The Origins of Form

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

chick and snake embryos

Hox genes determine the form, number, and evolution of repeating parts, such as the number and type of vertebrae in animals with backbones. In the developing chick (left), the Hoxc-6 gene controls the pattern of the seven thoracic vertebrae (highlighted in purple), all of which develop ribs. In the garter snake (right), the region controlled by the Hoxc-6 gene (purple) is expanded dramatically forward to the head and rearward to the cloaca.

Brian McOmber and Ann C. Burke

A large body of work—on birds, frogs, mammals, and snakes, as well as insects, shrimp, and spiders—has proved that shifts in where Hox genes are expressed in embryos are responsible for the major differences among both vertebrates and arthropods.

Those shifts account, for instance, for the way a snake forms its unique long body, with hundreds of rib-bearing vertebrae and essentially no neck, in contrast to other vertebrates [see photograph left]. The shifts explain why insects have just six legs and other arthropods have eight or more. The new imagery of evo-devo can pinpoint when and how the development of these animals diverges. The study of Hox genes has shown how, at an entirely new and fundamental level, these animals are the products of variations on ancient body plans—not wholly independent inventions.

Shifts in the expression of tool-kit genes during development not only account for large-scale differences in animal forms; they can also explain differences among closely related species, or even populations of the same species. For example, the three-spined stickleback fish occurs in two forms in many lakes in northern North America [see photograph below]. One is a short-spined, shallow-water, bottom-dwelling form. The other is long-spined and lives in open water. The two forms have evolved rapidly in these lakes since the end of the last ice age, about 10,000 years ago. The length of the fishes’ pelvic spine is under pressure from predation. In the open water, long spines help protect the stickleback from being swallowed by large predators. But on the lake bottom, long pelvic spines are a liability: dragonfly larvae seize and feed on young sticklebacks by grabbing them by their spines.

Pelvic spines are part of the fishes’ pelvic fin skeleton. Short spines in bottom-dwelling populations can be traced to a reduction in the development of the pelvic-fin bud in the embryo. David Kingsley, a geneticist at Stanford University, Dolph Schluter, a biologist at the University of British Columbia in Vancouver, and their collaborators have demonstrated that the change in spine length in short-spined sticklebacks can be traced to one specific tool-kit gene. The expression of the gene is altered so as to reduce the pelvic fin bud and, ultimately, the pelvic skeleton. The research has connected a change in DNA to a specific event in embryonic development, which in turn gives rise to a major adaptive change in body form that directly affects the ecology of a species.

The insights from the little three-spined stickleback may reach far beyond the fish’s particular natural history. The pelvic fin is the evolutionary precursor of the vertebrate hind limb. Hind-limb reduction is not at all rare in vertebrates. In two groups of mammals—the cetaceans (dolphins and whales) and the manatees—the hind limbs became greatly reduced in size as the animals evolved from their land-dwelling ancestors into fully aquatic forms. Similarly, legless lizards have evolved many times. The study of sticklebacks has shown how natural selection can lead to changes in major features of animal skeletons in a relatively short time.

In addition to showing how evolution can change the number and kind of repeated body structures, evo-devo is shedding light on how novel structures and new patterns evolve. Bird feathers, for instance, are prominent examples of novelties that have emerged from changes in the ways tool-kit genes are expressed. So are the hands and feet of four-legged vertebrates, the insect wing, and the geometric color patterns on the wings of butterflies. It is easy to imagine that insects invented “wing” genes, or birds “feather” genes, or vertebrates “hand” and “finger” genes. But there is no evidence that such genes ever arose. On the contrary, innovation seems to be more a matter of teaching old genes new tricks.

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