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Polyneoptera

Polyneoptera is a major clade of hemimetabolous within the superorder Neoptera, encompassing approximately 40,000 described extant species distributed across 10 traditional orders, including (grasshoppers, crickets, and katydids), (cockroaches and termites), Mantodea (mantises), (stick insects and leaf insects), Dermaptera (earwigs), (stoneflies), (webspinners), (angel insects), Grylloblattodea (rock crawlers), and Mantophasmatodea (gladiators). These orders represent a diverse array of terrestrial and semi-aquatic forms, with many species playing significant ecological roles as herbivores, predators, decomposers, and occasional pests or disease vectors. A defining synapomorphy of Polyneoptera is the presence of a fan-like anal region in the hind s, which folds efficiently over the , facilitating wing flexion and protection during through vegetation or soil. Most polyneopterans exhibit incomplete , with nymphs resembling wingless or partially winged adults and undergoing gradual development through multiple instars. Ancestral traits include biting-chewing mouthparts adapted for a wide range of diets—from omnivory and herbivory to carnivory—and elongate, segmented abdominal cerci or other appendages for sensory or defensive functions. Forewings are often thickened into protective tegmina or elytra-like structures in several groups, such as and , enhancing durability in ground-dwelling or plant-climbing lifestyles. Phylogenetically, Polyneoptera originated around 400 million years ago during the period, with early ancestors likely terrestrial and wing evolution initially serving gliding functions rather than powered flight in aquatic settings. Molecular and morphological studies support its monophyly, though internal relationships remain debated, with robust clades like ( + Isoptera + Mantodea) and (Ensifera + ) emerging consistently. Social behaviors, such as in or subsocial care in earwigs, have evolved convergently multiple times within the group, highlighting its . Polyneoptera's evolutionary history underscores the transition from terrestrial pioneers to modern biodiversity hotspots, influencing ecosystems through pollination, pest dynamics, and as indicators of environmental health.

Characteristics

Morphology

Polyneoptera are characterized by a suite of shared morphological traits that distinguish them from other insect lineages, particularly in their wing structure and overall adapted for terrestrial lifestyles. A key synapomorphy is the presence of an enlarged anal in the hindwings, consisting of radiating veins that allow the wings to fold compactly like a fan when at rest, typically concealed beneath the forewings. This folding mechanism enables efficient storage and deployment during flight, though some orders exhibit reductions or modifications. In many polyneopteran orders, the forewings are modified into leathery tegmina, which are thickened and sclerotized to provide protection for the delicate hindwings and often serve roles in or . The mouthparts of Polyneoptera are predominantly type, equipped with robust mandibles suited for processing plant material, , or other , reflecting their primarily herbivorous or detritivorous diets. On the , all polyneopterans bear cerci—paired sensory appendages at the terminal segment—that vary in form and function across orders, from filiform sensors for environmental detection to more specialized structures. The comprises three distinct segments: the , mesothorax, and metathorax, with approximately equal dimensions that support diverse locomotor adaptations such as running or jumping. Representative examples illustrate these traits' variations. In (e.g., grasshoppers and crickets), the hind legs feature elongated femora and tibiae, with powerful extensor muscles enabling explosive jumps for escape or predation. Conversely, in Dermaptera (earwigs), the cerci are modified into forceps-like pincers, used for defense, prey capture, or folding wings, and exhibit with males having more curved forms.

Life Cycle

Polyneoptera exhibit hemimetabolous, or incomplete, , characterized by a gradual transformation through three primary life stages: , , and , without an intervening pupal stage. This developmental pattern, known as paurometabolism, allows nymphs to progressively develop features resembling those of the adult form while remaining active and feeding throughout their growth. The life cycle begins with the stage, where females typically deposit eggs in protective structures such as oothecae or pods within or tissues, providing safeguards against and predation. Hatching produces that closely resemble miniature adults but lack fully developed and reproductive organs. Nymphs undergo a variable number of instars (typically 4 to 15, but up to 30 or more in some species like stoneflies), marked by molts that enable incremental growth and maturation. During these instars, external wing pads appear and expand progressively, with fan-like hindwings becoming evident in later stages as the nymph approaches adulthood. The final molt yields the winged adult, capable of , completing the direct developmental trajectory without a larval-pupal transformation. While paurometabolism is the norm across Polyneoptera, variations exist; for instance, in (webspinners), nymphs in early instars possess specialized silk-producing glands in the foretarsi, enabling them to construct protective galleries from hatching onward, a shared with adults. Reproductive strategies emphasize oviposition in concealed sites like crevices or plant material, often in clusters encased for protection, facilitating survival in diverse terrestrial habitats. The overall lifespan from to death in Polyneoptera varies widely from several months to several years, depending on the and environmental factors such as , which accelerates and molting at higher levels while potentially shortening longevity. Lower temperatures prolong nymphal instars, extending the total cycle duration.

