Mesozoic evolution of cicadas and their origins of vocalization and root feeding.

Extant cicada (Hemiptera: Cicadoidea) includes widely distributed Cicadidae and relictual Tettigarctidae, with fossils ascribed to these two groups based on several distinct, minimally varying morphological differences that define their extant counterparts. However, directly assigning Mesozoic fossils to modern taxa may overlook the role of unique and transitional features provided by fossils in tracking their early evolutionary paths. Here, based on adult and nymphal fossils from mid-Cretaceous Kachin amber of Myanmar, we explore the phylogenetic relationships and morphological disparities of fossil and extant cicadoids. Our results suggest that Cicadidae and Tettigarctidae might have diverged at or by the Middle Jurassic, with morphological evolution possibly shaped by host plant changes. The discovery of tymbal structures and anatomical analysis of adult fossils indicate that mid-Cretaceous cicadas were silent as modern Tettigarctidae or could have produced faint tymbal-related sounds. The discovery of final-instar nymphal and exuviae cicadoid fossils with fossorial forelegs and piercing-sucking mouthparts indicates that they had most likely adopted a subterranean lifestyle by the mid-Cretaceous, occupying the ecological niche of underground feeding on root. Our study traces the morphological, behavioral, and ecological evolution of Cicadoidea from the Mesozoic, emphasizing their adaptive traits and interactions with their living environments.

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.

A new method for examining the co-occurrence network of fossil assemblages.

Currently, studies of ancient faunal community networks have been based mostly on uniformitarian and functional morphological evidence. As an important source of data, taphonomic evidence offers the opportunity to provide a broader scope for understanding palaeoecology. However, palaeoecological research methods based on taphonomic evidence are relatively rare, especially for body fossils in lacustrine sediments. Such fossil communities are not only affected by complex transportation and selective destruction in the sedimentation process, they also are strongly affected by time averaging. Historically, it has been believed that it is difficult to study lacustrine entombed fauna by a small-scale quadrat survey. Herein, we developed a software, the TaphonomeAnalyst, to study the associational network of lacustrine entombed fauna, or taphocoenosis. TaphonomeAnalyst allows researchers to easily perform exploratory analyses on common abundance profiles from taphocoenosis data. The dataset for these investigations resulted from fieldwork of the latest Middle Jurassic Jiulongshan Formation near Daohugou Village, in Ningcheng County of Inner Mongolia, China, spotlighting the core assemblage of the Yanliao Fauna. Our data included 27,000 fossil specimens of animals from this deposit, the Yanliao Fauna, whose analyses reveal sedimentary environments, taphonomic conditions, and co-occurrence networks of this highly studied assemblage, providing empirically robust and statistically significant evidence for multiple Yanliao habitats.

The associated evolution of raptorial foreleg and mantispid diversification during 200 million years.

Mantispidae have developed multidimensional specializations of predation that are leveraged by trade-offs involving attack properties, which is revealed by interdisciplinary analyses of phylogeny, morphometrics, and mechanical modeling. The lineage diversification was stimulated by its raptorial foreleg evolution, and was influenced by the ecosystem of corresponding periods, involving biotic and physical factors.

Endophytic ancestors of modern leaf miners may have evolved in the Late Carboniferous.

Endophytic feeding behaviors, including stem borings and galling, have been observed in the fossil record from as early as the Devonian and involve the consumption of a variety of plant (and fungal) tissues. Historically, the exploitation of internal stem tissues through galling has been well documented as emerging during the Pennsylvanian (c. 323-299 million years ago (Ma)), replaced during the Permian by galling of foliar tissues. However, leaf mining, a foliar endophytic behavior that today is exhibited exclusively by members of the four hyperdiverse holometabolous insect orders, has been more sparsely documented, with confirmed examples dating back only to the Early Triassic (c. 252-250 Ma). Here, we describe a trace fossil on seed-fern foliage from the Rhode Island Formation of Massachusetts, USA, representing the earliest indication of a general, endophytic type of feeding damage and dating from the Middle Pennsylvanian (c. 312 Ma). Although lacking the full features of Mesozoic leaf mines, this specimen provides evidence of how endophytic mining behavior may have originated. It sheds light on the evolutionary transition to true foliar endophagy, contributes to our understanding of the behaviors of early holometabolous insects, and enhances our knowledge of macroevolutionary patterns of plant-insect interactions.

