The barren Namibian desert in southern Africa, the dry outback of South Australia and the Winter Coast of the White Sea in northwestern Russia might seem unpromising Edens. But the rocks exposed in those far-flung areas hold the oldest record of animal life, a prelude to the evolutionary explosion of animal body plans that was to come. Preserved in those ancient marine sediments, which date from nearly 550 million years ago during an interval geologists call the Neoproterozoic, is a startling variety of frond-like fossils resembling sea pens, disc-shaped forms resembling jellyfish and a number of completely enigmatic forms that do not resemble any creatures living in modern oceans. The animals that left this ancient record were nearly all soft-bodied; hard skeletal remains are represented by only a few scrappy tubes whose biological affinities are uncertain. However, the activities of worms or slug-like animals are recorded by trails and burrows left behind as they crawled and dug about on their ancient sea floor. These ancient traces of animal activity closely resemble those produced by present-day organisms, and thus provide insights into the expanding anatomical complexity and behavioral repertoires of these early forms, another piece of the puzzle posed by the spectacular appearance of a diversified skeletonized fauna over only a few million years, beginning nearly 530 million years ago–the Cambrian explosion.
The Cambrian record of life is in sharp contrast with that of the preceding eons. The remains of single-celled organisms can be traced back to nearly the oldest sediments on the planet, about 3.5 billion years ago. And for the next 3 billion years or so, the earth was chiefly populated by single-celled organisms, although algae achieved a multicellular grade about 1 billion years ago. About 565 million years ago, the larger, multicellular animals of the Neoproterozoic appear in the fossil record, with their striking variety of form, only to be overshadowed about 35 million years later by the explosion of body plans recorded in early Cambrian rocks: Nearly all known kinds of shelled invertebrates appear then, including clams, snails and arthropods (the group including crabs and trilobites), soon joined by echinoderms and soon thereafter by chordates, the lineage that gave rise to humans and all other vertebrates. All of the basic architectures of animals were apparently established by the close of the Cambrian explosion; subsequent evolutionary changes, even those that allowed animals to move out of the sea onto land, involved only modifications of those basic body plans. About 37 distinct body architectures are recognized among present-day animals and form the basis of the taxonomic classification level of phyla.
The fossil record of the last 3.5 billion years thus shows not a gradual accumulation of biological form, but a relatively abrupt transition from body plans of single cells to those of a rich diversity of animal phyla. In geological terms, an explosion indeed. Was this explosion real, or is it an artifact of a strangely biased fossil record?
Over the past few years new fossil discoveries have greatly clarified the sequence of events up to and during the Cambrian explosion. This in turn has set the stage for integrating information from several fields that had once operated in near isolation. Modern techniques for extracting and analyzing molecular data have shed new light on the evolutionary relationships among the living animal groups whose roots extend back to, or even precede, the beginning of Cambrian time. Perhaps most extraordinary have been the discoveries in developmental biology. Molecular techniques have shown that the developmental systems that control patterns from eggs through embryos to adults, and thus determine animal architectures, are remarkably similar across a wide range of phyla. In spite of their similarities, which have persisted despite the long separation of the phyla, the systems produce very disparate body plans. Evolutionary biologists can now reconstruct basic aspects of the developmental control systems of long-extinct animals, and can attempt to track not only the diversification of animal form but also the establishment and evolution of the genetic controls that regulate it. Taken together, all these advances are permitting a new, multidisciplinary look at the early history of animals and into the mysteries of the Cambrian explosion.
The Family Tree of Animals
Choosing appropriate genes to study can be difficult, however, because different genes evolve at different rates. If the changes in sequence are too few, there is not enough difference among species to resolve the branching pattern on an evolutionary tree; too many changes overwhelm or "saturate" the DNA, so that any original similarities resulting from common ancestry are lost. Thus, for example, a gene that changes rapidly enough to be useful for examining the differences between two recently separated species of mice evolves too rapidly to be appropriate for examining the differences between the ancestors of a mouse, an earthworm and a fly, which lived over half a billion years ago.
Even with the appropriate genes, the molecular tree of life is difficult to interpret. For one thing, many of the phyla appear to have branched within a relatively short period of time. Therefore, the slowly evolving genes suitable for probing such ancient events changed relatively little between successive divergences, and it may be difficult or impossible to resolve the order of branching. Furthermore, with only four nucleic acids involved in the genes, similarities can arise by chance or through biases in substitutions of one nucleic acid for another that are unrelated to kinship among the species. More than 100 different numerical techniques have been developed to counter such problems, and whereas many of the divergences among phyla remain uncertain, others seem to be well established by the new molecular analysis.
The pattern of divergence among the phyla does not solve the larger problem, for the branching sequence tells biologists too little about when the body plans themselves originated. This is because at the branchpoints–when the lineages split and the molecules began to change independently–each branch had precisely the same body plan, and it may have been many millions of years before a new body plan arose. Consider an evolutionary tree depicting a swordfish, a fly and Marilyn Monroe. Marilyn would be placed closer to the swordfish than to the fly. However, the divergence between Marilyn and the swordfish, which happened over 400 million years ago, did not immediately produce their disparate architectures. When these lineages first separated they shared nearly all morphologic characteristics and differed in very few; it would have taken an expert to distinguish them. Not any more. And when did these striking architectural changes take place? To reconstruct the events that led from the branchings to the various animal body plans we must leave the molecules and turn to the fossil record.
