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.

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.

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.

Holocene shifts in the assembly of plant and animal communities implicate human impacts.

Understanding how ecological communities are organized and how they change through time is critical to predicting the effects of climate change. Recent work documenting the co-occurrence structure of modern communities found that most significant species pairs co-occur less frequently than would be expected by chance. However, little is known about how co-occurrence structure changes through time. Here we evaluate changes in plant and animal community organization over geological time by quantifying the co-occurrence structure of 359,896 unique taxon pairs in 80 assemblages spanning the past 300 million years. Co-occurrences of most taxon pairs were statistically random, but a significant fraction were spatially aggregated or segregated. Aggregated pairs dominated from the Carboniferous period (307 million years ago) to the early Holocene epoch (11,700 years before present), when there was a pronounced shift to more segregated pairs, a trend that continues in modern assemblages. The shift began during the Holocene and coincided with increasing human population size and the spread of agriculture in North America. Before the shift, an average of 64% of significant pairs were aggregated; after the shift, the average dropped to 37%. The organization of modern and late Holocene plant and animal assemblages differs fundamentally from that of assemblages over the past 300 million years that predate the large-scale impacts of humans. Our results suggest that the rules governing the assembly of communities have recently been changed by human activity.

Florivory of Early Cretaceous flowers by functionally diverse insects: implications for early angiosperm pollination.

Florivory (flower consumption) occurs worldwide in modern angiosperms, associated with pollen and nectar consumption. However, florivory remains unrecorded from fossil flowers since their Early Cretaceous appearance. We test hypotheses that earliest angiosperms were pollinated by a diverse insect fauna by evaluating 7858 plants from eight localities of the latest Albian Dakota Formation from midcontinental North America, in which 645 specimens (8.2%) were flowers or inflorescences. Well-preserved specimens were categorized into 32 morphotypes, nine of which displayed 207 instances of damage from 11 insect damage types (DTs) by four functional-feeding groups of hole feeding, margin feeding, surface feeding and piercing-and-sucking. We assessed the same DTs inflicted by known florivores on modern flowers that also are their pollinators, and associated insect mouthpart types causing such damage. The diverse, Dakota florivore-pollinator community showed a local pattern at Braun's Ranch of flower morphotypes 4 and 5 having piercing-and-sucking as dominant and margin feeding as minor interactions, whereas Dakotanthus cordiformis at Rose Creek I and II had an opposite pattern. We found no evidence for nectar robbing. These data support the rapid emergence of early angiosperms of florivore and associated pollinator guilds expressed at both the local and regional community levels.

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.

Priors and Posteriors in Bayesian Timing of Divergence Analyses: The Age of Butterflies Revisited.

The need for robust estimates of times of divergence is essential for downstream analyses, yet assessing this robustness is still rare. We generated a time-calibrated genus-level phylogeny of butterflies (Papilionoidea), including 994 taxa, up to 10 gene fragments and an unprecedented set of 12 fossils and 10 host-plant node calibration points. We compared marginal priors and posterior distributions to assess the relative importance of the former on the latter. This approach revealed a strong influence of the set of priors on the root age but for most calibrated nodes posterior distributions shifted from the marginal prior, indicating significant information in the molecular data set. Using a very conservative approach we estimated an origin of butterflies at 107.6 Ma, approximately equivalent to the latest Early Cretaceous, with a credibility interval ranging from 89.5 Ma (mid Late Cretaceous) to 129.5 Ma (mid Early Cretaceous). In addition, we tested the effects of changing fossil calibration priors, tree prior, different sets of calibrations and different sampling fractions but our estimate remained robust to these alternative assumptions. With 994 genera, this tree provides a comprehensive source of secondary calibrations for studies on butterflies.

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.

Phanerozoic pO2 and the early evolution of terrestrial animals.