Insect herbivore and fungal communities on Agathis (Araucariaceae) from the latest Cretaceous to Recent.

Agathis (Araucariaceae) is a genus of broadleaved conifers that today inhabits lowland to upper montane rainforests of Australasia and Southeast Asia. A previous report showed that the earliest known fossils of the genus, from the early Paleogene and possibly latest Cretaceous of Patagonian Argentina, host diverse assemblages of insect and fungal associations, including distinctive leaf mines. Here, we provide complete documentation of the fossilized Agathis herbivore communities from Cretaceous to Recent, describing and comparing insect and fungal damage on Agathis across four latest Cretaceous to early Paleogene time slices in Patagonia with that on 15 extant species. Notable fossil associations include various types of external foliage feeding, leaf mines, galls, and a rust fungus. In addition, enigmatic structures, possibly armored scale insect (Diaspididae) covers or galls, occur on Agathis over a 16-million-year period in the early Paleogene. The extant Agathis species, throughout the range of the genus, are associated with a diverse array of mostly undescribed damage similar to the fossils, demonstrating the importance of Agathis as a host of diverse insect herbivores and pathogens and their little-known evolutionary history.

Arthropod and Pathogen Damage on Fossil and Modern Plants: Exploring the Origins and Evolution of Herbivory on Land.

The use of the functional feeding group-damage type system for analyzing arthropod and pathogen interactions with plants has transformed our understanding of herbivory in fossil plant assemblages by providing data, analyses, and interpretation of the local, regional, and global patterns of a 420-Myr history. The early fossil record can be used to answer major questions about the oldest evidence for herbivory, the early emergence of herbivore associations on land plants, and later expansion on seed plants. The subsequent effects of the Permian-Triassic ecological crisis on herbivore diversity, the resulting formation of biologically diverse herbivore communities on gymnosperms, and major shifts in herbivory ensuing from initial angiosperm diversification are additional issues that need to be addressed. Studies ofherbivory resulting from more recent transient spikes and longer-term climate trends provide important data that are applied to current global change and include herbivore community responses to latitude, altitude, and habitat. Ongoing paleoecological themes remaining to be addressed include the antiquity of modern interactions, differential herbivory between ferns and angiosperms, and origins of modern tropical forests. The expansion of databases that include a multitude of specimens; improvements in sampling strategies; development of new analytical methods; and, importantly, the ability to address conceptually stimulating ecological and evolutionary questions have provided new impetus in this rapidly advancing field.

Sampling bias and the robustness of ecological metrics for plant-damage-type association networks.

Plants and their insect herbivores have been a dominant component of the terrestrial ecological landscape for the past 410 million years and feature intricate evolutionary patterns and co-dependencies. A complex systems perspective allows for both detailed resolution of these evolutionary relationships as well as comparison and synthesis across systems. Using proxy data of insect herbivore damage (denoted by the damage type or DT) preserved on fossil leaves, functional bipartite network representations provide insights into how plant-insect associations depend on geological time, paleogeographical space, and environmental variables such as temperature and precipitation. However, the metrics measured from such networks are prone to sampling bias. Such sensitivity is of special concern for plant-DT association networks in paleontological settings where sampling effort is often severely limited. Here, we explore the sensitivity of functional bipartite network metrics to sampling intensity and identify sampling thresholds above which metrics appear robust to sampling effort. Across a broad range of sampling efforts, we find network metrics to be less affected by sampling bias and/or sample size than richness metrics, which are routinely used in studies of fossil plant-DT interactions. These results provide reassurance that cross-comparisons of plant-DT networks offer insights into network structure and function and support their widespread use in paleoecology. Moreover, these findings suggest novel opportunities for using plant-DT networks in neontological terrestrial ecology to understand functional aspects of insect herbivory across geological time, environmental perturbations, and geographic space.

Correction: Insect herbivory on Catula gettyi gen. et sp. nov. (Lauraceae) from the Kaiparowits Formation (Late Cretaceous, Utah, USA).

[This corrects the article DOI: 10.1371/journal.pone.0261397.].

