The winged insects (Pterygota) comprise three main lineages — mayflies (Ephemeroptera), dragonflies and damselflies (Odonata), and all remaining winged insects (Neoptera) — and the order in which these three lineages split from their common ancestor remains one of the longest-standing open questions in insect systematics. Three competing hypotheses — Palaeoptera (Ephemeroptera + Odonata), Metapterygota (Odonata + Neoptera), and Chiastomyaria (Odonata basal to Ephemeroptera + Neoptera) — have each received strong apparent support from different datasets. A phylogenomic (expressed-sequence-tag supermatrix) study by Simon, Strauss, von Haeseler and Hadrys (2009) reported conclusive support for Chiastomyaria, but subsequent phylogenomic, morphological, relaxed-clock, and mitogenomic analyses have recovered all three topologies and shown the node to be highly sensitive to outgroup choice, taxon sampling, and substitution-model misspecification. The problem therefore remains open: no analysis to date has resolved the basal pterygote branching order in a way that is demonstrably robust to systematic error.

Background

Pterygota, the winged insects, originated in the Devonian (roughly 400 million years ago) and split early into three extant lineages: Ephemeroptera (mayflies, aquatic nymphs with non-folding wings), Odonata (dragonflies and damselflies, also with non-folding wings and aquatic juveniles), and Neoptera (all other winged insects, unified by the ability to fold their wings over the abdomen). Because the three lineages apparently diverged within a short geological window, the internal branches (internodes) of the tree connecting them are extremely short, and the two outgroup lineages have had hundreds of millions of years to accumulate substitutions, so the phylogenetic signal tracking the true split order is weak and easily overprinted by systematic error. Three hypotheses have been debated for over a century: (1) Palaeoptera, grouping Ephemeroptera + Odonata as sister to Neoptera; (2) Metapterygota, grouping Odonata + Neoptera with Ephemeroptera basal (historically favored by morphologists on wing-vein, mandibular, and respiratory characters); and (3) Chiastomyaria, placing Odonata as the sister group of Ephemeroptera + Neoptera. Single-gene and few-gene analyses never settled the question. A phylogenomic approach concatenates many genes into a supermatrix to accumulate signal; expressed sequence tags (ESTs) are fragments of transcribed genes sampled by sequencing random cDNA clones. The source study (Simon et al. 2009) added new EST data for the then-unsampled crucial orders (the mayfly Baetis and the damselfly Ischnura elegans) and analyzed two concatenated matrices — 15 taxa / 125 genes / 31,643 amino-acid positions and 8 taxa / 150 genes / 42,541 positions — under maximum likelihood and Bayesian inference, placing Odonata at the base of the winged insects and statistically rejecting Palaeoptera and Metapterygota. The authors themselves cautioned that systematic biases could mislead the result: long-branch attraction (LBA), the artifact whereby rapidly evolving lineages are pulled together as artificial sister groups; substitution-model misspecification; and the very limited taxon sampling. Which topology is correct matters biologically because the first pterygote split determines the ancestral condition of the winged insect — in particular whether the ancestor could already fold its wings, and which lineage's flight apparatus is ancestral versus derived — making this node, known as the Palaeoptera problem, central to scenarios for the origin of insect flight.

Problem Statement

Determine the true branching order of the three principal winged-insect lineages — Ephemeroptera (mayflies), Odonata (dragonflies and damselflies), and Neoptera (all other winged insects) — that is, establish which of the three competing hypotheses is correct: Palaeoptera (Ephemeroptera + Odonata as sister to Neoptera), Metapterygota (Odonata + Neoptera with Ephemeroptera basal), or Chiastomyaria (Odonata basal to Ephemeroptera + Neoptera, the topology supported by Simon et al. 2009). A valid resolution must demonstrate that the recovered topology is robust to the recognized sources of systematic error at this node — long-branch attraction, outgroup choice, limited taxon sampling, and substitution-model misspecification — by any defensible route, including comprehensive taxon sampling across the basal pterygote lineages, analyses under site-heterogeneous and composition-aware models of sequence evolution that can track the short ancient internodes created by the rapid mid-Devonian radiation, explicit signal-partition or quartet analyses quantifying support for each competing topology, and, where possible, congruence with morphological evidence beyond head characters and with the fossil record. A resolution counts as valid when the result is stable across outgroup choices and taxon subsets and under a composition-aware, site-heterogeneous model of sequence evolution, and formal topology tests either uniquely and significantly support one of the three hypotheses or fail to reject a hard polytomy. Correspondingly, an explicit conclusion that the node is unresolvable beyond a hard polytomy is itself a valid resolution, provided that the non-resolution is demonstrated to be robust to the same sources of systematic error. The problem also requires explaining why genome-scale datasets analyzed to date continue to recover different, strongly supported topologies for this same node.

References

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