Holasicia rasnitsyni, from Lutz Koch.

Belongs within: Panhexapoda.
Contains: Palaeoptera, Polyneoptera, Paraneoptera, Holometabola.

The Pterygota are the winged insects, the first group of animals to have evolved the power of flight. Ancestrally, two pairs of wings are present, though one pair of wings has been lost or modified in a number of sublineages.

The origin of insect wings
16 January 2010
Photo by Daniel Oakley.

Flight has evolved among animals on four separate occassions—birds, bats, pterosaurs and winged insects—and much speculation has arisen about the circumstances of each. For only one of these clades, the birds, do we have access to a detailed fossil record demonstrating how their wings evolved; for each of the others we are still forced to rely on more indirect evidence. Winged insects are without doubt the most mysterious of the four. Vertebrate wings are instantly recognisable as modications of pre-existing forelimbs, but insect wings (at least at first glance) appear to have arisen de novo, without obvious homologues in any other arthropod group.

A long-popular hypothesis was that insect wings were derived from paranotal lobes—lateral extensions of the thorax, originally not articulated and probably used for gliding. Proposed support for the paranotal hypothesis came from the presence in a number of Palaeozoic insect groups of just such lateral projections, complete with wing-like venation, on the first segment of the thorax in addition to the actual wings on the second and third segments (contrary to many popular accounts, these insects were not ‘six-winged’, because the anterior lobes were fixed in place and not mobile like wings). Smaller projections in thysanurans (silverfish), the living sister group to winged insects, do allow them limited gliding ability, further supporting the proposal.

Reconstruction of the Permian insect Lemmatophora by F. M. Carpenter, showing the large ‘wing-like’ prothoracic lobes. Image via Oceans of Kansas.

During the latter part of the last century, however, an alternative hypothesis became prominent. Kukalová-Peck (1987 and other publications) pointed out that a major problem with the paranotal theory is that the insect wing articulation is not a simple structure. Insect wings are articulated by a set of small plates surrounding the junction of the wings and the thorax. In Kukalová-Peck’s view, positing the development of this articulation completely de novo strained credulity. Instead, Kukalová-Peck proposed that the wings were derived from exites, lateral branches of the legs found in crustaceans. The fossil record of marine arthropods indicates that branched legs were part of the original arthropod ground-plan and many crustaceans that retain them show modifications of the exites into alternative structures. The gills of crabs and lobsters, for instance, are modified exites. According to Kukalová-Peck’s proposal, exites present in the ancestral insects were moved into a dorsal position on the thorax to give rise to the wings. As the exites would have been articulated from the start, this removed the question of how the wing articulation developed. Kukalová-Peck proposed that the exites had originally been developed as gills in aquatic ancestral insects – the two basalmost living orders of winged insects, mayflies and dragonflies, are both aquatic as nymphs (as are the stoneflies, which Kukalová-Peck regarded as the next most basal order), and mayfly nymphs have winglet-like gills on the abdomen. It was suggested that the original gills could have been transformed into wings via their development as sails for skimming across the water surface (many living stoneflies use their wings in this way). To clinch the deal, Kukalová-Peck (1987) described a number of Carboniferous insect fossils retaining exites on their legs. Strong support for an exite origin of wings came from studies of Drosophila development—many of the same genes are expressed in the development of Drosophila wings and crustacean gills, while cells involved in wing development migrate dorsally from the leg primordia (Shubin et al. 1997). By the late 1990s, the exite theory had become generally accepted.

Figure of Gerarus danielsi specimen from Kukalová-Peck & Brauckmann (1992), as reproduced in Béthoux & Briggs (2008), showing exites attached to the legs.

However, the question was far from settled. The exite theory centred around an aquatic origin for winged insects, but this is doubtful. Successive sister-groups to winged insects (silverfish and archaeognathans) are terrestrial, as were the palaeodictyopteroids, one of the earliest groups of winged insects. Living winged insects other than mayflies and dragonflies form a clade called Neoptera that was probably also ancestrally terrestrial (most current researchers no longer regard stoneflies as basal among neopterans—e.g. Terry & Whiting 2005). Adaptations to aquatic life in mayflies and dragonflies are very distinct, and the fossil and anatomical evidence suggests that these groups may have evolved aquatic nymphs independently. While fossils of winged insects are abundant by the Late Carboniferous, aquatic insects are not well-established in the fossil record until the Triassic nearly 100 million years later (Grimaldi & Engel 2005), though a small number of aquatic nymphs have been claimed for the Permian—interpretation of these specimens is currently debated (Beckemayer & Hall 2007). Though all the usual caveats around negative evidence still apply, the near or total absence of aquatic nymphs from Palaeozoic deposits contrasts strongly with their later abundance in Mesozoic and Cenozoic deposits, especially when one considers the presence of Carboniferous stem-dragonflies far larger than any later successor (such as the two-foot-plus-wingspan Meganeuropsis permiana) that might be expected to have had similarly robust nymphs.

