Middle Jurassic insect mines on gymnosperms provide missing links to early mining evolution.

We investigated the mining mode of insect feeding, involving larval consumption of a plant's internal tissues, from the Middle Jurassic (165 million years ago) Daohugou locality of Northeastern China. Documentation of mining from the Jurassic Period is virtually unknown, and results from this time interval would address mining evolution during the temporal gap of mine-seed plant diversifications from the previous Late Triassic to the subsequent Early Cretaceous. Plant fossils were examined with standard microscopic procedures for herbivory and used the standard functional feeding group-damage-type system of categorizing damage. All fossil mines were photographed and databased. We examined 2014 plant specimens, of which 27 occurrences on 14 specimens resulted in eight, new, mine damage types (DTs) present on six genera of bennettitalean, ginkgoalean, and pinalean gymnosperms. Three conclusions emerge from this study. First, these mid-Mesozoic mines are morphologically conservative and track plant host anatomical structure rather than plant phylogeny. Second, likely insect fabricators of these mines were three basal lineages of polyphagan beetles, four basal lineages of monotrysian moths, and a basal lineage tenthredinoid sawflies. Third, the nutrition hypothesis, indicating that miners had greater access to nutritious, inner tissues of new plant lineages, best explains mine evolution during the mid-Mesozoic.

Specialized ovipositor sensilla of Cretaceous wasps (Insecta: Hymenoptera) possibly reveal a unique way of host detection.

Insects have evolved complex sensory systems that are important for feeding, defence and reproduction. Parasitoid wasps often spend much time and effort in searching for concealed hosts with the help of specialized sensilla. However, the early evolution of such behaviour and sensilla is poorly known. We describe two fossil female wasps, †Tichostephanus kachinensis sp. nov. and †Tichostephanus longus sp. nov., from mid-Cretaceous Kachin amber. Phylogenetic analyses based on morphological data retrieved †Tichostephanus as deeply nested within Evanioidea and closely related to extant Gasteruptiidae and Evaniidae. Both of these Cretaceous wasps possess features, e.g. coronal tubercles and flexible ovipositor sheaths, that indicate that they might have laid eggs in wood where their larvae possibly parasitized insect larvae. They have a peculiar and unique 'bottle brush' of sensilla close to the apex of their ovipositor sheaths, which has not been observed in any extant parasitoid wasps. These sensilla comprise many regularly arranged plate-shaped setae, attached in relatively large sockets and with rows of longitudinal ridges. Such specialized sensilla perhaps served to enhance the ability to detect hosts inside wood.

Independent wing reductions and losses among stick and leaf insects (Phasmatodea), supported by new Cretaceous fossils in amber.

BACKGROUND: Phasmatodea (stick and leaf insects) play a central role on the debate regarding wing reduction and loss, and its wings are putative reacquisition from secondarily wingless ancestors based solely on extant species. A pivotal taxon in this respect is the species-poor Timematodea, consisting of approximately 21 wingless extant species, which form the sister group of all remaining winged or wingless stick and leaf insects, the Euphasmatodea. RESULTS: Herein, the new fossils of Timematodea from mid-Cretaceous Kachin amber are reported, with winged and wingless species co-occurring. The palaeogeographic distributions of all fossils of Holophasmatodea are summarized, showing their wide paleo-distributions. The phylogenetic analysis based on morphological characters confirms the earliest-diverging lineage of winged Breviala cretacea gen. et sp. nov. in Timematodea, and the possible relationships among all families of Holophasmatodea. These are critical for the reconstruction of patterns of wing evolution in early Phasmatodea. CONCLUSIONS: The new fossils suggest that Timematodea once had wings, at least during the mid-Cretaceous. The palaeogeographic occurrences imply that Timematodea probably have been widely distributed since at least the Jurassic. The phylogenetic analysis with the ancestral-state reconstruction of wings indicates that the common ancestors of Holophasmatodea were winged, the reductions and losses of wings among Timematodea and Euphasmatodea have occurred independently since at least the Cretaceous, and the reduction or loss of the forewing earlier than the hind wings.

