Insect Flight: Early Fossil Record & Physiology

The insect wing is not just a membrane that juts of the insect’s body. It’s a complex of membranes, veins, folds and flexures – looking at it laterally, it is in no way a simple two-dimensional structure. Even more mind-boggling is the wing base, with all sorts of sclerites as muscle attachment sites, plates, vein sources and the notal margin. It is to the wing base that all the power generated by the thoracic muscles goes, so it is also imperative to the way an insect flies.

Because I’ve received some complaints before about what exactly is meant by ‘wing venation pattern’, here’s a side-by-side example, using plecopteran wings. On the left side, you see the interpretation, on the right is the actual picture. But again, there’s no real point in going into the details of wing veins because it’s just too specific and honestly not very didactic.

Wing venation (Antarctopleura spp.). Béthoux (2005).

Interpreting and homologising insect wings is one of the major goals of insect systematics. The wing bases of Neoptera already have a system, as do the mayflies. The odonates though are a different story. The complexity of their wing base has caused all sorts of misunderstandings, even to the point of some authors suggesting that insect flight evolved twice independently (quite a fringe opinion though, since pterygotan monophyly is more or less certain).

At the risk of going into completely unfamiliar territory, the main difference between the wing base in odonates and other insects is that in Neopterans and mayflies, the muscles attach on multiple detached axillary sclerites, whereas in the odonates, there is just one sclerite called the axillary plate. The importance of these sclerites is that they determine wing folding. A more significant (in terms of flight physiology) is the vein called the basalare, which is where the direct flight muscles are inserted: in odonates, it is greatly expanded in order to transfer power to the costa (the rigid vein that supports the wing), whereas in the others, it is a simple vein.

In fact, there are only two structures in the wing that have been certainly homologised: the basal hinge and the subcostal vein, since they are generally conserved across all the winged insects.  I only mention this because the majority of the (early) insect fossil record is based on isolated wings, or pieces of wings, compressed in stone, so wing venation patterns obviously have a distinct importance.

The insect fossil record really starts at ~320 Ma (Early Carboniferous), although their time of origin is speculated and calculated to be earlier (there is a Romer’s Gap in the earliest insect fossil record), to coincide with the origin and evolution of the first trees in the Devonian (~380 Ma) – the initial radiation of the winged insects is completely missing from the fossil record.

There were definitely land plants in the Upper Silurian (~430 Ma), and the invasion may already have happened earlier during the Ordovician. At this time, the typical plants (e.g. Cooksonia) had a very simple structure, were knee-high at best and had to stay near water for reproduction. The completely terrestrial plants did not come about until the Devonian, when you get the earliest ‘trees’ and proper forests. This was also significant in terms of chemical changes, with oxygen levels increasing and carbon dioxide levels correspondingly decreasing in the atmosphere, and of course all sorts of soil development.

We are extremely lucky to have an awesome taphonomic window from this period, in the form of the Rhynie Chert, wherein fossils are preserved in 3D down to an ultrastructural level: plant cell walls can be seen, as can arachnid book lungs. Of the specimens found here, two of them are of importance to us. Rhyniella praecursor, a collembolan, and Rhyniognatha hirsti, a probable insect mandible (see picture below). The presence of those two fossils alone tells us that there had already been a radiation of hexapods, and that the Collembola, Diplura, Protura, Archaeognatha and Dicondylia had already originated (that is, if we are certain of our phylogenetic hypothesis, which we more or less are). In fact, if we accept Rhyniognatha as a metapterygote, it would not be out of place to say that there was some sort of flying going on by this time.

Rhyniognatha hirsti. Engel & Grimaldi (2004).

Then we come to the Carboniferous. In the Lower Carboniferous (360-325 Ma), swamps and moors were the norm around the world, with meters-high forests of ferns, lycopods and horsetails. Extremely unfortunately, until now no hexapod fossils from this time have been found. This is a torrid situation, as what we see in the Upper Carboniferous hints at some pretty remarkable happenings during the Lower Carboniferous.

