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.

Evolution of sexual conflict in scorpionflies.

Sexual conflict - opposite reproductive/genetic interests between sexes - can be a significant driver of insect evolution. Scorpionflies (Insecta: Mecoptera) are models in sexual conflict research due to their large variety of mating practices, including coercive behaviour and nuptial gift provisioning. However, the role of palaeontology in sexual conflict studies remains negligible, namely due to the paucity of well-preserved fossils. Here, we describe three male scorpionflies from Cretaceous and Eocene ambers. The structure of notal and postnotal organs is analysed in extant and extinct forms; a depression below the base of the notal organ in different panorpid species spatially matches the anterior fold of the female's wing. Based on disparate abdominal configurations and correlations in extant relatives, we posit that each new fossil taxon had a different mating approach along a nuptial gifting-coercive spectrum. The Eocene specimen possesses extreme female clamping abdominal armature, suggesting a degree of sexual coercion greater than in any other known scorpionfly, extinct or extant. The fossil record of abdominal modifications in male scorpionflies documents a relatively late evolution (Eocene) of long notal organs indicating oppressive behaviour toward a female during mating. Our findings reveal a wider array of mating-related morphological specialisations among extinct Panorpoidea, likely reflecting more diversified past mating strategies and behaviours in this group, and represent first steps towards gaining a deep-time perspective on the evolution of sexual conflict over mating among insects.

Dinosaur bonebed amber from an original swamp forest soil.

Dinosaur bonebeds with amber content, yet scarce, offer a superior wealth and quality of data on ancient terrestrial ecosystems. However, the preserved palaeodiversity and/or taphonomic characteristics of these exceptional localities had hitherto limited their palaeobiological potential. Here, we describe the amber from the Lower Cretaceous dinosaur bonebed of Ariño (Teruel, Spain) using a multidisciplinary approach. Amber is found in both a root layer with amber strictly in situ and a litter layer mainly composed of aerial pieces unusually rich in bioinclusions, encompassing 11 insect orders, arachnids, and a few plant and vertebrate remains, including a feather. Additional palaeontological data-charophytes, palynomorphs, ostracods- are provided. Ariño arguably represents the most prolific and palaeobiologically diverse locality in which fossiliferous amber and a dinosaur bonebed have been found in association, and the only one known where the vast majority of the palaeontological assemblage suffered no or low-grade pre-burial transport. This has unlocked unprecedentedly complete and reliable palaeoecological data out of two complementary windows of preservation-the bonebed and the amber-from the same site.

Earwig fan designing: Biomimetic and evolutionary biology applications.

Technologies to fold structures into compact shapes are required in multiple engineering applications. Earwigs (Dermaptera) fold their fanlike hind wings in a unique, highly sophisticated manner, granting them the most compact wing storage among all insects. The structural and material composition, in-flight reinforcement mechanisms, and bistable property of earwig wings have been previously studied. However, the geometrical rules required to reproduce their complex crease patterns have remained uncertain. Here we show the method to design an earwig-inspired fan by considering the flat foldability in the origami model, as informed by X-ray microcomputed tomography imaging. As our dedicated designing software shows, the earwig fan can be customized into artificial deployable structures of different sizes and configurations for use in architecture, aerospace, mechanical engineering, and daily use items. Moreover, the proposed method is able to reconstruct the wing-folding mechanism of an ancient earwig relative, the 280-million-year-old Protelytron permianum This allows us to propose evolutionary patterns that explain how extant earwigs acquired their wing-folding mechanism and to project hypothetical, extinct transitional forms. Our findings can be used as the basic design guidelines in biomimetic research for harnessing the excellent engineering properties of earwig wings, and demonstrate how a geometrical designing method can reveal morphofunctional evolutionary constraints and predict plausible biological disparity in deep time.

Phloem sap in Cretaceous ambers as abundant double emulsions preserving organic and inorganic residues.

