xenonomia. Nonetheless, divergence dates of these groups remain poorly constrained, and their evolutionary history debated, as the few well-identified fossils, characterized by a suite of morphological features similar to that of extant forms, are comparatively young. Notably, the extant forms of both groups are wingless, whereas most of the pre-Cretaceous insect fossil record is composed of winged insects, which represents a major shortcoming of the taxonomy. Here, we present new specimens embedded in mid-Cretaceous amber from Myanmar and belonging to the recently described species Aristovia daniili. The abundant material and pristine preservation allowed a detailed documentation of the morphology of the species, including critical head features. Combined with a morphological data set encompassing all Polyneoptera, these new data unequivocally demonstrate that A. daniili is a winged stem Grylloblattodea. This discovery demonstrates that winglessness was acquired independently in Grylloblattodea and Mantophasmatodea. Concurrently, wing apomorphic traits shared by the new fossil and earlier fossils demonstrate that a large subset of the former "Protorthoptera" assemblage, representing a third of all known insect species in some Permian localities, are genuine representatives of Xenonomia. Data from the fossil record depict a distinctive evolutionary trajectory, with the group being both highly diverse and abundant during the Permian but experiencing a severe decline from the Triassic onwards.

Little bits of dragonfly history repeating exemplified by a new Pennsylvanian family.

During its 320 Myr evolution, dragon- and damselfly (Odonata) wing morphology underwent intense modifications. The resulting diversity prompted comparative analyses focusing on phylogeny. However, homoplasy proved to plague wing-related characters. Concurrently, limited benefits were obtained from considering fossil taxa, similarly impacted. Herein, we investigate two aspects particularly affected by convergence, namely the acquisition of vein-like structuring elements derived from regular cross-venation, termed conamina; and the evolution of butter knife wing shape. Conamen implementation is found to be consistently linked with vein curvature sharpening, itself generating potential breaking points. Conamina therefore likely evolved to address wing integrity issues during ever-more-demanding flight performance. Moreover, an existing conamen is likely to trigger the acquisition of further, associated conamina. As for butter knife shape, previously documented in the extinct Archizygoptera and among damselflies, we report a new, 315 Ma occurrence with the rare species Haidilaozhen cuiae gen. et sp. nov. (family Haidilaozhenidae fam. nov.), from the Xiaheyan locality (China). The repeated acquisition of butter knife-shaped wing can be related to slow speed flight and, in turn, predator avoidance. In both cases of iterated regularities, the unique 'network-and-membrane' wing design proper to insects is found to compose a strong, constraining factor.

Disparification and extinction trade-offs shaped the evolution of Permian to Jurassic Odonata.

Owing to their prevalence in nowadays terrestrial ecosystems, insects are a relevant group to assess the impact of mass extinctions on emerged land. However, limitations of the insect fossil record make it difficult to assess the impact of such events based on taxonomic diversity alone. Therefore, we documented trends in morphological diversity, i.e., disparity, using wings of Permian to Jurassic Odonata as model. Our results show a decreasing trend in disparity while species richness increased. Both the Permian-Triassic and Triassic-Jurassic transitions are revealed as important events, associated with strong morphospace restructuring due to selective extinction. In each case, a recovery was assured by the diversification of new forms compensating the loss of others. Early representatives of Odonata continuously evolved new shapes, a pattern contrasting with the classical assertion of a morphospace fulfilled early and followed by selective extinctions and specialization within it.

A Cambrian tommotiid preserving soft tissues reveals the metameric ancestry of lophophorates.

