Fossil leaves reveal drivers of herbivore functional diversity during the Cenozoic.

Herbivorous arthropods are the most diverse group of multicellular organisms on Earth. The most discussed drivers of their inordinate taxonomic and functional diversity are high niche availability associated with the diversity of host plants and dense niche packing due to host partitioning among herbivores. However, the relative contributions of these two factors to dynamics in the diversity of herbivores throughout Earth's history remain unresolved. Using fossil data on herbivore-induced leaf damage from across the Cenozoic, we infer quantitative bipartite interaction networks between plants and functional feeding types of herbivores. We fit a general model of diversity to these interaction networks and discover that host partitioning among functional groups of herbivores contributed twice as much to herbivore functional diversity as host diversity. These findings indicate that niche packing primarily shaped the dynamics in the functional diversity of herbivores during the past 66 my. Our study highlights how the fossil record can be used to test fundamental theories of biodiversity and represents a benchmark for assessing the drivers of herbivore functional diversity in modern ecosystems.

An integrated leaf trait analysis of two Paleogene leaf floras.

Objectives: This study presents the Integrated Leaf Trait Analysis (ILTA), a workflow for the combined application of methodologies in leaf trait and insect herbivory analyses on fossil dicot leaf assemblages. The objectives were (1) to record the leaf morphological variability, (2) to describe the herbivory pattern on fossil leaves, (3) to explore relations between leaf morphological trait combination types (TCTs), quantitative leaf traits, and other plant characteristics (e.g., phenology), and (4) to explore relations of leaf traits and insect herbivory. Material and Methods: The leaves of the early Oligocene floras Seifhennersdorf (Saxony, Germany) and Suletice-Berand (Ústí nad Labem Region, Czech Republic) were analyzed. The TCT approach was used to record the leaf morphological patterns. Metrics based on damage types on leaves were used to describe the kind and extent of insect herbivory. The leaf assemblages were characterized quantitatively (e.g., leaf area and leaf mass per area (LMA)) based on subsamples of 400 leaves per site. Multivariate analyses were performed to explore trait variations. Results: In Seifhennersdorf, toothed leaves of TCT F from deciduous fossil-species are most frequent. The flora of Suletice-Berand is dominated by evergreen fossil-species, which is reflected by the occurrence of toothed and untoothed leaves with closed secondary venation types (TCTs A or E). Significant differences are observed for mean leaf area and LMA, with larger leaves tending to lower LMA in Seifhennersdorf and smaller leaves tending to higher LMA in Suletice-Berand. The frequency and richness of damage types are significantly higher in Suletice-Berand than in Seifhennersdorf. In Seifhennersdorf, the evidence of damage types is highest on deciduous fossil-species, whereas it is highest on evergreen fossil-species in Suletice-Berand. Overall, insect herbivory tends to be more frequently to occur on toothed leaves (TCTs E, F, and P) that are of low LMA. The frequency, richness, and occurrence of damage types vary among fossil-species with similar phenology and TCT. In general, they are highest on leaves of abundant fossil-species. Discussion: TCTs reflect the diversity and abundance of leaf architectural types of fossil floras. Differences in TCT proportions and quantitative leaf traits may be consistent with local variations in the proportion of broad-leaved deciduous and evergreen elements in the ecotonal vegetation of the early Oligocene. A correlation between leaf size, LMA, and fossil-species indicates that trait variations are partly dependent on the taxonomic composition. Leaf morphology or TCTs itself cannot explain the difference in insect herbivory on leaves. It is a more complex relationship where leaf morphology, LMA, phenology, and taxonomic affiliation are crucial.

Marginal leaf galls on Pliocene leaves from India indicate mutualistic behavior between Ipomoea plants and Eriophyidae mites.

We report a new type of fossil margin galls arranged in a linear series on dicot leaf impressions from the latest Neogene (Pliocene) sediments of the Chotanagpur Plateau, Jharkhand, eastern India. We collected ca. 1500 impression and compression leaf fossils, of which 1080 samples bear arthropod damage referable to 37 different damage types (DT) in the 'Guide to Insect (and Other) Damage Types in Compressed Plant Fossils'. A few leaf samples identified as Ipomoea L. (Convolvulaceae) have specific margin galls that do not match any galling DT previously described. This type of galling is characterized by small, linearly arranged, irregular, sessile, sub-globose, solitary, indehiscent, solid pouch-galls with irregular ostioles. The probable damage inducers of the present galling of the foliar margin might be members of Eriophyidae (Acari). The new type of gall suggests that marginal gall-inducing mites on leaves of Ipomoea did not change their host preference at the genus level since the Pliocene. The development of marginal leaf galling in Ipomoea is linked to extrafloral nectaries that do not offer protection against arthropod galling but indirectly protect the plant against herbivory from large mammals.

