Harvard Associate Prof. Arkhat Abzhanov on Archosaurs, paedomorphosis, and evolution of birds
One of the biggest challenges in evolutionary biology is trying to understand the origin of true novelties. Some of these novelties, innovations in evolution, are also called key innovations because they allow a group of organisms to take over a whole ecological niche and expand well beyond their ancestors. There are very few examples of such novelties which I actually try to explain. One of the novelties we are trying to understand is evolution of the avian skull with its beak and its very unusual characteristics which make it very different from the skulls of its ancestors, the theropod dinosaurs. How it evolved? Why it evolved? And what molecular processes took place?
The class Aves is one of the most successful groups of animals on our planet: there are over ten thousand species, there are dozens of families and orders of these animals, they can be found anywhere on the planet, they can be found in the water, under the surface, above the surface. They are capable of powered flight; there are two groups of vertebrates which are capable of powered flight. And they are extremely successful. And they are successful because again the ability to fly and their highly unusual skull and very interesting, very diverse beaks which allow them to feed on different types of food, do different functions, very complicated tool. That’s what we are trying to explain.
To understand evolution of birds we need to look at the history and the entire lineage of Archosauria that began back in the Triassic. About 250 million years ago the reptiles spread into two major groups. One group stayed small and they focused on small prey such as insects, and these are the ancestors of modern day lizards and snakes, they are called Squamata. The other group was large, they tended to stay large and they focused on large prey, this is a group called Archosauria, which means from Latin “following reptiles”, because they were dominants, they are again very large, and they tended to dominate the ecological systems in which they lived, which they occupied for hundreds of millions of years. Even now, again, birds combined with their close relatives the crocodiles they are still very abundant and very successful.
The Archosauria lineage gives rise to a number of different species during history. Their most basal members include crocodilians which are still around, luckily. The Archosuars also give rise to Pterosaurs, the flying reptiles, which were highly successful during their time and all the dinosaurs: the plant eating dinosaurs including these giant dinosaurs and the bipedal carnivore dinosaurs which include the theropod dinosaurs and which also include, eventually, the birds. So, the entire lineage from basal members, the crocodilians, all the way to the crown members, that was derived and which is the birds, belongs to the Archosauria.
In order to understand the evolution of Archosauria we wanted to trace the changes in the skulls of these animals all the way from the beginning, from primitive Archosaurs all the way to birds. And this work involved close collaboration with some important paleontologists including Dr. Mark Norell from the American Museum of Natural History, his chairman and a curator for paleontology, he is actually concerned to be number one dinosaur guide and probably one of the most famous living dinosaurs experts in the world and even more importantly he has a wonderful collection in his museum of dinosaur eggs, he was the first to discover dinosaur theropod eggs in Mongolia and in many other locations, and many of those eggs contained fossilized embryos. And this will become very important for our work, being able to understand the changes and the genetic changes which happened in the dinosaurs will be quite critical for explaining the evolution of the birds.
Our campaign with paleontologists produced some really interesting findings. During one of my meetings with Mark Norell I realized that both of us were speaking about something quite alike, he mentioned the effect that after handling hundreds of skulls of dinosaurs and primitive parrots he remark how similar the skulls of primitive birds and modern birds were to the skulls of juvenile dinosaurs. And the same time I was working on a different project I was looking at development of alligator embryos, looking how their heads and their bodies, and then I realized that how bird like the heads were of the alligator embryos. We decided to test this hypothesis, that modern birds are somehow resembling juvenile dinosaurs, more formally.
We decided to focus on skulls again of all the Archosaurs from primitive Archosaurs, animals like Proterosuchidae, which represents one of the really primitive Archosaurs, it’s a very large animal, size of a monitor lizard, but has a number of primitive characteristics, all the way from primitive dinosaurs to advanced dinosaurs to primitive birds and modern birds. We took the skull, we put lots of landmarks on it, so, regenerated the CT scans and asked the computer to tell us how the skulls changed at the time, so, which part of the skulls changed and in which direction. That’s been done and we published our report which was very clearly that during evolution of the Archosaurs, particularly the dinosaurs, the skulls began to elongate so that the snout became longer and longer, so, by the time you evolved this really advanced theropod dinosaurs which were the last raptors, for example, this very aggressive eating, very advanced dinosaurs, again, they had very long snouts with lots, lots of teeth, they had relatively small eyes, they had very small brain and small skull.
But this is not how they actually began the development. If you look at those embryos inside those eggs which are just about to hatch or just hatched, these really young dinosaurs, their snouts are very short, they have only few teeth and they have big eyes and the big brain. That’s basically how the bird’s skulls look like. So, if you look at the skulls of both juvenile and adult primitive birds like Archaeopteryx. Archaeopteryx, we have animals which are about two times difference in size, some of them are juvenile, some of them are essentially adult, and the skulls are very similar to each other, and both of those are very similar to the skulls of dinosaur embryos, that is they have very short snouts, they still have teeth but not very many and they are small, and they have big eyes and they have very big skull.