Fossilized remains preserved in amber provide abundant data on the paleobiota surrounding the resin-producing plants, but relatively scarcer information about the resinous sources themselves. Here, dark pseudoinclusions in kidney-shaped amber pieces from the Early Cretaceous (Albian) amber from Spain are studied. This type of fossilized remain, abundant in Cretaceous ambers, was first interpreted as fossilized vacuole-bearing microorganisms, but later regarded as artifactual and probably secreted by the resinous trees, although their origin remained unclear. Using complementary microscopy (light, electron, confocal), spectroscopy (infrared, micro-Raman), mass spectrometry and elemental analysis techniques, we demonstrate that the pseudoinclusions correspond to droplets of phloem sap containing amber spheroids and preserving both organic and inorganic residues consistent with degraded components from the original sap. The amber pieces containing pseudoinclusions are fossilized, resin-in-sap-in-resin double emulsions, showing banding patterns with differential content of resin-in-sap emulsion droplets. Our findings represent the first time fossilized phloem sap, 105 million years old, has been recognized and characterized, and open new lines of paleontological research with taxonomic, taphonomic, physiological and ecological implications.

A mantidfly in Cretaceous Spanish amber provides insights into the evolution of integumentary specialisations on the raptorial foreleg.

Multiple predatory insect lineages have developed a raptorial lifestyle by which they strike and hold prey using modified forelegs armed with spine-like structures and other integumentary specialisations. However, how structures enabling the raptorial function evolved in insects remains largely hypothetical or inferred through phylogeny due to the rarity of meaningful fossils. This is particularly true for mantidflies (Neuroptera: Mantispidae), which have a scarce fossil record mostly based on rock compressions, namely isolated wings. Here, Aragomantispa lacerata gen. et sp. nov. is described from ca. 105-million-year-old San Just amber (Spain), representing the oldest and one of the few mantidflies hitherto described from amber. The fossil shows exquisitely preserved forefemoral spine-like structures composed of integumentary processes each bearing a modified seta, and prostrate setae on foretibiae and foretarsi. The fine morphology of these structures was unknown in fossil mantidflies. An assessment of integumentary specialisations from raptorial forelegs across mantispoid lacewings is provided. The present finding reveals how the specialised foreleg armature associated to the raptorial lifestyle in extant mantidflies was present yet not fully established by the Early Cretaceous, at least in some lineages, and provides palaeontological evidence supporting certain evolutionary patterns of acquisition of integumentary specialisations related to the raptorial function in the group.

A soil-carrying lacewing larva in Early Cretaceous Lebanese amber.

Diverse organisms protect and camouflage themselves using varied materials from their environment. This adaptation and associated behaviours (debris-carrying) are well known in modern green lacewing larvae (Neuroptera: Chrysopidae), mostly due to the widespread use of these immature insects in pest control. However, the evolutionary history of this successful strategy and related morphological adaptations in the lineage are still far from being understood. Here we describe a novel green lacewing larva, Tyruschrysa melqart gen. et sp. nov., from Early Cretaceous Lebanese amber, carrying a preserved debris packet composed by soil particles entangled among specialised setae of extremely elongate tubular tubercles. The new morphotype has features related to the debris-carrying habit that are unknown from extant or extinct green lacewings, namely a high number of tubular tubercle pairs on the abdomen and tubular tubercle setae with mushroom-shaped endings that acted as anchoring points for debris. The current finding expands the diversity of exogenous materials used by green lacewing larvae in deep time, and represents the earliest direct evidence of debris-carrying in the lineage described to date. The debris-carrying larval habit likely played a significant role during the initial phases of diversification of green lacewings.

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.

False Blister Beetles and the Expansion of Gymnosperm-Insect Pollination Modes before Angiosperm Dominance.

During the mid-Cretaceous, angiosperms diversified from several nondiverse lineages to their current global domination [1], replacing earlier gymnosperm lineages [2]. Several hypotheses explain this extensive radiation [3], one of which involves proliferation of insect pollinator associations in the transition from gymnosperm to angiosperm dominance. However, most evidence supports gymnosperm-insect pollinator associations, buttressed by direct evidence of pollen on insect bodies, currently established for four groups: Thysanoptera (thrips), Neuroptera (lacewings), Diptera (flies), and now Coleoptera (beetles). Each group represents a distinctive pollination mode linked to a unique mouthpart type and feeding guild [4-9]. Extensive indirect evidence, based on specialized head and mouthpart morphology, is present for one of these pollinator types, the long-proboscid pollination mode [10], representing minimally ten family-level lineages of Neuroptera, Mecoptera (scorpionflies), and Diptera [8, 10, 11]. A recurring feature uniting these pollinator modes is host associations with ginkgoalean, cycad, conifer, and bennettitalean gymnosperms. Pollinator lineages bearing these pollination modes were categorized into four evolutionary cohorts during the 35-million-year-long angiosperm radiation, each defined by its host-plant associations (gymnosperm or angiosperm) and evolutionary pattern (extinction, continuation, or origination) during this interval [12]. Here, we provide the first direct evidence for one cohort, exemplified by the beetle Darwinylus marcosi, family Oedemeridae (false blister beetles), that had an earlier gymnosperm (most likely cycad) host association, later transitioning onto angiosperms [13]. This association constitutes one of four patterns explaining the plateau of family-level plant lineages generally and pollinating insects specifically during the mid-Cretaceous angiosperm radiation [12].