Among extant animals, Lophotrochozoa accounts for the majority of phyla.1 This bilaterian clade radiated rapidly during the Cambrian explosion, obfuscating its phylogenetic relationships and rendering many aspects of its early evolution uncertain. Many early lophotrochozoans are known only from isolated skeletal microfossils, "small shelly fossils," often derived from larger animals with complex multi-element skeletons.2 The discovery of articulated fossils has revealed surprising insights into the animals from which these skeletal pieces were derived, such as paired shells in the mollusc Halkieria.3 Tommotiids are a key group of phosphatic early skeletal fossils that first appear in the late early Cambrian.4,5 Although their affinities were previously obscure, discoveries of partial scleritomes and investigations of growth and microstructure6 provide links with Brachiopoda7,8 and Phoronida,9 two of the lophophorate phyla. By contrast, the body plan of camenellan tommotiids remains a palaeontological mystery, with hypothetical reconstructions representing motile, benthic, dorsally armored worms.4,10 Here, we describe an articulated camenellan (Wufengella bengtsoni gen. et sp. nov.) from the Cambrian Chengjiang Biota, China, revealing the morphology of the scleritome and the first soft tissues from an adult tommotiid. Wufengella carries two dorsal rows of sclerites in a highly asymmetric arrangement, flanked by smaller, cap-shaped sclerites. The scleritome was fringed by iterated fascicles of chaetae and two layers of flattened lobes. Phylogenetic analysis confirms that camenellans occupy a deep branch in lophophorate phylogeny, prior to the acquisition of a sessile lifestyle. Wufengella reveals direct evidence for a metameric body plan reminiscent of annelids early in the evolutionary history of lophophorates.11,12.

Evolutionary history and divergence times of Odonata (dragonflies and damselflies) revealed through transcriptomics.

Dragonflies and damselflies are among the earliest flying insects with extant representatives. However, unraveling details of their long evolutionary history, such as egg laying (oviposition) strategies, is impeded by unresolved phylogenetic relationships, particularly in damselflies. Here we present a transcriptome-based phylogenetic reconstruction of Odonata, analyzing 2,980 protein-coding genes in 105 species representing nearly all the order's families. All damselfly and most dragonfly families are recovered as monophyletic. Our data suggest a sister relationship between dragonfly families of Gomphidae and Petaluridae. According to our divergence time estimates, both crown-Zygoptera and -Anisoptera arose during the late Triassic. Egg-laying with a reduced ovipositor apparently evolved in dragonflies during the late Jurassic/early Cretaceous. Lastly, we also test the impact of fossil choice and placement, particularly, of the extinct fossil species, †Triassolestodes asiaticus, and †Proterogomphus renateae on divergence time estimates. We find placement of †Proterogomphus renateae to be much more impactful than †Triassolestodes asiaticus.

Ovipositor and mouthparts in a fossil insect support a novel ecological role for early orthopterans in 300 million years old forests.

A high portion of the earliest known insect fauna is composed of the so-called 'lobeattid insects', whose systematic affinities and role as foliage feeders remain debated. We investigated hundreds of samples of a new lobeattid species from the Xiaheyan locality using a combination of photographic techniques, including reflectance transforming imaging, geometric morphometrics, and biomechanics to document its morphology, and infer its phylogenetic position and ecological role. Ctenoptilus frequens sp. nov. possessed a sword-shaped ovipositor with valves interlocked by two ball-and-socket mechanisms, lacked jumping hind-legs, and certain wing venation features. This combination of characters unambiguously supports lobeattids as stem relatives of all living Orthoptera (crickets, grasshoppers, katydids). Given the herein presented and other remains, it follows that this group experienced an early diversification and, additionally, occurred in high individual numbers. The ovipositor shape indicates that ground was the preferred substrate for eggs. Visible mouthparts made it possible to assess the efficiency of the mandibular food uptake system in comparison to a wide array of extant species. The new species was likely omnivorous which explains the paucity of external damage on contemporaneous plant foliage.

The wing venation of a new fossil species, reconstructed using geometric morphometrics, adds to the rare fossil record of Triassic Gondwanian Odonata.