If you again ask the computer to tell you where the birds belong to, what you find is that you have these changes in adult Archosaurs skulls, and they move from primitive Archosaurs to primitive dinosaurs to advanced dinosaurs, this is where adult advanced dinosaurs set, but separately from those there is a baby space, that’s where the dinosaurs begin as babies, and then they move from this location to this location, it’s a very long road, it takes about seven to nineteen years for a dinosaur to become fully grown, fully adult. And this baby space that’s where we find birds. That’s where we find primitive birds like archaeopteryx both juveniles and adults, that’s where we find modern birds, in a fact modern birds become even more what we call paedomorphic.
Paedomorphosis is a phenomenon of evolution where a change in timing of developments can cause interesting morphological change. Paedomorphosis is when the adults are the descendants, resemble the juveniles of their own ancestors. And there are actually two different ways to become paedomorphic. One of them is called neoteny, one famous example of neoteny is salamanders. Axolotl, for example, axolotl is a larva looking mature adult salamander. So, it looks like a larva of its ancestor but it’s actually a sexual mature adult. That’s neoteny when your somatic development is retarded relative to your sexual development. You develop very-very slowly but at the time you are mature you still look like a larva.
The other way to become paedomorphic is called progenesis and that’s basically what the birds are doing. And in progenesis your body is developing normally but you become sexual mature much-much-much faster. If you look at the time, when it took for the dinosaurs or the crocodilians to become mature, it takes about for them 9 to 10 years to become mature adults, to primitive birds and then to modern birds, the time actually becomes shorter and shorter and shorter. The time you get to the songbirds which are the most advanced modern birds it takes near weeks, just a few weeks, for them to become sexual mature, for example, if you think about a modern bird from a time of hatching for a robin, for example, it takes about two weeks for it to look like an adult, so, by the time it fly just off the nest it looks very similar to its adult much of the size, much of the shape. It’s done developmentally. So, its development is much truncated relative to its ancestors.
The birds in other words, and we can show that using morphometric analysis of skulls, are highly paedomorphic versions. That is very juvenile versions of their ancestors, the theropod dinosaurs. They have very baby like skulls. And what we are trying to do now, we are trying to understand some of the molecular developmental mechanisms of how that change is actually possible. So, this is, again, overall, paedomorphosis considered to be an example of heterochrony which is a very important concept in evolutionary biology: how timing, how playing with timing development, with timing or order of events development can produce significant morphological changes. We are able to show, again, that birds are result of such heterochronic shifts, they are paedomorphic dinosaurs, baby like dinosaurs.
The second approach out of three approaches, we’ve done the morphometric part now, we figured out what actually happened morphologically during the evolution of birds. Now we are doing the comparative biology part. I mentioned the fact that dinosaurs died out, everybody knows that, but luckily we do have primitive Archosaurians, the crocodilians are still around. For this work we are actually comparing development of heads in bird embryos, in chicken embryos, early stages when the face is just being put together and alligator embryos. We go down to a national preserve in Louisiana, it’s in the United States, and we collect alligator embryos, bring them back to the lab, we raise them here, we incubate them here and we then compare the development of the alligator embryos, how they put their much more primitive looking faces with very long snouts, to those of the chickens. And that allowed us to identify particular molecular changes that must have occurred during evolution of the birds because we found that the faces of the Archosaurs actually patterned very similar to the way how chameleon faces, for example, chameleon embryos or lizard faces have patterned. They grow snout, they have these two centers of signaling, basically two grow zones which push the face forward and produce a snout.
The birds are different because the birds unlike their cousins, the crocodilians, they have a new novel signal centre right in the middle of the face, there is a novel signal in molecule which commands the fusion of all the structures that form the beak and it causes the expansion. What we wanted to do – we wanted to deconstruct this so that we could actually attempt to push the evolution backwards. What we did, we used a very specific inhibitors of the signaling molecule and we blocked this breed specific signals centre and we essentially restored, we left these lateral signal centers in place which are still there but we blocked again this novel breed specific one. And that actually produced a face which in patterning was actually very similar and from the way how it actually developed earlier to that of the crocodilians, and if you do that what happens is that the structures which normally in birds fused to form a beak, a skeleton forms convert, turn from the snout to a beak, actually undergoes the opposite kind of transformation that is the structures do not longer fuse, in fact, they form very large paired balance and the overall face begins to look much more snout like.
If you actually now put landmarks on this skull of manipulated experimental embryos of the chicken, we can grow them almost to hatching, it is embryos which we manipulated and we can subject them to the same morphological analysis that we used to understand the ancestors. And if you do that, what you see is that the skulls of these experimental embryos they no longer are found in the space occupied by birds, in fact, they leave it and you find now them among the snouted forms, among the forms they are actually right within their more primitive lineages which give rise to birds. By deconstructing the birds specific signaling environment, by deconstructing the birds specific changes we are able to push the morphology all way back to the ancestors, and the experiments are ongoing but we expect, we predict that the more accurate reconstruction of the ancestral signaling environment would allow us to reconstruct the ancestral faces, the faces of the ancestors of the birds much more accurately as well.
That’s the direction in which this work is going, and we are showing also that how these approaches: the morphometric analysis combined with comparative biology and function experiments can be successfully applied not only to understanding micro evolution changes but also to understand macro evolution changes as well.