Concurrent gaps in the Late Devonian/Mississippian fossil records of insects and tetrapods (i.e. Romer's Gap) have been attributed to physiological suppression by low atmospheric pO2 Here, updated stable isotope inputs inform a reconstruction of Phanerozoic oxygen levels that contradicts the low oxygen hypothesis (and contradicts the purported role of oxygen in the evolution of gigantic insects during the late Palaeozoic), but reconciles isotope-based calculations with other proxies, like charcoal. Furthermore, statistical analysis demonstrates that the gap between the first Devonian insect and earliest diverse insect assemblages of the Pennsylvanian (Bashkirian Stage) requires no special explanation if insects were neither diverse nor abundant prior to the evolution of wings. Rather than tracking physiological constraint, the fossil record may accurately record the transformative evolutionary impact of insect flight.

Benefits from living together? Clades whose species use similar habitats may persist as a result of eco-evolutionary feedbacks.

Contents 66 I. 67 II. 68 III. 69 IV. 70 V. 73 VI. 75 VII. 77 78 References 78 SUMMARY: Recent decades have seen declines of entire plant clades while other clades persist despite changing environments. We suggest that one reason why some clades persist is that species within these clades use similar habitats, because such similarity may increase the degree of co-occurrence of species within clades. Traditionally, co-occurrence among clade members has been suggested to be disadvantageous because of increased competition and enemy pressure. Here, we hypothesize that increased co-occurrence among clade members promotes mutualist exchange, niche expansion or hybridization, thereby helping species avoid population decline from environmental change. We review the literature and analyse published data for hundreds of plant clades (genera) within a well-studied region and find major differences in the degree to which species within clades occupy similar habitats. We tentatively show that, in clades for which species occupy similar habitats, species tend to exhibit increased co-occurrence, mutualism, niche expansion, and hybridization - and rarely decline. Consistently, throughout the geological past, clades whose species occupied similar habitats often persisted through long time-spans. Overall, for many plant species, the occupation of similar habitats among fellow clade members apparently reduced their vulnerability to environmental change. Future research should identify when and how this previously unrecognized eco-evolutionary feedback operates.

Taxonomic description of in situ bee pollen from the middle Eocene of Germany.

The middle Eocene Messel and Eckfeld localities are renowned for their excellently preserved faunas and diverse floras. Here we describe for the first time pollen from insect-pollinated plants found in situ on well-preserved ancient bees using light and scanning electron microscopy. There have been 140 pollen types reported from Messel and 162 pollen types from Eckfeld. Here we document 23 pollen types, six from Messel and 18 from Eckfeld (one is shared). The taxa reported here are all pollinated by insects and mostly not recovered in the previously studied dispersed fossil pollen records. Typically, a single or two pollen types are found on each fossil bee specimen, the maximum number of distinct pollen types on a single individual is five. Only five of the 23 pollen types obtained are angiosperms of unknown affinity, the remainder cover a broad taxonomic range of angiosperm trees and include members of several major clades: monocots (1 pollen type), fabids (7), malvids (4), asterids (5) and other core eudicots (1). Seven types each can be assigned to individual genera or infrafamilial clades. Since bees visit only flowers in the relative vicinity of their habitat, the recovered pollen provides a unique insight into the autochthonous palaeo-flora. The coexistence of taxa such as Decodon, Elaeocarpus, Mortoniodendron and other Tilioideae, Mastixoideae, Olax, Pouteria and Nyssa confirms current views that diverse, thermophilic forests thrived at the Messel and Eckfeld localities, probably under a warm subtropical, fully humid climate. Our study calls for increased attention to pollen found in situ on pollen-harvesting insects such as bees, which can provide new insights on insect-pollinated plants and complement even detailed palaeo-palynological knowledge obtained mostly from pollen of wind-pollinated plants in the dispersed pollen record of sediments. In the case of Elaeocarpus, Mortoniodendron, Olax and Pouteria the pollen collected by the middle Eocene bees represent the earliest unambiguous records of their respective genera.

New data from the Middle Jurassic of China shed light on the phylogeny and origin of the proboscis in the Mesopsychidae (Insecta: Mecoptera).