Probably the most common rock-imprint fossil-insect remain is an incomplete isolated wing. This pitfall has been traditionally addressed by manually reconstructing missing parts, which is not ideal to comprehend long-term evolutionary trends in the group, in particular for morphological diversity (i.e., disparity) approaches. Herein we describe a new Triassic relative of dragon- and damselflies (Odonata), Moltenophlebia lindae gen. et sp. nov., from the Molteno Formation (Karoo Basin, South Africa), on the basis of three incomplete, isolated wings. In order to provide a reconstruction of the complete wing venation of the species, we formalized and applied a repeatable method aiming at inferring the missing parts of a given specimen. It is based on homologous veins automatically identified thanks to a standardized color-coding. The dedicated script can be applied broadly to the fossil record of insect wings. The species is identified as a member of the Zygophlebiida, within the Triadophlebiomorpha. This discovery, therefore, represents the first ascertained occurrence of the latter group in Gondwana, an area where the fossil record of Odonata is depauperate.

Author Correction: Phylogenomic analysis sheds light on the evolutionary pathways towards acoustic communication in Orthoptera.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Phylogenomic analysis sheds light on the evolutionary pathways towards acoustic communication in Orthoptera.

Acoustic communication is enabled by the evolution of specialised hearing and sound producing organs. In this study, we performed a large-scale macroevolutionary study to understand how both hearing and sound production evolved and affected diversification in the insect order Orthoptera, which includes many familiar singing insects, such as crickets, katydids, and grasshoppers. Using phylogenomic data, we firmly establish phylogenetic relationships among the major lineages and divergence time estimates within Orthoptera, as well as the lineage-specific and dynamic patterns of evolution for hearing and sound producing organs. In the suborder Ensifera, we infer that forewing-based stridulation and tibial tympanal ears co-evolved, but in the suborder Caelifera, abdominal tympanal ears first evolved in a non-sexual context, and later co-opted for sexual signalling when sound producing organs evolved. However, we find little evidence that the evolution of hearing and sound producing organs increased diversification rates in those lineages with known acoustic communication.

An integrative phylogenomic approach illuminates the evolutionary history of cockroaches and termites (Blattodea).

Phylogenetic relationships among subgroups of cockroaches and termites are still matters of debate. Their divergence times and major phenotypic transitions during evolution are also not yet settled. We addressed these points by combining the first nuclear phylogenomic study of termites and cockroaches with a thorough approach to divergence time analysis, identification of endosymbionts, and reconstruction of ancestral morphological traits and behaviour. Analyses of the phylogenetic relationships within Blattodea robustly confirm previously uncertain hypotheses such as the sister-group relationship between Blaberoidea and remaining Blattodea, and Lamproblatta being the closest relative to the social and wood-feeding Cryptocercus and termites. Consequently, we propose new names for various clades in Blattodea: Cryptocercus + termites = Tutricablattae; Lamproblattidae + Tutricablattae = Kittrickea; and Blattoidea + Corydioidea = Solumblattodea. Our inferred divergence times contradict previous studies by showing that most subgroups of Blattodea evolved in the Cretaceous, reducing the gap between molecular estimates of divergence times and the fossil record. On a phenotypic level, the blattodean ground-plan is for egg packages to be laid directly in a hole while other forms of oviposition, including ovovivipary and vivipary, arose later. Finally, other changes in egg care strategy may have allowed for the adaptation of nest building and other novelties.

A new Raspy Cricket from the northern Australian Rainforests (Orthoptera: Gryllacrididae).

An Australian Raspy Cricket, Chauliogryllacris acaropenates Rentz, Su, Béthoux, sp. nov. is described. This cricket was found to harbor a number of mite species of interest to acarologists and the name was needed for them to proceed with their studies. A key to the males of the described species of Chauliogryllacris is provided along with numerous illustrations of the described cricket. Observations and comments on its biology, behavior and ecology are presented.

Functional morphology of tegmina-based stridulation in the relict species Cyphoderris monstrosa (Orthoptera: Ensifera: Prophalangopsidae).

