Symbiosis between Cretaceous dinosaurs and feather-feeding beetles.

Extant terrestrial vertebrates, including birds, have a panoply of symbiotic relationships with many insects and arachnids, such as parasitism or mutualism. Yet, identifying arthropod-vertebrate symbioses in the fossil record has been based largely on indirect evidence; findings of direct association between arthropod guests and dinosaur host remains are exceedingly scarce. Here, we present direct and indirect evidence demonstrating that beetle larvae fed on feathers from an undetermined theropod host (avian or nonavian) 105 million y ago. An exceptional amber assemblage is reported of larval molts (exuviae) intimately associated with plumulaceous feather and other remains, as well as three additional amber pieces preserving isolated conspecific exuviae. Samples were found in the roughly coeval Spanish amber deposits of El Soplao, San Just, and Peñacerrada I. Integration of the morphological, systematic, and taphonomic data shows that the beetle larval exuviae, belonging to three developmental stages, are most consistent with skin/hide beetles (family Dermestidae), an ecologically important group with extant keratophagous species that commonly inhabit bird and mammal nests. These findings show that a symbiotic relationship involving keratophagy comparable to that of beetles and birds in current ecosystems existed between their Early Cretaceous relatives.

Evolutionary history of interactions among terrestrial arthropods.

The study of terrestrial arthopod fossils preserved with microscopic fidelity in amber and as permineralized replicas has been revolutionized by CT scanning. Fine preservation facilitates phylogenetic interpretation of fossils, but molecular divergence-time models still commonly use insufficient fossil calibrations, skewing estimates away from the direct (i.e. fossil, morphological) evidence. Interactions among terrestrial arthropods (predation, parasitoidism; phoresy, social symbionts) are briefly reviewed from the fossil record. Predation is the oldest and most widespread, originating with arachnids since probably the Silurian. The first phoretic arthropods were probably mites (Acari). Parasitoidism extends to the early Jurassic ~200 mya, with four main episodes proposed by [1•]. 100-myo Burmese amber, the most diverse Cretaceous paleobiota, is unique for our understanding of insect eusociality and interrelationships among terrestrial arthropods. Eusocial insect colonies are ecological sinks for thousands of symbiont species; ages of the major eusocial groups and some of their nest symbionts are discussed. Fossilized arthropod interrelationships in Miocene Dominican amber are presented as visual exemplars.

Another Laurasian connection in the Early Eocene of India: Myrmecarchaea spiders (Araneae, Archaeidae).

The first fossil Archaeidae in Cambay amber from India, of Eocene age, is documented. The inclusion is a spider exuvium and is placed as Myrmecarchaea based on the presence of elongated legs, a slightly elongated pedicel with lateral spurs, and a diastema between coxae III and IV that is similar to M.antecessor from Oise amber. The previous occurrences of the genus are from Baltic and Oise amber, both of Eocene age. Because most spiders, including Archaeidae, only molt as juveniles, the exuvium does not have adult features nor have distinct species-specific features, and a new taxon is not erected. This new record further extends the distribution of the family and genus to India 50-52 million years ago. Myrmecarchaea in Indian Cambay amber provides additional evidence that India in the Early Eocene had affinities with the Palearctic mainland rather than showing Gondwanan insularity.

Flowers of Apocynaceae in amber from the early Eocene of India.

PREMISE: Early Eocene ambers of the Cambay lignite in Gujarat, India, are well known for their diverse insect fauna and dispersed pollen, but the included flowers have received limited attention. The fossil record of Apocynaceae is relatively poor, and the distinctive floral characters of this family have not been recognized in the fossil record before. METHODS: Remains of tiny flowers in amber were studied by micro-CT scanning, reflected light, and epifluorescence microscopy. RESULTS: Flowers of Maryendressantha succinifera gen. et. sp. n. have actinomorphic, pentamerous, tubular corollas 2.2-2.3 mm wide, and 1.7-2.1 mm deep with sinistrorse aestivation and androecia consisting of a whorl of five stamens attached by short filaments to the lower half of the corolla tube. Anthers are ovate, rounded basally and apically tapered with their connectives convergent with one another in a conical configuration. The pollen is globose, psilate, tricolporate, and very small (10-11 µm). The combined characters indicate a position within the grade known as subfamily Rauvolfioideae. CONCLUSIONS: These fossils, as the oldest remains of Rauvolfioids, complement the fossil records of Apocynoid and Asclepioid fossil seeds from other regions, demonstrating that the Apocynaceae were well established by the early Eocene, mostly consistent with prior divergence estimates for the phylogeny of this family. Potential pollinators, also preserved in the Cambay amber, include mosquitos, gnats, small moths, and stingless bees.

