Insect Clades Research Articles

Enhanced flight performance and adaptive evolution of Mesozoic giant cicadas.

Insects have evolved diverse ecological flight behaviors and adaptations that played a key role in their large-scale evolutionary patterns. However, the evolution of their flight performance is poorly understood because reconstructing flight abilities of extinct insects is highly challenging. Here, we propose an integrated approach to reveal the evolution of flight performance of Palaeontinidae (giant cicadas), a Mesozoic arboreal insect clade with large bodies and wings. Our analyses unveil a faunal turnover from early to late Palaeontinidae during the latest Jurassic-earliest Cretaceous, accompanied by a morphological adaptive shift and remarkable improvement in flight abilities including increased flight speed and enhanced maneuverability. The adaptive aerodynamic evolution of Palaeontinidae may have been stimulated by the rise of early birds, supporting the hypothesis of an aerial evolutionary arms race (Air Race) between Palaeontinidae and birds. Our results provide a potential example of predator-induced morphological and behavioral macroevolution and contribute to our understanding of how powered flight has shaped animal evolution.

The contribution of the Middle Triassic fossil assemblage of Monte San Giorgio to insect evolution

The Triassic represents a critical period for understanding the turnover of insect fauna from the Paleozoic to the Mesozoic following the end-Permian mass extinctions (EPME); however, fossil deposits from the Early-Middle Triassic are scarce. The exceptionally preserved 239 million-year-old fossil insect fauna recorded at Monte San Giorgio (Switzerland), including 248 fossils representing 15 major insect clades is presented here. Besides the exceptional features, including their small size and excellent preservation, the fossils have importance in the evolutionary history of the group. The taxonomic and ecological diversity recovered, including both freshwater (dragonflies and caddisflies) and terrestrial taxa (true bugs and wasps), demonstrates that complex environments sustained a paleocommunity dominated by monurans (thought not to have survived the EPME), midges, and beetles. Interestingly, a blattodean-like fossil bearing an external ootheca was also found, important for understanding Paleozoic roachoids to extant cockroaches’ transition and the evolution of maternal brood care. Moreover, the youngest and first complete specimen of †Permithonidae and the oldest sawfly fossils were discovered. Finally, round-shaped bodies, compatible with seminal capsules or lycophyte spores, were found on the abdomens of several midge-like individuals. If these are spores, non-seed-bearing plants could have been the first entomophilous plants rather than gymnosperms, as recently supposed. Altogether, these fossils contribute substantially to understanding insect evolution and Paleozoic-Mesozoic faunal turnover.

Phylogenomics resolves long-standing questions about the affinities of an endangered Corsican endemic fly.

Recent studies on oestroidean Diptera (Brachycera) are providing a comprehensive and nuanced understanding of the evolutionary history of this remarkably diverse clade of holometabolous insects. The Oestroidea, which includes formidable pests such as various blowflies, botflies, and flesh flies that infest livestock, pets and humans, are mostly composed of beneficial species that act as scavengers or parasitoids on various pest insects. In our research, we used genomic methods to elucidate the phylogenetic position of Nesodexia corsicanaVilleneuve, 1911(Diptera: Calliphoridae), a mysterious oestroid species endemic to Corsica and characterized by distinctive morphological features that have puzzled taxonomists for years. Contrary to initial hypotheses, our results place Nesodexia Villeneuve, 1911within the Calliphoridae subfamily Rhinophorinae, a small lineage of terrestrial isopod parasitoids. Through detailed morphological analysis of adults of both sexes and eggs, we uncovered significant insights consistent with our phylogenomic reconstruction. The unique morphological features of the species, coupled with its restricted and fragmented habitat, highlight its potential conservation importance. We delineated the area of occupancy for N. corsicana and assessed its "threatened" category using specific IUCN Red List criteria. In addition, we mapped the available habitat within its range and determined potential key biodiversity areas (KBA) triggered by N. corsicana. New potential KBAs are only partially covered by the Corsican Regional Park. Finally, we mapped the distribution of habitats on the island to assess the potential distribution of the species beyond its currently known geographic range.

