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Background

For a pair of games I am working on, I'm trying to work in a VERY basic evolutionary timeline for a lot of the more mythical creatures to set up design language of some of the creatures. This timeline will give me an idea of which creatures are related to which in order to help guide the design process of each game world as I go forward. The two settings are very different, but have a similar problem that just have different means of getting to similar end results.

The problem

Winged quadrupeds are something that don't really exist in our world (some avian dinosaurs may have walked with their wings, but I don't count them as quadrupeds.) As has been pointed out in multiple questions on the topic of flying quadrupeds, evolving extra limbs is a very expensive and unlikely event. Having it happen multiple times for different animals would be even stranger.

Solution

So, instead of making each one have their own separate events where something evolved the extra pair of limbs, I thought I'd make it so they had a smaller number of evolutionary ancestors shared by multiple creatures that are similar enough (gryphons and hippogryphs and giving dragon-like creatures shared evolutionary ancestors, etc.)

For one of these game worlds, there will be centuries worth of strange magic saturating the world that will have the side-effect of speeding up evolution to the point of millions of years worth of evolution happening every century, so mutations like this are at least more likely for that one. Humans will have been in a magical slumber to hide from the effects of this magic, returning to find their world much different. The other game's setting is a far older planet than our Earth, having far more time for such creatures to evolve before intelligent life came to be.

The question

Going down that path for the solution, would it be more likely/logical for a flightless quadruped to evolve extra limbs that would eventually become wings? Or for a bipedal flying creature to grow an extra pair of legs/claws?

I should note that I am looking for answers that work for both worlds. The magical side-effects mentioned for one of the worlds is more of a catalyst to speed things up so I can have humans wake from their slumber and still find some serviceable infrastructure among the ruins of the old world (though there will be some mutations that are strictly magic in nature like elemental imbuements, they are not relevant to this particular question.)

EDIT: I suppose a better way to ask this is which of the two body plans (bipedal avian or quadruped) would benefit more from the additional limbs/wings?

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    $\begingroup$ Almost hexapodal (they use ribs instead) Draco lizards $\endgroup$ Oct 12 '20 at 18:35
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    $\begingroup$ In Flight of Dragons, Peter Dickenson hypothesizes that dragon wings would have developed as extensions of the dragons' ribs, rather than as limbs at all. $\endgroup$
    – FuzzyChef
    Oct 13 '20 at 2:05
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    $\begingroup$ This magically accelerated evolution... does it have effect to the lifespan of the animals? Because if not, there could be an accumulation of mutation in one organism, that would not take place in "normal" evolution. Then a combination of mutations could be successful, where the single mutations alone would not... This would cancel "conservative" evolution... $\endgroup$ Oct 13 '20 at 5:17
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    $\begingroup$ Do you need them to have exactly 4 limbs? Or can they have more? Do they need to be vertebrates? All flying insects would fit the bill if you allow for more legs. And some did get quite large: en.wikipedia.org/wiki/Meganisoptera $\endgroup$
    – jcaron
    Oct 13 '20 at 10:03
  • $\begingroup$ Why are you ruling out thousands of flying insect species? A better way to Ask this might be what world are you building where local conditions don't make it obvious which body plans would work best? I don't know of a real flying quadruped and the only fictional example I remember is in google.com/… and so what? In any case, how is this not solely the author's task? $\endgroup$ Oct 13 '20 at 21:05

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How about neither? Tetrapods evolved straight from lobe-finned fish; essentially no-limbs to four-limbs. You could have a similar process, except when the fish were developing limbs they ended up with six instead of four. This would probably give you six-legged amphibians; I would expect six legs before four-legs-and-wings. However, if you wanted to throw in weird outliers, you could have some of these hexapods at like flying fish, potentially developing flight (possibly even with multiple sets of wings) before they developed legs of any sort. For a basic sketch though, I think your best bet is fish-->six legs-->legs and wings. As a side note, unless you postulate parallel evolution of tetrapods, this would mean that pretty much every land-dwelling animal would have six legs.

