by Peter Ward
The third breakthrough was the appearance of skeletons, great numbers of tiny skeletal elements, in strata less than 550 million years in age. They are very small spines and scales of calcium carbonate that would have covered the animals with a coating of these small skeletons, almost like tiles. Finally, the larger fossilized animals appeared, including trilobites, the clam-like brachiopods, spiny echinoderms, and many kinds of snail-like mollusks, all in strata younger than 530 million years in age. In Darwin’s day, none of the earlier three were known, and the Cambrian was marked by the first appearance of trilobites in sedimentary strata. The reasons for this sequence might be deceptively simple: oxygen levels, which rose to their highest levels of the world up until then.
Today we know that this succession of animal life originations appeared comparatively rapidly in the fossil record, and new dating techniques now puts the time of the first complex fossils (the small skeletal fossils, which are 20 to 10 million years younger than the first trace fossils) at slightly older than 540 million years ago, with the first trilobites appearing in the record some 20 million years after that.
The appearance of animals in the fossil record recorded a significant event, which has been called the Cambrian explosion. To paleontologists the Cambrian explosion marked the first appearance of most major animal phyla large enough to leave remains in the rock record. To molecular geneticists, the Cambrian marked the first evolution of animals. The controversy raged through the 1990s, to be solved in the early years of this century when new molecular studies5 using more sophisticated analyses essentially confirmed the younger date for the origin of animals that had been championed by paleontologists. There is now agreement that animal life on Earth did not predate 635 million years ago,6 and might be closer to 550 million years in age.
Left, the cone shape represents the traditional model for increasing disparity. Right, the inverted cone represents diversification and decimation.
The Cambrian period is now dated from 542 to about 495 million years ago (although the latter date, for the base of the Ordovician, might be slightly older). However, the vast majority of animal phyla first appeared in a small portion of this interval, between 530 and 520 MA. All specialists agree that this is the third or fourth most important event in the entire history of life, superseded in importance only by the first appearance of life on Earth, the adaptation to molecular oxygen, and the origin of the eukaryotic cell.7
According to our best new information, the oxygen level soon after the start of the Cambrian explosion was about 13 percent (compared to 21 percent today),8 but then fluctuated. During this time carbon dioxide levels were far higher than they are in the world today—hundreds of times higher, in fact, and such high levels would have produced an intense greenhouse effect, sufficiently high to overcome the fact that the sun at this time was ~5 percent less intense than it is today. Even with the drop in CO2 levels at the end of this interval, temperatures of this time would have been perhaps the highest of any period in the history of animal life on Earth. Since less oxygen is dissolved in seawater with higher temperatures, the already anoxic conditions of the oceans would have been exacerbated.
The panoply of fossils that have been preserved showing both hard and their soft-parts fossils from the fantastic and newly discovered deposits in the Chengjiang region of China has given us a new window into the origin of the animal phyla on Earth, and the nature of life on the Cambrian planet prior to the most famous of all fossil deposits, the Burgess Shale of British Columbia. The Chengjiang beds are now known to have been deposited between 520 and 515 million years ago, whereas the Burgess Shale is now thought to be no older than 505 million years in age. The approximately 10 million years separating the age of these two deposits thus gives us a new view of how animals diversified.
Because both Chengjiang and the Burgess preserve soft parts as well as skeletonized animals,9 we have a good picture of what was there, in what relative abundance. Without this added view yielded by the preservation of soft parts, we would never be sure about the relative abundance of various kinds of animals, for perhaps there was a huge abundance of creatures like soft worms and jellyfish, forms that did not have skeletons. Thus our surprise at what appears to be a clear view of the nature of the fauna at both sites. There have now been over fifty thousand fossils collected from the Burgess Shale (and a lesser number of from Chengjiang). In their masterful summary of the Burgess fauna, Derek Briggs, Doug Erwin, and Fred Collier (in their 1994 book The Fossils of the Burgess Shale10) list a total of 150 species of animals. Almost half are arthropods or arthropod-like. But an even more interesting number relates to the number of individuals. Well over 90 percent of all fossils are from arthropods, followed by sponges and brachiopods. Like the earlier Chengjiang, the Burgess sea bottom was dominated both in kinds and numbers of animals by the arthropods.
Arthropods are among the most complex of all invertebrates, and yet, in these almost earliest of fossil deposits in the time of animals, they are diversified and common. It speaks to a long evolution prior to their first appearance in the record—perhaps seabeds crawling with millimeter-long (or less) arthropods, with many more species swimming or floating in the open sea itself.
One of the great surprises of a visit to the Burgess Shale (which both of the authors of this book have been fortunate enough to do) is the realization that the most common fossils come not from the exotic taxa, the many exquisite, soft-bodied creatures that fill the pages of the many books devoted to the Burgess Shale fauna and flora, but the fact that most of the fossils come from trilobites. They, and the less numerous but highly diverse arthropods of the Burgess dominate the assemblage,11 in sheer numbers of individuals and species, and in sheer numbers of different kinds of body plans, which is described by a measure called disparity (and compared to diversity, which refers to the number of different kinds of taxa). The arthropods seem to have been the most successful of Cambrian animals. How much of this success was due to their principal body plan characteristic: segmentation?