In the Upper Carboniferous (325-290 Ma), we suddenly have the preservation of diversified pterygotes that apparently appeared quite suddenly in a Cambrian Explosion-like radiation. Of course, it’s unlikely that this is the case, and it’s more imagineable that the Lower Carboniferous is a Romer’s Gap – a stretch of the fossil record where no relevant fossils are found due to bad taphonomy (or not enough searching!). Whatever the case may be, these Late Carboniferous pterygotes are phylogenetically diverse, with mayflies, odonates and various neopterans flying around (note that I am being loose in my terminology; strictly-speaking many of these fossils are stem-group taxa). Also included are various now-extinct orders, such as the Palaeodictyoptera, Megasecoptera, Dicliptera and Diaphanopterodea (these can be seen as ‘wastebasket taxa’, where we just throw in stem group fossils just for the sake of giving them a classification, because we humans have an irrational obsession with taxonomy).

Anyone who has seen any documentary on the Palaeozoic will know about the gigantic faunas of the period; particularly charming are the gigantic, 50+ cm wingspan odonates. The gigantism is also seen in other arthropods, such as scorpions and centipedes. Notably, it is not observed among the neopterans. The cause of the gigantism is most probably the record-high amount of oxygen in the atmosphere. This hyperoxic atmosphere must be considered whn trying to figure out the origin of flight in insects, because flying is an energetically very costly activity, and it is in flying insects (and flying vertebrates) that the most oxygen uptake relative to body size takes place.

The most obvious link is with oxygen delivery: the tracheal system delivers oxygen straight to the muscle tissue, so the amount of oxygen basically disappears as a limiting factor; the very high amount of oxygen may have allowed the initial development of very active muscles (there was no pressure agaisnt having them). We can see the advantages of the tracheal system even in today’s less oxygen-rich atmosphere: aerobic metabolism can last much longer in insects than in vertebrates, where oxygen is the limiting factor (the whole blood-lung system is simply too slow to cope). A side-effect of this is the heat output.

In biology, energy = heat (and vice versa); flying insects are among the hottest. They need the heat to power flight, but temperature must be regulated (too little heat or too much heat and the body shuts down). Insects can be roughly classed as endotherms (‘warm-blooded’), with most of the heat derived from the muscles. One important way for them to get warmth is to ‘shiver’ by rubbing their flight muscles together; the initiation of it involves a different biochemical pathway than in regular muscle contraction (a different set of enzymes gets used to split the ATP) and is mediated by the nervous system. There is no coordinated muscle movement, just small contractions. They do this before take-off, increasing the local temperature in the thorax by over 10°C, allowing them to fly even in colder weather.

Since we’re on the subject of energy, some biochemistry wouldn’t hurt. Social insects or insects that only fly for short periods of time, such as bees or wasps, generally use just carbohydrates, glycogen and trehalose found in the blood. For those of you familiar with the Krebs Cycle, these insects have some elegant modifications to it that increase the total yield of energy. Typical muscle tissues don’t use the enzyme pyruvate carboxylase, but flight muscle in these groups does. The basic consequence is that the amount of oxaloacetate is increased, therefore there’s more substrate that goes into the Krebs Cycle, thereofre more net energy yield – for animals that survive solely on carbohydrates, this is an easy fix.

In contrast, there are the long-term, migratory fliers like locusts or moths. They use fat predominantly (either fat exclusively, or use up the carbohydrate stores and then switch to fat). Again, an interesting modification to the metabolic cycles here is their dependence on proline (observed in some beetles, locusts, the tse-tse-fly, among others). This serves to again increase the amount of energy derived.

Back to the fossils. Interestingly, some Late Carboniferous pterygotes (never mayflies) had prothoracic paranota, i.e. three pairs of wings, one on each thoracic segment. This extra wing later got reduced independently many times as the musculature and flight behaviour became centered around the mid- and hind wings, as we see it today.

There’s no point in going into the Permian and gradually more recent fossil record, as the next post will be about the origin of flight in insects.


Béthoux, O. 2005. Wing venation pattern of Plecoptera (Insecta: Neoptera). Illiesia 1, 52-81. [Warning: PDF!]

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

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