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    $\begingroup$ 6 limbs to 4 limbs and 2 wings is just about the only way this could evolve, developing new limbs is just too difficult once you are a complex organism. $\endgroup$
    – John
    Oct 11 '20 at 19:43
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    $\begingroup$ To support this consider that all 3 groups of vertebrates that developed wings turned limbs in to wings. $\endgroup$
    – John
    Oct 11 '20 at 20:05
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    $\begingroup$ The fish did have limbs, it's just that they were small fins. Fish do have more than four fins, too. Perhaps the easiest evolutionary path would be to bifurcate the anal fin, then follow the same evolutionary path as our 4-limbed ancestors. Or why not 5 limbs? Three - pectoral and anal - developing into legs, the pelvic fins becoming wings: en.wikipedia.org/wiki/Fish_fin $\endgroup$
    – jamesqf
    Oct 12 '20 at 2:43
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    $\begingroup$ Every land-dwelling animal would have six limbs, not necessarily all legs. You might have variations of 4 legs and 2 arms, 2 legs and 4 arms, 2 legs 2 arms and 2 wings, 4 legs and 2 wings, 2 legs and 4 wings, or even all 6 arms (as a parallel, think of the various real-world primates with prehensile feet). It probably wouldn't split on odd numbers given that most complex life has bilateral symmetry, though you could throw out that rule in your fictional world for the odd 3 leg 3 arm etc. mixes, but that seems far less likely. $\endgroup$ Oct 12 '20 at 14:05
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    $\begingroup$ @DarrelHoffman, there's no requirement that every terrestrial animal has six limbs: note that Earth has gone from 4 to 0 multiple times in reptiles and amphibians, and the carnatosaurs and other theropods came close to going from 4 to 2. What would be correct would be that every terrestrial animal is derived from a 6-limbed ancestor. $\endgroup$ Oct 13 '20 at 2:03
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Pleomorphic Dragons and Monsters:

Rather than trying to justify something in the normal way that is so controversial, let's propose a new thing all together. What if the ancestors of dragons and other monsters developed in a new but not unheard of manner? What if all dragons are a form of conjoined identical twins?

Identical twins exist, as do conjoined twins. So let's envision a developmental mutation that caused ALL embryos to split into identical twins, and then conjoin. By itself, it would not be a radical change, and wouldn't be lethal or greatly harmful. But what if it was occuring at a regular developmental stage, where some external signal (heat, light, space, or whatever) already led to a differential development between the two embryos? Normal starting development would be a winged creature with two wings and two legs. If you want to be bold, the (bird/lizard) is capable of developing two body forms depending on environmental conditions - either forelegs or wings.

While the original conjoinment happened without any obvious external sign, the conjoinment later meant the two embryos experienced different conditions in the egg. This new conjoinment isn't perfect, but generally leads to development of two forelegs and a head from one, and wings plus back legs from the other. It does require a stable and predictable pattern of conjoinment, but this species was already doing that before. It was just that no one could tell.

Surprisingly, these strange critters are able to grow and thrive in a time of many empty evolutionary niches. They give rise to an entire genus of hexapods.

Dragons have always been described extremely variably, and this would be perfect. No one can say how many limbs they have, or if they have wings or not, because environmental factors and sheer dumb luck cause a variety of conjoinments and differentiations. Some have two wings and two back legs, some have two, four, six or even eight legs depending on how things turn out. some might have no legs and move like snakes. You could even have those with two heads or two tails. Four wings, even. Over enough generations of these pleomorphic creatures, they might develop different ways of connecting nerves so all these possible forms can function seamlessly. There will be badly dysfunctional things that come crawling out of some of the eggs, and this only adds to the fun and horror of monsters. They'll be like mutants, but developmental ones.

Is it likely? No. But then neither is the platypus. It means that you can have dragons, basilisks, wyverns, wyrms, lindorms, and so many more wonderful things, and they can be one or a few related species.

The same logic can be applied to other species, with similar results. The developmental abnormalities can even switch off, giving you a stable species with a stable body plan. It's up to you.

  • alternatively, you can have a hox mutation that causes a bird-like creature to develop a second identical set of wings. Usually, such things are non-functional, but given a sheltered environment (like flightless parrots on an island) such a creature could mutate into a function for the extra wings, then re-evolve flight. Perhaps the four wings allow a really large bird like an ostrich-sized bird to fly and exploit a unique hunting niche. Who knows? Why not?
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    $\begingroup$ +1: That is a properly epic explanation for dragon forms! Well done :) $\endgroup$ Oct 13 '20 at 16:44
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Your best bet is to have an early magical event that creates a 6 limbed lizard, that can evolve into the other 6 limbed forms you need.

repurposing unused limbs is pretty common evolutionarily speaking, so it can evolve into whatever else you need. Consider using something from Sauria they evolved a wide variety of forms (crocodiles, dinosaurs, birds, pterosaurs) so you can conceivable get beaks, scales, feathers whatever you need without much trouble.

If you need to get something like an ungulate just make it superficially like an ungulate and use dinosaur like details (dental battery, proto feather hair, ect) you can even give it 3 toes and just make the first and third very small.