Overwintering strategy regulates phenological sensitivity and consequences for ecological services in a clade of temperate North American insects

Abstract Recent reports of insect declines have raised concerns about the potential for concomitant losses to ecosystem processes. However, understanding the causes and consequences of insect declines is challenging, especially given the data deficiencies for most species. Needed are approaches that can help quantify the magnitude and potential causes of declines at levels above species. Here we present an analytical framework for assessing broad‐scale plant–insect phenologies and their relationship to community‐level insect abundance patterns. We intentionally apply a species‐neutral approach to analyse trends in phenology and abundance at the macroecological scale. Because both phenology and abundance are critical to ecosystem processes, we estimate aggregate metrics using the overwintering (diapause) stage, a key species trait regulating phenology and environmental sensitivities. This approach can be used across broad spatiotemporal scales and multiple taxa, including less well‐studied groups. Using community (‘citizen’) science butterfly observations from multiple platforms across the Eastern USA, we show that the relationships between environmental drivers, phenology and abundance depend on the diapause stage. In particular, egg‐diapausing butterflies show marked changes in adult‐onset phenology in relation to plant phenology and are rapidly declining in abundance over a 20‐year span across the study region. Our results also demonstrate the negative consequences of warmer winters for the abundance of egg‐diapausing butterflies, irrespective of plant phenology. In sum, the diapause stage strongly shapes both phenological sensitivities and developmental requirements across seasons, providing a basis for predicting the impacts of environmental change across trophic levels. Utilizing a framework that ties thermal performance across life stages in relation to climate and lower‐trophic‐level phenology provides a critical step towards predicting changes in ecosystem processes provided by butterflies and other herbivorous insects into the future. Read the free Plain Language Summary for this article on the Journal blog.

Genome evolution and divergence in cis-regulatory architecture is associated with condition-responsive development in horned dung beetles.

Phenotypic plasticity is thought to be an important driver of diversification and adaptation to environmental variation, yet the genomic mechanisms mediating plastic trait development and evolution remain poorly understood. The Scarabaeinae, or true dung beetles, are a species-rich clade of insects recognized for their highly diversified nutrition-responsive development including that of cephalic horns-evolutionarily novel, secondary sexual weapons that exhibit remarkable intra- and interspecific variation. Here, we investigate the evolutionary basis for horns as well as other key dung beetle traits via comparative genomic and developmental assays. We begin by presenting chromosome-level genome assemblies of three dung beetle species in the tribe Onthophagini (> 2500 extant species) including Onthophagus taurus, O. sagittarius, and Digitonthophagus gazella. Comparing these assemblies to those of seven other species across the order Coleoptera identifies evolutionary changes in coding sequence associated with metabolic regulation of plasticity and metamorphosis. We then contrast chromatin accessibility in developing head horn tissues of high- and low-nutrition O. taurus males and females and identify distinct cis-regulatory architectures underlying nutrition- compared to sex-responsive development, including a large proportion of recently evolved regulatory elements sensitive to horn morph determination. Binding motifs of known and new candidate transcription factors are enriched in these nutrition-responsive open chromatin regions. Our work highlights the importance of chromatin state regulation in mediating the development and evolution of plastic traits, demonstrates gene networks are highly evolvable transducers of environmental and genetic signals, and provides new reference-quality genomes for three species that will bolster future developmental, ecological, and evolutionary studies of this insect group.

Resource adaptation drives the size-complexity rule in termites.

The size-complexity rule posits that the evolution of larger cooperative groups should favour more division of labour. Examples include more cell types in larger multicellular organisms, and more polymorphic castes in larger eusocial colonies. However, a correlation between division of labour and group size may reflect a shared response of both traits to resource availability and/or profitability. Here, this possibility was addressed by investigating the evolution of sterile caste number (worker and soldier morphotypes) in termites, a major clade of eusocial insects in which the drivers of caste polymorphism are poorly understood. A novel dataset on 90 termite species was compiled from the published literature. The analysis showed that sterile caste number did increase markedly with colony size. However, after controlling for resource adaptations and phylogeny, there was no evidence for this relationship. Rather, sterile caste number increased with increasing nest-food separation and decreased with soil-feeding, through changes in worker (but not soldier) morphotype number. Further, colony size increased with nest-food separation, thus driving the false correlation between sterile caste number and colony size. These findings support adaptation to higher energy acquisition as key to the rise of complex insect societies, with larger size being a by-product.