Gliding ant Cephalotes atratus, by Alex Wild.

Also problematic is the complete absence of thoracic leg exites in any living insect, including archaeognathans and silverfish (Update: Günter Bechly has corrected me that thoracic exites are present in archaeognathans). It is not impossible that winged insects, silverfish and archaeognathans could have each lost their exites independently. Exites have been lost by numerous arthropod groups and their corresponding absence in arachnids and myriapods (centipedes and millipedes) suggests that the loss of exites is somehow closely connected to adoption of a terrestrial lifestyle (I think terrestrial isopods still have them). Besides, any amount of recent absences should be instantly trumped by the fossil presences recorded by Kukalová-Peck (1987). However, not all authors have accepted Kukalová-Peck’s interpretations. Béthoux & Briggs (2008) examined some of the specimens from which exites had been reported (including the stem-orthopteran Gerarus) and found that the supposed ‘exites’ were artefacts created by overenthusiastic specimen preparation. Whether any basal insect possessed exites therefore requires confirmation – it may be difficult to support derivation of wings from exites if no exites were present for them to be derived from. Unfortunately, many of the supposedly exite-bearing specimens described by Kukalová-Peck remain in private collections and are not readily available for re-examination.

Emerging mayflies, from here.

So of the currently contending explanations for the origin of insect wings, the genetic and developmental data seems to be consistent with an exite origin, but fossil and phylogenetic considerations appear more consistent with a paranotal origin. The challenge for researchers will be to reconcile this conflicting data. My personal suspicion is that some degree of genetic co-option is involved. Comparative studies on developmental genetics indicate that the evolution of new structures often involves the redeployment of pre-existing genetic pathways, and that separate lineages will often redeploy the same pathways. For instance, closely related genes are involved in the development of arthropod and vertebrate legs, despite the origins of both from legless ancestors (Shubin et al., 1997). Spider spinnerets appear developmentally homologous to abdominal legs, despite the loss of abdominal legs in arachnids a long time prior to the origin of spider spinnerets. It would be very interesting to see what the roles are in silverfish of the genes uniting insect wings and crustacean gills.

A Devonian pterygote?
Published 2 August 2012

I was going to write a post today on Strudiella devonica, the new fossil insect described from the Late Devonian of Belgium in today’s Nature (Garrouste et al. 2012). Unfortunately, there’s a limit to what I can really say. The stratigraphic significance of the specimen is undeniable: it sits well within a gap of about sixty million years that previously divided the earlier known insect fossils from the lower Devonian from the earliest known unequivocal winged insects in the mid-Carboniferous. Unfortunately, and I say this in the nicest possible way, the specimen itself is roadkill:

Photograph and interpretative drawing of Strudiella devonica, from Garrouste et al. (2012). Scale bar equals 1 mm.

Ah well, we simply have to work with what we’re given, don’t we? I think it’s fairly reliable that this is, indeed, an insect: there seems a clear separation into a well-defined head, thorax, and legless abdomen, with no more than three legs visible on a single side of the thorax. The forward-protruding mandibles and antennae with broader basal segments are also insect-like rather than entognath-like (so it’s not a stem dipluran or something like that). However, Garrouste et al. suggest that this specimen not only represents an insect, but also a crown-group pterygote. This I feel is a little more problematic.

Assignment of Strudiella to pterygotes relies on two characters: the relatively elongate legs, and the appearance of the mandibles. I suspect that it would not be that difficult for elongate legs to evolve convergently, and the supposed Carboniferous dipluran Testajapyx appears to have relatively long hind legs at least (Kukalova-Peck 1987). The mandible structure is a bit more difficult to hand-wave, though: Garrouste et al. interpret Strudiella as having an orthopteroid mandible, which is believed to be a synapomorphy of the Metapterygota, the particular clade within the pterygotes uniting the Neoptera and Odonata.

Hexapod phylogeny with representative mandible types, from Engel & Grimaldi (2004).