Body Plans: A Neoproterozoic Prologue
Molecular data indicate that the metazoa--multicellular animals--arose from single-celled organisms related to choanoflagellates, a group that apparently originated about one billion years ago; the date is not closely constrained. Just when the first animals evolved is also uncertain, but it must have been sometime before the oldest traces of wormlike forms appeared, about 565 million years ago. Morphological and molecular evidence agree that the most primitive of living animal phyla are the sponges (Phylum Porifera). Sponges have only a few cell types differentiated to perform specialized functions, and they lack the sort of cell-to-cell junctions that form sheets of tissues in higher forms. Fossil sponges have recently been discovered in Neoproterozoic sediments.
The next most advanced phyla are Ctenophora (comb-jellies) and Cnidaria (jellyfish and sea anemones), which have two thin but well-differentiated tissue layers separated by a gelatinous material: a protective one surrounding the body and a digestive one lining the gut. The majority of the late Neoproterozoic soft-bodied fossils most resemble representatives of these two phyla.
Most analyses suggest the next major branch produced a body type with three primary tissue layers, the flatworms (Platyhelminthes), whose inner tissue layer produces muscles and some other organs. However, flatworms do not have a circulatory system, so oxygen must be transported to their inner tissue layer by diffusion, and thus they must be flat in order to keep these tissues near their surface oxygen supplies. Flatworm guts, like those of jellyfish, contain only one opening, so all of the contents enter and exit through the same aperture. Although most molecular and morphologic evidence indicates that flatworms evolved very early in the history of animals, they are small and soft-bodied; consequently no fossil flatworms are definitely identified in the fossil record.
The meandering trails and burrows of the Neoproterozoic were made by organisms capable of displacing sediments to form grooves and tubes, sometimes marked by structures that indicate pulses of creeping or burrowing, and in some cases containing pellets that are interpreted as fecal remains. Most of these are traces that cannot be attributed to sponges, anemones, or even flatworms; some of those animals can disturb sediments, but they do not produce elongate rounded burrows or fecal pellets. To produce such traces requires an organism that is not flat, can propel itself by generating peristaltic waves (waves of contraction and expansion moving along the body or along its ventral surface, as a "foot") and has a complete gut. Thus the fossil record puts a minimum age on an important branchpoint in metazoan evolution: The earliest known animal traces must have been produced by lineages more advanced than flatworms.
The kind of peristaltic locomotion that must have produced the early traces requires a "skeleton" of fluid-filled spaces inside a muscular sheath that can be deformed into waves to displace sediment. Two main kinds of fluid-filled spaces that could act as such hydrostatic skeletons are found within animal bodies: hemocoelic (blood) spaces, which develop between the tissue layers mentioned above, and coelomic spaces, which develop inside the third or innermost layer. In general, animals with only blood spaces are found in lower branches of the tree than are animals with coelomic spaces.
Flatworms lack both sorts of body spaces, but above them on the animal tree is the most famous branchpoint of all, a division that gave rise to a wealth of more complex animals that have one or both types of body space. One branch, the deuterostomes, includes echinoderms (starfish and sea urchins), chordates (from fish to mammals) and a number of minor groups. The second branch, the protostomes, contains most of the familiar invertebrate animals, including arthropods (crabs and insects), annelids (earthworms), molluscs (snails, clams and squid) and a host of other phyla known mostly to those lucky enough to have had an in-depth course in invertebrate zoology. It is quite likely that most or all of the Neoproterozoic traces were made by organisms with hemocoel-based locomotive systems.
Among living phyla, a simple body plan that could be responsible for some of the traces is that of the phylum Priapulida, which has a complete gut surrounded by a capacious hemocoel that is sheathed in turn by the muscles of the body wall. Priapulids burrow in soupy sediments at the surface of the sea floor. Other traces look as if they were formed by creeping snail-like animals of the phylum Mollusca, although, as snails themselves do not appear until significantly later, the Neoproterozoic traces may have been made by a common ancestor of molluscs and their relatives. Just such a form, known as Kimberella, has recently been reconstructed from a large number of body fossils from the White Sea of Russia. This is the first solid indication of what some of the creeping animals were like. The diversity of these traces increases throughout the late Neoproterozoic, and they probably represent a variety of body types.
Interpreting the enigmatic body fossils of the Neoproterozoic has proved more difficult than assessing the trace fossils. If the body fossils could reliably be assigned to some living phyla, it would pinpoint a minimum date for the origin of the specific body plan involved. Unfortunately, this is not yet possible. Although the soft-bodied fossils that appear about 565 million years ago are animal-like, their classifications are hotly debated. In just the past few years these fossils have been viewed as protozoans; as lichens; as close relatives of the cnidarians; as a sister group to cnidarians plus all other animals; as representatives of more advanced, extinct phyla; and as representatives of a new kingdom entirely separate from the animals. Still other specialists have parceled the fauna out among living phyla, with some assigned to the Cnidaria and others to the flatworms, annelids, arthropods and echinoderms. This confusing state of affairs arose because these body fossils do not tend to share definitive anatomical details with modern groups, and thus the assignments must be based on vague similarities of overall shape and form, a method that has frequently proved misleading in other cases.