Plant-Insect Interactions on Aquatic and Terrestrial Angiosperms from the Latest Albian (Early Cretaceous) of Estercuel (Northeastern Spain) and Their Paleoenvironmental Implications.

Fossils of plant-insect interactions are direct evidence of paleoecological relationships between these two dominant groups in terrestrial ecosystems. We present a variety of plant-insect interactions from the late Early Cretaceous (latest Albian) in the Estercuel locality in northeastern Spain (Iberian Peninsula), affecting two types of terrestrial angiosperms and the basal eudicot Klitzschophyllites, which is one of the oldest putative members of aquatic Ranunculales found to date. The study of these interactions revealed 23 different damage types belonging to eight functional feeding groups (hole feeding, margin feeding, skeletonization, surface feeding, piercing and sucking, mining, oviposition and galling), suggesting these angiosperms were an important source of food and lodging for insects in the Iberian ecosystems during the late Early Cretaceous. Notably, the diversity of damage in the leaves of angiosperms suggests a diverse community of herbivorous insects and a variety of strategies of interactions with plants at the end of the Early Cretaceous in the southwestern Tethys realm.

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.

High acoustic diversity and behavioral complexity of katydids in the Mesozoic soundscape.

Acoustic communication has played a key role in the evolution of a wide variety of vertebrates and insects. However, the reconstruction of ancient acoustic signals is challenging due to the extreme rarity of fossilized organs. Here, we report the earliest tympanal ears and sound-producing system (stridulatory apparatus) found in exceptionally preserved Mesozoic katydids. We present a database of the stridulatory apparatus and wing morphology of Mesozoic katydids and further calculate their probable singing frequencies and analyze the evolution of their acoustic communication. Our suite of analyses demonstrates that katydids evolved complex acoustic communication including mating signals, intermale communication, and directional hearing, at least by the Middle Jurassic. Additionally, katydids evolved a high diversity of singing frequencies including high-frequency musical calls, accompanied by acoustic niche partitioning at least by the Late Triassic, suggesting that acoustic communication might have been an important driver in the early radiation of these insects. The Early-Middle Jurassic katydid transition from Haglidae- to Prophalangopsidae-dominated faunas coincided with the diversification of derived mammalian clades and improvement of hearing in early mammals, supporting the hypothesis of the acoustic coevolution of mammals and katydids. Our findings not only highlight the ecological significance of insects in the Mesozoic soundscape but also contribute to our understanding of how acoustic communication has influenced animal evolution.

Exceptional preservation of internal organs in a new fossil species of freshwater shrimp (Caridea: Palaemonoidea) from the Eocene of Messel (Germany).

A new species of extinct freshwater shrimp was discovered in the Eocene deposit of the Messel Pit Konservat-Lagerstätte. This rare find is represented by only a few specimens, one of which showing exceptionally preserved soft tissues and other internal parts like the stomach with possibly gastric ossicles in place, branchiae, the ovary, and the left mandible, never described in a fossil shrimp. The new species Bechleja brevirostris n. sp. is characterized by a short rostrum bearing 6-8 dorsal spines and one ventral tooth, and long second pereiopods with strong chelae. One additional specimen shows a slightly different morphology and might belong to a different species. The systematic position of the species among the superfamily Palaemonoidea is discussed, as well as implications for the knowledge of the paleoenvironment of Lake Messel and the paleobiogeography of the Eocene.

The First Representative of the Roachoid Family Spiloblattinidae (Insecta, Dictyoptera) from the Late Pennsylvanian of the Iberian Peninsula.

Sysciophlebia 'sp. form Villablino', the first Iberian representative of the Palaeozoic-Early Mesozoic family Spiloblattinidae, is described and illustrated. Its forewing colour pattern is strongly similar to those of the Gzhelian-early-middle Asselian species Sysciophlebia euglyptica, Sysciophlebia ilfeldensis, Sysciophlebia rubida, and 'Sysciophlebia sp. form KBQ', supporting the currently proposed Gzhelian age for its type locality. It supports the use of the representatives of the Spiloblattinidae for stratigraphic purposes. The diagnoses and limits of the families Subioblattidae, Phyloblattidae, Compsoblattidae, Spiloblattinidae, and of the spiloblattinid genera are discussed.

Traces of calcium oxalate biomineralization in fossil leaves from late Oligocene maar deposits from Germany.