A Revision of the Drosophila spinipes Species Group (Diptera: Drosophilidae).

Two African drosophilids have distinctive protarsal spines in both sexes: Drosophila spinipes Lamb, 1914 from the Seychelles and D. suma Burla, 1954 from the Ivory Coast. Both were later classified in the genus Hirtodrosophila Duda of the Zygothrica genus group, and suma synonymized under spinipes by Tsacas (2006). We resurrect suma from synonymy, define the spinipes species group, and add seven new species in the group from Africa and Madagascar: Drosophila cameroonensis n. sp., D. freidbergi n. sp., D. hypandrilata n. sp., D. jambiya n. sp., D. malagasy n. sp., D. nigrospinipes n. sp., and D. phalloserra n. sp. Another four species are reported but not described. Detailed morphology informs that these anthophilous flies do not belong to the Zygothrica genus group, and they are returned to the genus Drosophila (unplaced to subgenus), albeit primitive members with some very distinctive specialized features. All distribution records, published and new, are presented along with a key to all nine named species.

Transcriptomes reveal expression of hemoglobins throughout insects and other Hexapoda.

Insects have long been thought to largely not require hemoglobins, with some notable exceptions like the red hemolymph of chironomid larvae. The tubular, branching network of tracheae in hexapods is traditionally considered sufficient for their respiration. Where hemoglobins do occur sporadically in plants and animals, they are believed to be either convergent, or because they are ancient in origin and their expression is lost in many clades. Our comprehensive analysis of 845 Hexapod transcriptomes, totaling over 38 Gbases, revealed the expression of hemoglobins in all 32 orders of hexapods, including the 29 recognized orders of insects. Discovery and identification of 1333 putative hemoglobins were achieved with target-gene BLAST searches of the NCBI TSA database, verifying functional residues, secondary- and tertiary-structure predictions, and localization predictions based on machine learning. While the majority of these hemoglobins are intracellular, extracellular ones were recovered in 38 species. Gene trees were constructed via multiple-sequence alignments and phylogenetic analyses. These indicate duplication events within insects and a monophyletic grouping of hemoglobins outside other globin clades, for which we propose the term insectahemoglobins. These hemoglobins are phylogenetically adjacent and appear structurally convergent with the clade of chordate myoglobins, cytoglobins, and hemoglobins. Their derivation and co-option from early neuroglobins may explain the widespread nature of hemoglobins in various kingdoms and phyla. These results will guide future work involving genome comparisons to transcriptome results, experimental investigations of gene expression, cell and tissue localization, and gas binding properties, all of which are needed to further illuminate the complex respiratory adaptations in insects.

Morphological stasis in the first myxomycete from the Mesozoic, and the likely role of cryptobiosis.

Myxomycetes constitute a group within the Amoebozoa well known for their motile plasmodia and morphologically complex fruiting bodies. One obstacle hindering studies of myxomycete evolution is that their fossils are exceedingly rare, so evolutionary analyses of this supposedly ancient lineage of amoebozoans are restricted to extant taxa. Molecular data have significantly advanced myxomycete systematics, but the evolutionary history of individual lineages and their ecological adaptations remain unknown. Here, we report exquisitely preserved myxomycete sporocarps in amber from Myanmar, ca. 100 million years old, one of the few fossil myxomycetes, and the only definitive Mesozoic one. Six densely-arranged stalked sporocarps were engulfed in tree resin while young, with almost the entire spore mass still inside the sporotheca. All morphological features are indistinguishable from those of the modern, cosmopolitan genus Stemonitis, demonstrating that sporocarp morphology has been static since at least the mid-Cretaceous. The ability of myxomycetes to develop into dormant stages, which can last years, may account for the phenotypic stasis between living Stemonitis species and this fossil one, similar to the situation found in other organisms that have cryptobiosis. We also interpret Stemonitis morphological stasis as evidence of strong environmental selection favouring the maintenance of adaptations that promote wind dispersal.