Cretaceous lophocoronids with short proboscis and retractable female genitalia provide the earliest evidence for their feeding and oviposition habits.

We describe two new species of Lophocoronidae: Acanthocorona hedida Zhang, Shih and Engel sp. n. and Acanthocorona venulosa Zhang, Shih and Engel sp. n., and an undetermined specimen from mid-Cretaceous Kachin amber. Phylogenetic analysis of basal lepidopteran lineages, including three extinct families, was undertaken. The analysis supported monophyly of Glossata although internal relationships remain controversial. Acanthocorona and Lophocorona form a monophyletic group. It is likely that short and simply structured proboscides of Acanthocorona were used to sip water droplets, pollination drops from gymnosperms, nectar from early flowers, or sap from injured leaves. Both retracted and extended ovipositors are preserved in the material reported here, revealing their morphology and indicating that these Cretaceous lophocoronids inserted eggs into the tissues of their host plants.

Behaviors and Interactions of Insects in Mid-Mesozoic Ecosystems of Northeastern China.

During the past 20 years, more than 1,600 species of well-preserved fossil insects, including members of over 270 families within 24 orders, have been described from the Middle Jurassic Yanliao Entomofauna and Early Cretaceous Jehol Entomofauna in Northeastern China. Diversified fossil insects not only document the origin, systematics, and early evolution of many lineages, but also reveal these lineages' behaviors and interactions with coexisting plants, vertebrates, and other insects in their ecosystems. Fossil evidence has been documented, for example, regarding insects' feeding and pollination mutualism with gymnosperms; ectoparasitic feeding on blood of vertebrates; camouflage, mimicry of gymnosperm plants, and eyespot warning; sound stridulation for attracting potential mates; and sexual display, mating, egg-laying, and parental care. In this article, we review the diverse taxonomy of mid-Mesozoic insects of Northeastern China and elucidate their behaviors and interactions within their ecosystems, which have impacted their early evolution and development into extant insects.

Early Cretaceous mealybug herbivory on a laurel highlights the deep-time history of angiosperm-scale insect associations.

Insect fluid-feeding on fossil vascular plants is an inconspicuous and underappreciated mode of herbivory that can provide novel data on the evolution of deep-time ecological associations and indicate the host-plant preferences of ancient insect herbivores. Previous fossil studies have documented piercing-and-sucking herbivory but often are unable to identify culprit insect taxa. One line of evidence are punctures and scale-insect impression marks made by piercing-and-sucking insects that occasionally provide clues to the systematic identities and relationships of particular insect herbivores. We report here the earliest occurrences of piercing and sucking on early angiosperms as evidenced by scale insect covers, impression marks, punctures and body fossils - notably a mealybug - from the Lower Cretaceous Rose Creek Flora of the Dakota Formation (c. 103 Ma), in southeastern Nebraska, USA. The mealybug, two other scale insect taxa, and several distinctive damage types on laurel leaves and seed-plant stems at Rose Creek document a diverse guild of piercing-and-sucking insects on early angiosperms. The discovery of an Early Cretaceous female mealybug indicates an early herbivorous association with a laurel host. These data provide direct evidence for co-associations and possible coevolution of scale insects and their plant hosts during early angiosperm diversification.

Regional assemblages shaped by historical and contemporary factors: Evidence from a species-rich insect group.

Understanding diversity patterns requires accounting for the roles of both historical and contemporary factors in the assembly of communities. Here, we compared diversity patterns of two moth assemblages sampled from Taihang and Yanshan mountains in Northern China and performed ancestral range reconstructions using the Multi-State Speciation and Extinction model, to track the origins of these patterns. Further, we estimated diversification rates of the two moth assemblages and explored the effects of contemporary ecological factors. From 7,788 specimens we identified 835 species belonging to 23 families, using both DNA barcode analysis and morphology. Moths in Yanshan mountains showed higher species diversity than in Taihang mountains. Ancestral range analysis indicated Yanshan as the origin, with significant historical dispersals from Yanshan to Taihang. Asymmetrical diversification, population expansion, along with frequent and considerable gene flow were detected between communities. Moreover, dispersal limitation or the joint effect of environment filtering and dispersal limitation were inferred as main driving forces shaping current diversity patterns. In summary, we demonstrate that a multiscale (community, population and species level) analysis incorporating both historical and contemporary factors can be useful in delineating factors contributing to community assembly and patterning in diversity.