Data, metrics, and methods for arthropod and fungal herbivory at the dawn of angiosperm diversification: The Rose Creek plant assemblage of Nebraska, U.S.A.

The data presented in this article are related to the research article titled "Arthropod and fungal herbivory at the dawn of angiosperm diversification: The Rose Creek plant assemblage of Nebraska, U.S.A." (Xiao et al., 2021). These data correspond to an examination of arthropod and fungal herbivory on 2084 plant specimens from the Early Cretaceous (late Albian) Rose Creek locality of southeastern Nebraska, USA. Ten datasets have been assembled to describe and contextualize the diversity and intensity of herbivory at Rose Creek, as documented in Appendices of the online supplementary material. Appendices S4 and S5 provide a list and the frequency distributions by major clade and species/morphotype of all plant taxa examined. Appendix S6 outlines general procedures for documenting herbivory on plants and how the data was acquired. Appendix S9a and S9b provide rarefaction analyses for plant taxa to demonstrate sampling sufficiency, which is paralleled by rarefaction analyses of Appendix S9c and S9d that indicate sampling of damage types are robust. The comprehensive dataset of Appendix S12 lists plant taxa horizontally by major clade/group and species/morphotype versus vertically listed feeding classes, functional feeding groups (FFGs) and damage types (DTs). The basic metrics of DTs, feeding event occurrences, DT host-plant specialization, and number of matrix cells are displayed, with data subtotals and totals. This data matrix serves as the central source of data for the study, and records the six metrics of DT richness, DT frequency, DT host-plant specialization, percent of area herbivorized, and feeding event occurrences. Three of these metrics are used for establishing component community structure of the three most herbivorized taxa (Figs 8-10), and the relationships among plant hosts and FFGs in the non-metric multidimensional scaling analysis (Fig. 11) (Xiao et al., 2021). Appendix S15 is a list DTs, with their assigned host-plant specialization of 1 for generalized, 2 for intermediate specificity, and 3 for specialized. Appendix S16 is a table that provides plant surface areas (cm2) and their percentages that have been removed due to herbivory. Appendix S18 provides descriptions and ancillary data for 14 new DTs described from Rose Creek. A listing of the herbivory index (herbivorized surface area divided by total surface area) of plant assemblages and individual plant species in Appendix S19 provides comparisons among Rose Creek, other fossil, and modern plant assemblages. Lastly, Appendix S23 lists from the literature of arthropod species forming the well-documented herbivore component communities of five modern plant species to the three most herbivorized taxa at Rose Creek shown in Fig. 12. Some of the metrics used to quantitatively measure the diversity and intensity of herbivory are recent, such as feeding event occurrences, whereas others such as herbivorized surface area and host-plant specialization values have had a longer use in plant-arthropod studies.

The Invasion of the Land in Deep Time: Integrating Paleozoic Records of Paleobiology, Ichnology, Sedimentology, and Geomorphology.

The invasion of the land was a complex, protracted process, punctuated by mass extinctions, that involved multiple routes from marine environments. We integrate paleobiology, ichnology, sedimentology, and geomorphology to reconstruct Paleozoic terrestrialization. Cambrian landscapes were dominated by laterally mobile rivers with unstable banks in the absence of significant vegetation. Temporary incursions by arthropods and worm-like organisms into coastal environments apparently did not result in establishment of continental communities. Contemporaneous lacustrine faunas may have been inhibited by limited nutrient delivery and high sediment loads. The Ordovician appearance of early land plants triggered a shift in the primary locus of the global clay mineral factory, increasing the amount of mudrock on the continents. The Silurian-Devonian rise of vascular land plants, including the first forests and extensive root systems, was instrumental in further retaining fine sediment on alluvial plains. These innovations led to increased architectural complexity of braided and meandering rivers. Landscape changes were synchronous with establishment of freshwater and terrestrial arthropod faunas in overbank areas, abandoned fluvial channels, lake margins, ephemeral lakes, and inland deserts. Silurian-Devonian lakes experienced improved nutrient availability, due to increased phosphate weathering and terrestrial humic matter. All these changes favoured frequent invasions to permament establishment of jawless and jawed fishes in freshwater habitats and the subsequent tetrapod colonization of the land. The Carboniferous saw rapid diversification of tetrapods, mostly linked to aquatic reproduction, and land plants, including gymnosperms. Deeper root systems promoted further riverbank stabilization, contributing to the rise of anabranching rivers and braided systems with vegetated islands. New lineages of aquatic insects developed and expanded novel feeding modes, including herbivory. Late Paleozoic soils commonly contain pervasive root and millipede traces. Lacustrine animal communities diversified, accompanied by increased food-web complexity and improved food delivery which may have favored permanent colonization of offshore and deep-water lake environments. These trends continued in the Permian, but progressive aridification favored formation of hypersaline lakes, which were stressful for colonization. The Capitanian and end-Permian extinctions affected lacustrine and fluvial biotas, particularly the invertebrate infauna, although burrowing may have allowed some tetrapods to survive associated global warming and increased aridification.