The earliest hexapods possessed a mandible with a single articulation (the condyle) to the head; such a mandible is still present in springtails, diplurans and bristletails. The clade uniting silverfish and pterygotes developed a second articulation (the acetabulum) on the inside of the mandible. In silverfish and mayflies, the acetabulum is anterior to the condyle, and the acetabular articulation is relatively loose. In the metapterygotes, the acetabulum has moved back to become more level with the condyle, and the mandible’s articulation with the head is a lot more solid. The fossil remains of Strudiella do not appear to show the mandible articulation itself, but the general shape and orientation of the triangular mandible is more similar to the metapterygote arrangement than to the more basal morphology. Besides, such a morphology is has more clearly been demonstrated in the Lower Devonian Rhyniognatha, known only from a pair of preserved mandibles that are even older than Strudiella (Engel & Grimaldi 2004).

The ultimate question, then, is: is this one character enough to cement these taxa as crown pterygotes, with the implication that winged insects must have evolved considerably earlier than their fossil record currently indicates? Strudiella itself shows no sign of wings; Garrouste et al. suggest that it may be a nymph of a winged adult. I would counter that it also doesn’t appear to possess any incipient wing buds, but of course it is debatable whether the preservation is good enough to be confident on this point.

If winged insects have been around since the Early Devonian, why do we find no direct evidence of them until the mid-Carboniferous? Wings are among the most commonly preserved insect remains—to the extent that if, as the adage goes, mammalian palaeontology is all about ‘the tooth, the whole tooth, and nothing but the tooth’, insect palaeontology often threatens to be ‘all in vein’. For my part, I’m not inherently opposed to the idea of Devonian winged insects, but I don’t think I’d really be willing to accept them until we’re shown the actual wings.

Systematics of Pterygota

Synapomorphies (from Grimaldi & Engel 2005): Eversible vesicles absent; transverse stipital muscle present; pleural apophyses fused with sternal apophyses; pterothoracic walls strengthened by pleural sulcus; two coxal proprioreceptor organs present; corporotentorium present; two pairs of wings present; sperm transfer through copulation.

<==Pterygota (see below for synonymy)
    |--Megalometer lataR02b
    |--Anthracotremma [Anthracotremmatidae]R02b
    |    `--A. robustaR02b
    |--Evenka [Evenkidae]R02b
    |    `--E. archaica Rasnitsyn 1977IB02
       `--Neoptera [Caloneuridea, Planoneoptera, Platyptera, Termitina, Termitini]GE05
            |  i. s.: Cymbopsis [Cymbopsidae]R02c
            |           `--C. excelsa Kukalová 1965BN02
            |         GlaphyrokorisR02c
            |         CymenophlebiaR02c
            |         KliveriaR02c
            |         EndoiasmusR02c
            |         Metropatorites kassenbergensis Keller 1934IB11
            |         Micropalentomum [Micropalentomidae]IB11
            |           `--M. minusculum Schmidt 1962IB11
            |         Controversala miomopteroides Brauckmann & Herd 2005IB11
Pterygota incertae sedis:
  Herbstiala [Herbstialidae]R02a
  Hadentomum Handlirsch 1906 [Hadentomidae]BN05
  Rhyniognatha hirsti Tillyard 1928FT05
  Stereopteron Carpenter 1950 [Stereopteridae]BN02
  Archaeologus falcatus Handlirsch 1906BN02
  Proedischia [Proedischiidae]BN02
    `--P. mezzalarai Pinto & Pinto de Ornellas 1978BN02
  Rigattoptera [Rigattopteridae]BN02
    `--R. ornellasae Pinto 1996BN02
  Platyphlebopteron Germer 1971BN02
    `--P. jakobyi Germer 1971BN02
    |--‘Fergania’ Sharov 1968 non Mandelstam in Mandelstam et al. 1957BN02
    `--Parafergania Gorokhov 1987BN02
         `--P. sharovi Gorokhov 1987BN02
  Strudiella Garrouste, Clément et al. 2012GC12
    `--*S. devonica Garrouste, Clément et al. 2012 [=Strudiella antennata (l. c.)]GC12

Pterygota [Ephemeridea, Exopterygota, Libelluliformes, Metapterygota, Opisthoptera, Protorthoptera, Pterodicera, Scarabaeona, Scarabaeones, Stharopodina, Subulicornes]

*Type species of generic name indicated


Beckemeyer, R. J., & J. D. Hall. 2007. The entomofauna of the Lower Permian fossil insect beds of Kansas and Oklahoma, USA. African Invertebrates 48 (1): 23–39.