It is important your first event is both magical and normal terrestrial limbs. Functional limb duplication basically can't happen in vertebrates, becasue you have to duplicate not only the limbs but an entire body segment to have the supporting musculature, but that will duplicate internal organ pathways which will be very lethal. I recommend duplicating the hind limbs since that is slightly more plausible as it will not result in the duplication of major organs but it is a good thing you are using magic to explain it.

Of course you can add a few 4 limbed descendants in the mix since loss of limbs has occurred several times, which can further confuse matters, maybe there are flightless dragons or something similar. You can also have marine forms evolve since again it has happened several times before (whales and ichthyosaurs)

People have already worked out similar evolutionary histories, so consider searching around for inspiration. enter image description here Source: Birvan from DeviantArt

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Evolution is not a predetermined path where from A follows necessarily B. It follows the laws of probability: random mutations happen all the time in a random fashion, if they happen to giving their bearer an advantage they are promoted in the life lottery.

Look at sharks and dolphins: they show that in at least two cases a similar hydrodynamic profile has been picked at the evolution lottery, at a few tens million years of evolution apart.

It's not a matter of where you start from, but if the mutation bring some advantage or not in the specific environment where it happens to be.

would it be more likely/logical for a flightless quadruped to evolve extra limbs that would eventually become wings? Or for a bipedal flying creature to grow an extra pair of legs/claws?

I would say that both are highly unlikely: body plans are pretty stiff, and changing them is hardly possible. If ever it's easier to lose some limbs than to grow more: look at vertebrates: they started with 4 limbs plus a tail and some of them have lost the tail and/or the limbs, but none of them has grown more than 4 limbs.

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  • $\begingroup$ I guess a better question to ask would be which of the two body plans would benefit more from the additional limbs/wings? $\endgroup$
    – Arvex
    Oct 11 '20 at 20:31
  • $\begingroup$ To sharks and dolphins, you can add ichthyosaurs; land-evolved reptilians that returned to the sea and which look very like the true fish (sharks) and mammalian (dolphins) versions. Three times that convergence has happened. $\endgroup$ Oct 12 '20 at 14:23
  • $\begingroup$ And over a little more than 10's of millions of years. Sharks stabilised in the Late Ordovician some 450mya. Cetaceans evolved some 50mya, and Ichthyosaurs evolved some 250mya. You can also make similar analysis for dugongs. $\endgroup$
    – Kain0_0
    Oct 14 '20 at 6:35
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They started at six limbs.

I have read a manga -Centaur no Nayami- where evolution went a road where terrestrial creatures had six limbs, to justify centaurs. But it checks out! if there were 6 to begin with, two of them can become wings, and if you don't want the rest of your fauna to have 6 limbs, they can become vestigial members and disappear visually. If the situation call for it, these can even grow back up to whatever utility you want them to have.

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Evolution tends to be very conservative when it comes to creating completely new body parts, but very creative when it comes to reusing and adapting body parts. So rather than starting with a smaller set of limbs and gaining new ones, think about starting with a different combination of limbs, and then specialising them.

An interesting comparison here are arthropods: their original ancestor is believed to have had a set of identical segments with multi-purpose appendages, which in various groups of descendants have become legs or wings, but also antennae and mouth parts. Among those descendants are all insects, whose basic body plan consists of 3 pairs of legs and 2 pairs of wings, but which include such variations as beetles, where the front pair of wings have evolved into hardened wing-cases; and mantises, where the front-most pair of legs have evolved into something more like arms.

An even more familiar example would be our own body plan: we consider ourselves bipedal, with an "extra" pair of arms; but it is clear that we did not evolve from an armless ancestor with only two legs, instead specialising our front limbs until they were almost completely unsuitable for walking on.

So to get back to the question: the most plausible evolutionary origin for something that is "quadrupedal and winged" is an ancestral body plan with six limbs, from which you can derive various specialisations. Six is actually quite a sensible number - for instance, six legs allows for more stable walking over uneven terrain, because you can have more points of contact during a step. An arthropod-style system of repeated segments is quite a likely mechanism, because "repeat 3 times" is a simple instruction for the ancestral DNA to arrive at.

If you want some creatures to have our familiar four limbs, they could either be a separate evolutionary line - just as the existence of arthropods on Earth doesn't rule out the existence of mammals; or they could have one pair of limbs become completely vestigial - think of flightless birds, for instance.

