Cambrian explosion

The Cambrian explosion describes the geologically sudden appearance of hard-bodied animals in the fossil record, around. This is accompanied by a profound diversification of life on Earth. Prior to around, organisms were on the whole simple, comprised of individual cells occasionally organised into colonies. Over the subsequent 70-80 million years, the rate of evolution would accelerate by an order of magnitude, and the diversity of life would begin to resemble today's.

The Cambrian explosion has generated extensive scientific debate. The seemingly rapid appearance of fossils in the "Primordial Strata" was noted as early as the mid 19th century, and Charles Darwin saw it as one of the principal objections that could be lodged against his theory of evolution by natural selection.

The long-running puzzlement about the appearance of the Cambrian fauna, seemingly abruptly and from nowhere, centers on three key points: the existence of the "Cambrian explosion", its causes and its relation with the origin and possible evolution of animals. A limited supply of evidence, based mainly on an incomplete fossil record and chemical signatures left in Cambrian rocks, makes interpretation difficult.

History and significance of the concept
Geologists as long ago as Buckland (1784-1856) realised that a dramatic step change in the fossil record occurred around the base of what we now call the Cambrian. Charles Darwin considered this sudden appearance of many animal groups with few or no antecedents to be the greatest single objection to his theory of evolution: indeed, he devoted a substantial chapter of The Origin of Species to this problem.

Victorian scientists grappled with the conundrum, and American paleontologist Charles Walcott proposed that an interval of time, the “Lipalian”, was either not represented in the fossil record, or did not preserve fossils — and that the ancestral forms to the Cambrian taxa evolved during this time.

The intense modern interest in the subject was probably sparked by the work of Harry B. Whittington and colleagues, whose redescription of the Burgess Shale (see below) from 1970 onwards, together with Stephen Jay Gould’s popular 1989 account of this work, Wonderful Life, brought the matter into the public eye, raising questions about what the explosion represented: whilst differing significantly in the detail, both proposed a sudden appearance of all animal types.

Advances in scientific techniques, along with new fossil finds, help refine scientific insights into the processes behind the explosion. Debate currently focuses on a number of points: firstly, whether the explosion of the fossil record represents an explosion of life's diversity; also, what the explosion tells us about animals' origins, and early evolution; and further, what — if anything — may have caused this geologically abrupt phenomenon.

Dating the Cambrian
The Cambrian explosion has proven difficult to study, partly because of the problems involved in matching up rocks of the same age across disparate continents. It should be kept in mind that absolute radiometric dates for much of the Cambrian, obtained by detailed analysis of radioactive elements contained within rocks, have only recently become available and that, especially for the Lower Cambrian, detailed biostratigraphic correlation — which uses widespread but short-lived species to match rocks of the same age — remains rather tenuous, particularly around the internationally-defined Precambrian/Cambrian boundary section. Dating of important boundaries, and description of faunal successions, should thus be regarded with some degree of caution until better data becomes available.

Trace fossils
Trace fossils — broadly speaking, the traces made by organisms in the sediments they lived in or on — are of considerable importance in unravelling the Cambrian explosion. Bona fide burrows first appear in the Precambrian, from about onwards; at first, only simple horizontal burrows occur. These marks were made by creatures moving across and below soft surfaces: the organisms making the traces were clearly not exploiting deep sediments, but only the topmost layers. As the Cambrian got underway, new forms of trace fossil appeared, including vertical burrows and traces normally attributed to arthropods. These represent a “widening of the behavioural repertoire”, both in terms of abundance and complexity.

Trace fossils are particularly significant because they represent a data source that is not directly connected to the presence of easily-fossilized hard parts, which are of course rare during the Cambrian; indeed, many traces appear an appreciable period of time before the body fossils of the animals that are thought to make them. Whilst exact assignment of trace fossils to their makers is difficult, the trace fossil record seems to indicate that at the very least, large, bottom-dwelling, bilaterally symmetrical organisms were rapidly diversifying during the early Cambrian.

