The question on Quora was:

What’s the possible explanation for powered flight appearing only once in invertebrates and at least three times in vertebrates?

My answer was:

Interesting question that had never occurred to me before. I have a couple of thoughts, but these are just guesses.

(Edit to update: The premise of the question may not be quite right, because it’s been suggested that flight in insects has arisen multiple times:  Loss and recovery of wings in stick insects.)

First, what broad classes of invertebrates are there that could plausibly develop powered flight?  There are vast numbers of invertebrates, but things like corals, sea urchins, jellyfish, and so on aren’t really good candidates for developing flight.  We should only consider terrestrial species.  And then we should probably exclude things like the various types of worms; again, this isn’t a flight-friendly lifestyle.  So we’re left mainly with arthropods, and we have to exclude aquatic arthropods, and we’re left with mainly insects and arachnids.

But still: Why did insects only develop powered flight once (assuming that’s what happened, which I think is still a little unclear)? Why didn’t arachnids develop powered flight?

Maybe it’s a little unfair to blame insects for only developing powered flight once.  It arose pretty early, and there are lots and lots of insect fliers.  Some of the other lineages trying to develop flight later on would run into huge competition from the already well-adapted fliers up there.  But even so, it seems at first glance odd.

But maybe we gigantic humans underestimate the risks and overestimate the benefits of flight. The prevalence of mountain and insular apterism suggests that there may be a significant downside to flight among very small animals (i.e. most terrestrial invertebrates).  Darwin pointed out that island and mountain insects often lost their wings, and argued that this might be because flying insects would risk being blown out to sea, or away from their mountain, so that there was a benefit to remaining firmly attached to the ground.  Others have also suggested that aptery might have metabolic benefits in harsh environments, reducing heat loss, for example.  So the advantages of flight in many environments might be overstated.

The benefits of flight are also potentially lower for very small animals, since they have essentially no risk from falling.  Unlike larger animals, insects can carelessly launch themselves into space from any height and land safely.  So there’s a large class of benefits that invertebrates don’t gain.

Still, there are benefits of flight, even for tiny things.  We’d point to dispersal as a major one, and then to avoiding predation, to predating on other things, and to long-distance foraging as a fourth.  So: Why aren’t there flying arachnids, say?

Well, there are flying arachnids.  Ballooning spiders have developed a complex set of adaptations that let them travel for hundreds of miles.  It’s not “powered flight”, but it serves the same purpose of dispersal.

(And stretching the point even further, we can point to parasitic worms and so on that force their host to be eaten by birds, and to aquatic invertebrates that attach their eggs to waterfowl feet, thus attaining flight and dispersal in a very indirect way.)

Avoiding predation and predating on others falls into the category I mentioned above — because insect flight arose so early, attempts at either of these would run into ferociously well-adapted flying predators already, either as competition or as threats (or both).

So the one benefit that’s left is long-distance foraging, and that really only makes good sense to social insects, where long-distance travel and return is beneficial.  There aren’t many social things, and of them only bees and wasps (that I can think of) use this strategy (ants and termites use flight for dispersal only).  So it’s a highly specialized approach that probably isn’t useful for most things.

So at the end of the day, maybe the answer is that we as humans overrate the advantages of flight to a tiny thing.  Most invertebrate lifestyles won’t benefit from flight, and those that would either have developed flight already, or faced too much competition by the time it would be useful.

All speculation, and I’d be interested in hearing better ideas.