Cretaceous winged stick insects clarify the early evolution of Phasmatodea.

Wingless and shorter winged stick insects are very common today, but most known extinct stick insects had fully developed wings, leading to contentious affinities among the extinct winged and extant groups. We report herein three male winged stick insects, assigned to Pterophasmatidae fam. nov., from mid-Cretaceous Myanmar (Burmese) amber. Pterophasmatidae fam. nov. are regarded as transitional taxa from extinct winged to modern wingless and shorter winged stick insects based on their similar tegmina venation with extinct Susumanioidea and some body features the same as extant Phasmatodea. However, their symmetric phallic organs comprising two consistent phallomeres are different from those of all living groups. Phylogenetic analyses suggest that the extinct winged taxa, including the new family, are the stem groups of modern stick and leaf insects, and all of them constitute the clade of Phasmatodea. New findings indicate winged and wingless stick insects' morphologies diversified significantly during or before the mid-Cretaceous.

Stick insect in Burmese amber reveals an early evolution of lateral lamellae in the Mesozoic.

Extant stick and leaf insects commonly imitate twigs or leaves, with lateral lamellae used to enhance crypsis or achieve mimicry for protection. However, the origin and early evolution of such lateral expansions among Phasmatodea are unknown, because all known Mesozoic phasmatodeans hitherto lack preserved evidence of such structures. We report here the first Mesozoic stick insect, Elasmophasma stictum gen. et sp. nov., with well-preserved, thin, lateral lamellae on the thoracic pleura, the terga of abdominal segments I-X and the ventrolateral margins of all femora. This new species, from the mid-Cretaceous amber of northern Myanmar, has a clear, stick-like body and is assigned to Euphasmatodea. The abdominal structures of E. stictum exhibit traces of multiple expansions of the terga, suggesting that such structure might have been an early development of body expansions used to improve crypsis for stick or leaf insects when they sprawled on twigs or leaves.

Phylogenetic analyses with four new Cretaceous bristletails reveal inter-relationships of Archaeognatha and Gondwana origin of Meinertellidae.

Based on fifteen Archaeognatha (=Microcoryphia) specimens from Myanmar (Burmese) amber, including males, females and immatures, two new genera and four species, Cretaceomachilis longa sp.n., Unimeinertellus abundus gen. et sp.n., U. bellus sp.n. and Nullmeinertellus wenxuani gen. et sp.n., are described. Phylogenetic analyses of taxa in Archaeognatha were conducted using Maximum parsimony and Bayesian inference based on morphological characters and DNA sequence data. Our results confirm the phylogenetic position of the new genera, clarify the monophyly of Meinertellidae and indicate that the 'paleo-types' excluding Ditrigoniophthalmus are nested within the Machilidae group, but suggest that the three subfamilies within Machilidae may be artificial. The diversity of meinertellids with derived characters found from the Cretaceous indicate that the divergence time of Machilidae and Meinertellidae is much earlier than the Cretaceous. We propose the possibility that Meinertellidae might have originated on Gondwana.

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 new xyelotomid (Hymenoptera) from the Middle Jurassic of China displaying enigmatic venational asymmetry.

