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Brains and beaks

I’m always telling people you need to understand development to understand the evolution of form, because development is what evolution modifies to create change. For example, there are two processes most people have heard of. One is paedomorphosis, the retention of juvenile traits into adulthood — a small face and large cranium are features of young apes, for instance, and the adult human skull can be seen as a child-like feature. A complementary process is peramorphosis, where adult characters appear earlier in development, and then development continues along the morphogenetic trajectory further than normal, producing novel attributes. You may have encountered examples of this in fiction: the best known are the Pak Protectors in Niven’s science-fiction stories, which are the result of longer-lived humans continuing the processes of aging to reach a novel form. There’s also the story of After Many a Summer Dies the Swan, a novel by Aldous Huxley, in which a paedomorphic species (a human) lives for a very long time and develops to reach the ancestral state — a more primitive apelike form.

Just to make it more complicated, though, this isn’t to say that evolution proceeds by arresting the whole of development, turning the adult into an overgrown baby. What’s going on here is that genes that control the rate of development are being tweaked by genetic change, and there are many of those genes. There can be all sorts of mixing and matching — one organ or feature can undergo paedomorphosis in a species at the same time that another is undergoing peramorphosis.

A beautiful example has recently been published in Nature: the evolution of the avian skull. The postcranial bird skeleton can’t be neatly categorized as changes in rate: wings, the correlated changes in the pelvis and thorax, all that is a messy collection of novelties. The skull, though, can at least be broken down into a couple of key avian adaptions: brains and beaks. The cranium has gone through a set of changes with all the behavioral and sensory changes (big eyes, motor aspects of flight, navigation), while the beak has obviously diversified for different feeding strategies. The beak has changed to take over the manipulatory role lost as forelimbs became wings.

Here’s how the role of heterochrony (changes in rate of development) of different species was determined. The authors collected quantitative morphological data on a set of fossil dinosaurs and birds and extant birds for which there were both embryological and adult data. There are some straightforward observations that just leap out at you. For instance, embryonic alligator skulls have the same proportions as the skull of adult Confuciusornis, a crow-sized bird from the Cretaceous.


Similarity of embryonic Alligator and adult Confuciusornis skulls. Superimposition of Alligator embryo skull (green) onto Alligator adult skull (red, left) and onto Confuciusornis adult skull (red, right), showing the nearly identical skull configuration of the latter two and indicating paedomorphic cranial morphology in Confuciusornis.

Another common and long-hallowed technique in developmental biology is to trace a standard skull onto a 2-D grid and then determine what distortions of the grid are necessary to reshape the skull into a specific form. This method makes the stretching and skewing and compression that had to have occurred over time to sculpt these skulls from an ancestor. Here are the ontogenetic changes for different species, illustrating how they changed shape as they grew up.


Summary of ontogenetic changes in archosaur skulls; outlines on deformation grids from average. a, Alligator. b, Compsognathidae. c, Therizinosauridae. d, Archaeopteryx. e, Enantiornithes. f, Confuciusornis. g, Ostriches (Struthio).

If you can do this kind of assessment of transformations over development, you can also do it over phylogeny. Below are shown the trends observed in dinosaur and avian evolution.


Summary of heterochrony and phylogeny in bird skull evolution. emu Dromaius. Heterochronic transformations referred to in the text are A phylogenetic sequence with skull outlines set on deformation grids is enumerated with Roman numerals. Major anatomical regions involved in depicted from the primitive stem-group archosaur Euparkeria to the modern heterochronic transformations are labelled.

The coordinate system on which those skulls are mapped is a little tricky to explain. With all the numerical data available from their skull measurements, the authors did a principal component analysis, determining metrics that accounted for most of the variability between skulls. What they found were two axes of change: one is in the shape of the cranium, which exhibited paedomorphic patterns of change (although the contents of that cranium, the brain, is known to have undergone more complex heterometric change); the second was in the beak, which shows a pattern of peramorphic change.

