Taxonomic generality of biomechanically inferred mechanical linkages among insect head characters and their power to resolve basal pterygote relationships (the Palaeoptera problem)

A 2017 study combined synchrotron micro-computed tomography, multibody dynamics analysis and finite-element analysis of the damselfly head to show that traditionally used head characters (ridges, endoskeletal elements, mandibular joints) are mechanically linked during biting, that these characters are statistically correlated in a morphological matrix, and that excluding the redundant correlated characters supports a sister-group relationship of dragonflies and mayflies (Palaeoptera). Whether this mechanical-linkage structure is taxonomically widespread, robust to modelling choices and empirical validation, and whether biomechanics-informed character exclusion stabilizes the still-contested relationships among Ephemeroptera, Odonata and Neoptera remains untested: no later study has built comparable models across the three lineages, retested the correlation structure, or repeated the phylogenetic exclusion analysis.

Background

The relationships among the earliest branches of winged insects (Pterygota) — mayflies (Ephemeroptera), dragonflies and damselflies (Odonata), and all remaining winged insects (Neoptera) — have resisted a century of debate. Three competing hypotheses circumscribe the node: Palaeoptera (Odonata + Ephemeroptera as sister groups), Metapterygota (Odonata + Neoptera), and Chiastomyaria (Ephemeroptera + Neoptera). Large-scale molecular datasets have not settled the question: a phylogenomic reanalysis found overall support for Palaeoptera but substantial hidden signal for Chiastomyaria, with inferred topologies switching under different models, taxon sampling and partitioning of genes. Morphological data have historically favoured Palaeoptera, but morphological characters risk being functionally correlated rather than independent, which can mislead phylogenetic inference. Head characters illustrate the problem: ridges, endoskeletal elements (internal apodermal supports of the head capsule) and mandibular joints may be mechanically interdependent because biting loads couple them into one structure, so their character states cannot evolve independently. Earlier work by Blanke and colleagues (2012, 2013) supported Palaeoptera from head characters and from a statistical detection of concerted convergence — correlated, repeated evolution of character states — while explicitly noting that correlation alone cannot distinguish adaptive convergence from the shared retention of ancestral states (concerted plesiomorphy), which mathematical convergence tests cannot detect. To give this debate an objective, functional foundation, Blanke, Watson, Holbrey and Fagan (2017) combined two engineering techniques for the first time with phylogenetics: multibody dynamics analysis (MDA), which simulates the motion of coupled rigid bodies — here the mandibles, their joints and their muscles — to predict muscle and joint reaction forces, and finite-element analysis (FEA), which computes stress and strain distributions within a structure — here the head capsule — under those loads. Their model, of unprecedented detail, was built for a single damselfly species, Lestes virens, from synchrotron radiation micro-computed tomography (SR-µCT, high-resolution X-ray tomography at a synchrotron source), yielding a mesh of 9.7 million elements. Biting simulations showed that a range of head characters are indeed mechanically linked, that these characters are highly significantly correlated in an existing morphological data matrix, and that phylogenetic tree reconstruction under data-exclusion schemes based on the correlation analysis unambiguously supports Palaeoptera. The authors themselves flagged the open issues this record addresses: intrinsic muscle stress had to be assumed as $25\ \mathrm{N\,cm^{-2}}$ (literature values for insects span $13.7$–$49\ \mathrm{N\,cm^{-2}}$); one small muscle connecting two movable parts (the M. hypopharyngomandibularis) had to be omitted; cuticle material properties ($E = 7.3\ \mathrm{GPa}$, $\nu = 0.3$) were taken from the literature rather than measured on the specimen; the predicted bite force (0.39 N) could only be compared with a measurement from a different dragonfly species; and load cases B and C used simplified, non-physiological muscle representations purely to probe sensitivity.