Body fossils
Body fossils are the physical remains of organisms, which, often after chemical alteration, are preserved in the rock record. The fossil record of the Cambrian is often divided into two categories, the “conventional” and “exceptional” record, which of course grade into one another.

The conventional record
The conventional fossil record consists only of readily-preserved parts of organisms, above all their mineralized shells. Since these fragments are usually found disarticulated, and the majority of organisms lack hard parts, reconstruction of ecosystems — or any other analysis of the Cambrian world — based only on these data is difficult.

The first organisms with hard parts in fact pre-date the Precambrian/Cambrian boundary, and the complex stalked structure called Namacalathus. and appear to have become extinct shortly before the base of the Cambrian. The beginning of the Cambrian itself is marked chiefly by the appearance of new trace fossils, but a variety of small skeletal fossils, the small shelly fauna, gradually appear over the next few million years. This fauna incorporates a variety of tubes, caps, shells, and sclerites, mostly of uncertain affinity - perhaps including early molluscs such as Latouchella, and a variety of sponge spicules. During the second stage of the Cambrian, the Tommotian, a much greater variety of small shelly fossils start to appear, including the first probable brachiopods. However, it is not until the next stage, the Atdabanian, that a significant proportion of the body fossil record can be readily attributed to modern groups. Groups represented include the trilobites, echinoderms, and many more with probable molluscan and brachiopod affinities. Although the dating and correlation of Cambrian strata, as noted above, is not particularly secure, this pre-Atdabanian early Cambrian period may represent a period of time spanning over 20, and perhaps as many as 30, million years from the appearance of widely-recognised trace fossils.

Instances of exceptional preservation
For reasons that are by no means clear — perhaps the particular tectonic regime, or the low abundance of burrowing animals — the Cambrian is marked by an unusually high number of exceptionally preserved faunas, of which the most significant are the Lower Cambrian Maotianshan shale faunas of Chengjiang (Yunnan, China) and Sirius Passet (Greenland), the Middle Cambrian Burgess Shale (British Columbia, Canada) fauna, and the Upper Cambrian Orsten (Sweden) fauna. Exceptional faunas preserve a much wider range of tissue types than the conventional record, and thus many types of organisms are only represented in the fossil record by this sort of preservation. The exceptional faunas have therefore played a critical role in driving debates about the Cambrian explosion.

Whilst they have been known since the early 20th century, exceptional faunas rose to prominence in the 1970s and 1980s after they were “rediscovered”. The Burgess Shale has, in particular, yielded many of the most famous fossils ever discovered, and forms the subject of Gould’s Wonderful Life. The exceptional record displays a fauna dominated by arthropods, with less abundant sponges and echinoderms; in the case of the Chengjiang, purported representatives of many other phyla, even including vertebrates, are present. A smaller but significant number of taxa, including the famous Opabinia, Anomalocaris, Yunnanozoon, Halkieria, Odontogriphus, Wiwaxia and Hallucigenia, have consistently excited attention since their description, because these organisms do not fit readily into modern taxonomic categories. In addition, most, or even all, of the agreed arthropods from the exceptional faunas do not seem to fit into any modern arthropod class such as the insects, crustaceans or chelicerates. The information from the Burgess Shale is supplemented greatly by the stream of fossils described from the rather older Chengjiang fauna from China, and, to a lesser extent, from the potentially older still Sirius Passet fauna from North Greenland, both of which seem to date from close to the Atdabanian/Botoman boundary, and thus well within the Lower Cambrian.

Molecular phylogenetics
The field of molecular phylogenetics attempts to reconstruct the relationships between organisms by comparing details of their biochemistry, such as their DNA. It provides an alternative line of evidence into the Cambrian, although the need for calibration against the fossil record means it is not entirely independent. Further, since the "clocks" measure molecular evolution, a period of rapid evolution is indistinguishable from a longer period of slow change, adding a huge margin of error to Cambrian considerations. Whilst the rapidly developing science must be treated with a degree of caution, it has yielded some useful results: for example, evidence that the three major animal groups diverged some time before the Cambrian, then independently underwent a rapid Cambrian diversification — although the implications of this apparent finding are a matter for discussion.