Direct evidence for eudicot pollen-feeding in a Cretaceous stinging wasp (Angiospermae; Hymenoptera, Aculeata) preserved in Burmese amber.

Angiosperms and their insect pollinators form a foundational symbiosis, evidence for which from the Cretaceous is mostly indirect, based on fossils of insect taxa that today are anthophilous, and of fossil insects and flowers that have apparent anthophilous and entomophilous specializations, respectively. We present exceptional direct evidence preserved in mid-Cretaceous Burmese amber, 100 mya, for feeding on pollen in the eudicot genus Tricolporoidites by a basal new aculeate wasp, Prosphex anthophilos, gen. et sp. nov., in the lineage that contains the ants, bees, and other stinging wasps. Plume of hundreds of pollen grains wafts from its mouth and an apparent pollen mass was detected by micro-CT in the buccal cavity: clear evidence that the wasp was foraging on the pollen. Eudicots today comprise nearly three-quarters of all angiosperm species. Prosphex feeding on Tricolporoidites supports the hypothesis that relatively small, generalized insect anthophiles were important pollinators of early angiosperms.

Remarkable new fossil species of Schistostoma Becker (Diptera: Dolichopodidae: Microphorinae) from mid-Cretaceous Burmese amber.

Two closely related and distinctive species of Schistostoma Becker, i.e. Schistostoma burmanicum sp. nov. and Schistostoma foliatum sp. nov., are described from two male specimens preserved in mid-Cretaceous Burmese amber and recorded as the first known fossil representatives of this extant genus of Microphorinae. Both species possess greatly enlarged lamellate fore tibiae and modified leg chaetotaxy that are presumably male secondary sexual features. The generic limits of Schistostoma are briefly discussed and a rationale for the inclusion of these new species is provided.

Rediscovery, redescription, and reclassification of the rare and unusual fly Pyrgometopa penicillata Kertész (Diptera: Drosophilidae).

For slightly more than a century only the type specimen has been known for Pyrgometopa penicillata, a monotypic genus of Drosophilidae whose sole species has an ocellar triangle distended into a bizarre tubercle bearing a tuft of large, spine-like bristles in both sexes. Here we report additional specimens of both sexes of the species, recently rediscovered from Brazil, Peru and French Guyana, allowing us to state that Pyrgometopa is a junior synonym for Stegana, a large cosmopolitan genus. A detailed redescription of Stegana penicillata (Kertész) new combination is provided, including new morphological information, like the male and female terminalia, the egg and a short discussion is provided about its hallmark feature.

Amber.

David Grimaldi introduces amber and the fossils contained therein.

Comprehensive inventory of true flies (Diptera) at a tropical site.

Estimations of tropical insect diversity generally suffer from lack of known groups or faunas against which extrapolations can be made, and have seriously underestimated the diversity of some taxa. Here we report the intensive inventory of a four-hectare tropical cloud forest in Costa Rica for one year, which yielded 4332 species of Diptera, providing the first verifiable basis for diversity of a major group of insects at a single site in the tropics. In total 73 families were present, all of which were studied to the species level, providing potentially complete coverage of all families of the order likely to be present at the site. Even so, extrapolations based on our data indicate that with further sampling, the actual total for the site could be closer to 8000 species. Efforts to completely sample a site, although resource-intensive and time-consuming, are needed to better ground estimations of world biodiversity based on limited sampling.

A late Cretaceous fagalean inflorescence preserved in amber from New Jersey.