BACKGROUND: Pterygota insects typically have symmetric veins in left and right wings. For studying taxonomy and phylogeny of fossil insects, venational patterns are commonly used as diagnostic characters, in conjunction with preserved body characters. Some examples of asymmetrical venation are known among extant insects, but only a few fossil insects with asymmetric wings have been reported, among which a previously described xyelotomid of Hymenoptera, Xyelocerus diaphanous, displays an unusual, small cell of vein Rs in the left forewing, but not in the right. RESULTS: Herein we report a new sawfly of the family Xyelotomidae, Aethotoma aninomorpha gen. et sp. nov., from the late Middle Jurassic of China having a simple Sc in the forewing and Sc with two branches in the hind wing. In additional, the new specimen exhibits an enigmatic venational asymmetry. In the right forewing, crossvein 2r-rs of forms a loop, then forks into 2 long branches reaching Rs, while 2r-rs of the left forewing forks into 2 short branches reaching Rs, in contrast to a linear 2r-rs in typical fossil and extant sawflies. CONCLUSION: Such rare asymmetrical venation found from fossil sawflies provides a glance at early occurrences of venational variability and instability, or possibly aberrational development, for insects in the late Middle Jurassic.

Convergent evolution of ramified antennae in insect lineages from the Early Cretaceous of Northeastern China.

Antennae are important, insect sensory organs that are used principally for communication with other insects and the detection of environmental cues. Some insects independently evolved ramified (branched) antennae, which house several types of sensilla for motion detection, sensing olfactory and chemical cues, and determining humidity and temperature levels. Though ramified antennae are common in living insects, occasionally they are present in the Mesozoic fossil record. Here, we present the first caddisflies with ramified antennae, the earliest known fossil sawfly, and a scorpionfly also with ramified antennae from the mid-Lower Cretaceous Yixian Formation of Northeastern China, dated at 125 million years ago (Ma). These three insect taxa with ramified antennae consist of three unrelated lineages and provide evidence for broad structural convergence that historically has been best demonstrated by features such as convergent mouthparts. In addition, ramified antennae in these Mid-Mesozoic lineages likely do not constitute a key innovation, as they are not associated with significantly increased diversification compared with closely related lineages lacking this trait, and nor are they ecologically isolated from numerous, co-occurring insect species with unmodified antennae.

The evolutionary convergence of mid-Mesozoic lacewings and Cenozoic butterflies.

Mid-Mesozoic kalligrammatid lacewings (Neuroptera) entered the fossil record 165 million years ago (Ma) and disappeared 45 Ma later. Extant papilionoid butterflies (Lepidoptera) probably originated 80-70 Ma, long after kalligrammatids became extinct. Although poor preservation of kalligrammatid fossils previously prevented their detailed morphological and ecological characterization, we examine new, well-preserved, kalligrammatid fossils from Middle Jurassic and Early Cretaceous sites in northeastern China to unravel a surprising array of similar morphological and ecological features in these two, unrelated clades. We used polarized light and epifluorescence photography, SEM imaging, energy dispersive spectrometry and time-of-flight secondary ion mass spectrometry to examine kalligrammatid fossils and their environment. We mapped the evolution of specific traits onto a kalligrammatid phylogeny and discovered that these extinct lacewings convergently evolved wing eyespots that possibly contained melanin, and wing scales, elongate tubular proboscides, similar feeding styles, and seed-plant associations, similar to butterflies. Long-proboscid kalligrammatid lacewings lived in ecosystems with gymnosperm-insect relationships and likely accessed bennettitalean pollination drops and pollen. This system later was replaced by mid-Cretaceous angiosperms and their insect pollinators.

Phylogenetic analyses elucidate the inter-relationships of Pamphilioidea (Hymenoptera, Symphyta).

The phylogeny of the superfamily Pamphilioidea is reconstructed using morphology and DNA sequence data of living and fossil taxa by employing two phylogenetic methods (maximum parsimony and Bayesian inference). Based on our results, the monophyly of Pamphilioidea and Pamphiliidae are corroborated, whereas two extinct families, Xyelydidae and Praesiricidae, are not monophyletic. Because members of Praesiricidae together with Megalodontes form a monophyletic group, we propose that the paraphyletic Praesiricidae is synonymized under Megalodontesidae (syn. nov.). The origin of Pamphilioidea is hypothesized to be as early as the Early Jurassic. To better understand morphological evolution in the early lineages of Pamphilioidea, ancestral states of the first flagellomere and the first and second abdominal terga are reconstructed on the morphology-based tree. In addition, three new genera (Medilyda, Brevilyda, Strenolyda) with five new species (Medilyda procera, M. distorta, Brevilyda provecta, Strenolyda marginalis and S. retrorsa) are described based on well-preserved xyelydid fossils from the Middle Jurassic Jiulongshan Formation of north-eastern China.