A defensive behavior and plant-insect interaction in Early Cretaceous amber--The case of the immature lacewing Hallucinochrysa diogenesi.

Amber holds special paleobiological significance due to its ability to preserve direct evidence of biotic interactions and animal behaviors for millions of years. Here we review the finding of Hallucinochrysa diogenesi Pérez-de la Fuente, Delclòs, Peñalver and Engel, 2012, a morphologically atypical larva related to modern green lacewings (Insecta: Neuroptera) that was described in Early Cretaceous amber from the El Soplao outcrop (northern Spain). The fossil larva is preserved with a dense cloud of fern trichomes that corresponds to the trash packet the insect gathered and carried on its back for camouflaging and shielding, similar to that which is done by its extant relatives. This finding supports the prominent role of wildfires in the paleoecosystem and provides direct evidence of both an ancient plant-insect interaction and an early acquisition of a defensive behavior in an insect lineage. Overall, the fossil of H. diogenesi showcases the potential that the amber record offers to reconstruct not only the morphology of fossil arthropods but, more remarkably, their lifestyles and ecological relationships.

Long-Proboscid Flies as Pollinators of Cretaceous Gymnosperms.

The great evolutionary success of angiosperms has traditionally been explained, in part, by the partnership of these plants with insect pollinators. The main approach to understanding the origins of this pervasive relationship has been study of the pollinators of living cycads, gnetaleans, and basal angiosperms. Among the most morphologically specialized living pollinators are diverse, long-proboscid flies. Early such flies include the brachyceran family Zhangsolvidae, previously known only as compression fossils from the Early Cretaceous of China and Brazil. It belongs to the infraorder Stratiomyomorpha, a group that includes the flower-visiting families Xylomyidae and Stratiomyidae. New zhangsolvid specimens in amber from Spain (ca. 105 mega-annum [Ma]) and Myanmar (100 Ma) reveal a detailed proboscis structure adapted to nectivory. Pollen clumped on a specimen from Spain is Exesipollenites, attributed to a Mesozoic gymnosperm, most likely the Bennettitales. Late Mesozoic scorpionflies with a long proboscis have been proposed as specialized pollinators of various extinct gymnosperms, but pollen has never been observed on or in their bodies. The new discovery is a very rare co-occurrence of pollen with its insect vector and provides substantiating evidence that other long-proboscid Mesozoic insects were gymnosperm pollinators. Evidence is thus now gathering that visitors and probable pollinators of early anthophytes, or seed plants, involved some insects with highly specialized morphological adaptations, which has consequences for interpreting the reproductive modes of Mesozoic gymnosperms and the significance of insect pollination in angiosperm success.

Unearthing the secrets of ancient immature insects.

Jurassic fossils of a bizarre fly larva that lived in water as a blood-sucking parasite highlight how much can be learnt from the study of the fossils of immature insects.

Early evolution and ecology of camouflage in insects.

Taxa within diverse lineages select and transport exogenous materials for the purposes of camouflage. This adaptive behavior also occurs in insects, most famously in green lacewing larvae who nestle the trash among setigerous cuticular processes, known as trash-carrying, rendering them nearly undetectable to predators and prey, as well as forming a defensive shield. We report an exceptional discovery of a green lacewing larva in Early Cretaceous amber from Spain with specialized cuticular processes forming a dorsal basket that carry a dense trash packet. The trash packet is composed of trichomes of gleicheniacean ferns, which highlight the presence of wildfires in this early forest ecosystem. This discovery provides direct evidence of an early acquisition of a sophisticated behavioral suite in stasis for over 110 million years and an ancient plant-insect interaction.