PREMISE OF THE STUDY: An inflorescence with three pistillate flowers in amber from the early Upper Cretaceous (Turonian, ~90-94 million years ago) of central New Jersey represents the oldest known flowers with features present in an early stem complex of the Fagales. The inflorescence has characteristics of Nothofagaceae, but also has strikingly distinct characters that suggest it is intermediate between Nothofagus and other Fagales. This intermediacy is consistent with its northern hemisphere distribution. METHODS: We investigated this new fossil by comparing it with extant and fossil members of the Fagales using light microscopy and nano-computed tomography. In addition, for exploring its relationships, we mapped the morphological characters onto a widely accepted molecular-based tree of modern basal Fagales using standard methods of character optimization. KEY RESULTS: The phylogenetic position of the fossil inflorescence can be unequivocally determined by the presence of unique features, singly and in combination, that are found only in "basal" members of Fagales. The fossil adds critical information on the features of the early stem Fagales, evolution of the cupule in Nothofagaceae and Fagaceae, and a reasonable biogeographic hypothesis for the differentiation of southern (e.g., Nothofagaceae) and northern hemisphere Fagales. CONCLUSIONS: This new fossil provides insight into the early evolution of Fagales and suggests that early stem Fagales that had not yet differentiated into modern families were present in the Late Cretaceous of North America. Based on available evidence, the fossil is best interpreted as an early stem member of the Fagales, with features that suggest a transition from a more generalized Nothofagus-like fagalean ancestor with some unique presumably plesiomorphic features. The presence of an enlarged perianth and flexuous styles also suggests the possibility of insect pollination, which has been lost in all Fagales with the exception of some members of subfamily Castaneoideae in Fagaceae sensu stricto (which otherwise are very different from this fossil). The poorly developed, bract-like cupule valves of the fossil can be interpreted as primitive (i.e., incipient) or as reduced from more developed cupules that are found in most modern Fagaceae and Nothofagaceae.

Remarkable fly (Diptera) diversity in a patch of Costa Rican cloud forest: Why inventory is a vital science.

Study of all flies (Diptera) collected for one year from a four-hectare (150 x 266 meter) patch of cloud forest at 1,600 meters above sea level at Zurquí de Moravia, San José Province, Costa Rica (hereafter referred to as Zurquí), revealed an astounding 4,332 species. This amounts to more than half the number of named species of flies for all of Central America. Specimens were collected with two Malaise traps running continuously and with a wide array of supplementary collecting methods for three days of each month. All morphospecies from all 73 families recorded were fully curated by technicians before submission to an international team of 59 taxonomic experts for identification.        Overall, a Malaise trap on the forest edge captured 1,988 species or 51% of all collected dipteran taxa (other than of Phoridae, subsampled only from this and one other Malaise trap). A Malaise trap in the forest sampled 906 species. Of other sampling methods, the combination of four other Malaise traps and an intercept trap, aerial/hand collecting, 10 emergence traps, and four CDC light traps added the greatest number of species to our inventory. This complement of sampling methods was an effective combination for retrieving substantial numbers of species of Diptera. Comparison of select sampling methods (considering 3,487 species of non-phorid Diptera) provided further details regarding how many species were sampled by various methods.        Comparison of species numbers from each of two permanent Malaise traps from Zurquí with those of single Malaise traps at each of Tapantí and Las Alturas, 40 and 180 km distant from Zurquí respectively, suggested significant species turnover. Comparison of the greater number of species collected in all traps from Zurquí did not markedly change the degree of similarity between the three sites, although the actual number of species shared did increase.        Comparisons of the total number of named and unnamed species of Diptera from four hectares at Zurquí is equivalent to 51% of all flies named from Central America, greater than all the named fly fauna of Colombia, equivalent to 14% of named Neotropical species and equal to about 2.7% of all named Diptera worldwide. Clearly the number of species of Diptera in tropical regions has been severely underestimated and the actual number may surpass the number of species of Coleoptera.        Various published extrapolations from limited data to estimate total numbers of species of larger taxonomic categories (e.g., Hexapoda, Arthropoda, Eukaryota, etc.) are highly questionable, and certainly will remain uncertain until we have more exhaustive surveys of all and diverse taxa (like Diptera) from multiple tropical sites.        Morphological characterization of species in inventories provides identifications placed in the context of taxonomy, phylogeny, form, and ecology. DNA barcoding species is a valuable tool to estimate species numbers but used alone fails to provide a broader context for the species identified.

Publisher Correction: Ticks parasitised feathered dinosaurs as revealed by Cretaceous amber assemblages.

The originally published version of this Article was updated shortly after publication to add the word 'Ticks' to the title, following its inadvertent removal during the production process. This has now been corrected in both the PDF and HTML versions of the Article.

parasitised feathered dinosaurs as revealed by Cretaceous amber assemblages.