Calcium oxalate (CaOx) is one of the most common bio-mineral in extant plants and is believed to serve a variety of functions such as calcium storage and herbivore defense. However, traces of CaOx crystals have rarely been identified in fossil plants, and they are primarily known from fossil gymnosperms, where empty cavities of former CaOx crystals or ghost crystals have been reported from leaf cuticles of some Late Cretaceous and Cenozoic conifers. Here we investigate fossil angiosperm leaves from the late Oligocene Rott Fossil Lagerstätte and report ghost crystals of various shapes, sizes and topology (distribution patterns), and cavities. These micromorphological structures of fossil leaves are compared to CaOx deposits in leaves of extant plants: globular structures in fossil leaves resemble CaOx druses (crystal aggregates) in fresh leaves in size and distribution; and angular or brick-shaped structures in the vascular system of fossil leaves closely resemble prismatic CaOx crystals in the vascular system of extant leaves in both size and topology. Chemically, CaOx druses have survived fossilization as cavities only, and were replaced by organic matter and ghost minerals containing Ca, Si, Al, S, and Fe. The identification of former CaOx remains in leaf fossils provides novel insights on the fate of plant bio-minerals during fossilization. More importantly, it provides an additional aspect of the ecophysiology of fossil plants thus improving the accuracy of palaeoecological reconstructions and can provide a broader perspective on the evolution of CaOx and their rule in plant ecology across geological timescales. Alternative interpretations of the fossil microstructures are discussed but ruled out.

Insect and Plant Diversity in Hot-Spring Ecosystems during the Jurassic-Cretaceous Boundary from Spain (Aguilar Fm., Palencia).

Hydrothermal palaeoenvironments are very uncommon in Upper Jurassic and Lower Cretaceous deposits worldwide. We present new plant and insect remains from travertines formed during the Jurassic-Cretaceous boundary in northern Spain (Aguilar Fm., Palencia province). A total of 136 plant specimens and three insect wings were collected and studied. This entomofauna consists of dragonfly (Odonata) wings including Cymatophlebiidae and an undetermined new genus and species of Aktassiidae, representing the first report of these families for the Iberian Peninsula. The fossil flora shows different morphotypes of plants, which have been tentatively assigned to three different genera. The taphocoenosis of the flora was dominated by Bennettitales (98.5%) including cf. Pterophyllum sp., Ptilophyllum cf. acutifolium, Ptilophyllum cf. pecten, Ptilophyllum cf. pectiniformis and cf. Ptilophyllum sp., and the occasional presence of ferns (1.5%) represented by the taxon Cladophlebis cf. denticulata. The presence of the Anisoptera Cymatophlebia cf. longialata suggests a higher affinity for a Tithonian age of the studied site, and the anatomy and palaeogeographical distribution of this species suggest capacity to migrate for rather long distances. The floristic composition of the site differs remarkably from other Tithonian-Berriasian floras of the Iberian Peninsula. The presence of Odonata and the distinctive flora in (semi)arid conditions could be due to the hot-spring providing an environmental niche with constant conditions of warmth and humidity forming an 'ecological oasis'.

Widespread mineralization of soft-bodied insects in Cretaceous amber.

Fossilized tree resin, or amber, commonly contains fossils of animals, plants and microorganisms. These inclusions have generally been interpreted as hollow moulds or mummified remains coated or filled with carbonaceous material. Here, we provide the first report of calcified and silicified insects in amber from the mid-Cretaceous Kachin (Burmese) amber. Data from light microscopy, scanning electron microscopy (SEM), energy-dispersive and wavelength-dispersive X-ray spectroscopy (EDX and WDX), X-ray micro-computed tomography (Micro-CT) and Raman spectroscopy show that these Kachin fossils owe their preservation to multiple diagenetic mineralization processes. The labile tissues (e.g. eyes, wings and trachea) mainly consist of calcite, chalcedony and quartz with minor amounts of carbonaceous material, pyrite, iron oxide and phyllosilicate minerals. Calcite, quartz and chalcedony also occur in cracks as void-filling cements, indicating that the minerals formed from chemical species that entered the fossil inclusions through cracks in the resin. The results demonstrate that resin and amber are not always closed systems. Fluids (e.g. sediment pore water, diagenetic fluid and ground water) at different burial stages have chances to interact with amber throughout its geological history and affect the preservational quality and morphological fidelity of its fossil inclusions.

Evolutionary history and divergence times of Odonata (dragonflies and damselflies) revealed through transcriptomics.

