What in goodness's name could the common ancestor of Equestria's winged sapient races have been? Gilda, Dash and Skystar all have a common ancestor. What the heck could it have looked like?

Also is Dash more closely related to her fellow Ponies or to the Avians?

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These creatures live in a world where Grogar went about haphazardly creating monsters as he deemed fit. Believe me, you bring up a very interesting topic, but I think there's more mythology than biology to be had here. (Pegasus reference not intended)

But, if I had to give a scientific answer, maybe creatures in MLP have much looser gene structures that allow other species to crossbreed. For example, eons ago, a griffon and a pegasus crossed to get a hippogriff. And somehow their descendants were fertile. How wings ended up on a horse, I'll leave to your imagination, but we know there were multiple tribes of pony races, which suggests a few genetic bottlenecks.

I would be tempted to ascribe the similarities to a roughly even mix of convergent evolution and intelligent magical tampering.

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Also btw, at least pegasi, dont actually have bird wings. even though they have feathers. whenever a Pegasus gets electrified in the Show, we see on their x-ray, that their wingbones resemble more closely a thumbless Hand.

It might be a platypus Thing, where it Looks like a Beaver/duck-hybrid, but it just happens to resemble those animals, instead of being related to either, like how Dolphins resemble fish in Body shape, but are actually mammals.

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I'm tossing my hat in the creation camp. We flat out see this in some of the monsters in Tartarus in the S8 finale. A cockatrice is flat out a snake and chicken fused together with magic. It's easy to see that a lot of creatures could easily be a combination of magic and genetic engineering.

Personally my headcanon for equestrian ancient history (like 100s of thousands of years before the show) involves several advanced precurser species and one of which had a tendency to create new lifeforms.

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One biologist right here (Let me know if I have started throwing around too much scientific terms below, I’ll try to explain some other way.)

It would be really good to try and create a proper phylogeny of Equestrian creatures, but it seems quite impossible, given the haphazard variety that we see in the show. Just think about the fact that pegasi have two additional limbs, yet they don’t seem to have diverged from the other ponies much in other aspects. And while wing evolution is fast, it still takes time, especially if it was hindered by crossbreeding with the other soon-to-be-tribes. (Given that, it is much more likely that the original pony bauplan resembled an alicorn, the three tribes being basically knock-outs for certain traits.)

However, if you decide that evolution as we know it functions in Equestria with some magical enhancements, you can suddenly explain a lot of things. For example, it’s possible to imagine some kind of magic-mediated horizontal gene transfer between species, one that allowed them to acquire sets of genes to grow wings and other complex traits.

As for the common ancestor of all these three, we can safely say that it belonged within Amniota. I can’t think of a way of specifying it closer than that though.

7080537 Many species can develop the same trait independently. They don't have to be related to have wings. All that is needed is for them to live in similar conditions that favor wings.

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Well, that’s a rather simplified view. If we are talking analogous traits, the probability that they will evolve and look the same increases as their complexity decreases. For example, if such a trait consists of a few specialized cilliated cells used for filtering haemolymph, then that evolving independly many times is not surprising at all. The same goes for analogous structures of the same function, but varied design—for example, the wings of birds, bats and insects. All are used for flight, but their anatomy and function varies. This is mainly what you describe in your comment. However, the problem with wings is that they are highly complex structures and as such, them evolving independently twice or thrice with the very same design is highly unlikely—I’m not saying it’s impossible, just very very unlikely. Not to speak about the issue of the three creatures above acquiring another pair of limbs, which adds a whole another level of complexity to this problem.

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(Let me know if I have started throwing around too much scientific terms below, I’ll try to explain some other way.)

Before I changed my major, I did serve some time in my university's science lab. My sentence was to count flies and sort them by eye color and determine which mutations were found on the sex-linked chromosomes. Genetics was my favorite part, and I could talk about Punnett Squares till I'm blue in the face, and I even went so far as to determine how unicorn horns and pegasus wings are passed down through a mixed lineage. (They're recessive, as demonstrated by the Cake Twins.)