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Develop wings from display structures

Evolutionary assumptions: As remarked in several answer evolution tends to be conservative. Every step in the evolutionary path needs to have a benefit over the parent creature otherwise it would loose the evolutionary race. So extra limbs that have no benefit until completely developed are evolutionary not viable. Also as noted nature will tend to energy efficient models, (dolphins and sharks which end up the same via completely different evolutionary paths) the fact that all larger animals mammals and dinosaurs alike had four legs suggest that this is the most efficient system. Remember that an extra set of legs might be beneficial for stability, but it also requires extra attention and more food to mantain.

So assuming that you don't care about how the creature is developed as long as it is feasible I would go for developing wings from display structures. A bit based on the comment of Clockwork-Muse who pointed out the Draco lizards.

Evolutionary path: An ape like tree dwelling creature that would have a set of dorsal fins for display (mating) or camouflage purposes should be able to evolve. That bigger and more flexible dorsal fins would allow for easier attraction of a mate (or better camouflage) pushing the creature in the way of bigger and stronger dorsal fins. If the dorsal fins were situated in such a way that they could extend the range of jumps from tree to tree by increasing the gliding distance this would add the evolutionary push to slowly transform them into wings. With this evolutionary path you could create wings with a benefit for the creature every step of the way.

Critical points: Whether you could create a gryphon this way would be questionable. Evolving from an ape like into something gryphon like is possible. Creating an animal with the size (and more importantly the weight) of a lion and be able to get enough energy for flight is very questionable for me. The largest flying animal was the Pterosuar, with an estimated weight of 250kg, but these were cold blooded, for comparison the wandering albatross (bird with largest wingspan) weighs 12 kg.

Another point against it is that as soon as you would have a gryphon due to evolution it would quickly tend to loose its shape for a more favourable aerodynamic shape. What might be a possibility is that a gryphon would mainly be a ground animal and only use flight to dive upon its pray from above after stalking it on the ground.

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In the magic-infused world

In this case, there's no need for special reasoning - magic can do strange things. Evolution is already happening rapidly (and thus skipping the intermediary stages that can occur), so you just need some form of evolutionary force to push the creatures to evolve in that way.

So simply ask yourself, why does each creature have wings, and why does each creature have four legs?

Perhaps the pegasus evolved from horses because some predator was causing major problems with the species, and magic provided an escape path - the air. And so, the four-legged creature gained wings.

Perhaps the hippogriff, despite its similarities to the pegasus, evolved from eagles, and needed to be able to be more agile on the ground due to the formation of tunnels (created by another new creature), thus developing quadrupedal movement.

It all comes down to the evolutionary force causing the change.

In the non-magical world

When magic isn't driving it, the cause will need to be more nuanced. Evolution is normally a very slow and undirected process - the question becomes, why did the pegasus develop little mini-wings, or why did the hippogriff start to grow a second pair of legs? Without magic to drive it, you're going to have trouble justifying the transition from four limbs to six.

Fortunately, in a world where evolution is very slow, and there's no need for the conceit of humans waking up to find things changed, this can be handled slightly differently.

Rather than having "normal" beings evolve into winged quadrupeds, work the other way around.

Rather than a pegasus being the result of a horse evolving, make the horse the result of a pegasus evolving. A pegasus's wings would be a large metabolic addition. In situations in which a group of pegasi have no need to fly, the wings would atrophy. Eventually, evolution would dummy them out - there would be some residual joints where the wings used to be, but there's just no need for them. And voila, you have horses.

To make this work neatly, all animals and humans would have, ultimately, evolved from winged quadrupeds. This can create interesting extra details - there could be humans with vestigial winglets, for example.

Alternatively, perhaps humans evolved from centaurs, who originally had wings, but they became arms over time. Then the front legs became less useful because mobility on the spot became more important than fast movement forwards, and they became bipedal - now the humans might have vestigial fore-hips.

The underlying driving force is the same. It just runs in the opposite direction.

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Start your thinking from polydactyly. It is quite common that (at least) mammals grow extra fingers. So they develop extra something of something existing.

If I am not wrong, there are people born with extra (no fully-formed) arms, or other parts of their bodies.

From here we can form a rule: it is likely that a mutation occurs, to create a new species with extra something which already exists.


You have in mind two paths of evolution.

  1. 2 legs + 2 wings -> 4 legs + 2 wings

This is quite close to what is already seen.

  1. 4 legs + 0 wings -> 4 legs + 2 wings

Now, the situation is a lot more complicated. Even if the bones of the wings are similar to the bones of the legs, they must be covered with something to provide lift. Feathers (like birds), membranes (like bats) or any magic, whatever you want. Additionally, the brain must evolve also, to be able to control the wings. Movement changes from 2D to 3D, so the vision has to evolve also. If they have to fly very high, breathing needs an upgrade too. So this is the path less likely to happen.


