The Origins of Form

Ancient genes, recycled and repurposed, control embryonic development in organisms of striking diversity.

embryo

Chemical changes in various regions of an animal embryo (here, a developing fruit fly) reflect the activities of tool-kit genes; the changes can be imaged by laser-dye probes long before the physical form of an animal emerges. The upper image shows the pattern of activity of a single gene, Engrailed, that marks the back end of each developing segment of the insect’s body. In the lower image a different set of laser-dye probes reveal where each of seven Hox genes are active, corresponding to various parts of the body; for example, bright yellow indicates the segments that will form the fly’s rear end, whereas fuchsia and light blue mark segments that will form mouthparts. Photomicrograph at top by James Langland and Steve Paddock www.molbio.wisc.edu/carroll/ Photomicrograph at bottom by Dave Kosman, Ethan Bier, and William McGinnis / University of California, San Diego (see Kosman et al., Science, v. 305, no. 5685, p. 846, 6 August 2004). Description of techniques that generated this picture: superfly.ucsd.edu/~davek/; McGinnis Lab www.biology.ucsd.edu/labs/mcginnis/

Just as the invention of the telescope revolutionized astronomy, new technologies were pivotal to conceptual breakthroughs in developmental biology. New techniques for cloning and manipulating genes, together with new kinds of microscopes, enabled the body-building genes to be observed in action. Chemical changes in an embryo could be visualized long before the appearance of physical structures. Workers could thereby directly observe the earliest events in the formation of segments, limbs, or a brain.

I realize it may be hard to get excited about how a maggot develops. What can that teach us about the more majestic creatures people care about, such as mammals, the rest of the animal kingdom, our own species? Indeed, the common perception twenty years ago—reinforced by a wide cultural divide between biologists who worked with furry animals and those who worked with bugs or worms—was that the rules of development would differ enormously among such different forms.

The body parts of fruit flies, for instance, would not appear to have much in common with our own. We don’t have antennae or wings. We walk around on two long, bony legs, not six little ones reinforced by an exoskeleton. We have a single pair of movable, camera-type eyes, not compound bug eyes staring out from a fixed position. Our blood is pumped by a four-chambered heart through a closed circulatory system with arteries and veins; it does not just slosh around in our body cavity. Given such great differences in structure and appearance, one might well conclude that there is nothing to learn from the study of a fly about how our own organs and body parts are formed. But that would be so wrong.

The first and perhaps most important lesson from evo-devo is that looks can be quite deceiving. Virtually no biologist expected to find what turned out to be the case: most of the genes first identified as body-building and organ-forming genes in the fruit fly have exact counterparts, performing similar jobs, in most mammals, including humans. The very first shots fired in the evo-devo revolution revealed that despite their great differences in appearance, almost all animals share a common “tool kit” of body-building genes. That discovery—actually a series of discoveries—vaporized many previous ideas about how animals differ from one another.

For example, the origin of eyes has received a lot of attention throughout the history of evolutionary biology. Darwin devoted considerable effort in Origin to explaining how such “organs of extreme perfection” could evolve by natural selection. What has puzzled and intrigued biologists ever since Darwin is the variety of eye types in the animal kingdom. We and other vertebrates have camera-type eyes with a single lens. Flies, crabs, and other arthropods have compound eyes in which many, sometimes hundreds, of individual ommatidia, or unit eyes, gather visual information. Even though they are not close relatives of ours, squids and octopuses also have camera-type eyes, whereas their own close relatives, the clams and the scallops, have three kinds of eyes—camera, compound, and a mirror-type.

The great diversity and crazy-quilt distribution of eyes throughout the animal kingdom was, for more than a century, thought to be the result of the independent invention of eyes in various animal groups. The late evolutionary biologist Ernst Mayr and his colleague L. von Salvini-Plawen suggested, on the basis of cellular anatomy, that eyes had been invented independently between some forty and sixty-five times. Discoveries in evo-devo have forced a thorough reexamination of this accepted idea.

In 1994 Walter Gehring and his colleagues at the University of Basel, Switzerland, discovered that a gene required for eye formation in fruit flies is the exact counterpart of a gene required for eye formation in humans and mice. The gene, dubbed Pax-6, was subsequently found to play a role in eye formation in a host of other animals, including a species of squid. Those discoveries suggested that despite their vast differences in structure and optical properties, the evolution of different eyes has involved a common genetic ingredient.

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