New fossil ephialtitids elucidating the origin and transformation of the propodeal-metasomal articulation in Apocrita (Hymenoptera).

BACKGROUND: Apocrita has a special structure that its first abdominal segment has been incorporated into the thorax as the propodeum. The remaining abdomen, metasoma, is connected to this hybrid region via a narrow propodeal-metasomal articulation forming a "wasp waist", which serves an important function of providing maneuverability, flexibility and posture for oviposition. However, the origin and transformation of the propodeal-metasomal articulation are still vague. Ephialtitidae, as the basal group of Apocrita from the Early Jurassic to the Early Cretaceous, have shown various types of propodeal-metasomal articulations. RESULTS: This study describes and illustrates two new genera with three new species, Acephialtitia colossa gen. et sp. nov., Proephialtitia acanthi gen. et sp. nov. and P. tenuata sp. nov., collected respectively from the Early Cretaceous Yixian Formation at Liutiaogou and the Middle Jurassic Jiulongshan Formation at Daohugou, both in Inner Mongolia, China. These genera are assigned to the Ephialtitidae based on their complete wing venation, e.g. 2r-rs, 2r-m, 3r-m and 2 m-cu always present in the forewings and Rs, M and Cu in the hind wings. These new fossil ephialtitids have well-preserved propodeal-metasomal articulations indicating metasoma is broadly attached to propodeum. CONCLUSION: The broad articulation between the propodeum and metasoma in basal Ephialtitidae, likely passed on from a still more basal family Karatavitidae, suggests three separate pathways of the transformation of the "wasp waist" in three different derived lineages leading from Ephialtitidae to: (i) Kuafuidae and further to the remaining Apocrita, (ii) Stephanidae, and (iii) Evanioidea. In addition, the demise of ephialtitid wasps lagging behind the flourishing of angiosperms suggests that ephialtitid extinction might have been mainly driven by competition with numerous new taxa (eg. the abundant Cretaceous xylophilous Baissinae and Ichneumonoidea) appeared just before or/and soon after the J/K boundary.

Jurassic mimicry between a hangingfly and a ginkgo from China.

A near-perfect mimetic association between a mecopteran insect species and a ginkgoalean plant species from the late Middle Jurassic of northeastern China recently has been discovered. The association stems from a case of mixed identity between a particular plant and an insect in the laboratory and the field. This confusion is explained as a case of leaf mimesis, wherein the appearance of the multilobed leaf of Yimaia capituliformis (the ginkgoalean model) was accurately replicated by the wings and abdomen of the cimbrophlebiid Juracimbrophlebia ginkgofolia (the hangingfly mimic). Our results suggest that hangingflies developed leaf mimesis either as an antipredator avoidance device or possibly as a predatory strategy to provide an antiherbivore function for its plant hosts, thus gaining mutual benefit for both the hangingfly and the ginkgo species. This documentation of mimesis is a rare occasion whereby exquisitely preserved, co-occurring fossils occupy a narrow spatiotemporal window that reveal likely reciprocal mechanisms which plants and insects provide mutual defensive support during their preangiospermous evolutionary histories.

A new Cretaceous genus of xyelydid sawfly illuminating nygmata evolution in Hymenoptera.

