Field of Science

The Origin of Insect Wings


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: see comments below). 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.

REFERENCES

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.

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

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.

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

24 comments:

  1. The origin of insect wings is something I've often wondered about--thanks for detailing it! It seems like both theories have merit. This may be a silly question, but could the two be united somehow?

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  2. Genetic co-option or reactivation would be a kind of unification of the two, but it's still an area where (as far as I know) our understanding of the processes involved is still at the early stages.

    Some authors have suggested a 'hybrid' origin of wings. Insect wings are constructed from distinct dorsal and ventral layers, and some authors have suggested that the dorsal layer may be derived from thoracic lobes (supplying the wing plane) while the ventral layer might be derived from exites (supplying the articulation). It's an interesting idea, but it currently lacks evidence.

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  3. My impression (I'm afraid I'm a vertebrate chauvinist, and don't follow the arthropod literature very closely) is that (molecular in particular) evidence was solidly in favor of a close relationship between Crustaceans and Insects-- to the extent of extant Crustacea being paraphyletic with regard to insects. Is this the right impression to have? And is the placement of the silverfish (and the non-Insect hexapods) in this scheme something the people who study arthropod phylogeny feel confident about?

    (B.t.w.: thanks for intersting state of play account: I wasn't really aware of the alternatives to Kukalova-Peck's theory.)

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  4. Yes, support is currently strong for Crustacea + Insecta to the exclusion of myriapods and chelicerates, but at present there's no real confidence about whether or not crustaceans are paraphyletic. The main contenders (in terms of living taxa only) are probably "insects as sister group to crown crustaceans", "insects as sister to branchiopods" or "insects as sister to malacostracans" but I really wouldn't want to be laying out my bets as yet.

    In terms of hexapod monophyly, monophyly of insects in the strict sense (archaeognathans, thysanurans, pterygotes) is pretty rock solid and I'm not aware of anyone who has suggested otherwise. However, recent molecular analyses suggest that the other hexapod groups (springtails, proturans, diplurans) may not form a clade with insects. I'm still personally rather skeptical of hexapod polyphyly, but I still thought it safest to leave non-insect hexapods out of the discussion for now. If hexapods are monophyletic (as the morphological data still supports), then that makes it more likely that thoracic exites were lost some time prior to the origin of wings (springtails and such don't have exites either).

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  5. Chris Taylor-- Thanks for reply! That was very helpful.

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  6. Cool post. I've been interested in this for a while, but not enough to actually chase down any of the most recent literature. Thanks for the state-of-the-science report.

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  7. "closely related genes are involved in the development of arthropod and vertebrate legs, despite the origins of both from legless ancestors" How?
    Arthropods and vertebrates have no legless ancestors, since jointed legs derive from oral digital apparati AFAICT.

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  8. Arthropods and vertebrates have no legless ancestors, since jointed legs derive from oral digital apparati AFAICT.

    Ummm.... say wha..?

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  9. How did legs sprout from legless ancestors? Sounds like a tale!

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  10. If wings were derived from paranotal lobes, how could paranotal lobes & wings could have been present on some species at the same time? Does this mean some pairs of paranotal lobes evolved into wings, while others remained as lobes?

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  11. There's never paranotal lobes and wings on the same segment.

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  12. The author of this blog post said:
    "Also problematic is the complete absence of thoracic leg exites in any living insect, including archaeognathans and silverfish"

    This is factually incorrect. Indeed many Recent species of Archaeognatha do possess thoracic exites on the coxae of the mid and hind legs!
    (e.g. see Grimaldi & Engel, 2005, Fig. 5.1)

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  13. I'd missed that the styli were also present in the thorax of archaeognaths (I've inserted a correction to that effect in the post). However, Grimaldi and Engel (2005) also note that the thoracic exites in archaeognaths lack associated musculature, so an exite origin for wings would still require a certain degree of parallelism in archaeognaths and thysanurans (not impossible, as noted in the post).

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  14. I'm sure you know of the fruit fly mutation where wings grew where eyes should be and legs grew where antennae should be; eyes (transparent lens) are never on the thorax AFAIK, (often transparent) wings are, I consider them as derived from the same primitive organ.

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  15. I must be slow; what is AFAIK?

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  16. David Marjanović23 July 2012 17:54

    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.

    If those nymphs were restricted to freshwater, it suddenly makes sense AFAIK, because most Palaeozoic sites are marine or brackish to some extent. Many coal forests were mangroves.

    Unfortunately, many of the supposedly exite-bearing specimens described by Kukalová-Peck remain in private collections and are not readily available for re-examination.

    HULK SMASH

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  17. If those nymphs were restricted to freshwater, it suddenly makes sense AFAIK, because most Palaeozoic sites are marine or brackish to some extent.

    At least some Odonata have nymphs that are able to live in brackish water, bu in general your point stands.

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  18. How could very large dragonfly nymphs obtain sufficient O2 for submerged active carnivory (fresh or brackish)? I thought reliance on simple air tubes limited their size in water, unlike the fanning adults in an high O2 atmosphere. My speculation was that the nymphs were small in water and quickly transformed into small winged adults (hexapod raptors) which remained carnivorous around open water to get protein for body growth, as opposed to mere calories for energy and some protein for egg production.

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  19. I thought reliance on simple air tubes limited their size in water

    They don't have 'simple air tubes'. They have gills.

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  20. Thanks for the correction, Christopher.

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  21. Christopher, what I meant was that the larvae did have simple air tubes to oxygenate, initially, and gradually developed independent supplementary oxygenation equipment (gills) or behavior (bubbles) depending on environmental pressures and niche advantages.

    http://en.wikipedia.org/wiki/Aquatic_insects
    "The larvae and nymphs of mayflies, dragonflies and stoneflies still retain the air tubes they need for adult stage but when in larval stage they are equipped with gills that strain out oxygen in the water."

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  22. Christopher, Diptera spp. have 2 mesothoracic flight wings and 2 metathoracic alteres (strepsiptera have opposite condition).

    Many 4-wing insects have knobby antennae (unlike diptera), might these function for improved flight, analogous to the halteres in some fashion?

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