BACKGROUND: The Mesopsychidae is an extinct family of Mecoptera, comprising eleven described genera from Upper Permian to Lower Cretaceous deposits. In 2009, several well-preserved mesopsychids with long proboscides were reported from the mid Mesozoic of Northeastern China, suggesting the presence of pollination mutualisms with gymnosperm plants and highlighting their elevated genus-level diversity. Since that time, additional mesopsychid taxa have been described. However, the phylogeny of genera within Mesopsychidae has not been studied formally, attributable to the limited number of well-preserved fossils. RESULTS: Here, we describe two new species, Lichnomesopsyche prochorista sp. nov. and Vitimopsyche pristina sp. nov. and revise the diagnosis of Lichnomesopsyche daohugouensis Ren, Labandeira and Shih, 2010, based on ten specimens from the latest Middle Jurassic Jiulongshan Formation of Inner Mongolia, China. After compiling data from these new fossil species and previously reported representative taxa, we conducted phylogenetic analyses and geometric morphometric studies that now shed light on the taxonomy and phylogeny of Mesopsychidae. We also evaluate the recurring origin of the siphonate proboscis in the Mecoptera and propose an evolutionary developmental model for its multiple origins. CONCLUSIONS: Phylogenetic and geometric morphometric results confirm the establishment of two new species, each to Lichnomesopsyche and Vitimopsyche. Vitimopsyche pristina sp. nov. extends the existence of the genus Vitimopsyche Novokshonov and Sukacheva, 2001, from the mid Lower Cretaceous to the latest Middle Jurassic. Two methods of analyses indicate an affiliation of Mesopsyche dobrokhotovae Novokshonov, 1997 with Permopsyche Bashkuev, 2011. A phylogenetic analysis of the Mesopsychidae supports: 1), Mesopsychidae as a monophyletic group; 2), Mesopsyche as a paraphyletic group, to be revised pending future examination of additional material; and 3), the independent origin of the proboscis in the Pseudopolycentropodidae, its subsequent loss in earliest Mesopsychidae such as Epicharmesopsyche, its re-origination in the common ancestor (or perhaps independently) in the Vitimopsyche and Lichnomesopsyche clades of the Mesopsychidae. The third conclusion indicates that the proboscis originated four or five times within early Mecoptera, whose origin is explained by an evolutionary developmental model.

Convergent evolution of ramified antennae in insect lineages from the Early Cretaceous of Northeastern China.

Antennae are important, insect sensory organs that are used principally for communication with other insects and the detection of environmental cues. Some insects independently evolved ramified (branched) antennae, which house several types of sensilla for motion detection, sensing olfactory and chemical cues, and determining humidity and temperature levels. Though ramified antennae are common in living insects, occasionally they are present in the Mesozoic fossil record. Here, we present the first caddisflies with ramified antennae, the earliest known fossil sawfly, and a scorpionfly also with ramified antennae from the mid-Lower Cretaceous Yixian Formation of Northeastern China, dated at 125 million years ago (Ma). These three insect taxa with ramified antennae consist of three unrelated lineages and provide evidence for broad structural convergence that historically has been best demonstrated by features such as convergent mouthparts. In addition, ramified antennae in these Mid-Mesozoic lineages likely do not constitute a key innovation, as they are not associated with significantly increased diversification compared with closely related lineages lacking this trait, and nor are they ecologically isolated from numerous, co-occurring insect species with unmodified antennae.

The evolutionary convergence of mid-Mesozoic lacewings and Cenozoic butterflies.

Mid-Mesozoic kalligrammatid lacewings (Neuroptera) entered the fossil record 165 million years ago (Ma) and disappeared 45 Ma later. Extant papilionoid butterflies (Lepidoptera) probably originated 80-70 Ma, long after kalligrammatids became extinct. Although poor preservation of kalligrammatid fossils previously prevented their detailed morphological and ecological characterization, we examine new, well-preserved, kalligrammatid fossils from Middle Jurassic and Early Cretaceous sites in northeastern China to unravel a surprising array of similar morphological and ecological features in these two, unrelated clades. We used polarized light and epifluorescence photography, SEM imaging, energy dispersive spectrometry and time-of-flight secondary ion mass spectrometry to examine kalligrammatid fossils and their environment. We mapped the evolution of specific traits onto a kalligrammatid phylogeny and discovered that these extinct lacewings convergently evolved wing eyespots that possibly contained melanin, and wing scales, elongate tubular proboscides, similar feeding styles, and seed-plant associations, similar to butterflies. Long-proboscid kalligrammatid lacewings lived in ecosystems with gymnosperm-insect relationships and likely accessed bennettitalean pollination drops and pollen. This system later was replaced by mid-Cretaceous angiosperms and their insect pollinators.