The Scorpionfly (Panorpa cognata) Genome Highlights Conserved and Derived Features of the Peculiar Dipteran X Chromosome.

Many insects carry an ancient X chromosome-the Drosophila Muller element F-that likely predates their origin. Interestingly, the X has undergone turnover in multiple fly species (Diptera) after being conserved for more than 450 My. The long evolutionary distance between Diptera and other sequenced insect clades makes it difficult to infer what could have contributed to this sudden increase in rate of turnover. Here, we produce the first genome and transcriptome of a long overlooked sister-order to Diptera: Mecoptera. We compare the scorpionfly Panorpa cognata X-chromosome gene content, expression, and structure to that of several dipteran species as well as more distantly related insect orders (Orthoptera and Blattodea). We find high conservation of gene content between the mecopteran X and the dipteran Muller F element, as well as several shared biological features, such as the presence of dosage compensation and a low amount of genetic diversity, consistent with a low recombination rate. However, the 2 homologous X chromosomes differ strikingly in their size and number of genes they carry. Our results therefore support a common ancestry of the mecopteran and ancestral dipteran X chromosomes, and suggest that Muller element F shrank in size and gene content after the split of Diptera and Mecoptera, which may have contributed to its turnover in dipteran insects.

Fusarium phytopathogens as insect mutualists.

As vectors of numerous plant pathogens, herbivorous insects play a key role in the epidemiology of plant disease. But how phytopathogens impact the metabolism, physiology, and fitness of their insect vectors is often unexplored within these tripartite interactions. Here, we examine the diverse symbioses forged between insects and members of the ascomycete fungal genus Fusarium. While Fusarium features numerous plant pathogens that are causal to diseases such as wilts and rots, many of these microbes also engage in stable mutualisms across several insect clades. Matching a diversity in symbiont localization and transmission routes, we highlight the various roles fusaria fulfill towards their insect hosts, from upgrading their nutritional physiology to providing defense against natural enemies. But as the insect partner is consistently herbivorous, we emphasize the convergent benefit Fusarium derives in exchange: propagation to a novel host plant. Collectively, we point to the synergy arising between a phytopathogen and its insect vector, and the consequences inflicted on their shared plant.

Autorecoding A-to-I RNA editing sites in the Adar gene underwent compensatory gains and losses in major insect clades.

As one of the most prevalent RNA modifications in animals, adenosine-to-inosine (A-to-I) RNA editing facilitates the environmental adaptation of organisms by diversifying the proteome in a temporal-spatial manner. In flies and bees, the editing enzyme Adar has independently gained two different autorecoding sites that form an autofeedback loop, stabilizing the overall editing efficiency. This ensures cellular homeostasis by keeping the normal function of target genes. However, in a broader range of insects, the evolutionary dynamics and significance of this Adar autoregulatory mechanism are unclear. We retrieved the genomes of 377 arthropod species covering the five major insect orders (Hemiptera, Hymenoptera, Coleoptera, Diptera, and Lepidoptera) and aligned the Adar autorecoding sites across all genomes. We found that the two autorecoding sites underwent compensatory gains and losses during the evolution of two orders with the most sequenced species (Diptera and Hymenoptera), and that the two editing sites were mutually exclusive among them: One editable site is significantly linked to another uneditable site. This autorecoding mechanism of Adar could flexibly diversify the proteome and stabilize global editing activity. Many insects independently selected different autorecoding sites to achieve a feedback loop and regulate the global RNA editome, revealing an interesting phenomenon during evolution. Our study reveals the evolutionary force acting on accurate regulation of RNA editing activity in insects and thus deepens our understanding of the functional importance of RNA editing in environmental adaptation and evolution.

Variable organization of symbiont-containing tissue across planthoppers hosting different heritable endosymbionts.