Geochemical observations
The ratios of three major isotopes, 87Sr / 86Sr, 34S / 32S and 13C / 12C, undergo dramatic fluctuations around the beginning of the Cambrian.

This chemical signature in the rocks of the Precambrian/Cambrian boundary is difficult to interpret, and may be related to continental break-up, the end of a “global glaciation”, or a catastrophic drop in productivity caused by a mass extinction just before the beginning of the Cambrian. However, the wide variety of possible causes for these fluctuations means that geochemistry is currently an exciting new source of data, which is still to be interpreted in a settled way.

Survey of the evidence in the rocks
This lists the main items in order of the time when the relevant rocks were formed, because timing is the central issue in the Cambrian explosion - but remember that dating rocks from the Cambrian and earlier rocks is very difficult. The survey also starts well before the start of the Cambrian and finishes in the early Ordovician, because some scientists think that the diversification of animal life started before and finished after the Cambrian.

It covers body fossils, trace fossils and geochemical evidence, because these are all found in rocks which can be dated at least approximately. Arguments based on molecular phylogenetics will appear in a separate section, because this type of evidence is much harder to date with confidence.

Explanation of a few scientific terms
To avoid becoming even longer this article uses some scientific terms, and this is a good place for some simple explanations.

Triploblastic means consisting of 3 layers, which are formed in the embryo (before the animal is born / hatched). The innermost layer forms the digestive tract (gut); the outermost forms skin, muscles, etc; and the middle one forms all the internal organs except the digestive system. All living animals except Porifera (sponges) and Cnidaria (jellyfish, sea anemones, etc.) are triploblastic.

Bilaterian means having 2 sides; this implies that they also have top and bottom surfaces and, perhaps more importantly, distinct front and back ends. All known bilaterian animals are triploblastic, and all known triploblastic animals are bilaterian except for echinoderms (but sea cucumbers do have distinct front and back ends; and echinoderm larvae have 2 sides). Porifera (sponges) and Cnidaria (jellyfish, sea anemones, etc.) are radially symmetrical (like wheels).

Most of the phyla in the debate about the Cambrian explosion are coelomates; (priapulids are an important exception). Coelomate means having a body cavity (coelom) which contains the internal organs. Arthropods, [annelid] worms, molluscs, echniderms (starfish, sea urchins, sea cucumbers, sea lilies) and inchordates (including us vertebrates) are coelomates. All coelomate animals are triploblastic, but some triploblastic animals do not have a coelom (e.g. flatworms; their organs are surrounded by unspecialized tissues). Some bilaterian animals are not coelomates (e.g. flatworms). Echinoderms are coelomates but not completely bilaterian.

Trace fossils 1 billion years ago?
Trace fossils found in rocks about 1 billion years old in India may represent marks of creatures moving across and below soft surfaces. The organisms making the traces were clearly not exploiting deep sediments, but only the layers immediately below the mat of cyanobacteria that covered the seabed. The researchers concluded that the burrows were produced by the peristaltic action of triploblastic metazoans up to 5mm wide - in other words by animals about the diameter of earthworms, about as complex and possibly coelomates. But other researchers have dismissed this and other purported finds of trace fossils older than about 600M years ago, usually on the grounds that they were produced by physical processes rather than by organisms.

Ediacaran organisms
Strange-looking fossils were found first at Ediacara in Australia and then in marine sediments from many parts of the world, with dates between 610M and 543M years ago (right up to the start of the Cambrian). Most of the Ediacaran biota were at least a few centimeters long, significantly larger than previous finds.

Many were unlike anything that appeared before or since, resembling discs, mud-filled bags, or quilted mattresses - one paleontologist proposed that the strangest organisms should be classified as a separate kingdom, Vendozoa. The earliest known body fossils of complex organisms are of one of these strange organisms, Charnia, from about 580M years ago.

But some were probably early forms of the phyla at the heart of the debate about the "Cambrian explosion". Kimberella was very probably a mollusc (see below). Spriggina was probably a trilobite and therefore an arthropod. Arkarua  was probably an echinoderm, although it lacked a feature present in later echinoderms (stereom, a unique crystalline form of calcium carbonate from which their skeletons are built).