Male grigs, bush crickets and crickets produce mating calls by tegminal stridulation: the scraping together of modified forewings functioning as sound generators. Bush crickets (Tettigoniidae) and crickets (Gryllinae) diverged some 240 million years ago, with each lineage developing unique characteristics in wing morphology and the associated mechanics of stridulation. The grigs (Prophalangopsidae), a relict lineage more closely related to bush crickets than to crickets, are believed to retain plesiomorphic features of wing morphology. The wing cells widely involved in sound production, such as the harp and mirror, are comparatively small, poorly delimited and/or partially filled with cross-veins. Such morphology is similarly observed in the earliest stridulating ensiferans, for which stridulatory mechanics remains poorly understood. The grigs, therefore, are of major importance to investigate the early evolutionary stages of tegminal stridulation, a critical innovation in the evolution of the Orthoptera. The aim of this study is to appreciate the degree of specialization on grig forewings, through identification of sound radiating areas and their properties. For well-grounded comparisons, homologies in wing venation (and associated areas) of grigs and bush crickets are re-evaluated. Then, using direct evidence, this study confirms the mirror cell, in association with two other areas (termed 'neck' and 'pre-mirror'), as the acoustic resonator in the grig Cyphoderris monstrosa Despite the use of largely symmetrical resonators, as found in field crickets, analogous features of stridulatory mechanics are observed between C. monstrosa and bush crickets. Both morphology and function in grigs represents transitional stages between unspecialized forewings and derived conditions observed in modern species.

A first higher-level time-calibrated phylogeny of antlions (Neuroptera: Myrmeleontidae).

In this study, we reconstruct the first time-calibrated phylogeny of the iconic antlion family, the Myrmeleontidae (Neuroptera: Myrmeleontiformia). We use maximum likelihood and Bayesian inference to analyse a molecular dataset based on seven mitochondrial and nuclear gene markers. The dataset encompasses 106 species of Neuroptera, including 94 antlion species. The resulting phylogenetic framework provides support for a myrmeleontid classification distinguishing four subfamilies: Acanthaclisinae, Myrmeleontinae, Palparinae, and Stilbopteryginae. Within Myrmeleontinae, Myrmecaelurini and Nemoleontini are recovered as monophyletic clades; Gepini also appears as a valid tribe, distinct from Myrmecaelurini whereas Myrmecaelurini and Nesoleontini on one hand and Brachynemurini and Dendroleontini on the other hand, appear closely related. Some preliminary information related to generic and specific levels are also implied from our results, such as the paraphyly of several genera. Dating analyses based on thoroughly evaluated fossil calibrations indicate that the antlion family likely originated in the Cretaceous, between 135 and 138 million years ago (depending on the set of fossil calibrations), and that all higher-level lineages appeared during the Early Cretaceous. This first phylogenetic hypothesis will provide a valuable basis to further expand the taxonomic coverage and molecular sampling, and to lay the foundations of future systematic revisions.

The first fossil salmonfly (Insecta: Plecoptera: Pteronarcyidae), back to the Middle Jurassic.

BACKGROUND: The fossil record of Plecoptera (stoneflies) is considered relatively complete, with stem-groups of each of the three major lineages, viz. Antarctoperlaria, Euholognatha and Systellognatha (and some of their families) represented in the Mesozoic. However, the family Pteronarcyidae (the salmonflies; including two genera, Pteronarcys and Pteronarcella) has no fossil record to date, and the family has been suggested to have diverged recently. RESULTS: In this paper, we report on a set of specimens belonging to a new fossil species of stonefly, discovered from the Middle Jurassic Daohugou locality (China). Our comparative analysis of wing venation and body characters demonstrates that the new species belongs to the Pteronarcyidae, and is more closely related to Pteronarcys than to Pteronarcella. However, it differs from all known species of the former genus. It is therefore assigned to a new genus and named Pteroliriope sinitshenkovae gen. et sp. nov. under the traditional nomenclatural procedure. The cladotypic nomenclatural procedure is also employed, with the resulting combination Pteroliriope nec Pteronarcys sinitshenkovae sp. nov. CONCLUSIONS: The first discovery of a fossil member of the Pteronarcyidae demonstrates that the corresponding lineage is not a very recent offshoot but was already present ca. 165 million years ago. This discovery concurs with the view that divergence of most stonefly families took place very early, probably in the Triassic, or even in the Permian. This contribution demonstrates the need for (re-)investigations of the systematics of fossil stoneflies to refine divergence date estimates for Plecoptera lineages.