Sap-feeding hemipteran insects live in associations with diverse heritable symbiotic microorganisms (bacteria and fungi) that provide essential nutrients deficient in their hosts' diets. These symbionts typically reside in highly specialized organs called bacteriomes (with bacterial symbionts) or mycetomes (with fungal symbionts). The organization of these organs varies between insect clades that are ancestrally associated with different microbes. As these symbioses evolve and additional microorganisms complement or replace the ancient associates, the organization of the symbiont-containing tissue becomes even more variable. Planthoppers (Hemiptera: Fulgoromorpha) are ancestrally associated with bacterial symbionts Sulcia and Vidania, but in many of the planthopper lineages, these symbionts are now accompanied or have been replaced by other heritable bacteria (e.g., Sodalis, Arsenophonus, Purcelliella) or fungi. We know the identity of many of these microbes, but the symbiont distribution within the host tissues and the bacteriome organization have not been systematically studied using modern microscopy techniques. Here, we combine light, fluorescence, and transmission electron microscopy with phylogenomic data to compare symbiont tissue distributions and the bacteriome organization across planthoppers representing 15 families. We identify and describe seven primary types of symbiont localization and seven types of the organization of the bacteriome. We show that Sulcia and Vidania, when present, usually occupy distinct bacteriomes distributed within the body cavity. The more recently acquired gammaproteobacterial and fungal symbionts generally occupy separate groups of cells organized into distinct bacteriomes or mycetomes, distinct from those with Sulcia and Vidania. They can also be localized in the cytoplasm of fat body cells. Alphaproteobacterial symbionts colonize a wider range of host body habitats: Asaia-like symbionts often colonize the host gut lumen, whereas Wolbachia and Rickettsia are usually scattered across insect tissues and cell types, including cells containing other symbionts, bacteriome sheath, fat body cells, gut epithelium, as well as hemolymph. However, there are exceptions, including Gammaproteobacteria that share bacteriome with Vidania, or Alphaproteobacteria that colonize Sulcia cells. We discuss how planthopper symbiont localization correlates with their acquisition and replacement patterns and the symbionts' likely functions. We also discuss the evolutionary consequences, constraints, and significance of these findings.

Completeness analysis for over 3000 United States bee species identifies persistent data gap

Native bee species in the United States provide invaluable pollination services. Concerns about native bee declines are growing, and there are calls for a national monitoring program. Documenting species ranges at ecologically meaningful scales through coverage completeness analysis is a fundamental step to track bees from species to communities. It may take decades before all existing bee specimens are digitized, so projections are needed now to focus future research and management efforts. From 1.923 million records, we created range maps for nearly 88% (3158 species) of bee species in the contiguous United States, provided the first analysis of inventory completeness for digitized specimens of a major insect clade, and perhaps most important, estimated spatial completeness accounting for all known bee specimens in USA collections, including undigitized bee specimens. Completeness analyses were very low (3–37%) across four examined spatial resolutions when using the currently available bee specimen records. Adding a subset of observations from community science data sources did not significantly increase completeness, and adding a projected 4.7 million undigitized specimens increased completeness by only an additional 12–13%. Assessments of data, including projected specimen records, indicate persistent taxonomic and geographic deficiencies. In conjunction with expedited digitization, new inventories that integrate community science data with specimen‐based documentation will be required to close these gaps. A combined effort involving both strategic inventories and accelerated digitization campaigns is needed for a more complete understanding of USA bee distributions.

Pereboriidae: a Permian clade of hemipteran insects with disjunctive distribution between the Northern and Southern parts of Pangea

Pereboriidae: a Permian clade of hemipteran insects with disjunctive distribution between the Northern and Southern parts of Pangea

Multiple drivers and lineage-specific insect extinctions during the Permo–Triassic

The Permo–Triassic interval encompasses three extinction events including the most dramatic biological crisis of the Phanerozoic, the latest Permian mass extinction. However, their drivers and outcomes are poorly quantified and understood for terrestrial invertebrates, which we assess here for insects. We find a pattern with three extinctions: the Roadian/Wordian (≈266.9 Ma; extinction of 64.5% insect genera), the Permian/Triassic (≈252 Ma; extinction of 82.6% insect genera), and the Ladinian/Carnian boundaries (≈237 Ma; extinction of 74.8% insect genera). We also unveil a heterogeneous effect of these extinction events across the major insect clades. Because extinction events have impacted Permo–Triassic ecosystems, we investigate the influence of abiotic and biotic factors on insect diversification dynamics and find that changes in floral assemblages are likely the strongest drivers of insects’ responses throughout the Permo–Triassic. We also assess the effect of diversity dependence between three insect guilds; an effect ubiquitously found in current ecosystems. We find that herbivores held a central position in the Permo–Triassic interaction network. Our study reveals high levels of insect extinction that profoundly shaped the evolutionary history of the most diverse non-microbial lineage.

