All insect species on Earth have exactly six legs—a pair on each of three thoracic (middle) body segments. Look at the larger group of arthropods, however, and you will see a striking variation in leg number, including finding legs on abdominal segments. These dramatic differences in morphology represent changes in self-contained body units (modules). The modular changes can arise through relatively small changes in key regulatory genes. In this tutorial we will examine an example of such modular changes in insects. We will also see how relatively small changes in the timing or place of expression of key regulatory genes can affect the morphology of different species—in this case comparing the hindlimbs of ducks (webbing) to those of chickens (no webbing).
The fruit fly Drosophila melanogaster provides a good example of modularity in an organism. Early in development, the fly embryo forms segments—or modules—each of which later develops an identity, becoming head, thoracic, or abdominal segments.
The expression of homeotic, or Hox, genes establishes segment identity. For example, the Antennapedia (Antp) gene is expressed at its highest level in the second thoracic segment, where the gene promotes leg development. If this gene is misexpressed in the head, it causes the developing fly to produce legs in the place of antennae, thus changing the head segment identity.
While all insects have evolved to have just six legs, other arthropods have a variable number of legs—some having legs on all thoracic and abdominal segments. Evolutionary biologists attribute this dramatic diversification to arthropod modularity and to specific mutations in a Hox gene, called Ultrabithorax, or Ubx.
The sequences of the Ubx gene are known for many different arthropods. Insects are unique in that they have an alanine repeat in their Ubx protein sequence.
In insects and all other arthropods, Ubx protein is expressed in the abdomen. However, the insect form of the protein can repress a gene, called Distal-less, that is required for leg development. Therefore, in the abdomen of insects, legs do not develop.In other arthropods, the Ubx protein, which lacks the alanine repeat, does not repress Distal-less, and therefore abdominal legs develop.
The Ubx protein provides an example of how mutations in genes that regulate developmental processes can lead to evolutionarily important morphological changes. Such evolutionary changes can also occur through changes in the time or place of the expression of developmental regulatory genes.
The feet of developing ducks and chicks offer an example of changes in the place of expression of developmental regulatory genes. In developing chick and duck hindlimbs, a gene called BMP4 is expressed in the webbing between the toes. The protein encoded by this gene triggers cell death, which would eliminate the webbing.However, duck hindlimbs also express a gene called Gremlin in the cells of the webbing, while chick hindlimbs do not. The Gremlin protein represses the activity of BMP4, and thereby prevents cell death in the webbing of duck feet. This differential expression results in markedly different morphologies in the different species.
If lack of Gremlin expression results in cell death in the webbing, we can inquire whether artificial Gremlin expression could result in webbed feet in chicks. The scientists inserted Gremlin-protein containing beads into the webbing of developing chick feet. When these chicks hatched, their feet showed webbing similar to that of ducks, suggesting Gremlin protein inhibits cell death.
Modular changes in organisms have the potential to create dramatic changes in a species. Because modules are self-contained units, changing a module often has no deleterious effect on the functioning of the body as a whole. If a module can change without significant harm to the organism, over the course of evolution species can change the identity of individual modules, resulting in better (or worse) adaptation of the species to its environment. Through understanding the roles of key developmental regulatory genes, scientists are learning that many of these dramatic changes in morphology can arise through relatively small changes in genes.