Insect herbivory on Catula gettyi gen. et sp. nov. (Lauraceae) from the Kaiparowits Formation (Late Cretaceous, Utah, USA).

The Upper Cretaceous (Campanian Stage) Kaiparowits Formation of southern Utah, USA, preserves abundant plant, invertebrate, and vertebrate fossil taxa. Taken together, these fossils indicate that the ecosystems preserved in the Kaiparowits Formation were characterized by high biodiversity. Hundreds of vertebrate and invertebrate species and over 80 plant morphotypes are recognized from the formation, but insects and their associations with plants are largely undocumented. Here, we describe a new fossil leaf taxon, Catula gettyi gen et. sp. nov. in the family Lauraceae from the Kaiparowits Formation. Catula gettyi occurs at numerous localities in this deposit that represent ponded and distal floodplain environments. The type locality for C. gettyi has yielded 1,564 fossil leaf specimens of this species, which provides the opportunity to circumscribe this new plant species. By erecting this new genus and species, we are able to describe ecological associations on C. gettyi and place these interactions within a taxonomic context. We describe an extensive archive of feeding damage on C. gettyi caused by herbivorous insects, including more than 800 occurrences of insect damage belonging to five functional feeding groups indicating that insect-mediated damage on this taxon is both rich and abundant. Catula gettyi is one of the best-sampled host plant taxa from the Mesozoic Era, a poorly sampled time interval, and its insect damage is comparable to other Lauraceae taxa from the younger Late Cretaceous Hell Creek Flora of North Dakota, USA.

Insect herbivory immediately before the eclipse of the gymnosperms: The Dawangzhangzi plant assemblage of Northeastern China.

The Early Cretaceous terrestrial revolution involved global shifts from gymnosperm- to angiosperm-dominated floras. However, responses of insect herbivores to these changes remain unexamined. We evaluated 2 176 highly sampled plant specimens representing 62 species/morphotypes from the 126 Ma Dawangzhangzi plant assemblage of Northeastern China. Our study consisted of horsetails, ferns, ginkgoaleans, czekanowskialeans, conifers, and an angiosperm. Their herbivory was evaluated by the functional feeding groups of hole feeding, margin feeding, and surface feeding (ectophytic feeders); piercer and suckers, and ovipositing insects (ectoendophytic feeders); mining, galling, and borings (endophytic feeders); and pathogens, collectively constituting 65 damage types (DTs). The plant assemblage was assessed for herbivory richness by DT richness, component community structure, and DT specialization on plant hosts; for herbivory intensity, it was evaluated for DT frequency, herbivorized surface area, and feeding event occurrences. Using feeding event occurrences, the data supported seven species/morphotypes as most intensely herbivorized: Liaoningocladus boii (76.6%), Czekanowskia sp. 1 (8.4%), Czekanowskia rigida (4.10%), Lindleycladus lanceolatus (3.5%), Ginkgoites sp. 2 (2.0%), Podozamites sp. 1 (1.1%), and Solenites sp. 1 (0.9%). The most herbivorized taxa were pinaleans (conifers), then czekanowskialeans, and lastly ginkgoaleans; the monodominant component community was the conifer Liaoningocladus boii. DT host specialization levels were low. The plant assemblage had an overall low 0.86% of foliage removed by herbivores, explained by physical and chemical antiherbivore defenses, and parasitoid attack. Although Paleozoic, gymnosperm-dominated assemblages had greater herbivory, component community structure of the three most herbivorized taxa are more similar to modern bracken fern and willow than modern gymnosperm taxa.

