Picture an animal – any animal, maybe your favorite animal. Then ask a nearby kid to name her or his favorite animal. I think it's a pretty safe bet that neither of you chose a sponge or a sea squirt, or a planarian or a sea pen, or a moth or a mosquito. And let's hope that neither of you chose a tapeworm or a trombiculid mite. Those unlikely choices are all animals. But it's more likely that you both chose a vertebrate, and I think it's highly likely that you both chose atetrapod vertebrate – an animal with legs and/or wings, a skull and a backbone. Maybe we prefer these creatures because they're a lot like us, or because they make good pets (or food), or because they're big enough to make an impression, or because they were the animal representatives pictured on the ark in board books. (Or maybe you chose a butterfly, and now you feel a little left out.) What matters is that there is something extra interesting about tetrapod vertebrates.
As you might have guessed, tetrapods are vertebrate animals that have four limbs. The group includes reptiles, amphibians, birds, mammals... you know, the usual suspects. (Snakes and whales, which don't have those limbs, are nonetheless classified as tetrapods, and we'll come back to that.) At first, this might look like a wildly diverse crowd of animals with almost nothing in common: tiny hummingbirds in the air, gigantic whales in the ocean, frogs that come from tadpoles, salamanders that can regrow severed limbs, cats that eat only other vertebrates, misnamed “bears” that eat only eucalyptus leaves. But on closer inspection, some extraordinary patterns emerge. These animals, in all of their magnificent variety, seem to be built in very similar ways. It's as though some kind of master plan has been tweaked over and over, to make a huge collection of variations on a theme.
This master plan for building tetrapods includes numerous components: plans for building backbones, for making skin, for growing a brain. Some of those components are unique to tetrapods; some are more widely employed in animals. Our focus will be the one that is most clearly associated with the tetrapods. We will explore the building of limbs – arms, legs, wings and flippers; and hands, feet, paws and paddles.
Consider, then, the human forelimb, better known as the arm. You may already be familiar with its skeletal structure, nicely illustrated in the 17th-century chalk drawing below.
The upper arm contains a single large bone, the humerus, which is attached to the shoulder and to the elbow. The lower arm sports two parallel bones: the radius and the ulna. Those two bones link the elbow to the wrist. The wrist is composed of a group of small bones called the carpals (made famous by Carpal Tunnel Syndrome, which is reportedly exacerbated by the typing of blog posts). Attached to the carpals are the metacarpals, which are the bones of the fingers. So, the skeletal components of the human arm are as follows: one bone (humerus) attached to two bones (radius and ulna) attached to a set of small blocky bones (the carpals), which anchor finger bones. It's an interesting pattern, but all by itself it's not necessarily remarkable.
Now let's look at the human hindlimb, or leg. The bones have a different set of names, which you may know all too well. Have a look at the 19-century illustration below.
The upper leg contains a single large bone, the femur, which is attached to the hip and to the knee. The lower leg sports two parallel bones: the tibia and the fibula. Those two bones link the knee to the ankle and foot. The ankle and foot are composed of a group of bones that includes a set of small bones called the tarsals. Attached to the tarsals are the metatarsals, which are the bones of the toes. So, the skeletal components of the human leg are as follows: one bone (femur) attached to two bones (tibia and fibula) attached to a set of smaller blocky bones (tarsals and others), which anchor toe bones. It's an interesting pattern, but all by itself it's not necessarily remarkable.
But wait. The leg pattern is essentially identical to the arm pattern. Why just one pattern? Why that pattern? Is there something special, maybe even somehow universal, about the pattern?
Questions like those were the domain of the great Richard Owen, the British naturalist and contemporary of Darwin. Owen's detailed study of limb structure led him to write one of the more influential works in the history of biology: On the Nature of Limbs, first published in 1849 and most recently reprinted in 2007. In that book, Owen argued that all vertebrate limbs were modifications of a basic pattern or plan, called an archetype.
To see why Owen reached this conclusion, consider the wonderful lithograph below, created in Owen's time (1860) by Benjamin Waterhouse Hawkins, who also contributed illustrations to Darwin's Zoology of the Voyage of the HMS Beagle. The limbs of the horse are constructed in an interesting pattern, depicted in the upper left. One large bone is attached to two parallel bones that have fused over most of their length. Those two bones attach to a collection of bones which then attach to some longer bones that form the ends of the limbs.