Ticks are currently among the most prevalent blood-feeding ectoparasites, but their feeding habits and hosts in deep time have long remained speculative. Here, we report direct and indirect evidence in 99 million-year-old Cretaceous amber showing that hard ticks and ticks of the extinct new family Deinocrotonidae fed on blood from feathered dinosaurs, non-avialan or avialan excluding crown-group birds. A †Cornupalpatum burmanicum hard tick is entangled in a pennaceous feather. Two deinocrotonids described as †Deinocroton draculi gen. et sp. nov. have specialised setae from dermestid beetle larvae (hastisetae) attached to their bodies, likely indicating cohabitation in a feathered dinosaur nest. A third conspecific specimen is blood-engorged, its anatomical features suggesting that deinocrotonids fed rapidly to engorgement and had multiple gonotrophic cycles. These findings provide insight into early tick evolution and ecology, and shed light on poorly known arthropod-vertebrate interactions and potential disease transmission during the Mesozoic.

First fossil of an oestroid fly (Diptera: Calyptratae: Oestroidea) and the dating of oestroid divergences.

Calyptrate flies include about 22,000 extant species currently classified into Hippoboscoidea (tsetse, louse, and bat flies), the muscoid grade (house flies and relatives) and the Oestroidea (blow flies, bot flies, flesh flies, and relatives). Calyptrates are abundant in nearly all terrestrial ecosystems, often playing key roles as decomposers, parasites, parasitoids, vectors of pathogens, and pollinators. For oestroids, the most diverse group within calyptrates, definitive fossils have been lacking. The first unambiguous fossil of Oestroidea is described based on a specimen discovered in amber from the Dominican Republic. The specimen was identified through digital dissection by CT scans, which provided morphological data for a cladistic analysis of its phylogenetic position among extant oestroids. The few known calyptrate fossils were used as calibration points for a molecular phylogeny (16S, 28S, CAD) to estimate the timing of major diversification events among the Oestroidea. Results indicate that: (a) the fossil belongs to the family Mesembrinellidae, and it is identified and described as Mesembrinella caenozoica sp. nov.; (b) the mesembrinellids form a sister clade to the Australian endemic Ulurumyia macalpinei (Ulurumyiidae) (McAlpine's fly), which in turn is sister to all remaining oestroids; (c) the most recent common ancestor of extant Calyptratae lived just before the K-Pg boundary (ca. 70 mya); and (d) the radiation of oestroids began in the Eocene (ca. 50 mya), with the origin of the family Mesembrinellidae dated at ca. 40 mya. These results provide new insight into the timing and rate of oestroid diversification and highlight the rapid radiation of some of the most diverse and ecologically important families of flies. ZooBank accession number-urn:lsid:zoobank.org:pub:0DC5170B-1D16-407A-889E-56EED3FE3627.

Lygistorrhinidae (Diptera: Bibionomorpha: Sciaroidea) in early Eocene Cambay amber.

One new genus and three new species of Lygistorrhinidae in early Eocene Cambay amber from India are described, which significantly increases our knowledge about this group in the Eocene. Lygistorrhina indica n. sp. is the oldest fossil known from this extant genus. Indorrhina sahnii n. gen. et sp. shows morphological similarities to each of the two extant genera Lygistorrhina and Asiorrhina. Palaeognoriste orientale is the third species known from a group that has only been recorded from Eocene Baltic amber before. The latter finding reveals faunal links between Cambay amber and the probably slightly younger Baltic amber, adding further evidence that faunal exchange between Europe/Asia and India took place before the formation of Cambay amber.

The Cretaceous Fossil Burmaculex antiquus Confirmed as the Earliest Known Lineage of Mosquitoes (Diptera: Culicidae).

A second female of mid-Cretaceous Burmaculex antiquus Borkent & Grimaldi, preserved in 99 myo Burmese amber, and the oldest known member of the Culicidae, is described in detail. Although generally opaque and distorted, some character states are added or refined. The discovery of well-developed scales on the legs shows that this feature must now be considered a synapomorphy of both the fossil and all extant members of the family. Previously described synapomorphies and further interpretation here confirm the phylogenetic position of this fossil as the sister group to extant and all known fossil Culicidae. It is placed in the new subfamily Burmaculicinae.