A Carboniferous Mite on an Insect Reveals the Antiquity of an Inconspicuous Interaction.

Symbiosis [1], understood as prolonged interspecific association, is as ancient as the eukaryotic cell [2, 3]. A variety of such associations have been reported in the continental fossil record, albeit sporadically. As for mites, which as a group have been present since the Devonian (ca. 390 mya) [4, 5] and are involved in a tremendous variety of modern-day symbioses, reported associations are limited to a few amber-preserved cases [6-11], with the earliest instance in the Cretaceous (ca. 85 mya) [11]. As a consequence, the antiquity and origin of associations involving small-sized mites and larger animals are poorly understood. Here we report, recovered from the Carboniferous Xiaheyan locality (ca. 320 mya), an oribatid mite located on the thorax of an extinct relative of grasshoppers, crickets, and katydids [12]. The mite was investigated using several methods, including phase-contrast tomography. The detailed morphological data allowed the placement of the mite in a new family within Mixonomata, whose fossil record is thus extended by ca. 250 Ma. Specimen and abundance distribution data derived from the fossil insect sample indicate that specimens from the corresponding excavation site were buried rapidly and were sub-autochthonous, indicating a syn vivo association. Moreover, the mite is located in a sequestered position on the insect. The observed interaction best fits the definition for phoresy, in which the benefit is transport and protection for the mite. This discovery demonstrates that this association, a trait shared by representatives of the most speciose mite taxa, arose very early during mite evolution.

A 365-Million-Year-Old Freshwater Community Reveals Morphological and Ecological Stasis in Branchiopod Crustaceans.

Branchiopod crustaceans are represented by fairy, tadpole, and clam shrimps (Anostraca, Notostraca, Laevicaudata, Spinicaudata), which typically inhabit temporary freshwater bodies, and water fleas (Cladoceromorpha), which live in all kinds of freshwater and occasionally marine environments [1, 2]. The earliest branchiopods occur in the Cambrian, where they are represented by complete body fossils from Sweden such as Rehbachiella kinnekullensis [3] and isolated mandibles preserved as small carbonaceous fossils [4-6] from Canada. The earliest known continental branchiopods are associated with hot spring environments [7] represented by the Early Devonian Rhynie Chert of Scotland (410 million years ago) and include possible stem-group or crown-group Anostraca, Notostraca, and clam shrimps or Cladoceromorpha [8-10], which differ morphologically from their modern counterparts [1, 2, 11]. Here we report the discovery of an ephemeral pool branchiopod community from the 365-million-year-old Strud locality of Belgium. It is characterized by new anostracans and spinicaudatans, closely resembling extant species, and the earliest notostracan, Strudops goldenbergi [12]. These branchiopods released resting eggs into the sediment in a manner similar to their modern representatives [1, 2]. We infer that this reproductive strategy was critical to overcoming environmental constraints such as seasonal desiccation imposed by living on land. The pioneer colonization of ephemeral freshwater pools by branchiopods in the Devonian was followed by remarkable ecological and morphological stasis that persists to the present day.

The Jurassic Bajanzhargalanidae (Insecta: Grylloblattida?): New genera and species, and data on postabdominal morphology.