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.

Persistent biotic interactions of a Gondwanan conifer from Cretaceous Patagonia to modern Malesia.

Many plant genera in the tropical West Pacific are survivors from the paleo-rainforests of Gondwana. For example, the oldest fossils of the Malesian and Australasian conifer Agathis (Araucariaceae) come from the early Paleocene and possibly latest Cretaceous of Patagonia, Argentina (West Gondwana). However, it is unknown whether dependent ecological guilds or lineages of associated insects and fungi persisted on Gondwanan host plants like Agathis through time and space. We report insect-feeding and fungal damage on Patagonian Agathis fossils from four latest Cretaceous to middle Eocene floras spanning ca. 18 Myr and compare it with damage on extant Agathis. Very similar damage was found on fossil and modern Agathis, including blotch mines representing the first known Cretaceous-Paleogene boundary crossing leaf-mine association, external foliage feeding, galls, possible armored scale insect (Diaspididae) covers, and a rust fungus (Pucciniales). The similar suite of damage, unique to fossil and extant Agathis, suggests persistence of ecological guilds and possibly the component communities associated with Agathis since the late Mesozoic, implying host tracking of the genus across major plate movements that led to survival at great distances. The living associations, mostly made by still-unknown culprits, point to previously unrecognized biodiversity and evolutionary history in threatened rainforest ecosystems.

Unlocking the mystery of the mid-Cretaceous Mysteriomorphidae (Coleoptera: Elateroidea) and modalities in transiting from gymnosperms to angiosperms.

The monospecific family Mysteriomorphidae was recently described based on two fossil specimens from the Late Cretaceous Kachin amber of northern Myanmar. The family was placed in Elateriformia incertae sedis without a clear list of characters that define it either in Elateroidea or in Byrrhoidea. We report here four additional adult specimens of the same lineage, one of which was described using a successful reconstruction from a CT-scan analysis to better observe some characters. The new specimens enabled us to considerably improve the diagnosis of Mysteriomorphidae. The family is definitively placed in Elateroidea, and we hypothesize its close relationship with Elateridae. Similarly, there are other fossil families of beetles that are exclusively described from Cretaceous ambers. These lineages may have been evolutionarily replaced by the ecological revolution launched by angiosperms that introduced new co-associations with taxa. These data indicate a macroevolutionary pattern of replacement that could be extended to other insect groups.

Lichen mimesis in mid-Mesozoic lacewings.

Animals mimicking other organisms or using camouflage to deceive predators are vital survival strategies. Modern and fossil insects can simulate diverse objects. Lichens are an ancient symbiosis between a fungus and an alga or a cyanobacterium that sometimes have a plant-like appearance and occasionally are mimicked by modern animals. Nevertheless, lichen models are almost absent in fossil record of mimicry. Here, we provide the earliest fossil evidence of a mimetic relationship between the moth lacewing mimic Lichenipolystoechotes gen. nov. and its co-occurring fossil lichen model Daohugouthallus ciliiferus. We corroborate the lichen affinity of D. ciliiferus and document this mimetic relationship by providing structural similarities and detailed measurements of the mimic's wing and correspondingly the model's thallus. Our discovery of lichen mimesis predates modern lichen-insect associations by 165 million years, indicating that during the mid-Mesozoic, the lichen-insect mimesis system was well established and provided lacewings with highly honed survival strategies.