Dragonflies and damselflies are among the earliest flying insects with extant representatives. However, unraveling details of their long evolutionary history, such as egg laying (oviposition) strategies, is impeded by unresolved phylogenetic relationships, particularly in damselflies. Here we present a transcriptome-based phylogenetic reconstruction of Odonata, analyzing 2,980 protein-coding genes in 105 species representing nearly all the order's families. All damselfly and most dragonfly families are recovered as monophyletic. Our data suggest a sister relationship between dragonfly families of Gomphidae and Petaluridae. According to our divergence time estimates, both crown-Zygoptera and -Anisoptera arose during the late Triassic. Egg-laying with a reduced ovipositor apparently evolved in dragonflies during the late Jurassic/early Cretaceous. Lastly, we also test the impact of fossil choice and placement, particularly, of the extinct fossil species, †Triassolestodes asiaticus, and †Proterogomphus renateae on divergence time estimates. We find placement of †Proterogomphus renateae to be much more impactful than †Triassolestodes asiaticus.

A case of long-term herbivory: specialized feeding trace on Parrotia (Hamamelidaceae) plant species.

Interactions between plants and insects evolved during millions of years of coevolution and maintain the trophic balance of terrestrial ecosystems. Documenting insect damage types (DT) on fossil leaves is essential for understanding the evolution of plant-insect interactions and for understanding the effects of major environmental changes on ecosystem structure. However, research focusing on palaeoherbivory is still sparse and only a tiny fraction of fossil leaf collections have been analysed. This study documents a type of insect damage found exclusively on the leaves of Parrotia species (Hamamelidaceae). This DT was identified on Parrotia leaves from Willershausen (Germany, Pliocene) and from Shanwang (China, Miocene) and on their respective endemic modern relatives: Parrotia perisca in the Hyrcanian forests (Iran) and Parrotia subaequalis in the Yixing forest (China). Our study demonstrates that this insect DT persisted over at least 15 Myr spanning eastern Asia to western Europe. Against expectations, more examples of this type of herbivory were identified on the fossil leaves than on the modern examples. This mismatch may suggest a decline of this specialized plant-insect interaction owing to the contraction of Parrotia populations in Eurasia during the late Cenozoic. However, the continuous presence of this DT demonstrates a robust and long-term plant-herbivore association, and provides new evidence for a shared biogeographic history of the two host plants.

Correction to: An integrative phylogenomic approach to elucidate the evolutionary history and divergence times of Neuropterida (Insecta: Holometabola).

An amendment to this paper has been published and can be accessed via the original article.

An integrative phylogenomic approach to elucidate the evolutionary history and divergence times of Neuropterida (Insecta: Holometabola).

BACKGROUND: The latest advancements in DNA sequencing technologies have facilitated the resolution of the phylogeny of insects, yet parts of the tree of Holometabola remain unresolved. The phylogeny of Neuropterida has been extensively studied, but no strong consensus exists concerning the phylogenetic relationships within the order Neuroptera. Here, we assembled a novel transcriptomic dataset to address previously unresolved issues in the phylogeny of Neuropterida and to infer divergence times within the group. We tested the robustness of our phylogenetic estimates by comparing summary coalescent and concatenation-based phylogenetic approaches and by employing different quartet-based measures of phylogenomic incongruence, combined with data permutations. RESULTS: Our results suggest that the order Raphidioptera is sister to Neuroptera + Megaloptera. Coniopterygidae is inferred as sister to all remaining neuropteran families suggesting that larval cryptonephry could be a ground plan feature of Neuroptera. A clade that includes Nevrorthidae, Osmylidae, and Sisyridae (i.e. Osmyloidea) is inferred as sister to all other Neuroptera except Coniopterygidae, and Dilaridae is placed as sister to all remaining neuropteran families. Ithonidae is inferred as the sister group of monophyletic Myrmeleontiformia. The phylogenetic affinities of Chrysopidae and Hemerobiidae were dependent on the data type analyzed, and quartet-based analyses showed only weak support for the placement of Hemerobiidae as sister to Ithonidae + Myrmeleontiformia. Our molecular dating analyses suggest that most families of Neuropterida started to diversify in the Jurassic and our ancestral character state reconstructions suggest a primarily terrestrial environment of the larvae of Neuropterida and Neuroptera. CONCLUSION: Our extensive phylogenomic analyses consolidate several key aspects in the backbone phylogeny of Neuropterida, such as the basal placement of Coniopterygidae within Neuroptera and the monophyly of Osmyloidea. Furthermore, they provide new insights into the timing of diversification of Neuropterida. Despite the vast amount of analyzed molecular data, we found that certain nodes in the tree of Neuroptera are not robustly resolved. Therefore, we emphasize the importance of integrating the results of morphological analyses with those of sequence-based phylogenomics. We also suggest that comparative analyses of genomic meta-characters should be incorporated into future phylogenomic studies of Neuropterida.