Segmented animals are the most diverse of all animals on the planet, and most are arthropods. All arthropods, including the highly diverse insects, show repeated body units and body regions based on groupings of individual segments that have specific functions for the animal. The feature uniting the group is the presence of a jointed exoskeleton that encloses the entire body. This exoskeleton even extends into the gut. The exoskeleton cannot grow, so it must be periodically molted and replaced by another slightly larger one. The body has a well-differentiated head, trunk, and posterior regions in varying proportions. Appendages are commonly specialized. On terrestrial arthropods the appendages are usually single (enormous), but the marine forms generally have two branches or parts per appendage, an inner leg branch and an outer gill branch, and are thus termed biramous. The exoskeleton encloses the soft parts like a suit of armor, and that may be its major function: protection. But the consequences of this kind of skeleton are huge: there can be no passive diffusion of oxygen across any part of the body. To obtain oxygen the first arthropods, all marine, had to evolve specialized respiratory structures or gills. Segmented animals are the most diverse of all animals on the planet. Arthropods are not alone in this trait: all annelids are segmented, and some members of generally nonsegmented groups, such as the monoplacophoran mollusks, show at least some segmentation. It appeared early in the history of animals, and indeed in the Cambrian trilobites we see that the most common of these early preserved animal fossils show this trait.
In his 2004 book, On the Origin of Phyla,12 James Valentine also reflects on what is a major evolutionary puzzle: why are there so many, and so many kinds of arthropods in the Cambrian? It is worthwhile to look at what he has written on this subject:
Although many early arthropods had non-mineralized cuticles, a marvelous diversity of early arthropod body types has come to light, so many and so distinctive as to pose important problems in applying the principles of systematics. These disparate arth
ropod types are phylogenetically puzzling … This evidently sudden burst of evolution of arthropod-like body types is outstanding even among the Cambrian Explosion taxa.
What we call arthropods are composed of what appear to be perhaps many independently evolved groups that have, through convergent evolution, produced body plans of great diversity save for one aspect: all have limbs on each segment that are biramous—each appendage carries a leg of some sort, and a second appendage, a long gill.
Why would basal animal groups opt for segmentation? Perhaps this is the wrong word, for Valentine and others note that the arthropods are not so much segmented—which at least in annelids is composed of largely separated chambers for each segment of the body—but repeated. Valentine proposes that this striking body plan arose in response to locomotor needs, stating, “Cleary, the segmented nature of the arthropod’s body is related to the mechanics of body movement, particularly to locomotion, with nerve and blood supplies in support.” There is no doubt that this type of body plan is an adaptation aiding locomotion. But a consequence of this kind of body plan is to allow repeated gill segments, each small enough to be held in optimal orientation beneath the segments. In these positions, flows of water can be actively pumped over and through the feather-shaped gills, thereby increasing the availability of oxygen molecules hitting the gills each second, a position suggested by Ward in 2006.13
Another animal found in abundance in the oldest of the Cambrian-aged deposits are sponges. Like the cnidarians, sponges show no respiratory structures, nor would we expect any. With a body plan built around a series of sacs (like the cnidarians, but with even less organization: there are no true tissues in a sponge), all sponges show a very high surface area to volume. In fact, sponges are like agglomerations of numerous single-celled organisms, with each cell essentially in contact with seawater. But even with this advantage, sponges show an even more efficient way of gaining oxygen. Their main feeding cell, called a choanocyte, causes large volumes of water to pass through the structure. Some sponge specialists have suggested that a sponge passes as much as ten thousand times its volume in seawater through its body each day. Consequently, sponges are capable of living in extremely low oxygen conditions because they so efficiently move large volumes of water through their body, getting enough oxygen even from water that has little.
The major groups of animals with hard parts in the Cambrian are obviously the huge tribe of arthropods, followed in numerical importance (in most Cambrian marine strata) by brachiopods, and then smaller numbers of echinoderms and mollusks. Brachiopods are a still-living group related to bryozoans that are routinely mistaken for bivalve mollusks. Yet while the shells of bivalves and brachiopods show a superficial similarity, the internal anatomy of the two groups are radically different. The major feature of a brachiopod is a feeding organ known as a lophophore, composed of a large loop with numerous long, thin fingers producing a delicate fanlike shape within the shell. This organ filters seawater for food—and as it is filled with a body fluid, and is very thin, it serves also as an exquisite respiratory organ. For some of us, the brachiopods are a tragic group. Perhaps the most common inhabitants of Paleozoic sea bottoms, they were nearly wiped out by the Permian extinction ~250 million year ago, and never regained dominance.