The pattern is much more striking when the limbs of diverse vertebrates are compared. Have a look at these two illustrations from On the Nature of Limbs. One is a dugong, a large aquatic mammal, and the other is a mole, a tiny mammal known for burrowing and defacing lawns. Do you see the pattern? One bone attaches to two bones which attach to blocky bones that support digits.
That pattern applies to bat wings and whale flippers and frog legs and chicken feet. It applies to dinosaurs and to newts. It's a universal feature of tetrapod limbs, front and back. Neil Shubin, in his brilliant book Your Inner Fish, summarizes the pattern as a simple chant: one bone, two bones, little blobs, digits. Owen's great insight was this: limbs are built according to a common pattern. One bone, two bones, blobs, digits.
Now, that's a remarkable fact about the animal world, and we curious hominids are itching for an explanation. Why are all tetrapod limbs based on the same underlying pattern?
We can use Owen and Darwin to sketch the two main competing explanations: design and descent. In the simple version of the story, Owen the anti-evolutionist, the design theorist of his day, concluded that the archetype was a design, a basic idea in the mind of the Creator. Darwin, of course, proposed a radically different explanation: the “archetype” is a common ancestor, and the variations on that “theme” are exemplars of descent with modification. There's no design, no Creator, just a lot of gradual tinkering with a setup that worked well enough at some time in the distant past.
That outline is hopelessly simplistic. Owen's views on evolution were complex and malleable; indeed, he got in some trouble for suggesting that tetrapods (even humans) were descended from fish through “slow and stately steps, guided by the archetypal light.” Later in life, in the midst of various nasty disputes with contemporaries (most notably with T.H. Huxley, known affectionately as “Darwin's Bulldog”), Owen did seem to oppose evolutionary ideas. But his writing in 1849 shows that he could see no reason to reject common ancestry while exploring the nature of the archetype. In other words, Owen was, at least earlier in his career, comfortable with common ancestry alongside strong conceptions of design.
And that is one theme that we will explore in this series. We will examine the evolution and development of limbs, to see how evolutionary explanations work and how strong and multidisciplinary the evidence for common descent really is. Common descent, I will argue, is really true, at least because it provides vast explanatory resources to those seeking to understand tetrapod limbs. But what about design? Can design also contribute explanatory resources? It's one thing to assert that the limb-construction blueprint proceeds from the mind of God; it's another thing to propose it as an explanation for why limbs are the way they are. Is there something about that plan – one bone, two bones, blobs, digits – that is superior? Could it have been otherwise? Those questions, I think, are the ones that we must address before we can advance design as an adjunct to – or a replacement for – common descent.
With those ideas in mind, let's explore the evolution of limbs. In the next post, we will explore the origins of those limbs, following the long search for their predecessors in the deep past and culminating in one of the most dramatic fossil finds in scientific history. In the third post, we will look at evidence from anatomy and developmental biology that supports the contention that fish fins and tetrapod limbs are variations on a theme. The fourth post will build on the third, looking at fascinating commonalities in the genetic systems that underlie the development of fins and limbs. In the fifth post, we will look at brand-new findings from developmental genetics that solidify and expand the fin-limb connection. The sixth and final post will look at the surprising links between fins, limbs and all other animal appendages, and will address oddities such as lost limbs in whales.
Bring your curiosity and your questions!
Neil Shubin (2009) Your Inner Fish: A Journey Into the 3.5-Billion-Year History of the Human Body. New York: Vintage Books.
Brian K. Hall, editor (2007) Fins into Limbs. Chicago: The University of Chicago Press.
Richard Owen (1849) On the Nature of Limbs. London: John Van Noorst. (Google eBook).
Brian Switek (2008) Richard Owen, the forgotten evolutionist. Blog entry at Laelaps.
Carl Zimmer (1999) At the Water's Edge. New York: Simon and Schuster.
The first three images (human arm, human leg, man on horse) are courtesy of Wellcome Images, Creative Commons license. The last two images are taken from On the Nature of Limbs (1849), free online at Google eBooks.