The fossil record and taphonomy of butterflies and moths (Insecta, Lepidoptera): implications for evolutionary diversity and divergence-time estimates.

BACKGROUND: It is conventionally accepted that the lepidopteran fossil record is significantly incomplete when compared to the fossil records of other, very diverse, extant insect orders. Such an assumption, however, has been based on cumulative diversity data rather than using alternative statistical approaches from actual specimen counts. RESULTS: We reviewed documented specimens of the lepidopteran fossil record, currently consisting of 4,593 known specimens that are comprised of 4,262 body fossils and 331 trace fossils. The temporal distribution of the lepidopteran fossil record shows significant bias towards the late Paleocene to middle Eocene time interval. Lepidopteran fossils also record major shifts in preservational style and number of represented localities at the Mesozoic stage and Cenozoic epoch level of temporal resolution. Only 985 of the total known fossil specimens (21.4%) were assigned to 23 of the 40 extant lepidopteran superfamilies. Absolute numbers and proportions of preservation types for identified fossils varied significantly across superfamilies. The secular increase of lepidopteran family-level diversity through geologic time significantly deviates from the general pattern of other hyperdiverse, ordinal-level lineages. CONCLUSION: Our statistical analyses of the lepidopteran fossil record show extreme biases in preservation type, age, and taxonomic composition. We highlight the scarcity of identified lepidopteran fossils and provide a correspondence between the latest lepidopteran divergence-time estimates and relevant fossil occurrences at the superfamily level. These findings provide caution in interpreting the lepidopteran fossil record through the modeling of evolutionary diversification and in determination of divergence time estimates.

Life habits, hox genes, and affinities of a 311 million-year-old holometabolan larva.

BACKGROUND: Holometabolous insects are the most diverse, speciose and ubiquitous group of multicellular organisms in terrestrial and freshwater ecosystems. The enormous evolutionary and ecological success of Holometabola has been attributed to their unique postembryonic life phases in which nonreproductive and wingless larvae differ significantly in morphology and life habits from their reproductive and mostly winged adults, separated by a resting stage, the pupa. Little is known of the evolutionary developmental mechanisms that produced the holometabolous larval condition and their Paleozoic origin based on fossils and phylogeny. RESULTS: We provide a detailed anatomic description of a 311 million-year-old specimen, the oldest known holometabolous larva, from the Mazon Creek deposits of Illinois, U.S.A. The head is ovoidal, downwardly oriented, broadly attached to the anterior thorax, and bears possible simple eyes and antennae with insertions encircled by molting sutures; other sutures are present but often indistinct. Mouthparts are generalized, consisting of five recognizable segments: a clypeo-labral complex, mandibles, possible hypopharynx, a maxilla bearing indistinct palp-like appendages, and labium. Distinctive mandibles are robust, triangular, and dicondylic. The thorax is delineated into three, nonoverlapping regions of distinctive surface texture, each with legs of seven elements, the terminal-most bearing paired claws. The abdomen has ten segments deployed in register with overlapping tergites; the penultimate segment bears a paired, cercus-like structure. The anterior eight segments bear clawless leglets more diminutive than the thoracic legs in length and cross-sectional diameter, and inserted more ventrolaterally than ventrally on the abdominal sidewall. CONCLUSIONS: Srokalarva berthei occurred in an evolutionary developmental context likely responsible for the early macroevolutionary success of holometabolous insects. Srokalarva berthei bore head and prothoracic structures, leglet series on successive abdominal segments - in addition to comparable features on a second taxon eight million-years-younger - that indicates Hox-gene regulation of segmental and appendage patterning among earliest Holometabola. Srokalarva berthei body features suggest a caterpillar-like body plan and head structures indicating herbivory consistent with known, contemporaneous insect feeding damage on seed plants. Taxonomic resolution places Srokalarva berthei as an extinct lineage, apparently possessing features closer to neuropteroid than other holometabolous lineages.