Perhaps relevant to the current discussion, Shining Armor's genes for unicorn are both recessive, since he has a horn. This will be indicated by a lowercase uu. However, in case you missed this fact, Shining Armor lacks wings, meaning he is a W_ for the wing gene, having at least one non-wing gene. Living in Canterlot, it is quite likely his family history is dominated by unicorns, so it would be safe to assume WW. Cadance on the other hoof is recessive for both traits, uuww. Any pairing of these two should be uuWw, a unicorn with the possibility for pegasus foals. (I have a theory that something magic-y disallows both recessive horn and wing genes, or else we would theoretically see alicorns everywhere.) However, what if Cadance was pregnant with Flurry Heart at the time of Sombra's return? Cadance wasn't born an alicorn, she was made one by magic. Same for Twilight. What if Flurry Heart was the same way? What if the magic in the Crystal Heart changed Flurry Heart from uuWw to uuww, an alicorn?

Such magical encounters would be unimaginably rare, but theoretically, it could explain the divergence between the three main pony races and the emergence of their wings and horns. I haven't considered crystal ponies, but maybe they work the same way?

BONUS: I've been trying off and on to work out coat colors, and it's super interesting that Rarity and Sweetie Belle both have one parent with a white coat, as do Twilight and Shining Armor. I think white coats may be dominant over other colors, but I'd need more evidence. Still, it's a promising start.

I've always assumed that ponies had a creator in the Biblical sense of the word (although without necessarily implying divinity); that, combined with all the magic running through Equestria which many of the species can access and use, thus making genetics kinda invalid. I also think it's possible for many different species to interbreed and produce hybrid offspring.

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When that table first came out, it all seemed pretty legit, but now that we've got dozens of other ponytypes it seems a tougher nut to crack. Where do batponies, kirin, zebras etc. fit on the chart? What happens if a unicorn and a batpony have a foal together? How about a zebra and a pegasus--might that produce a flying zebra?

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I have a theory that something magic-y disallows both recessive horn and wing genes, or else we would theoretically see alicorns everywhere.

There definitely has to be some sort of trade-off to being an alicorn, otherwise it'd be strange (evolutionary speaking) to disregard such advantageous mix of traits.

What if Flurry Heart was the same way? What if the magic in the Crystal Heart changed Flurry Heart from uuWw to uuww, an alicorn?

Interesting theory, one that I cannot disprove or support in any way. Could as well be some lingering magic within Cadance changing's Flurry's genotype during her ontogeny. (Also, have you considered magic having an epigenetic effect rather than directly changing the alleles?) Though a rather problematic part is that no matter the changes to the genotype of an adult pony--that is Twilight and Cadance--their fenotype shouldn't change much - definitely not on the level of growing wings or a horn, respectively.

Such magical encounters would be unimaginably rare, but theoretically, it could explain the divergence between the three main pony races and the emergence of their wings and horns.

I'm rather sceptical here, as that seems a little too rare for it to have such an impact. Furthermore, given the complexity of the structures we are talking here, it is highly unlikely these traits will be coded by one gene. A machinery of genes is probably at play here, with u and w serving as regulatory genes. The biggest problem is that according to your concept, magic may be able to change the dominance of alleles, but it does not explain where the 'horn' and 'wing' sets of genes came from. (And for your theory to work, everypony has to have these in their genomes, albeit partly dormant.)

BONUS: I've been trying off and on to work out coat colors, and it's super interesting that Rarity and Sweetie Belle both have one parent with a white coat, as do Twilight and Shining Armor. I think white coats may be dominant over other colors, but I'd need more evidence. Still, it's a promising start.

Very good point. Please let me know if you uncover some kind of significant pattern!

One of the individuals you depicted casually uses externally applied shapeshifting magic to go from aquatic to flying.

There is no real way of knowing WTF that sort of stuff lying around is doing to genetics. While many-or even most-shapeshifting spells in mlp seem to give temporary resuls, transformation brought about the pearl appears to last until another transformation is applied.