The Origin of Animal Body Plans

             Douglas Erwin, James Valentine and David Jablonski

                                  Section 5

                      Early Evolution of Hox  Clusters

As a first step towards a developmental history of animal architectures, we
can begin to reconstruct the evolution of the Hox clusters using information
from developmental biology and knowledge of the relationships between
different phyla. Any gene found in both flies and mice, for example, must
have evolved prior to the last common ancestor of the two lineages. As each
key developmental control gene is discovered, developmental biologists
quickly search for its cognate gene in distantly related groups, effectively
peering back in time to the ancestors of each lineage.

Six Hox genes are shared between mice and flies, indicating that their
common ancestor, which lived before the Cambrian explosion, had a Hox
cluster composed of at least six genes. As living arthropods have eight Hox
genes, two of them must have originated by duplication after the divergence
of the ancestors of arthropods and vertebrates. Today these two newer Hox
genes mediate the development of segments in the middle of the arthropod
body. Hox genes mediating the development of the midbody, in addition to
other developmental features, were also duplicated within the lineage
leading to mammals. Although not all phyla have been studied, and the
quality of the data remains variable, Hox clusters within phyla that have
been well studied are distinctive, produced by unique patterns of gene
duplication and loss.

Both mammals and arthropods have segmented body plans, and one might
reasonably conclude that their common ancestor might also have been
segmented, for each group employs the Hox gene array to control
segmentation. However, the evolutionary tree suggests that these two groups
arose from a nonsegmented ancestor in which Hox genes probably helped to
specify the production of a series of structures repeated along the body
axis, but not of segments, just as they mediate cell differentiation along
the axis of nematode worms today. A similar situation is found with the
genes that control the development of limbs: Some regulatory genes, such as
distalless and its relatives, help generate both arthropod and mammal legs,
yet both the family tree and the fossil record indicate that the common
ancestor of these groups lacked limbs, which evidently arose just before the
Cambrian explosion and thus after the groups diverged. Eyes provide still
another example: The regulatory gene at the top of the cascade that produces
eyes in mice (Pax-6) is so similar to that in insects that the genes can be
interchanged and still function correctly. Yet insect and mammal eyes are
both complicated structures and each quite different. Each eye has clearly
evolved independently from a very simple common precursor.

These examples begin to give biologists a picture of how body plans, and the
genetic machinery that generates them, actually evolved. As animals emerged,
developmental control genes evolved that regulated the architecture of their
multicellular, differentiated bodies. The fundamental job of these genes was
to mediate the production of various cell types by other genes farther down
the cascade of gene expression, and to array the cell types within tissues
and organs in the appropriate order. Even as body plans changed and
anatomical structures evolved, the basic regulatory genetic system
nevertheless remained intact. Doubtless, as body plans became more elaborate
and more cell types were required, the gene-regulatory systems were
enlarged. Still, it seems that regulatory genetic modules were conserved
during evolution and suites of genes already present were deployed to
generate novel structures. Thus the genes that direct animal development
evolve in the same quirky, opportunistic ways as the morphologies that they
produce.

Perhaps the relative abruptness with which metazoan body plans were
elaborated to produce the Cambrian explosion can be explained by this
organizational structure. A cascade of developmental signals, perhaps
organized into a complicated hierarchy of gene expression, was able to alter
the network of structural gene expressions and interactions, rapidly
producing distinctive body plans.
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