Cloudina is a small animal (diameter 0.3mm to 6.5 mm; length 8mm to 150 mm) which looks like a rather loose, wobbly stack of cones, sharp end downwards. It has been suggested that Cloudina is a stem group polychaete worm, but there is still much debate about how to classify it. More importantly it was one of the earliest animals to have a calcareous shell, i.e. hard parts in the paleontologists' sense.

Mollusc-like animals 555M years ago
A fossil bed in Russia contains a few layers of volcanic ash which have been dated by radiometric methods (uranium-lead ratios in zircons) to a little over 555M years ago. The fossils found there include Kimberella, the oldest well-documented triploblastic bilaterian. Kimberella was 3mm to 10cm long and had a radula (toothed chitinous "tongue"), which it used for scraping food off the seabed and which is the signature feature of modern molluscs except bivalves; and the rocks around the Kimberella fossils bear scratches which are very similar those made by the radulas of grazing molluscs.

Early Cambrian diversification of trace fossils
Around the start of the Cambrian (about 543M years ago) many new types of traces first appear, including well-known vertical burrows such as Diplocraterion and Skolithos, and traces normally attributed to arthropods, such as Cruziana and Rusophycus. The vertical burrows indicate that worm-like animals acquired new behaviors and possibly new physical capabilities. If traces such as Cruziana and Rusophycus were produced by arthropods, that would indicate that arthropods or their immediate predecessors had developed exoskeletons, although not necessarily as hard as they became later in the Cambrian.

Small shelly fauna
Fossils known as "small shelly fauna" have found in many parts on the world, and date from just before the Cambrian to about 10M years after the start of the Cambrian (the Nemakit-Daldynian and Tommotian ages; see timeline). These are a very mixed collection of fossils: spines, sclerites (armor plates), tubes, archeocyathids (sponge-like animals) and small shells very like those of brachiopods and snail-like molluscs - but all tiny, mostly 1 to 2mm long.

Early Cambrian trilobites and echinoderms
The earliest Cambrian trilobite fossils are about 530M years old, but even then they were quite diverse and world-wide, which suggests that these arthropods had been around for quite some time.

The earliest generally-accepted echinoderms appeared at about the same time, although it has been suggested that some Ediacaran organisms were echinoderms (see above). The early Cambrian Helicoplacus was a cigar-shaped creature up to 7 cm long that stood upright on one end. Unlike modern echinoderms it was not radially symmetrical with the mouth at the center, but had a spiral food groove on the outside along which food was moved to a mouth that is thought to be located on the side.

The Sirius Passet fauna
Sirius Passet is a lagerstätte in Greenland which was formed about 527M years ago. Its most common fossils are arthropods, but there is only a handful of trilobite species. There are also very few species with hard (mineralized) parts: trilobites, hyoliths, sponges, brachiopods, and no echinoderms or molluscs.

One of the arthropods, Pauloterminus, has a bivalve-like carapace.

Halkieria has features associated with more than one phylum, and is discussed below.

The strangest-looking animals from Sirius Passet are  Pambdelurion  and  Kerygmachela. They are generally regarded as anomalocarids because they have long, soft, bodies with a series of broad fin-like flaps along each side. The fossils found so far show no trace of gills or other breathing apparatus and no trace of segmentation. Both were apparently blind, as the fossils show no trace of eyes. Pambdelurion had a large mouth on the front of its head, flanked by a pair of thick, segmented appendages slightly longer than the swimming flaps and equipped with a flexible spine on each segment. It may have fed on plankton. Kerygmachela had a pair of long, slender trailing appendages at the rear end, and a small conical mouth flanked by robust, unsegmented appendages which had short spines on the front edge and were tipped with longer spines. The spiny front limbs suggest that it may have been a predator, but its small mouth suggests it would have been restricted to very small prey.

The Chengjiang fauna
There are several Cambrian fossil sites in the Chengjiang county, of China's Yunnan province. The most significant is the Maotianshan shale, a lagerstätte which preserves soft tissues very well. The Chengjiang fauna date to between 525M and 520M years ago, about the middle of the early Cambrian epoch, a few million years after Sirius Passet and at least 10M years earlier than the Burgess Shale.

