Winged insects (Pterygota) comprise three extant lineages whose order of divergence has never been settled: mayflies (Ephemeroptera), dragonflies and damselflies (Odonata), and the remaining winged orders (Neoptera). The source study (Blanke et al. 2012) revived the classical Palaeoptera hypothesis — Odonata + Ephemeroptera as a clade sister to Neoptera — from head morphology, while itself calling for re-evaluation with broad analyses integrating extensive molecular data and scrutiny of its proposed synapomorphies. A decade of subsequent work has deepened rather than settled the question: phylogenomic data give overall support to Palaeoptera but hide substantial conflicting signal for Chiastomyaria, mitochondrial genomes variously support all three possible topologies, and morphological arguments for Metapterygota continue to appear through 2026. The open problem is to determine the true basal pterygote branching — Palaeoptera, Metapterygota, or Chiastomyaria — by integrating well-documented morphology of all organ systems with extensive molecular data under controls for the identified systematic errors (outgroup choice, sparse sampling of basal lineages, compositional and long-branch effects, possible ancient rapid radiation), and in doing so to test whether the proposed head synapomorphies of Palaeoptera are genuine shared derived characters or correlated/homoplastic features.

Background

The winged insects, or Pterygota, are the most speciose animal group, and their extant diversity falls into three great lineages: Ephemeroptera (mayflies, aquatic juveniles with a unique winged preadult stage), Odonata (dragonflies and damselflies, aquatic predatory juveniles), and Neoptera (all remaining winged orders, united by the ability to fold the wings back over the abdomen). Because this trichotomy is the oldest branching event within winged insects, its resolution governs how we infer the origin of insect flight, the evolution of the flight apparatus, and whether the earliest winged insects were aquatic or terrestrial. Three mutually exclusive hypotheses compete. The Palaeoptera hypothesis groups Ephemeroptera and Odonata as a clade (characterized historically by wings held outstretched and unable to fold over the body) sister to Neoptera. The Metapterygota hypothesis instead places Ephemeroptera as the sister of all other winged insects, uniting Odonata with Neoptera on characters such as the absence of a winged subimago stage outside mayflies, mandibular articulation, and sperm-transfer features. The Chiastomyaria hypothesis places Odonata as the sister of the remaining Pterygota, i.e. groups Ephemeroptera with Neoptera. In cladistic methodology, a synapomorphy is a derived character shared by taxa due to common ancestry (evidence for a clade), whereas homoplasy is similarity arising independently by convergence or reversal (misleading evidence); an autapomorphy is a derived character unique to a single lineage and carries no grouping information. Morphological phylogenetics scores characters such as head structures across taxa and infers the tree by parsimony (preferring the tree requiring fewest character-state changes). Blanke et al. (2012) compiled a matrix of head characters — including antennal architecture (the pedicel is the second antennal segment), maxillary and labial musculature, and mandibular articulation — across the winged insects and their wingless relatives (bristletails and silverfish), and found parsimony analysis of these data unambiguously supports Palaeoptera, with Odonata and Ephemeroptera sharing presumably derived features of the antenna, maxilla, and labial musculature. A companion morphometric study (Blanke et al. 2013, Systematic Biology) showed that the supportive head signal is not explained by concerted convergence in feeding apparatus geometry. However, molecular data have never agreed: analyses of nuclear ribosomal genes and of whole mitochondrial genomes have variously been reported in support of all three hypotheses — mitochondrial genomes alone have, in different studies, supported each of the three — with outgroup choice (the selection of wingless relatives used to root the tree), limited taxon sampling of the species-poor basal lineages, compositional heterogeneity (lineage-to-lineage differences in nucleotide or amino-acid frequencies), long-branch attraction (the artifactual grouping of fast-evolving lineages), and a probable ancient rapid radiation (closely spaced divergence events yielding short internal branches and weak signal) identified as major sources of systematic error. A dedicated reanalysis of phylogenomic data (Simon et al. 2018) found overall support for Palaeoptera alongside substantial hidden signal for Chiastomyaria, small shifts in which can flip the strongly supported topology, and concluded that morphology-based tests were still restricted to head characters, leaving the problem open.

Problem Statement

Resolve the basal branching of the winged insects: determine which of the three competing hypotheses — Palaeoptera (Ephemeroptera + Odonata as sister clade of Neoptera), Metapterygota (Ephemeroptera sister to Odonata + Neoptera), or Chiastomyaria (Odonata sister to Ephemeroptera + Neoptera) — represents the true evolutionary relationships, by integrating well-documented morphological characters of all body regions with extensive molecular data (broad taxon sampling including basal extant lineages and, where character preservation permits, extinct taxa), under explicit controls for the systematic error sources established in this literature: outgroup choice, sparse taxon sampling of the species-poor basal lineages, compositional heterogeneity and long-branch attraction, and a possible ancient rapid radiation. This objective jointly requires, as scientifically linked components: (i) a decisive, well-supported topology for the Ephemeroptera/Odonata/Neoptera trichotomy whose support is demonstrably robust to the known sources of systematic error rather than an artifact of dataset or model choice; and (ii) a verdict on the proposed head-character synapomorphies of Palaeoptera (including the antennal characters such as the elongated pedicel and associated reductions) — whether they are genuine shared derived characters of Odonata + Ephemeroptera, or correlated with general antennal reduction or otherwise homoplastic and evolutionarily independent — so that morphology and molecules converge on one well-founded evolutionary scenario for the earliest pterygote divergence.

References

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