An integrative phylogenomic approach illuminates the evolutionary history of cockroaches and termites (Blattodea).

Phylogenetic relationships among subgroups of cockroaches and termites are still matters of debate. Their divergence times and major phenotypic transitions during evolution are also not yet settled. We addressed these points by combining the first nuclear phylogenomic study of termites and cockroaches with a thorough approach to divergence time analysis, identification of endosymbionts, and reconstruction of ancestral morphological traits and behaviour. Analyses of the phylogenetic relationships within Blattodea robustly confirm previously uncertain hypotheses such as the sister-group relationship between Blaberoidea and remaining Blattodea, and Lamproblatta being the closest relative to the social and wood-feeding Cryptocercus and termites. Consequently, we propose new names for various clades in Blattodea: Cryptocercus + termites = Tutricablattae; Lamproblattidae + Tutricablattae = Kittrickea; and Blattoidea + Corydioidea = Solumblattodea. Our inferred divergence times contradict previous studies by showing that most subgroups of Blattodea evolved in the Cretaceous, reducing the gap between molecular estimates of divergence times and the fossil record. On a phenotypic level, the blattodean ground-plan is for egg packages to be laid directly in a hole while other forms of oviposition, including ovovivipary and vivipary, arose later. Finally, other changes in egg care strategy may have allowed for the adaptation of nest building and other novelties.

A primitive honey bee from the Middle Miocene deposits of southeastern Yunnan, China (Hymenoptera, Apidae).

While fossils of honey bees (Apini: Apis Linnaeus) are comparatively abundant in European Oligocene and Miocene deposits, the available material from Asia is scant and represented by only a handful of localities. It is therefore significant to report a new deposit with a fossil honey bee from southern China. Apis (Synapis) dalica Engel & Wappler, sp. n., is described and figured from Middle Miocene sediments of Maguan County, southeastern Yunnan Province, China. This is the first fossil bee from the Cenozoic of southern China, and is distinguished from its close congeners present at the slightly older locality of Shanwang, Shandong in northeastern China. The species can be distinguished on the basis of wing venation differences from other Miocene Apis.

Plant-insect interactions patterns in three European paleoforests of the late-Neogene-early-Quaternary.

Plants and insects are constantly interacting in complex ways through forest communities since hundreds of millions of years. Those interactions are often related to variations in the climate. Climate change, due to human activities, may have disturbed these relationships in modern ecosystems. Fossil leaf assemblages are thus good opportunities to survey responses of plant-insect interactions to climate variations over the time. The goal of this study is to discuss the possible causes of the differences of plant-insect interactions' patterns in European paleoforests from the Neogene-Quaternary transition. This was accomplished through three fossil leaf assemblages: Willershausen, Berga (both from the late Neogene of Germany) and Bernasso (from the early Quaternary of France). In Willershausen it has been measured that half of the leaves presented insect interactions, 35% of the fossil leaves were impacted by insects in Bernasso and only 25% in Berga. The largest proportion of these interactions in Bernasso were categorized as specialist (mainly due to galling) while in Willershausen and Berga those ones were significantly more generalist. Contrary to previous studies, this study did not support the hypothesis that the mean annual precipitation and temperature were the main factors that impacted the different plant-insect interactions' patterns. However, for the first time, our results tend to support that the hydric seasonality and the mean temperature of the coolest months could be potential factors influencing fossil plant-insect interactions.

A Triassic-Jurassic window into the evolution of Lepidoptera.

On the basis of an assemblage of fossilized wing scales recovered from latest Triassic and earliest Jurassic sediments from northern Germany, we provide the earliest evidence for Lepidoptera (moths and butterflies). The diverse scales confirm a (Late) Triassic radiation of lepidopteran lineages, including the divergence of the Glossata, the clade that comprises the vast multitude of extant moths and butterflies that have a sucking proboscis. The microfossils extend the minimum calibrated age of glossatan moths by ca. 70 million years, refuting ancestral association of the group with flowering plants. Development of the proboscis may be regarded as an adaptive innovation to sucking free liquids for maintaining the insect's water balance under arid conditions. Pollination drops secreted by a variety of Mesozoic gymnosperms may have been non-mutualistically exploited as a high-energy liquid source. The early evolution of the Lepidoptera was probably not severely interrupted by the end-Triassic biotic crisis.