The Chengjiang sediments provide what are currently the oldest known chordates, the phylum to which all vertebrates belong. The 8 chordate species include Myllokunmingia, possibly a very primitive agnathid (jawless fish) and Haikouichthys, which may be related to lampreys. Yunnanozoon may be the oldest known hemichordate (a phylum closely related to chordates).

Vetulicola is a small swimming animal with a carapace covering the front half of its body. Its classification is uncertain: it has paired openings connecting the pharynx to the outside, which may primitive gill slits; because of these, some researchers argue that it is a deuterostome ("super-phylum" which includes chordates) and possibly even a larvacean (urochordate which remains free-swimming throughout its life); but others classify it as an arthropod.

Chenjian contains other animals which have puzzled paleontologists but are now regarded as lobopods and fairly closely related to arthropods. Anomalocaris was a mainly soft-bodied swimming predator which was gigantic for its time (up to 70cm = 2.1 feet long; some later species were 3 times as long); the body had a series of broad fin-like flaps along each side, and at the rear a pair of "fans" arranged in a "V" shape. The fossils found so far show no trace of gills or other breathing apparatus and no trace of segmentation. The two eyes were on long horizontal stalks; the mouth was a round-cornered square of plates which could not close completely; and in front of the mouth were two jointed appendages which were shaped like a shrimp's body, curved backwards and had short spines on the inside of the curve. Hallucigenia (picture at top of this article) looks like a long-legged caterpillar with spines on its back, and almost certainly crawled on the seabed.

Nearly half of the Chengjiang fossil species are arthropods, few of which had the hard, mineral-reinforced exoskeletons found in most later marine arthropods; only about 3% of the organisms known from Chengjiang have hard shells, and most of those are trilobites (although Misszhouia is a soft-bodied trilobite). Many other phyla are found there: Porifera (sponges) and Priapulida (burrowing "worms" which were ambush predators), Brachiopoda (these had bivalve-like shells, but fed by means of a lophophore, a fan-like filter which occupied about of half of the internal space), Chaetognatha (arrow worms), Cnidaria (jellyfish, sea anemones), Ctenophora (comb jellies), Echinodermata (starfish, sea urchins, etc.), Hyolitha (enigmatic animals with small conical shells), Nematomorpha (horse hair worms, parasites which are typically about 1m long and 1mm to 3mm in diameter), Phoronida (horseshoe worms which live in chitinous tubes and feed by means of a lophophore), and Protista (single-celled animals).

Molluscs, annelids or brachiopods?
Wiwaxia, found so far only in the Burgess Shale, had chitinous armor consisting of long vertical spines and short overlapping horizontal spines. It also had a radula (chitinous toothed "tongue"), a feature which is otherwise only known in molluscs. Some researchers think the pattern of its scales links its closely to the annelids (worms) or more specifically to the polychaetes ("many bristles"; marine annelids with leg-like appendages); but others disagree.

Orthrozanclus, also discovered in the Burgess Shale, had long spines like those of the wiwaxiids, and small armor plates plus a cap of shell at the front end like those of the halkieriids. The scientists who described it say it may have been closely related to the halkieriids and the wiwaxiids.

Halkieria resembled a rather long slug, but had a small cap of shell at each end and overlapping armor plates covering the rest of its upper surface - the shell caps and armor plates were made of calcium carbonate. Its fossils are found on almost every continent in early to mid Cambrian deposits, and the "small shelly fauna" deposits contain many fragments which are now recognized as parts of Halkieria's armor. Some researchers have suggested that halkieriids were closely related to the ancestors of brachiopods (the structure of halkieriids' front and rear shell caps resembles that of brachiopod shells) and to the wiwaxiids (the pattern of the scale armor over most of their bodies is very similar). Others think the halkieriids are closely related to molluscs and have a particularly strong resemblance to chitons.