The only problem is if you want the 4+6 beings to be mammals. Because mammals do not have wings by design (with a few degenerated cases, where the legs are joined by membranes, so no real wings: bats, flying foxes, flying squirrels, sugar gliders...).

If you decide the beings to be birds, then go ahead. Growing an extra pair of legs would look gross at the beginning, but in time it will become every-day life.

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  • $\begingroup$ I actually don't think that the brain needs to evolve to control limbs for different purposes as the brain is highly adaptive even in a single member of a species. Considering that humans are capable of learning things like cycling, swimming, etc., which all require very different movesets, I think it's safe to assume that the brain of a higher species would be capable of adapting to flight with neuroplasticity alone and without any need of further evolution. $\endgroup$
    – DLCom
    Oct 13 '20 at 18:20
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Perhaps it evolved from a separate group of lobe-finned fishes which had 2 pairs of pectoral fins through random mutation, which was found to be useful and so was selected for among that group of fishes. Over time, these fishes would go down a similar path their 4 finned relatives did, and evolve into hexapodal pseudoamphibians. Eventually, they would become very similar to normal reptiles, having scales and being able to survive indefinitely on land. Smaller species would probably develop wing flaps on their upper forearms so that they can glide through the air or open them up to scare predators. Eventually, they could evolve larger and more powerful wings that allow them to actually fly instead of glide. And it will still have 4 unmodified legs to walk on.

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You need to explain why they need six limbs (and maybe why other land vertebrates don't)

I agree with Sol and others; in a world where some vertebrates still have six limbs, it's most likely that all vertebrates would have had six limbs at some point.

However, even if their fish-like ancestors had six fin-legs, there would need to be some reason why some (or all) would keep six limbs over hundreds of millions of years of evolution. Given the increased energy requirements of six limbs over four, there would need to be some other advantage to it vs, say, two of them becoming vestigial over time.

Perhaps your world has very strong winds, and to stop themselves from blowing away the land animals all need at least one set of limbs to grip onto things? Maybe the terrain is dominated by vast cliffs that require extra limbs to climb? Plants that evolved fruits and nuts that require six hands to open?

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    $\begingroup$ I'm not convinced that there's any particular reason to assume that 4 limbs is the optimum number, rather than just the number that feels natural to us Earth mammals. The reason to keep limbs that had begun specialising as wings would be much the same as the reason we've kept our arms as well as our legs. $\endgroup$
    – IMSoP
    Oct 12 '20 at 18:13
  • $\begingroup$ I don't think four is the optimum, I'm saying that there is evolutionary pressure to lose limbs/organs that aren't useful, especially in flying animals where every gram counts from a power-to-weight point of view. You need to answer the question: once an animal can fly, why would it still need four legs? $\endgroup$
    – K. Morgan
    Oct 12 '20 at 21:37
  • $\begingroup$ That's a better point than what you've put into your answer, but I'm still not convinced - evolution doesn't jump to theoretical optima, and there are always competing pressures. From a starting point of four equally spaced legs plus one pair of wings, it only needs walking to continue as part of the animal's general habit to put selection pressure on keeping all four functional. Insects have six legs and four wings, which ought to be very wasteful under your logic, but evolution doesn't seem in a hurry to slim them down to two of each. $\endgroup$
    – IMSoP
    Oct 12 '20 at 21:58
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Yet another possibility would be to use symbiotes along the lines of those parasitic flatworms that cause frogs to grow extra legs. frog with multiple hind legs, photo taken by Dave Herasimtschuk

The parasite larvae penetrate the tadpoles' tissue and zero in on the developing limb buds, so that when a tadpole begins to metamorphose into a frog, its "primary system of locomotion doesn't work—it can't jump, can't swim," he said.

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Who told you that all the dinosaurs that evolved into birds were bipedal? We cannot be sure.
Back to the present, flying squirrels are not bipedal, should in the future some squirrels evolve from gliding to full flight probably they'll have to become bipedal with two limbs evolving into wings and the other two remaining for motion on the ground. Flying quadrupeds should have six limbs in the beginning for other reasons, developing a pair of limbs requires a long evolution during which the limbs are useful even when they are a little bit more than stumps.

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There is an extinct gliding reptile called Coelurosauravus jaekeli that had "wings" supported by bony rods growing out just below the shoulders instead of elongated rib bones that are currently used by gliding lizards. You could use that as an evolutionary starting point perhaps.

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