Béthoux, O., & D. E. G. Briggs. 2008. How Gerarus lost its head: stem-group Orthoptera and Paraneoptera revisited. Systematic Entomology 33 (3): 529–547.

[BN02] Béthoux, O., & A. Nel. 2002. Venation pattern and revision of Orthoptera sensu nov. and sister groups. Phylogeny of Palaeozoic and Mesozoic Orthoptera sensu nov. Zootaxa 96: 1–88.

[BN05] Béthoux, O., A. Nel, J. Lapeyrie & G. Gand. 2005. New data on Paleozoic grylloblattid insects (Neoptera). Journal of Paleontology 79 (1): 125–138.

Engel, M. S., & D. A. Grimaldi. 2004. New light shed on the oldest insect. Nature 427: 627–630.

[FT05] Fayers, S. R., & N. H. Trewin. 2005. A hexapod from the Early Devonian Windyfield Chert, Rhynie, Scotland. Palaeontology 48 (5): 1117–1130.

[GC12] Garrouste, R., G. Clément, P. Nel, M. S. Engel, P. Grandcolas, C. D’Haese, L. Lagebro, J. Denayer, P. Gueriau, P. Lafaite, S. Olive, C. Prestianni & A. Nel. 2012. A complete insect from the Late Devonian period. Nature 488: 82–85.

[GE05] Grimaldi, D., & M. S. Engel. 2005. Evolution of the Insects. Cambridge University Press: New York.

[IB11] Ilger, J.-M., & C. Brauckmann. 2011. The smallest Neoptera (Baryshnyalidae fam. n.) from Hagen-Vorhalle (early Late Cretaceous: Namurian B; Germany). ZooKeys 130: 91–102.

Kukalová-Peck, J. 1987. New Carboniferous Diplura, Monura, and Thysanura, the hexapod ground plan, and the role of thoracic side lobes in the origin of wings (Insecta). Canadian Journal of Zoology 65: 2327–2345.

[R02a] Rasnitsyn, A. P. 2002a. Subclass Scarabaeona Laicharting, 1781. The winged insects (=Pterygota Lang, 1888). In: Rasnitsyn, A. P., & D. L. J. Quicke (eds) History of Insects pp. 75–83. Kluwer Academic Publishers: Dordrecht.

[R02b] Rasnitsyn, A. P. 2002b. Infraclass Scarabaeones Laicharting, 1781. In: Rasnitsyn, A. P., & D. L. J. Quicke (eds) History of Insects pp. 84–85. Kluwer Academic Publishers: Dordrecht.

[R02c] Rasnitsyn, A. P. 2002c. Cohors Cimiciformes Laicharting, 1781. In: Rasnitsyn, A. P., & D. L. J. Quicke (eds) History of Insects pp. 104–115. Kluwer Academic Publishers: Dordrecht.

[RJ93] Ross, A. J., & E. A. Jarzembowski. 1993. Arthropoda (Hexapoda; Insecta). In: Benton, M. J. (ed.) The Fossil Record 2 pp. 363–426. Chapman & Hall: London.

[Sh02] Shcherbakov, D. E. 2002. Order Forficulida Latreille, 1810. The earwigs and protelytropterans (=Dermaptera DeGeer, 1773 +Protelytroptera Tillyard, 1931). In: Rasnitsyn, A. P., & D. L. J. Quicke (eds) History of Insects pp. 288–291. Kluwer Academic Publishers: Dordrecht.

Shubin, N., C. Tabin & S. Carroll. 1997. Fossils, genes and the evolution of animal limbs. Nature 388: 639–648.

[Si02] Sinitshenkova, N. D. 2002. Superorder Dictyoneuridea Handlirsch, 1906 (=Palaeodictyopteroidea). In: Rasnitsyn, A. P., & D. L. J. Quicke (eds) History of Insects pp. 115–124. Kluwer Academic Publishers: Dordrecht.

[SBG11] Staniczek, A. H., G. Bechly & R. J. Godunko. 2011. Coxoplectoptera, a new fossil order of Palaeoptera (Arthropoda: Insecta), with comments on the phylogeny of the stem group of mayflies (Ephemeroptera). Insect Systematics and Evolution 42: 101–138.

Terry, M. D., & M. F. Whiting. 2005. Mantophasmatodea and phylogeny of the lower neopterous insects. Cladistics 21: 240–257.

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