Problem Statement

Determine whether the mechanically inferred linkages among insect head characters identified in the damselfly Lestes virens — the coupling of ridges, endoskeletal elements and mandibular joints under biting load — are taxonomically widespread and robust, and whether excluding such mechanically linked (and hence non-independent) characters resolves the relationships of the basal winged insect lineages. Concretely, this requires: (i) building SR-µCT-based MDA+FEA head models comparable to the 2017 Lestes virens model for species spanning Odonata, Ephemeroptera, basal Neoptera and appropriate outgroups, and testing whether the same character sets are mechanically linked across them; (ii) establishing robustness to modelling choices — sensitivity of strains and linkage conclusions to the assumed intrinsic muscle stress (literature values span roughly $13.7$–$49\ \mathrm{N\,cm^{-2}}$), to literature-derived cuticle material properties, to the omission of muscles connecting two movable parts, and to simplified load cases — and validating the models against empirical data such as measured bite forces or in vivo muscle measurements for the modelled or closely related species; and (iii) analysing whether the mechanically linked characters are significantly correlated in a comparative morphological matrix across the broader taxon sample, and whether phylogenetic tree reconstruction under exclusion schemes for these correlated characters yields a stable resolution of the Ephemeroptera–Odonata–Neoptera branching order (Palaeoptera versus its alternatives). An answer in the negative — e.g., demonstration that the linkages are artefacts of the single-species model, that the characters are not correlated across a broad sample, or that exclusion does not alter or stabilize the inferred topology — resolves the question equally well.

References

1. Blanke A., Watson P.J., Holbrey R., Fagan M.J. (2017). Computational biomechanics changes our view on insect head evolution. Proceedings of the Royal Society B 284(1848): 20162412. DOI: 10.1098/rspb.2016.2412. https://doi.org/10.1098/rspb.2016.2412 (PMCID: PMC5310608)
2. Blanke A., Wipfler B., Letsch H., Koch M., Beckmann F., Beutel R., Misof B. (2012). Revival of Palaeoptera — head characters support a monophyletic origin of Odonata and Ephemeroptera (Insecta). Cladistics. DOI: 10.1111/j.1096-0031.2012.00405.x. https://doi.org/10.1111/j.1096-0031.2012.00405.x
3. Blanke A., Greve C., Wipfler B., Beutel R.G., Holland B.R., Misof B. (2013). The Identification of Concerted Convergence in Insect Heads Corroborates Palaeoptera. Systematic Biology. DOI: 10.1093/sysbio/sys091. https://doi.org/10.1093/sysbio/sys091
4. Blanke A., Pinheiro M., Watson P.J., Fagan M.J. (2018). A biomechanical analysis of prognathous and orthognathous insect head capsules: evidence for a many-to-one mapping of form to function. Journal of Evolutionary Biology. DOI: 10.1111/jeb.13251. https://doi.org/10.1111/jeb.13251
5. Büsse S., Gorb S.N. (2018). Material composition of the mouthpart cuticle in a damselfly larva (Insecta: Odonata) and its biomechanical significance. Royal Society Open Science. DOI: 10.1098/rsos.172117. https://doi.org/10.1098/rsos.172117
6. Simon S., Blanke A., Meusemann K. (2018). Reanalyzing the Palaeoptera problem — The origin of insect flight remains obscure. Arthropod Structure & Development. DOI: 10.1016/j.asd.2018.05.002. https://doi.org/10.1016/j.asd.2018.05.002
7. Boudinot B.E., Beutel R.G., Weingardt M., van de Kamp T., Hammel J.U., Li D., Richter A., Wipfler B. (2025). The insect head rewound: Clarifications to the groundplan of Hexapoda (Pancrustacea). Arthropod Structure & Development. DOI: 10.1016/j.asd.2025.101490. https://doi.org/10.1016/j.asd.2025.101490
8. Klunk C.L., Casadei-Ferreira A., Argenta M.A., Pie M.R. (2025). Ant head shape evolved to compromise bite-induced mechanical demands. bioRxiv preprint. DOI: 10.1101/2025.03.19.643247. https://doi.org/10.1101/2025.03.19.643247