Many insects mimic other organisms or use camouflage to hide from predators. For example, some modern animals mimic the organism lichens, which are formed from algae and fungus, and grow almost everywhere on Earth, from the Arctic to the desert. The most iconic example of an insect mimicking a species of lichen is the peppered moth. During the industrial revolution, darker colored moths were better at surviving. But when the revolution ended and pollution levels declined, species of lichen began to re-emerge and increase the survival of paler moths. Yet, it is unclear how and when insects first evolved this ingenious survival strategy, as distinctive examples of insects mimicking lichens are missing from fossil records. To answer this question, Fang et al. set out to find fossils of lichen-mimicking insects that occurred at the same time as fossils of lichens. This approach led to the discovery of two new species of lacewing insects and their related species of foliose lichen. Previous work suggested that the foliose lichen, which has a lobe like shape, did not exist more than 65 million years ago. However, the findings of Fang et al. indicate that the foliose lichen existed 165 million years ago during the age of dinosaurs, and therefore arose much earlier than previously thought. The two new species found in north-eastern China, form a new subgroup within the moth lacewing family that Fang et al. have named 'Lichenipolystoechotes'. Close examination of both species of lacewing and the lichen under the microscopy revealed a near perfect match in their appearance. The branching patterns of the insects' wing markings fit the branching patterns of the lichen. Taken together, these findings suggest that, not only did lichen mimics exist in the age of the dinosaurs, but that this strategy of using lichen mimicry as a form of survival was already very effective during this time period. This discovery suggests that, 165 million years ago, a micro-ecosystem of lichens and insects existed in north-eastern China. It invites new questions about how that ecosystem worked. For example, how did the lichen benefit from its relationship with lacewing insects? Further investigations could reveal the answers and uncover more interesting insects hidden in the fossil record.

Generalist Pollen-Feeding Beetles during the Mid-Cretaceous.

The Cretaceous fossil record of amber provides a variety of evidence that is essential for greater understanding of early pollination strategies. Here, we describe four pieces of ca. 99-million-year-old (early Cenomanian) Myanmar amber from Kachin containing four closely related genera of short-winged flower beetles (Coleoptera: Kateretidae) associated with abundant pollen grains identified as three distinct palynomorphotypes of the gymnosperm Cycadopites and Praenymphaeapollenites cenomaniensis gen. and sp. nov., a form-taxon of pollen from a basal angiosperm lineage of water lilies (Nymphaeales: Nymphaeaceae). We demonstrate how a gymnosperm to angiosperm plant-host shift occurred during the mid-Cretaceous, from a generalist pollen-feeding family of beetles, which served as a driving mechanism for the subsequent success of flowering plants.

A Cretaceous peak in family-level insect diversity estimated with mark-recapture methodology.

The history of insects' taxonomic diversity is poorly understood. The two most common methods for estimating taxonomic diversity in deep time yield conflicting results: the 'range through' method suggests a steady, nearly monotonic increase in family-level diversity, whereas 'shareholder quorum subsampling' suggests a highly volatile taxonomic history with family-level mass extinctions occurring repeatedly, even at the midpoints of geological periods. The only feature shared by these two diversity curves is a steep increase in standing diversity during the Early Cretaceous. This apparent diversification event occurs primarily during the Aptian, the pre-Cenozoic interval with the most described insect occurrences, raising the possibility that this feature of the diversity curves reflects preservation and sampling biases rather than insect evolution and extinction. Here, the capture-mark-recapture (CMR) approach is used to estimate insects' family-level diversity. This method accounts for the incompleteness of the insect fossil record as well as uneven sampling among time intervals. The CMR diversity curve shows extinctions at the Permian/Triassic and Cretaceous/Palaeogene boundaries but does not contain any mass extinctions within geological periods. This curve also includes a steep increase in diversity during the Aptian, which appears not to be an artefact of sampling or preservation bias because this increase still appears when time bins are standardized by the number of occurrences they contain rather than by the amount of time that they span. The Early Cretaceous increase in family-level diversity predates the rise of angiosperms by many millions of years and can be better attributed to the diversification of parasitic and especially parasitoid insect lineages.

Late Cretaceous domatia reveal the antiquity of plant-mite mutualisms in flowering plants.

Mite houses, or acarodomatia, are found on the leaves of over 2000 living species of flowering plants today. These structures facilitate tri-trophic interactions between the host plant, its fungi or herbivore adversaries, and fungivorous or predaceous mites by providing shelter for the mite consumers. Previously, the oldest acarodomatia were described on a Cenozoic Era fossil leaf dating to 49 Myr in age. Here, we report the first occurrence of Mesozoic Era acarodomatia in the fossil record from leaves discovered in the Upper Cretaceous Kaiparowits Formation (76.6-74.5 Ma) in southern UT, USA. This discovery extends the origin of acarodomatia by greater than 25 Myr, and the antiquity of this plant-mite mutualism provides important constraints for the evolutionary history of acarodomatia on angiosperms.