Cambrian echinoderms make up a weird assemblage of small boxlike animals. Among the earliest echinoderms were peculiar, pinecone-shaped helioplacoids, with some primitive stalked eocrinoids and edrioasteroids found in some deposits as well. More common than echinoderms were mollusks. Most during the Cambrian were small in size, and each of the major classes (gastropods, bivalves, and cephalopods) is found in Cambrian strata. The most common mollusks, however, were monoplacophorans, a minor class today, but common in the Cambrian. They had a limpet-like shell and a snail-like body with a broad, creeping foot. Most interestingly, alone among mollusks of the time they showed a body organization that suggests segmentation. From looking at muscle scars on the fossil shells and comparing anatomy from the still-living forms, we think the Cambrian monoplacophorans had multiple gills. Modern-day gastropods have a single pair of gills, or even just a single gill. But the Cambrian monoplacophorans, which lived a very snail-like existence in all likelihood, found it necessary to have multiple gills. They are celebrated as the ancestral mollusk that would give rise to all the rest: the gastropods, cephalopods, bivalves, chitons, and more minor molluscan classes.
Long thought to have gone extinct at the end of the Permian, the discovery of living monoplacophorans in deep-sea settings in the 1950s led to a much greater understanding of the life of the early mollusks. The living forms confirmed what muscle scars found on the interior of the earliest monoplacophoran fossils asserted—that there was more than a single pair of gills. In fact, multiple pairs of muscles line the entire length of the interior of the shell, leading to the conclusion that these early forms showed an evident segmentation or at least repeat of the gill–blood vessel system. Since it is only the gills (and supporting blood and filtering systems) that show this repeated pattern, it can be surmised that as in arthropods, this repeated pattern was an adaptation for increased respiratory surface area of the gills. A somewhat similar pattern of repetition, extending even to the shell, is found in the chitons, today commonly found on intertidal beaches.
Like the body of an echinoderm, the interior of a brachiopod shell is almost all water. There is very little flesh, and what is there stays in contact with a steady flow of seawater. The brachiopod lophophore creates several currents of seawater that pass into the sides of the shell, move across the lophophore, and are then sent out the front of the shell. This constant stream of new water entering a brachiopod has the same effect as the current passing through a sponge. The small volume of flesh to the great surface area of the lophophore, coupled with the steady flow of water (many times the volume of the interior of the shell), makes the brachiopod consummately adapted for a world of low oxygen.
PHYSICAL AND CHEMICAL EVENTS CAUSING THE CAMBRIAN EXPLOSION
Earlier in this book we noted the advance of entirely new disciplines of science, most notably astrobiology and its allied field, geobiology. But another field, this one a traditional mainstay of the biological sciences, mainly evolutionary development, has undergone a renaissance so important that it can almost be considered a new field as well. Its practitioners now call it evo-devo, and breakthroughs in this field have had a lot to say about the Cambrian explosion in the last decade. One of the greatest of evo-devo practitioners, Sean Carroll, has given us an exquisite tour of this newly revivified area of science in his 2005 book Endless Forms Most Beautiful.14 If there is any single theme in this work, it is that science can now understand far better one of the previously intractable problems in evolutionary biology: the origin of novelty. How evolutionary innovation took place over relatively short periods of time just could not be explained by traditional Darwinian concepts of evolution. The radical breakthroughs—be it the appearance of wings, legs for land, segmentation in arthropods, or even large size, the hallmark of the Cambrian explosion—could not stand up to stories about many and sudden mutations all working in concert to somehow radically change an organism. Evo-devo now seems to have solved this, and in his book, Carroll lists four aspects that combined can explain sudden evolutionary innovation that nicely encapsulates the new way of explaining how radical changes did take place.
The first “secret to innovation,” as Carroll puts it, is to “work with what is already present.” The concept that “nature works as a tinkerer” is central to this. Innovation does not always need a new set of equipment to build, or even a new set of tools. What is already present is the easiest route. Second and third are two aspects understood by Darwin himself: multifunctionality and redundancy.
Multifunctionality first is using an already present morphology or physiology to take over some second function in addition to that for which it was first evolved. Redundancy, on the other hand, is when some structure is composed
of several parts that complete some function. If one of these can be then co-opted for some new kind of job, while the remaining parts are still able to function as before, there is in place a clear path for innovation that is far easier to use than the total de novo formation of some entirely novel morphology from scratch. Cephalopod swimming and respiration are like this. Cephalopods routinely pump huge quantities of water over their gills, and like many invertebrates used separated “tubes” or designated channels for water coming in and water being expelled, to ensure that oxygen-rich water is not rebreathed. But with minor morphological “tinkering” with this excurrent tube, a powerful new means of locomotion came about. Breathing and moving could now take place using the same amount of energy by utilizing the same volume of water for respiration and movement.
The final secret is modularity. Animals built of segments, such as the arthropods, and to a lesser extent we vertebrates, are already composed of modules. The limbs branching off arthropod segments have been amazingly modified into feeding, mating, and locomotion, as well as many other functions. Arthropods are like a Swiss army knife, with each segment bearing limbs evolved to do a very specific function. The same is true in vertebrates with our digits, which have been modified to tasks as varied as walking on land to swimming to flying in the air. Not bad for some primitive fingers and toes! Where does the evo-devo come into play? It turns out that these morphologies are the soft putty for morphological change because they are underlain by systems of genetic “switches,” geographically located on the developing embryo in the same positions as the various limbs are found in the arthropod—or vertebrate.
