New Limbs from Old Fins, Part 6
In this series, we have looked at the evidence that has led biologists to conclude that the limbs of animals like birds, bats, and brachiosaurs have their historical roots in the fins of fish. We explored shared anatomical features, fossils of extinct transitional forms, conserved cellular signaling systems, and homology in genetic systems, and we discussed these data in the context of the concept of homology. Common descent, I have argued, provides a coherent and unified explanation for these observations. In fact, by looking at data of very different kinds, we have seen two major strengths of evolutionary theory – its explanatory power and its fruitfulness across various scientific disciplines. There is no competing scientific explanation, at least not today.
We will conclude our series by addressing two interesting questions that have come up along the way and by looking closely at the meaning of purpose and design in the context of evolutionary explanation.
Not just homology. Deep homology.
In the previous post, we saw that genetic control systems involved in the development of fish fins and animal limbs are strikingly similar, so much so that genetic switches can be transplanted among organisms as different as fish, birds, and mammals. Observations like those strengthen the conclusion that chick wings, mouse paws, and (amazingly) fish fins are homologous, meaning that they are altered versions of a common ancestor. Chick wings and mouse paws are classic examples of structures that display homology.
There are, however, zillions of other animals with legs. It's hard to think of an animal that doesn't have appendages of some kind. What about all those other legs? Are they all homologous to each other? Specifically, are the legs of insects somehow homologous to the limbs of mice? (I'll focus on insects here, but the same conclusions apply to all arthropods.)
The answer is: almost certainly not. For one thing, there are few structural similarities. More importantly, a look at the animal family tree shows that there are animals "between" insects and tetrapods that don't have structures comparable to either limbs or insect legs. In other words, fins and insect legs each developed in different organisms, who originally had no appendages at all. The two branches arose independently, as near as we can tell, and so fly legs and mouse paws are not homologous.
But, shockingly, the genetic systems that control their growth are strikingly similar. Fly leg development is controlled by Hox genes. More amazingly, fly leg development is controlled by many of the same Hox genes that perform similar tasks in mice. Fly legs are not homologous to mouse paws, but it looks like the genetic systems that control their development are, to a large extent, homologous. Neil Shubin, Cliff Tabin, and Sean Carroll coined the term 'deep homology' to describe this phenomenon in the influential 1997 article "Fossils, genes and the evolution of animals limbs". Deep homology, then, refers to historical continuity of genetic control systems that underlie patterns or forms that are not so evidently homologous—like fly legs and mouse paws.
Deep homology has been seen in other developmental contexts. One of the more famous examples is the development of the eye or, more accurately, the development of eyes. Eyes are wildly different in different kinds of animals (consider the camera-like human eye compared to the compound eye of a fly), and they develop in very different ways in different kinds of animals. They seem not to be homologous; on the contrary, they seem to have evolved independently dozens of times. But a look under the hood shows remarkable deep homology – the genetic control systems are homologous. In one of the most dramatic experiments in developmental genetics, scientists in Walter Gehring's lab in Germany were able to induce the growth of extra eyes in fruit flies, by flipping a genetic switch, and it didn't matter whether the switch came from a fly or from a mouse. The mouse switch could turn on eye development in a fly. The picture below shows a fly with eyes growing on all six of its legs! (The eyes are the reddish-brown blobs on the legs, which are on the left side of the photo.)
Deep homology has important implications for our understanding of the development of life on earth, and its discovery helped trigger the birth of a new branch of biology, a sort of hybrid of evolutionary biology and developmental biology: evolutionary developmental biology, or evo-devo. The fins-to-limbs story is an exemplar of evo-devo thought, which emphasizes the role of conserved genetic control systems in the development of the magnificent diversity of animal forms. The basic idea is that these ancient genetic control systems make excellent "toolkits" that can be modified extensively to generate those seemingly endless "variations on a theme" that fins and limbs exemplify so beautifully. Fly legs and human arms may not be structural homologs, but the deep homology in their genetic underpinnings suggests that they are variations on a theme – perhaps we can call it the "outgrowths" theme – that was established in some of the most ancient animals of all.
Tetrapods without limbs?
We saw in the first post that snakes and whales are classified as tetrapods, even though neither has four limbs. What's up with that?
The simplest explanation is this: snakes and whales are classified as tetrapods because they are descended from tetrapods. To a biologist interested in classification, the term 'tetrapod' refers to a group of organisms related by descent, and not necessarily to a group of organisms that have a particular set of features. This is more common than you might think. For example, there are flies that have neither wings nor legs, but are still classified as flies (and as insects). Darwin himself, in the Origin of Species, wrote that "all true classification is genealogical," meaning that life is best understood as a "community of descent." So, snakes and whales are animals with less than four limbs that have descended from animals with four limbs.
