Birds and bats get a lot of respect in our time for their ability to fly, but they were by no means the first to evolve this ability. That honour belongs to the insects, and their evolution of flight is arguably more astounding than in vertebrates, because insects evolved entirely new structures instead of just modifying existing forelimbs into wings.
There are two main hypotheses on how flying insects, known as Pterygotes, evolved wings. The Tergal Hypothesis suggests that wings evolved from gliding membranes originating from the top of the insect body wall, called the tergum. The competing Pleural Hypothesis argues that wings evolved from leg segments that merged with the body before migrating to the back. However, a more recent ‘dual origin’ hypothesis suggests that a fusion of the leg segments and dorsal membranes would have created the wings. Recent work on the genomes of flour beetles has provided some evidence for this theory.
This leads to the question, why did insects evolve dorsal membranes in the first place? It is suggested that thermoregulation was the adaptive factor that caused the membranes to evolve. Insects are ectothermic, meaning they must rely on external thermal sources to warm up. The veined thoracic lobes would have allowed the insects to warm up more and become active faster. Only when the lobes became larger and more articulated would they be able to be used in gliding, and later in powered flight through even more musculature and articulation.
There is much debate about when flying insects first evolved. The oldest known winged insect is the 325 million year old Delitzschala bitterfeldensis, from the Carboniferous period. Before this time, only a handful of fossils had been discovered, among them the 402 million year old Rhyniella praecursor, which is similar to modern Collembola, rather than true insects. As you can see in the figure below, there is a large amount of geological history where insects haven’t preserved well as fossils. This period is known as the Hexapoda Gap, a period of time between 385 and 325 million years ago.
That was until the discovery of Strudiella devonica in 2012, which dates back to 370 million years ago. However, another group of scientists questioned whether it was an insect at all, or another type of arthropod instead, going to show how unclear it is when insects as a group first evolved flight. Most studies into the genetics of insects put it at around 400 million years ago, in the Early Devonian period, but there is little fossil evidence for this.
One thing that is clear, if you can believe it, is that the development of flight in insects was a huge evolutionary innovation. With wings, insects could travel further, escape from predators and look for food more easily, allowing them to flourish and diversify into many new niches, and become the most abundant animal species on the planet.
 A modern dragonfly, which has evolved from ancestors in the Carboniferous period, such as Meganeura monyi. Available at: https://newatlas.com/dragonfly-nanostructures-anitbacterial-properties/53331/.
 An illustration showing the Hexapoda Gap in geological time, taken from Shear (2012). Available at: https://www.nature.com/articles/488034a#f1.
 The fossil and a reconstruction of Strudiella devonica. Scale bar: 1mm. Taken from Garrouste, et al, 2012. Available at: https://www.nature.com/articles/nature11281.
Information References and Further Sources
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