BACKGROUND: Nygmata are prominent glandular structures on the wings of insects. They have been documented in some extant insects, including several families of Neuroptera and Mecoptera, the majority of Trichoptera, and a few of the hymenopteran Symphyta. However, because nygmata are rarely preserved in compression fossils, their early development and evolution are still enigmatic. For example, the only documented nygmata in the Hymenoptera are on the forewings of the Triassic xyelids Asioxyela paurura and Madygenius primitives. RESULTS: This study describes and illustrates a new genus and species from the family Xyelydidae, Rectilyda sticta gen. et sp. nov., from the Early Cretaceous Yixian Formation of Duolun County, Inner Mongolia, China. This genus has 1-RS reclival and linearly aligned with 1-M, which is different from all other genera in the Xyelydidae. In addition, R. sticta gen. et sp. nov. has clearly preserved nygmata: four symmetrical nygmata on each forewing and two on each hind wing. CONCLUSION: Previous reports of nygmata on the forewings of Triassic xyelids and extant sawflies, together with this new fossil record of nygmata, provide rare insights into their developmental trends, as well as into the evolution of hymenopterans and insects in general.

The first flea with fully distended abdomen from the Early Cretaceous of China.

BACKGROUND: Fleas, the most notorious insect ectoparasites of human, dogs, cats, birds, etc., have recently been traced to its basal and primitive ancestors during the Middle Jurassic. Compared with extant fleas, these large basal fleas have many different features. Although several fossil species with transitional morphologies filled the evolutionary blank, the early evolution of these ectoparasites is still poorly known. RESULTS: Here we report a new flea with transitional characters, Pseudopulex tanlan sp. nov., assigned to Pseudopulicidae, from the Lower Cretaceous Yixian Formation of Liaoning Province, China. Different from the previously described pseudopulicids, P. tanlan has relatively smaller body size but lacking any ctenidia on the tibiae or body, while the male with comparatively smaller and shorter genitalia. On the other hand, P. tanlan has some characters similar to the transitional fleas of saurophthirids, such as, a small head, short compacted antennae, small pygidium and many stiff setae covering the body. CONCLUSIONS: Even though other possibilities can not be ruled out, the female specimen with extremely distended abdomen suggests that it might have consumed its last meal before its demise. Compared with other reported female flea fossils, we calculate and estimate that P. tanlan sp. nov. might have consumed 0.02 milliliter (ml) of blood, which is about 15 times of the intake volume by extant fleas. These new findings further support that fleas had evolved a broad diversity by the Early Cretaceous.

Mesozoic lacewings from China provide phylogenetic insight into evolution of the Kalligrammatidae (Neuroptera).

BACKGROUND: The Kalligrammatidae are distinctive, large, conspicuous, lacewings found in Eurasia from the Middle Jurassic to mid Early Cretaceous. Because of incomplete and often inadequate fossil preservation, an absence of detailed morphology, unclear relationships, and unknown evolutionary trends, the Kalligrammatidae are poorly understood. RESULTS: We describe three new subfamilies, four new genera, twelve new species and four unassigned species from the late Middle Jurassic Jiulongshan and mid Early Cretaceous Yixian Formations of China. These kalligrammatid taxa exhibit diverse morphological characters, such as mandibulate mouthparts in one major clade and siphonate mouthparts in the remaining four major clades, the presence or absence of a variety of distinctive wing markings such as stripes, wing spots and eyespots, as well as multiple major wing shapes. Based on phylogenetic analyses, the Kalligrammatidae are divided into five principal clades: Kalligrammatinae Handlirsch, 1906, Kallihemerobiinae Ren & Engel, 2008, Meioneurinae subfam. nov., Oregrammatinae subfam. nov. and Sophogrammatinae subfam. nov., each of which is accorded subfamily-level status. Our results show significant morphological and evolutionary differentiation of the Kalligrammatidae family during a 40 million-year-interval of the mid Mesozoic. CONCLUSION: A new phylogeny and classification of five subfamilies and their constituent genera is proposed for the Kalligrammatidae. These diverse, yet highly specialized taxa from northeastern China suggest that eastern Eurasia likely was an important diversification center for the Kalligrammatidae. Kalligrammatids possess an extraordinary morphological breadth and panoply of adaptations during the mid-Mesozoic that highlight our conclusion that their evolutionary biology is much more complex than heretofore realized.