Why do biologists think that snakes are descended from card-carrying tetrapods? The evidence they rely on is the same kind of evidence that we looked at throughout this series: shared anatomical features, fossil intermediates, conserved developmental and genetic toolkits. Consider, for example, the pelvic girdle (the part of the skeleton to which the legs attach) of a tetrapod. Some snakes (like pythons) still have that pelvic girdle, and those snakes grow tiny limb buds. Fossil snakes with tiny (and shrinking) hindlimbs have been clearly described. What about the genetic toolkit? It's conserved, with some changes that inactivate the limb-growing signal at just the right time. We know the signal is there because a limb bud from a python can cause limb growth in a chicken! Snakes, it seems, are elongated tetrapods with reduced (or erased) leg development.
The natural history of whales is better known thanks to some truly spectacular fossil intermediates discovered in the last 20 years or so. That story has been nicely covered previously on this blog, and the outline is familiar: common anatomical themes, striking fossil intermediates, and genetic data all point to a land-dwelling tetrapod mammal as the common ancestor of all whales (including dolphins). We can "watch" the hindlimbs disappear in a historical sketch based on fossils, and we can see what happens when the hindlimb-making program is accidentally turned back on. As you might have guessed, that rare event results in a dolphin with vestigial hindlimbs, arising from seemingly normal limb buds that occur in every dolphin embryo. Dolphins, it seems, are streamlined tetrapods with reduced (or erased) hindlimb development.
Descent versus design
The natural history of tetrapods is a superb example of the explanatory power of common ancestry. Each line of evidence – anatomy, fossils, developmental mechanisms, shared genetic toolkits – is interesting and suggestive. But taken together, the data form a distinctive body of observations that are convincingly explained by common descent. No competing explanation comes close.
Design, of course, is one proposed explanation for some of the data we've examined. As a competing explanation, design is currently a failure. Whether we look at structural themes or underlying genetic systems, we can identify no clearly-defined principles of functional optimization. In other words, we have no good reason to suppose that the tetrapod limb blueprint (one bone, two bones, blobs, digits) represents the only way – or even the best way – to build a limb (or a wing or a flipper). We have no good reason to suppose that Hox genes are the only way – or the best way – to turn on gene expression systems underlying limb development. We have no good reason to suppose that the Sonic Hedgehog protein is the only way – or even the best way – to send growth signals through a limb bud (or a fin bud). In each of those cases, we have no good reason to suppose that it could not have been otherwise, and in some cases, we know that it can work in other ways.
Design does not help us make sense of the patterns in the fossil record as exemplified by animals like Tiktaalik. Design does not help us make sense of the temporary hindlimbs of embryonic dolphins, nor does it account for deep homology. Design, to whatever extent it stands for functional optimization or even excellence, is unhelpful as an explanation when it comes to limbs and fins and their shared characteristics.
This could change, of course. Scientists may learn that there are yet-unknown design constraints that dictate one or a very few optimal configurations for limb and fin construction, such that things really could not have been otherwise. (Perhaps those scientists who prefer design-based explanation will take the lead on this one.) In fact, I argue that the only way to establish design as a competing explanation, one that can rival the explanatory power of common descent, is to convincingly demonstrate something akin to a set of profound biological design constraints. To unseat common ancestry, or at least to rival it, design theory has to show that life could not have been otherwise.
Descent with design
But design need not compete with common ancestry. Some design theorists do in fact accept common descent, and seek to identify marks of design in the processes by which the tree of life came to be. These attempts vary in quality, and the better-known examples have been discussed on this blog in detail. The point is that design thought, whether it posits supernatural "intervention" or mulls "front-loading," need not be inherently dismissive of the explanatory power of common ancestry.
In fact, I think some emphasis on design is important to retain while considering evolution. For Christians, one reason for this is simply the fact that we confess the biological world to be the creation of the Creator God. There's also another more subtle reason: design in some form may be a necessary explanatory principle. One point at which design and descent seem confluent is in the ideas and emphases of paleontologist Simon Conway Morris. Recently discussed on this blog, and now in a complete web site, Conway Morris' theme is evolutionary convergence – the striking tendency of evolution to repeatedly "discover" design themes. Perhaps ideas like his are pointing us to principles of design and purpose that run deep in the living world, or perhaps they simply tell us a bit more about how God's world really works.
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.
John Gerhart and Marc Kirschner (1997) Cells, Embryos, and Evolution. Malden (MA): Blackwell Scientific.
Neil Shubin, Cliff Tabin and Sean Carroll (2009) Deep homology and the origins of evolutionary novelty. Nature 457:818-823.
Sean B. Carroll (2005) Endless Forms Most Beautiful: The New Science of Evo Devo. New York: W.W. Norton & Co.
Sean B. Carroll (2008) Evo-Devo and an Expanding Evolutionary Synthesis: A Genetic Theory of Morphological Evolution. Cell 134:25-36.
Figure 2C of Gehring. (2011) Genome Biology and Evolution 3:1053-1066.