Classification

Extant Orders

Polyneoptera encompasses approximately 45,000–50,000 described extant species distributed across 10 orders, representing a significant portion of insect biodiversity with diverse morphologies and ecologies. These orders include , , Mantodea, , Dermaptera, , , , Grylloblattodea, and Mantophasmatodea; recent molecular studies support merging the last two into the single order based on shared morphological and molecular traits such as elongated cerci and similar structures, potentially reducing the count to 9 orders. Orthoptera (grasshoppers, crickets, katydids) is the most species-rich order within Polyneoptera, comprising about 30,000 species worldwide, characterized by powerful hind legs adapted for jumping and many species capable of for acoustic communication via wing rubbing or leg friction. These primarily herbivorous inhabit terrestrial environments, with some exhibiting migratory behaviors like swarms. Blattodea (cockroaches and ) includes roughly 7,500 species, notable for the social in , which form complex colonies with differentiation including workers, soldiers, and reproductives, while are often solitary with flattened bodies for navigating crevices. , in particular, rely on symbiotic gut microbes for digestion, enabling wood decomposition. Mantodea (mantises) consists of approximately 2,400 species, distinguished by forelegs for grasping prey, swiveling heads for enhanced vision, and , making them ambush predators predominantly in tropical regions. Phasmatodea (stick and leaf insects) features around 3,500 species, renowned for their extreme of twigs or leaves as a defense mechanism, with many parthenogenetic populations and slow movements to evade detection; most are herbivores feeding on foliage. Dermaptera (earwigs) encompasses about 2,000 , identified by their pincer-like cerci at the abdomen's end used for , prey capture, or folding wings beneath short tegmina, and they exhibit by guarding eggs and nymphs. Plecoptera (stoneflies) contains more than 4,000 , with aquatic nymphs featuring and adults often weak fliers associated with riparian zones; they serve as key indicators of due to their sensitivity to . Embioptera (webspinners) has approximately 400 species, unique for their silk-producing glands in the fore tarsi used to construct communal tunnel systems in or , where colonies of females and nymphs reside, feeding on mosses and . Zoraptera (angel insects) is one of the smallest orders with about 50 species, living gregariously in decaying wood, where winged and wingless forms coexist; they scavenge on fungi and mites using chewing mouthparts. Grylloblattodea (rock crawlers or ice crawlers) includes around 35 , adapted to cold, high-altitude environments with omnivorous habits, blending traits of and , such as long antennae and wingless bodies. Mantophasmatodea (gladiators or heelwalkers) is the rarest order with fewer than 20 , known from arid regions, featuring predatory behaviors with spiny legs and a posture where the abdomen is elevated; they are nocturnal hunters of small arthropods.

Fossil Taxa

The fossil record of Polyneoptera is sparse compared to other superorders, primarily due to their predominantly terrestrial lifestyles, which limit preservation to exceptional conditions such as fine-grained sediments forming compressions or in . These challenges result in a biased representation favoring small-bodied forms in deposits and larger winged specimens in sedimentary compressions, with overall rarity reflecting the group's avoidance of or environments. The earliest known polyneopteran fossils date to the Late , around 311 million years ago, exemplified by Archimylacris eggintoni, a stem-group dictyopteran from the Duckmantian stage in the Coseley of , . This species, preserved as a three-dimensional fossil via , exhibits primitive traits like elongated forewings with reduced venation, linking it to the broader through plesiomorphic features such as potential cerci and omnivorous mandibles. Key sites like the Mazon Creek in , , yield additional early polyneopterans, including proto-orthopterans and blattodeans, preserved in nodules that capture a diverse swampy . Notable extinct lineages within Polyneoptera include the , a group of giant predatory insects spanning the late to (approximately 300–200 million years ago), characterized by forelegs with stout spines and wingspans reaching up to 400 mm in species like Gigatitan vulgaris. These orthopteroid forms, often classified within Polyneoptera due to shared wing bracing and venation patterns, preyed on other insects, invertebrates, and possibly small tetrapods, with fossils primarily from outcrops in (e.g., ) and , as well as a recent discovery of Magnatitan jongheoni from the Upper Hasangdong Formation in . sites in and further document polyneopteran diversification, including orthopterans and plecopterans in lacustrine deposits. Recent discoveries have illuminated the Mesozoic record, such as Anisyutkin et al. (2022), who described new embiopteran genera and species from mid-Cretaceous (ca. 99 Ma), revealing plesiomorphic traits like postocular carinae and ocelli that refine subfamily diagnoses and highlight early diversification of webspinners within Polyneoptera. The fossil record indicates extinct polyneopteran was likely 20–30% higher than extant levels, driven by radiations in orthopteroids and plecopterans before selective extinctions reduced richness.

