Diying Huang

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.

Early Cambrian sipunculan worms from southwest China

We report the discovery of sipunculan worms from the Lower Cambrian Maotianshan Shale, near Kunming (southwest China). Their sipunculan identity is evidenced by the general morphology of the animals (sausage–shaped body with a slender retractable introvert and a wider trunk) and by other features, both external (e.g. perioral crown of tentacles, and hooks, papillae and wrinkle rings on the body surface) and internal (U–shaped gut, and the anus opening near the introvert–trunk junction). The three fossil forms (Archaeogolfingia caudata gen. et sp. nov., Cambrosipunculus tentaculatus gen. et sp. nov. and Cambrosipunculus sp.) have striking similarities to modern sipunculans, especially the Golfingiidae to which their evolutionary relationships are discussed. This study suggests that most typical features of extant sipunculans have undergone only limited changes since the Early Cambrian, thus indicating a possible evolutionary stasis over the past 520 Myr.

Diverse transitional giant fleas from the Mesozoic era of China

Fleas are one of the major lineages of ectoparasitic insects and are now highly specialized for feeding on the blood of birds or mammals. This has isolated them among holometabolan insect orders, although they derive from the Antliophora (scorpionflies and true flies). Like most ectoparasitic lineages, their fossil record is meagre and confined to Cenozoic-era representatives of modern families, so that we lack evidence of the origins of fleas in the Mesozoic era. The origins of the first recognized Cretaceous stem-group flea, Tarwinia, remains highly controversial. Here we report fossils of the oldest definitive fleas—giant forms from the Middle Jurassic and Early Cretaceous periods of China. They exhibit many defining features of fleas but retain primitive traits such as non-jumping hindlegs. More importantly, all have stout and elongate sucking siphons for piercing the hides of their hosts, implying that these fleas may be rooted among the pollinating ‘long siphonate’ scorpionflies of the Mesozoic. Their special morphology suggests that their earliest hosts were hairy or feathered ‘reptilians’, and that they radiated to mammalian and bird hosts later in the Cenozoic.

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 origin of crustaceans: new evidence from the Early Cambrian of China.

One of the smallest arthropods recently discovered in the Early Cambrian Maotianshan Shale Lagerstätte is described. Ercaia gen. nov. has an untagmatized trunk bearing serially repeated biramous appendages (long and segmented endopods and flap–like exopods), a head with an acron bearing stalked lateral eyes and a sclerite and two pairs of antennae. The position of this 520 million–year–old tiny arthropod within the Crustacea is supported by several anatomical features: (i) a head with five pairs of appendages including two pairs of antennae, (ii) highly specialized antennae (large setose fans with a possible function in feeding), and (iii) specialized last trunk appendages (segmented pediform structures fringed with setae). The segmentation pattern of Ercaia (5 head and 13 trunk) is close to that of Maxillopoda but lacks the trunk tagmosis of modern representatives of the group. Ercaia is interpreted as a possible derivative of the stem group Crustacea. Ercaia is likely to have occupied an ecological niche similar to those of some Recent meiobenthic organisms (e.g. copepods living in association with sediment). This new fossil evidence supports the remote ancestry of crustaceans well before the Late Cambrian and shows, along with other fossil data (mainly Early Cambrian in China), that a variety of body plans already coexisted among the primitive crustacean stock.

Mantophasmatodea now in the Jurassic

The Mantophasmatodea is the most recently discovered insect order. The fossil records of all other ‘polyneopteran’ orders extend far in the past, but the current absence of pre-Cenozoic fossils of the Mantophasmatodea contradicts a long evolutionary history, which has to be assumed from the morphological distinctness of the group. In this paper, we report the first Mesozoic evidence of a mantophasmatodean from the Middle Jurassic of Daohugou, Inner Mongolia, China. Furthermore, the new fossil shares apomorphic characters with Cenozoic and recent Mantophasmatodea, suggesting a longer evolutionary history of this order.