Until 1995 paleontologists had believed there was a substantial gap between the Neoproterozoic fossils and the first Cambrian fauna. Most estimates placed the soft-bodied Neoproterozoic fossils as between 600 and 640 million years old, separated from the Cambrian by a gap of several tens of millions of years. Then field work at late Neoproterozoic sections in Namibia revealed volcanic ash beds near the earliest body fossils and other ash beds close to the Cambrian boundary. These beds provided the first accurate radiometric dates and revealed that they were younger than 565 million years. Furthermore, there was no gap: Neoproterozoic fossils continued right up to the base of the Cambrian, which has been established as nearly 543 million years ago by analyses of rocks from northern Siberia. Other correlation techniques have suggested that many Neoproterozoic assemblages found elsewhere in the world are about the same age as those from Namibia. Thus the fossil record of the early metazoan diversifications, including the Cambrian explosion, is only about 40 million years long, from about 565 to 525 million years ago.
The Cambrian Explosion
One of the most remarkable discoveries of the past few years is that the major elements controlling animal development are quite similar across a wide range of body plans. Most animals start from a single cell, the fertilized egg or zygote. However, during development their cells multiply and differentiate into specialized cell types that make up muscles, nerves, glands and all the other tissues and organs. This is an extraordinary process, given that each and every cell in a developing embryo has exactly the same genetic information in its DNA. Unlike their unicellular ancestors, multicellular animals need a genetic regulatory system to specify different gene activities in the different cell types as development unfolds to produce an adult body plan. Many of the regulatory genes in butterflies, giraffes and squid, for example, are similar, having been inherited from their last common ancestor, the protostome–deuterostome ancestor, which lived at least half a billion years ago. Thus the striking changes in body plans have been accompanied by relatively modest tinkering with the machinery of early development of that long-extinct precursor.
Developmental regulation proceeds through the sequential activation of a series of regulatory switches that in turn activate networks of other genes. In general, the regulatory genes produce proteins that bind to and influence the activity of other genes. The protein products of these genes then activate still other genes, and the cascade continues. Regulatory genes that are active early in development help set up the body axes by determining which end of the embryo becomes the head and which the tail, which part becomes the back and which the belly. These early expressing genes also set up the basic tissue types. Genes that are active later in the cascade help block out distinctive morphological regions within the body–differentiating, say, a head from an abdomen. Later still in the cascade, genes mediate the growth of appendages such as limbs, until the most refined morphological details have been achieved. Many different classes of regulatory genes share a common DNA sequence known as the homeobox, which predates the origin of animals.
The best-studied class of homeobox-containing genes are the Hox genes, usually found clustered next to each other along animal chromosomes. In complex organisms the Hox cluster specifies the developmental fate of individual regions within the body, and usually the genes are activated and expressed in the body in the same order as their position in the cluster. Thus, in arthropods, the first genes in the cluster mediate the expression of the head and associated structures, those in the middle of the cluster control genes that produce legs and wings on appropriate body segments, and so on. In the phylum Nematoda, which lacks limbs or wings, the cluster simply mediates the expression of a series of different cell types along the body (along with other functions). Obviously such sophisticated control systems were not needed in the single-celled ancestors of animals, and thus their evolution is intimately associated with the establishment and initial elaboration of animal body plans.
The number of genes in the Hox cluster varies among animal phyla. Sponges, the most primitive of animals, have at least one Hox gene, whereas arthropods have eight. In mammals, the cluster has been repeatedly duplicated to form four clusters, all slightly different, with a total of 38 genes. It looks very much as if the Hox clusters become larger with increasing body plan complexity, although this cannot be the entire story. Some primitive forms have clusters unlike the Hox cluster of higher forms. Furthermore, mammals and arthropods both display a striking diversity of morphologies within each of their body plans, but this diversity is generated chiefly by genes active after the Hox-cluster genes have done their work. Many different body plans can be specified by similar genes early within a cascade, whereas morphological complexity can be achieved by regulatory evolution in many parts of the cascade. What seems clear is that morphological evolution of body plans, such as is documented by Neoproterozoic and Cambrian fossils, involved increases in the complexity of both the body plans and the regulatory systems that specified them. With each new variation, there is an alteration in the relation between the regulatory genes and the so-called structural genes that actually produce the proteins and eventually the lipids and other building blocks that make up an organism.
Combining molecular views of animal phylogeny with the trace-fossil record helps evolutionary biologists reconstruct the primitive body plans that gave rise to the living phyla. As the important findings of developmental biology lead to a greater understanding of gene regulation, scientists can begin to reconstruct primitive developmental systems and their pattern of evolution. The synthesis of these fields, which is just beginning, will yield a much more complete picture of the early evolution of animal life.
Early Evolution of Hox
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.
Hox Genes and
Early Body Plans
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 Next Questions about