But that’s the cool thing about this! We can quantitatively describe the plastic changes in the shape of the skull over evolutionary history as largely the product of two trends: a retention of the bulbous embryonic shape of the skull, and increased extension of the facial bones to form a beak. It’s not magic, it’s the expected incremental shifts in shape over long periods of time, in which we can actually visualize the pattern of transformation.

Now we just need to work out the genes behind these morphological changes, and their mode of action. That’s all. Hey, I think the developmental biologists have at least a century of gainful employment ahead of them…


Bhullar BA, Marugán-Lobón J, Racimo F, Bever GS, Rowe TB, Norell MA, Abzhanov A (2012) Birds have paedomorphic dinosaur skulls. Nature doi: 10.1038/nature11146. [Epub ahead of print]

Comments

  1. says

    Hey, I think the developmental biologists have at least a century of gainful employment ahead of them…

    Ah ha, just as the IDiots say, it’s all about job security.

    Of course, that’s a tad disingenuous when you realize they’re concerned about job security (if not for themselves, for any progeny dumb enough to take it up) because they fail to come up with any meaningful science.

    Great stuff anyhow. Maybe we’ll finally know how ravens and parrots get so much intelligence into those little heads.

    Glen Davidson

  2. clastum3 says

    Now we just need to work out the genes behind these morphological changes, and their mode of action

    There’s evidence that much of the difference is due less to the genes than to regulatory zones (located in the “junk”). There was an article I can’t trace in SciAm a year-or-so ago arguing the same.

    This at least puts the factoid that our genome is very closely related to that of other animals into perspective.

  3. davidbowden says

    PZ — thank you for these types of posts. As much fun as it is to read the other types of posts (which truthfully, is what I come here for), these postings supply a nice opportunity for someone who’s NOT a biologist to learn some of the underpinnings of biological science.

    Also — thanks for making it easy enough for even an electrical engineer to understand! Now if we could only get some of the creationist type EEs to read more biology…

  4. douglashudson says

    Wow, that’s fascinating. Birds have to be one of the most successful species on the planet (if you count their dinosaur ancestors), and its really cool to see how they developed over time.

  5. azportsider says

    Agree with davidbowden: I come here to read the fun anti-religion posts, and stay for the science. In this case, I’m especially grateful because avian origins and evolution are my main–though amateur–interests.

  6. paleotrent says

    I wish I could have been in the room when those researchers first superimposed the embryonic alligator and adult Confuciusornis skulls. Beautiful. Those kinds of moments in science are very rare indeed! I’ve only had one such moment in my career, twenty-something years ago when I was a graduate student (and unfortunately it wasn’t nearly as cool as the above).

  7. sapphire says

    It’s all a bit complicated for a poor physicist but surely no one can still deny that there is a huge body evidence for evolution when they see it clearly presented to them like this.
    Or maybe they can because it contradicts a 3,000 year old book of Hebrew myths.

  8. Roberto Aguirre Maturana says

    Cool! the first thing that came to my mind when you described peramorphosis were Pak Protectors!

  9. Sili (I have no penis and I must jizz) says

    Agree with davidbowden: I come here to read the fun anti-religion posts, and stay for the science. In this case, I’m especially grateful because avian origins and evolution are my main–though amateur–interests.

    I don’t understand.

    Gnu-Atheism is supposed to scare people and make them more religious. Only talking about science without any reference to politics is ever gonna make the public more educated and skeptical.

    Chris told me so, so it must be true. He has nice hair after all.

  10. David Marjanović says

    I wish I could have been in the room when those researchers first superimposed the embryonic alligator and adult Confuciusornis skulls. Beautiful.

    Seconded, thirded, fourthed and fifthed!!!!

  11. ChasCPeterson says

    regulatory zones (located in the “junk”)

    no, nobody thinks regulatory zones are junk.
    There’s plenty of actual junk.

  12. meursalt says

    Sorry to hit the thread late. This post was timely for me, as I had actually been wondering, about a week prior, what science has learned about the origin of the beak. None of the material on the dinosaur-bird transition I’ve been reading and watching has covered it, and I kept forgetting search for this specific topic.