Resource Availability Affects Seasonal Trajectories of Population-Level Learning.

AbstractEnvironmental effects on learning are well known, such as cognition that is mediated by nutritional consumption. Less known is how seasonally variable environments affect phenological trajectories of learning. Here, we test the hypothesis that nutritional availability affects seasonal trajectories of population-level learning in species with developmentally plastic cognition. We test this in bumble bees (Apidae: Bombus), a clade of eusocial insects that produce individuals at different time points across their reproductive season and exhibit organ developmental plasticity in response to nutritional consumption. To accomplish this, we develop a theoretical model that simulates learning development across a reproductive season for a colony parameterized with observed life history data. Our model finds two qualitative seasonal trajectories of learning: (1) an increase in learning across the season and (2) no change in learning across the season. We also find these two qualitative trajectories revealed by empirical learning data; the proportion of workers successfully completing a learning test increases across a season for two bumble bee species (Bombus auricomus, Bombus pensylvanicus) but does not change for another three (Bombus bimaculatus, Bombus griseocollis, Bombus impatiens). This study supports the novel consideration that resources affect seasonal trajectories of population-level learning in species with developmentally plastic cognition.

New stem-dictyopteran insects from the Pennsylvanian deposits at Mazon Creek and Sosnowiec (Insecta: Polyneoptera)

ABSTRACT Polyneopteran clade of insects is very diverse and has a remarkable fossil history starting in the Late Palaeozoic. Representatives of Dictyoptera comprise roaches, termites and mantids and their stem group relatives like the common Palaeozoic and Mesozoic roachoids, a group well known for its problematic taxonomy. In this study, two new taxa are described based on forewing venation well displaying convexity or concavity of the veins due to preservation in spherosideritic concretions. A new paoliid, Stephanopsis testai sp. nov. (Blattinopsidae), from Moscovian deposits at Mazon Creek (Illinois, U.S.A.), supplements Stephanopsis mirandus found at the same locality, which mainly differs in the branching patterns of MP and anal veins. A new stem dictyopteran, Sosnowiecia dareki gen. nov. et sp. nov. (?Mesorthopteridae), from Langsettian deposits at Sosnowiec-Klimontów (Lower Silesia, Poland) is problematic in terms of taxonomy as it has a mosaic of characters characteristic of Paoliida, Eoblattida and Grylloblattida, but retains affinities with roachoid insects, such as Miroblatta sp. Hence, these two new species increase the diversity of Carboniferous polyneopteran insects, but reveals the problem of depending only on alar characters in taxonomy. LSID urn:lsid:zoobank.org:pub:49299826-0F1E-4892-8D88-82FBDCC192BF

Early diversifications of angiosperms and their insect pollinators: were they unlinked?

The present-day ubiquity of angiosperm-insect pollination has led to the hypothesis that these two groups coevolved early in their evolutionary history. However, recent fossil discoveries and fossil-calibrated molecular dating analyses challenge the notion that early diversifications of angiosperms and insects were inextricably linked. In this article, we examine (i) the discrepancies between dates of emergence for angiosperms and major clades of insects; (ii) the long history of gymnosperm-insect pollination modes, which likely shaped early angiosperm-insect pollination mutualisms; and (iii) how the K-Pg (Cretaceous-Paleogene) mass extinction event was vital in propelling modern angiosperm-insect mutualisms. We posit that the early diversifications of angiosperms and their insect pollinators were largely decoupled until the end of the Cretaceous.

Geographic isolation drives speciation in Nearctic aphids

Across herbivorous insect clades, species richness and host-use diversity tend to positively covary. This could be because host-use divergence drives speciation, or because it raises the ecological limits on species richness. To evaluate these hypotheses, we performed phylogenetic path model analyses of the species diversity of Nearctic aphids. Here, we show that variation in the species richness of aphid clades is caused mainly by host-use divergence, whereas variation in speciation rates is caused more by divergence in non-host-related niche variables. Aphid speciation is affected by both the evolution of host and non-host-related niche components, but the former is largely caused by the latter. Thus, our analyses suggest that host-use divergence can both raise the ecological limits on species richness and drive speciation, although in the latter case, host-use divergence tends to be a step along the causal path leading from non-host-related niche evolution to speciation.