Evolutionary History

Phylogenetic Relationships

The monophyly of Polyneoptera is supported by shared morphological traits, such as the presence of an anal fan in the hindwing, which consists of multiple anal veins forming a fan-like structure during flight, and reinforced by genomic analyses demonstrating consistent molecular synapomorphies across the group. These traits distinguish Polyneoptera from other neopteran lineages and are evident in both extant and fossil taxa, providing a robust foundation for reconstructing internal relationships. Phylogenetic studies of Polyneoptera integrate morphological characters, including wing venation patterns and thoracic structures, with molecular data from sources like 18S rRNA genes, mitochondrial genomes, and large-scale transcriptomic datasets. Early molecular approaches using ribosomal RNA highlighted monophyly and basic clades but struggled with deep divergences due to long-branch attraction artifacts, while recent phylogenomic efforts employing thousands of protein-coding genes have improved resolution through maximum likelihood and Bayesian methods. A landmark study using transcriptomic data from 106 species across Polyneoptera recovered a well-supported phylogeny, with Dermaptera (earwigs) and forming a basal to the remaining lineages, followed by (stoneflies) as to a core Polyneoptera . Within this core, (comprising and Mantodea) emerges as a monophyletic , while (Grylloblattodea and Mantophasmatodea) is strongly supported as to (grasshoppers and crickets). Additionally, (webspinners) and (stick ) form the Eukinolabia, positioned to related groups. This , derived from 3,014 protein-coding genes, underscores multiple origins of key traits like wing reduction. Post-2020 phylogenomic analyses have refined specific placements within Polyneoptera, including internal relationships in , while the broader structure from prior work, including the sister-group relationship of to in Eukinolabia, is maintained. These updates integrate and maximum likelihood trees, resolving ambiguities in Eukinolabia. Despite these advances, controversies persist regarding the exact positions of certain orders. The placement of varies across studies, with some molecular datasets supporting it as sister to alone, while others align it within a broader clade including additional orthopterans; morphological evidence from structure contributes to this instability. Similarly, support for Dermaptera remains unstable, often shifting between basal positions with or allying with in alternative analyses, reflecting challenges in modeling compositional heterogeneity in phylogenomic data.

Origins and Diversification

The Polyneoptera superorder is estimated to have originated during the Late Devonian to Early period, approximately 350–300 million years ago (Ma), arising from stem-group ancestors. Fossil evidence indicates that the earliest polyneopterans appeared in the Early , representing a radiation about 53 million years earlier than previously suggested by molecular data alone. Although earlier hypotheses proposed aquatic origins linked to the aquatic nymphal stages of , comprehensive phylogenomic analyses support a fully terrestrial last common ancestor for Polyneoptera, with long appendages and biting mouthparts adapted to land-based lifestyles. Wings in this lineage evolved on land, not in aquatic environments, marking a key adaptation for terrestrial dispersal. Major diversification events within Polyneoptera followed significant geological upheavals, including a post-extinction diversification in the following the end-Permian mass around 252 Ma, which reshaped terrestrial ecosystems. This radiation was followed by further pulses in the , with recovery and expansion amid fluctuating atmospheric oxygen levels that initially constrained but later facilitated growth. The period saw another surge in insect diversification, driven by the rise of angiosperms. Key transitional events, such as those across the - boundary, shaped the dominance of , with fossil records showing Late extinctions followed by recoveries that established orthopterans as prominent herbivores. Survival through the -Paleogene (K-Pg) boundary extinction around 66 Ma was bolstered by terrestrial adaptability, including resilient life history strategies that allowed polyneopterans to endure habitat disruptions. Recent phylogenomic research, initiated by Misof et al. (2014) using transcriptomes from 144 species, has resolved the timing of polyneopteran and revealed several major shifts in diversification rates across the group's history. This work has been extended through the 1KITE (1K Insect Transcriptome ) project, incorporating thousands of s to refine these patterns, with several shifts aligning with polyneopteran radiations tied to environmental changes. Drivers of this diversification include co- with , which provided new ecological niches. The conserved trait of incomplete (hemimetaboly) further enhanced , enabling rapid development and adaptability to variable terrestrial conditions without the vulnerabilities of complete . Future research directions emphasize the need for more fossil-calibrated phylogenies to resolve basal nodes and refine estimates, integrating additional genomic with stratigraphic to better understand early polyneopteran splits.