    One thing that just struck me is that the dinosaur-bird lineage seems to make much more innovative use of skeletal bone than do mammals. Mammals have all sorts of modified teeth, and horns and antlers, but dinosaurs and birds have or had beaks, spikes in odd places, bony fins, bony crests (apparently as both display and with sinuses for vocal resonance), diverse profusions of cranial horns, bizarre vertebral processes, bony club tails,and other miscellaneous bony protrusions.

    On further reflection, mammals also have the bones of the inner ear. But these are essentially atrophies from their ancestral forms, so I don’t know if they are comparable to the types of adaptations listed above. I don’t really count bat wings as being a strange use of bone, since they are just modified fingers, still being used for locomotion.

    Contemporary reptiles have some interesting specialized bones, for instance, the shells of turtles. But they still don’t seem to have quite the diversity of dinosaurs in this area.

    Is this a real pattern I’m seeing, or am I just ignorant of examples of bone specialization in mammals? Our teeth certainly seem versatile, but we seem to make rather mundane use of the rest of our skeletons compared to dinosaurs and birds. I’m curious if science has learned anything in this area. Perhaps there is some common set of genes promoting bone growth, common to the dinosaur/bird lineage, but not mammals or more “primitive” reptiles? Or maybe the surrounding tissues are better suited for bony protrusions than in mammals? Oh well, time for more web searches and maybe a fresh perusal of talk.origins archives.

  13. meursalt says

    oops, should have read “essentially atrophied from their original forms” re: inner ear bones.

  14. paleotrent says

    @meursalt – last year a friend of mine gave a seminar at a neighboring university that I found fascinating, and his take on mammals vs. birds (and even mammals vs. frogs) is very similar to yours. He and his colleagues link these morphological differences to primordial germ cells, or PGCs. They maintain that how the PGCs are specified makes a huge amount of difference in terms of morphology, and even has an impact on macroevolutionary patterns. Epigenesis is the more ancient form of development in which the surrounding somatic tissues influence the PGCs’ development. The more derived pattern (which has evolved separately in multiple lineages) is a process called “preformation” in which PGCs are specified “cell-autonomously” by maternally-derived molecules known as germ plasm. This latter process seems to lead to wildly different body forms. Compare and contrast frogs, with their bizarre skeletal modification (long hindlimbs, abbreviated trunk, big heads, etc.), and whose PGCs develop via preformation, with boring old salamanders, whose PGCs develop via epigenesis. The PGCs of mammals (even, as you note, bats) have that more-or-less conservative body form as a result of following epigenesis. By contrast, birds are much more derived – and guess what – unlike mammals, their PGCs develop via preformation. He and his colleagues also note that taxa characterized by preformation tend to be more speciose than taxa whose PGCs develop via epigenesis. Really remarkable stuff.

    The most current reference for their work is:

    Johnson AD, et al. 2011. Evolution of the germ line-soma relationship in vertebrate embryos. Reproduction 141(3):291-300. DOI: 10.1530/REP-10-0474

  15. meursalt says

    @paleotrent, Thanks for the info! It’s cool that someone is doing work in this area. You’ve given me some good search terms to try to get a handle on this stuff. I only have a high school level background in biology; I’m more of a tech guy. But evolutionary biology fascinates me. Creationism and general anti-science attitudes really bother me (I think due to the sheer arrogance in dismissing several entire fields of science), and I’m trying to educate myself so I can hold my own on the rare occasions I choose to engage creationists. Thanks again; I’ll dig deeper based on the info you’ve given.

  16. meursalt says

    @paleotrent And on a second, closer reading of your post, preformation is some weird shit! germ plasm? wow! I had a vague idea of epigenesis from reading biology or physiology texts years ago, but I had no idea there were alternatives. Now I’m curious if the germ plasm is propagated from the original oocyte or is “seeded in” to the embryo some other way. I’ll do my own homework; I just wanted to express how cool and counterintuitive preformation is to me.

    Also, frogs are pretty damn weird now that you mention it.