Amphibious flies and paedomorphism in the Jurassic period

The species of the Strashilidae (strashilids) have been the most perplexing of fossil insects from the Jurassic period of Russia and China. They have been widely considered to be ectoparasites of pterosaurs or feathered dinosaurs, based on the putative presence of piercing and sucking mouthparts and hind tibio-basitarsal pincers purportedly used to fix onto the host’s hairs or feathers. Both the supposed host and parasite occur in the Daohugou beds from the Middle Jurassic epoch of China (approximately 165 million years ago). Here we analyse the morphology of strashilids from the Daohugou beds, and reach markedly different conclusions; namely that strashilids are highly specialized flies (Diptera) bearing large membranous wings, with substantial sexual dimorphism of the hind legs and abdominal extensions. The idea that they belong to an extinct order is unsupported, and the lineage can be placed within the true flies. In terms of major morphological and inferred behavioural features, strashilids resemble the recent (extant) and relict members of the aquatic fly family Nymphomyiidae. Their ontogeny are distinguished by the persistence in adult males of larval abdominal respiratory gills, representing a unique case of paedomorphism among endopterygote insects. Adult strashilids were probably aquatic or amphibious, shedding their wings after emergence and mating in the water.

Glypholomatine Rove Beetles (Coleoptera: Staphylinidae): a Southern Hemisphere Recent Group Recorded from the Middle Jurassic of China

Abstract A new fossil rove beetle, Juroglypholoma antiquum n. gen. n. sp., is described and figured based on a well-preserved specimen from the Middle Jurassic Daohugou biota (ca. 165 Ma), Inner Mongolia, northeastern China. It represents the first fossil belonging to one of the smallest and latest recognized staphylinid subfamilies, Glypholomatinae, which is now endemic to the Southern Hemisphere. The new genus is assigned to Glypholomatinae based on its body shape and size, clubbed antennae, relatively long elytra, abdominal intersegmental membranes with brick-wall-like pattern, metacoxae slightly excavate to receive the short metafemora, and paired curved ridges in the anterolateral margins of sternites IV–VI. It can be easily separated from the extant genera Glypholoma and Proglypholoma by a combination of shorter elytra with apical four abdominal segments exposed; and antennomeres 1 and 2 normal, not dilated, apical three antennomeres forming a slight club. The first discovery of a new species from the Middle Jurassic of China illustrates the antiquity of Glypholomatinae, and indicates that the Omaliine group of subfamilies had already originated by the Middle Jurassic.

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.

Early origin of parental care in Mesozoic carrion beetles.

Significance We report on the unique discovery of Jurassic and Cretaceous carrion beetles (Silphidae) from China and Myanmar, early relatives of one of the most protected of beetle species in North America, and which clearly preserve evidence indicative of complex parental care. This finding represents the earliest evidence of parental care, a behavioral repertoire that is the first step in the development of truly social behavior and one that is intensely studied by ecologists, ethologists, and evolutionary biologists alike. Our fossils clearly span the origins of parent–offspring communication and allow us to provide a robust estimate of the time of origin for this complex behavior. The reconstruction and timing of the early stages of social evolution, such as parental care, in the fossil record is a challenge, as these behaviors often do not leave concrete traces. One of the intensely investigated examples of modern parental care are the modern burying beetles (Silphidae: Nicrophorus), a lineage that includes notable endangered species. Here we report diverse transitional silphids from the Mesozoic of China and Myanmar that provide insights into the origins of parental care. Jurassic silphids from Daohugou, sharing many defining characters of Nicrophorinae, primitively lack stridulatory files significant for parental care communications; although morphologically similar, Early Cretaceous nicrophorines from the Jehol biota possess such files, indicating that a system of parental care had evolved by this early date. More importantly, burying beetles of the genus Nicrophorus have their earliest first record in mid-Cretaceous Burmese amber, and document early evolution of elaborate biparental care and defense of small vertebrate carcasses for their larvae. Parental care in the Early Cretaceous may have originated from competition between silphids and their predators. The rise of the Cretaceous Nicrophorinae implies a biology similar to modern counterparts that typically feed on carcasses of small birds and mammals.