Flap those gills and fly!

I am going mildly nuts right now—somehow, I managed to arrange things so multiple deadlines hit me on one day: tomorrow. I've got a new lecture to polish up for our introductory biology course, a small grant proposal due, and of course, tomorrow evening is our second Café Scientifique. Let's not forget that I also have a neurobiology lecture to give this afternoon, and I owe them a stack of grading which is not finished yet. I'm really looking forward to Wednesday.

Anyway, so my new lecture for our introductory biology course is on…creationism, yuck. What I'm planning to do is to describe some of the most common creationist arguments and then give a biologist's rebuttal. Creationism is really a waste of our class time, but using it to explain some general concepts that any informed biologist should understand (and that the creationists, including Mike Behe, are astonishingly clueless about) will make it a little more productive, I hope. We'll find out tomorrow.

One of the common creationist claims I plan to shoot down is the whole idea of "irreducible complexity" as an obstacle to evolution. I was going to bring up two ideas that invalidate it: the principle of scaffolding (which I discussed here), and exaptation, in which features evolved for some other purpose than the one that they play in an organism we observe today. I was looking for a good example, and then John Wilkins fortuitously sent me a paper that filled the bill (we evilutionists, you know, are sneakily sending each other data behind the scenes to help in our assault on ignorance. We're devious that way.)

The question is how insect wings evolved. Wings are a classic issue in evolution, because they aren't going to function for flight at all until they've achieved a certain minimal size—half a wing isn't any good at all for getting an animal in the air, so any explanation for their selective evolution has to incorporate alternative functions: as stabilizers for cursorial animals, for instance, or traps for catching small prey on the run.

In insects, we have an interesting origin explanation for wings: they're modified gills. It makes sense. For gills, you want to have an increased surface area for gas exchange, and you want them exposed to the external environment. Most animals evolved sophisticated gills with convoluted surfaces and tucked them away in a protective chamber, with a mechanism to pump water over them, but others took a simpler path. Mayflies, for instance, have flat vanes on each segment in the larval stage as respiratory surfaces—they even look like wings. Arthropods evolved a recipe for flat, cuticular structures to serve as gills, and perhaps one explanation for the evolution of wings is that they simply re-evoked that recipe as adults, used it for gliding, and then expanded and elaborated on the formula incrementally to generate flapping, powered flight.

More evidence for this hypothesis comes from an analysis of non-flying arthropods, the crustaceans. The arthropod limb is primitively complex with multiple branches, shown below, while insects have stripped it down to a simpler jointed stalk. Many crustaceans have retained the tripartite branching structure of the limb, with an endopod (the foot), an exopod, and of most interest to us right now, a dorsal epipod.

The insect arrangement is illustrated at the top. They have wings and legs, diagrammed as simple discs (appropriately; they form from imaginal discs in the larva). We also have a lot of information about patterns of gene expression in these structures in insects. A gene called engrailed (en) is expressed in just the posterior half of each segment, and this gene has the same pattern in crustaceans. There is also a gene called Distal-less (Dll) that is expressed in all appendages; that one isn't quite as interesting for this study. The genes that are particularly provocative are pdm, which is expressed only in the insect wing and not in the leg, and apterous (ap), which is expressed only in the dorsal half of the wing and in a narrow ring on the leg. The question is whether a) crustaceans also have pdm and ap, and b) if they do, are they expressed in the epipod, which would suggest that wings and epipods are homologous structures.

And the answer is yes to both. Genes homologous to the Drosophila ap and pdm genes were identified in Artemia, and they are active in just the epipods of the crustacean limb. Pdm is similarly active in the epipods of the crayfish.

Artemia thoracic limb. b)Expression of Dll in all outgrowing regions of the Artemia limb. c-e) Expression of pdm in Artemia. f-h) Expression of ap. i-k) pdm expression in the thoracic limbs of Pacifastacus leniusculus.

What it implies in the evolution of the arthropods is that the wings of pterygote insects are derived from epipod gills, or alternatively, have coopted a molecular pathway that first arose in epipods. While most of the terrestrial arthropods have been simplifying their limbs, the winged insects retained one element that gave them the power of flight.

It's this kind of history that invalidates Behe's notion of irreducible complexity. Sure, it's hard to imagine why an aquatic arthropod would begin the stepwise Darwinian process of assembling a set of wings for flight, but what this work shows is that there is an incremental pathway for expanding epipods as aqueous respiratory surfaces. The mistake creationists make, which seems intrinsic to their nature, is to assign functions erroneously to adaptations, when the simpler idea that structures have only local and immediate functions is far more productive over the long term. It's the same with Behe's favorite example, the flagellum: if it evolved as a secretory pump first, it wouldn't have required every feature of an "outboard motor" to function. His mistake is to assume that every step in its evolution was part of a drive to make a motor.

Averof M, Cohen SM (1997) Evolutionary origin of insect wings from ancestral gills. Nature 385:627-630.