Transposons and non-coding regions drive the intrafamily differences of genome size in insects

SummaryGenome size (GS) can vary considerably between phylogenetically close species, but the landscape of GS changes in insects remain largely unclear. To better understand the specific evolutionary factors that determine GS in insects, we examined flow cytometry-based published GS data from 1,326 insect species, spanning 700 genera, 155 families, and 21 orders. Model fitting showed that GS generally followed an Ornstein–Uhlenbeck adaptive evolutionary model in Insecta overall. Ancestral reconstruction indicated a likely GS of 1,069 Mb, suggesting that most insect clades appeared to undergo massive genome expansions or contractions. Quantification of genomic components in 56 species from nine families in four insect orders revealed that the proliferation of transposable elements contributed to high variation in GS between close species, such as within Coleoptera. This study sheds lights on the pattern of GS variation in insects and provides a better understanding of insect GS evolution.

Estimating the Drivers of Diversification of Stoneflies Through Time and the Limits of Their Fossil Record

AbstractDeciphering the timing of lineage diversification and extinction has greatly benefited in the last decade from methodological developments in fossil-based analyses. If these advances are increasingly used to study the past dynamics of vertebrates, other taxa such as insects remain relatively neglected. Our understanding of how insect clades waxed and waned or of the impact of major paleoenvironmental changes during their periods of diversification and extinction (mass extinction) are rarely investigated. Here, we compile and analyze the fossil record of Plecoptera (1,742 vetted occurrences) to investigate their genus-level diversification and diversity dynamics using a Bayesian process-based model that incorporates temporal preservation biases. We found that the Permian-Triassic mass extinction has drastically impacted Plecoptera, while the Cretaceous Terrestrial Revolution corresponds with a turnover of plecopteran fauna. We also unveiled three major gaps in the plecopteran fossil record: the Carboniferous-Permian transition, the late Early Cretaceous, and the late Cenomanian to Bartonian, which will need to be further investigated. Based on the life history of extant Plecoptera, we investigate the correlations between their past dynamic and a series of biotic (Red Queen hypothesis) and abiotic (Court Jester hypothesis) factors. These analyses highlight the major role of continental fragmentation in the evolutionary history of stoneflies, which is in line with phylogeny-based biogeographic analyses showing how vicariance drove their diversification. Our study advocates analyzing the fossil record with caution, while attempting to unveil the diversification and extinction periods plus the likely triggers of these past dynamics of diversification.

Atypical strategies for cuticle pigmentation in the blood-feeding hemipteran Rhodnius prolixus.

Pigmentation in insects has been linked to mate selection and predator evasion, thus representing an important aspect for natural selection. Insect body color is classically associated to the activity of tyrosine pathway enzymes, and eye color to pigment synthesis through the tryptophan and guanine pathways, and their transport by ATP-binding cassette proteins. Among the hemiptera, the genetic basis for pigmentation in kissing bugs such as Rhodnius prolixus, that transmit Chagas disease to humans, has not been addressed. Here, we report the functional analysis of R. prolixus eye and cuticle pigmentation genes. Consistent with data for most insect clades, we show that knockdown for yellow results in a yellow cuticle, while scarlet and cinnabar knockdowns display red eyes as well as cuticle phenotypes. In addition, tyrosine pathway aaNATpreto knockdown resulted in a striking dark cuticle that displays no color pattern or UV reflectance. In contrast, knockdown of ebony and tan, that encode N-beta-alanyl dopamine hydroxylase branch tyrosine pathway enzymes, did not generate the expected dark and light brown phenotypes, respectively, as reported for other insects. We hypothesize that R. prolixus, which requires tyrosine pathway enzymes for detoxification from the blood diet, evolved an unusual strategy for cuticle pigmentation based on the preferential use of a color erasing function of the aaNATpreto tyrosine pathway branch. We also show that genes classically involved in the generation and transport of eye pigments regulate red body color in R. prolixus. This is the first systematic approach to identify the genes responsible for the generation of color in a blood-feeding hemiptera, providing potential visible markers for future transgenesis.