The Origin of Animal Body Plans

             Douglas Erwin, James Valentine and David Jablonski

                                  Section 6

                       Hox  Genes and Early Body Plans

Although those of us who study evolution can infer a great deal about the
body plans of the first animals that left traces on the seafloor, we
obviously do not have their actual genes and cannot evaluate their
relationships from molecular evidence. We are sure that they were moderately
complex forms with three tissue layers, but we have no evidence of their
relationship to the many living phyla that came afterwards. For example, we
do not know whether the animals that made these early traces are more
closely related to vertebrates or arthropods, or include ancestors of both
groups. It is also quite possible that these early tracemakers originated
well before the last common ancestor of arthropods and vertebrates. We can
infer some of the developmental control genes that must have been present in
the common ancestor of arthropods and vertebrates, but, as these do not
specify particular structures, they do not constrain the morphology of that
ancestral form, and so we are not sure whether or not it was like the early
trace makers. The data that we do have permit us to frame three possible
scenarios for the relative timing of the evolution of the Hox genes and of
the body plans of animal phyla near the time of the Cambrian explosion.

The first scenario proposes an ancestor common to protostomes and
deuterostomes that lived nearly 565 million years ago, before the advent of
trace fossils. In this case, the ancestor was not capable of making the
sorts of trace fossils found later and must have been either tiny or flat,
or both. The presence of at least six Hox genes at this early stage implies
that Hox-cluster sizes and Hox-gene duplications are not closely linked to
morphological innovations, and indeed that some of the genetic evidence may
be misleading. The Cambrian explosion, then, must be related to some
pervasive environmental change, the evidence for which is still lacking,
which permitted or encouraged developmental evolution among many independent
lineages. Explanations range from an increase in atmospheric oxygen content
above some critical constraint, to an ecological arms race in which the
mutual evolutionary responses of predators and prey drove a host of lineages
independently to elaborate skeletons and behavioral repertoires.

Another possibility is that lineage divergence, Hox-gene duplications and
body-plan formation were spread through the 35-million-year interval between
the early traces and the Cambrian explosion. The last ancestor common to
vertebrates and arthropods could have lived nearly 565 million years ago or
even somewhat later. As in the previous scenario, developmental controls in
this ancestor presumably evolved first, reaching a level of sophistication
that permitted the rise of major morphological innovations and culminating
in the explosion of body plans during the late Neoproterozoic and early
Cambrian. This scenario might also include an environmental trigger to the
explosion.

          The final scenario assumes a tight linkage between lineage
          diversification, the duplication of the Hox cluster and the
formation of the body plans, all taking place rapidly nearly 535 million
years ago. In this case the Neoproterozoic traces were produced by animals
that predated the last ancestor common to mammals and arthropods. This
rather extreme view of the Cambrian explosion was held by some
paleontologists until fairly recently, and increasingly accurate radiometric
dating of fossil-bearing beds has actually shortened the timespan during
which the explosive appearance of body plans took place. At the same time
however, intensive collecting has produced fossils that tend to smear out
the metazoan diversification and to indicate that moderately complex body
plans were present at classic Neoproterozoic fossil localities.

Choosing between these three hypotheses, which are not mutually exclusive,
is difficult at present, although a growing body of evidence leads
paleontologists to discount the third scenario. We suspect that the answers
will eventually lie within the second scenario, with major innovations
appearing neither in the dim past before fossil evidence is available, nor
at the very instant that the fossils leap to our attention, but rather at
various times within the relatively brief late Neoproterozoic interval now
under such heavy study. By extending the perspective beyond the Hox cluster
to the myriad of other regulatory genes, biologists can begin to reconstruct
the regulatory architecture at other critical branchpoints. For example, the
same set of genes is responsible for head formation in both arthropods and
vertebrates, but it is unclear what the head of the ancestor common to
protostomes and deuterostomes was like. Similarly, the heart and
blood-vascular system in both lineages are also controlled by a set of
conserved regulatory genes, but the role of these genes in the ancestor of
protostomes and deuterostomes remains unknown.

These uncertainties culminate in the two very different visions of the
ancestor common to protostomes and deuterostomes. It is possible to
visualize this ancestor as the simplest animal permitted by this sort of
molecular evidence, assuming the conserved regulatory genes are relegated to
general functions but not to specific structures, even those that are
widespread in the body plans of their descendants. In this event the
protostome-deuterostome ancestor was a simple worm, lacking segmentation,
with minimal differentiation from head to tail and from back to belly and no
blood-vascular system. At the other extreme is a much more complex
protostome-deuterostome ancestor, with features associated with similar
control genes in living descendants, including a well-developed head,
nervous system and circulatory system and perhaps even limbs.

The differences between these two models are great, and the course of
body-plan evolution is likely to have involved a mosaic of changes
intermediate between these two extremes. The coming decade is sure to bring
a much deeper understanding of the evolutionary interplay between
developmental control genes and the morphologies they help to construct. A
partnership of paleontology, developmental biology and molecular systematics
has enormous potential to reveal the evolution of the fundamental body plans
that characterize all animals.
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