FEATURE ARTICLE
The Origin of Animal Body Plans
Recent fossil finds and new insights into animal development are providing fresh perspectives on the riddle of the explosion of animals during the Early Cambrian
Douglas Erwin, James Valentine, David Jablonski
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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