The presumed phylogenetic link between extant ice-crawlers (Grylloblattidae = 'crown-Grylloblattida') and fossil species of the taxon concept Grylloblattida sensu Storozhenko (2002) is essentially based on postabdominal morphology. However, the fossil data are limited, and the interpretation is open to debate. Here we investigate a sample of a poorly known fossil 'grylloblattidan' family, the Bajanzhargalanidae, collected from the Daohugou locality (Middle Jurassic, China). We describe Sinonele fangi gen. nov., sp. nov., Sinonele hei gen. nov., sp. nov., Sinonele phasmoides gen. nov., sp. nov., and Sinonele mini gen. nov., sp. nov. Thanks to the abundance and exceptional preservation of the material, we could document wing venation intra-specific variability, provide cues to identify male and female individuals, describe and tentatively interpret various body structures of both sexes, and discuss them with a broad pterygotan phylogenetic perspective. The Bajanzhargalanidae exhibit a puzzling combination of postabdominal characters leaving us inconclusive on their affinities, or lack thereof, with crown-Grylloblattida. Our contribution suggests that a substantial effort will be needed to further investigate postabdominal structures from comparatively ancient fossil insects preserved as rock imprints, because of their broad morphological disparity.

Under cover at pre-angiosperm times: a cloaked phasmatodean insect from the Early Cretaceous Jehol biota.

BACKGROUND: Fossil species that can be conclusively identified as stem-relatives of stick- and leaf-insects (Phasmatodea) are extremely rare, especially for the Mesozoic era. This dearth in the paleontological record makes assessments on the origin and age of the group problematic and impedes investigations of evolutionary key aspects, such as wing development, sexual size dimorphism and plant mimicry. METHODOLOGY/PRINCIPAL FINDINGS: A new fossil insect species, Cretophasmomima melanogramma Wang, Béthoux and Ren sp. nov., is described on the basis of one female and two male specimens recovered from the Yixian Formation (Early Cretaceous, ca. 126±4 mya; Inner Mongolia, NE China; known as 'Jehol biota'). The occurrence of a female abdominal operculum and of a characteristic 'shoulder pad' in the forewing allows for the interpretation of a true stem-Phasmatodea. In contrast to the situation in extant forms, sexual size dimorphism is only weakly female-biased in this species. The peculiar wing coloration, viz. dark longitudinal veins, suggests that the leaf-shaped plant organ from the contemporaneous 'gymnosperm' Membranifolia admirabilis was used as model for crypsis. CONCLUSIONS/SIGNIFICANCE: As early as in the Early Cretaceous, some stem-Phasmatodea achieved effective leaf mimicry, although additional refinements characteristic of recent forms, such as curved fore femora, were still lacking. The diversification of small-sized arboreal insectivore birds and mammals might have triggered the acquisition of such primary defenses.

At last, a Pennsylvanian stem-stonefly (Plecoptera) discovered.

BACKGROUND: Stem-relatives of many winged insect orders have been identified among Pennsylvanian fossils (Carboniferous Period). Owing to their presumed 'basal' position in insect phylogeny, stoneflies were expected to occur at this period. However, no relative has ever been designated convincingly. RESULTS: In this paper, we report specimens belonging to a new fossil insect species collected from the Tupo Formation (Pennsylvanian; China). The wing venation of Gulou carpenteri gen. et sp. nov. exhibits character states diagnostic of the order Plecoptera, but lack character states shared by unequivocal representatives of the order. Derived from this identification, the delimitation of the fossil species is ascertained based on comparison of several extant stonefly species. This comparative analysis allowed a trait present in G. carpenteri gen. et sp. nov., but rarely occurring in extant species, to be documented and highlighted as atavistic. Affinities of taxa formerly proposed as putative stem-stoneflies are reconsidered in the light of the new discovery. CONCLUSIONS: Gulou carpenteri gen. et sp. nov. is considered the only genuine Plecoptera reported from the Pennsylvanian. Continuing efforts on the systematics of Pennsylvanian winged insects indicate a fauna more diverse than previously appreciated. It suggests that insects already had a long, yet undocumented, history by this time.