Diversity and Ecology

Polyneoptera encompasses approximately 50,000 described (as of 2025) across its ten extant orders, representing a significant portion of despite comprising only about 5% of the roughly 1 million known worldwide. This total is derived from major orders such as with over 29,000 , (including ) with around 7,500 , with more than 3,500 , with about 3,700 , and Mantodea with approximately 2,400 , while smaller orders like Dermaptera (~2,000 ), Embioptera (~450 ), Zoraptera (~50 ), Grylloblattodea (~35 ), and Mantophasmatodea (~20 ) contribute fewer taxa. Estimates suggest the true diversity could reach up to 100,000 when accounting for undescribed taxa, particularly in tropical regions where exhibit high cryptic diversity and ongoing discoveries in understudied forest habitats, including recent descriptions of new in 2024–2025 via molecular barcoding. Species richness within Polyneoptera is highly skewed, with accounting for roughly 59% of described species—dominated by diverse suborders like Ensifera (crickets and katydids) and (grasshoppers)—and comprising about 15%, driven by the ecological success of both and in varied habitats. In contrast, minor orders such as include fewer than 100 species, mostly restricted to tropical leaf litter and wood, highlighting the uneven across the . is pronounced in isolated regions, exemplified by Mantophasmatodea, all of whose ~20 species are confined to the arid landscapes of , particularly and , where they represent relict populations adapted to unique microhabitats like rocky outcrops. Conservation concerns are mounting due to habitat loss and fragmentation, particularly in tropical and temperate ecosystems undergoing and urbanization. Key groups like serve as critical indicators of , with many listed on the as vulnerable or endangered owing to and hydrological alterations in freshwater systems; for instance, certain and North stonefly taxa have declined sharply, signaling broader aquatic degradation, and about 26% of are threatened. Discovery trends continue apace through molecular barcoding initiatives, which have accelerated identification of cryptic in orders like and , with the Polyneoptera Species File (Version 5.0) serving as a taxonomic database integrating nomenclatural, distributional, and genetic data across orders. Despite their moderate share of global insect diversity, Polyneoptera exert outsized ecological influence through roles in herbivory, , and , underscoring the urgency of conserving this group's uneven but vital .

Ecological Roles

Polyneoptera play diverse trophic roles in ecosystems, primarily as herbivores, detritivores, predators, and decomposers, contributing to and dynamics. Orthopterans, such as grasshoppers and locusts, and phasmatodeans, including stick , are significant herbivores that consume foliage, stems, and other plant parts, influencing structure and serving as primary consumers in terrestrial food webs. Blattodeans, encompassing and , function as key detritivores by breaking down decaying , facilitating and recycling in soils and forest floors. In predatory roles, mantodeans act as apex predators in arthropod communities, ambushing and consuming a wide range of insects, which regulates prey populations and exerts top-down control in terrestrial food webs. Plecopterans, or stoneflies, occupy central positions in aquatic food webs as both predators and prey; their nymphs prey on smaller invertebrates like mayfly larvae while serving as food for fish and birds, thus mediating energy transfer between detrital and predatory pathways in streams. Although not primary pollinators, some polyneopterans contribute minor roles to ; for instance, certain orthopterans like katydids visit flowers and transfer , while camel crickets aid in by consuming and excreting viable seeds of plants. Plecopterans serve as indicator for stream health due to their sensitivity to and habitat , with their presence signaling clean, oxygenated waters. Migratory locusts within exhibit heightened outbreak risks under , as warmer temperatures and altered rainfall patterns promote breeding and swarming, amplifying herbivory impacts on vegetation and agriculture. Human interactions with polyneopterans are dual-edged: locusts and act as major pests by devastating crops and structures, whereas provide benefits as prey in food chains and as edible protein sources in various cultures. Culturally, these insects feature in folklore across and beyond, symbolizing fertility, destruction, or spiritual entities in myths, art, and rituals involving grasshoppers, locusts, and . Symbiotic relationships enhance polyneopteran , particularly in , where gut microbes enable efficient lignocellulose through enzymatic of walls, supporting and energy acquisition from wood.

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