Odontogriphus is known from almost 200 specimens in the Burgess Shale. It was a flattened bilaterian up to 12cm (5 inches) long, oval in shape, with a ventral U-shaped mouth surrounded by small protrusions. The most recently found specimens are very well preserved and show what may be a radula, which led those who described these specimens to propose that it was a mollusc. But others disputed the finding of a radula and suggested Odontogriphus was a jawed segmented worm belonging to the Lophotrochozoa (a "super-phylum" which contains the annelids, brachiopods, molluscs and all other descendants of their last common ancestor).

The Burgess Shale
The Burgess Shale was the first of the Cambrian lagerstätten to be discovered (by Walcott in 1909), and the re-analysis of the Burgess Shale by  Whittington and others in the 1970s was the basis of  Gould's book  Wonderful Life, which was largely responsible for non-scientists' awareness of the Cambrian explosion. The fossils date from the mid Cambrian, about 515M years ago and 10M years later than the Chengjiang fauna.

The most common Burgess Shale fossils are arthropods, but many of them are unusual and difficult to classify, for example:
 * Marrella is the most common fossil (see picture above), but Whittington's re-analysis showed that it belonged to none of the known marine arthropod groups (trilobites, crustaceans, chelicerates;  well-known modern chelicerates include spiders and scorpions).
 * Yohoia was a tiny animal (7mm to 23mm long) with: a head shield; a slim, segmented body covered on top by armor plates; a paddle-like tail; 3 pairs of legs under the head shield; a single flap-like appendage fringed with setae (bristles) under each body segment, probably used for swimming and / or respiration; a pair of relatively large appendages at the front of the head shield, each with a pronounced "elbow" and ending in four long spines which may have functioned as "fingers". Yohoia is assumed to been a mainly benthic (bottom-dwelling) creature that swam just above the ocean floor and used its appendages to scavenge or capture prey. It may be a member of the arachnomorphs, a group of arthropods that includes the chelicerates and trilobites.
 * Naraoia was a soft-bodied animal (no mineralized parts) which is classified as a trilobite because its appendages (legs, mouth-parts) are very similar.
 * Waptia, Canadaspis and Plenocaris  had bivalve-like carapaces. It is uncertain whether these animals are related or acquired bivalve-like carapaces by convergent evolution.

Pikaia resembled the modern lancelet, and was the earliest known chordate until the discovery of the fish-like Myllokunmingia and Haikouichthys among the Chengjiang fauna.

But the "weird wonders", creatures that resembled nothing known in the 1970s, attracted the most publicity, for example:
 * The first presentation about Opabinia the audience laugh. The reconstruction showed a soft-bodied animal with: a slim, segmented body; a pair of flap-like appendages on each segment with gills above the flaps, except that the last 3 segments had no gills and the flaps formed a tail; five stalked eyes; a backward-facing mouth under the head; a long, flexible, hose-like proboscis which extended from under the front of the head and ended in a "claw" fringed with spines. Subsequent research has concluded that Opabinia is a lobopod, closely related to the arthropods and possibly even closer to ancestors of the arthropods.
 * Anomalocaris and Hallucigenia were first found in the Burgess Shale, but older specimens have been found in the Chengjiang fauna. They are now regarded as lobopods, and Anomalocaris is very similar to Opabinia in most respects (except the eyes and feeding mechanisms) - see above.
 * Odontogriphus is currently regarded as either a mollusc or a lophotrochozoa, i.e. fairly closely related to the ancestors of molluscs.

Magnitude (and existence?) of the explosion
The apparent suddenness of the Cambrian radiations led Darwin to propose that the origins of animals actually lies far back in Proterozoic time, and that the Cambrian explosion represents only an “unveiling” of true Proterozoic diversity. Such a view has been sporadically supported through time by the description of purported trace fossils from deep in the Proterozoic.

More recently and spectacularly, many molecular clock estimates place the origin of bilaterian animals well before the beginning of the Cambrian, perhaps more than 1 billion years ago Given that Cambrian animals are often large, sometimes had hard parts and could evidently make very abundant and obvious benthic trace fossils, their hypothesised Proterozoic predecessors could probably have none of these attributes without leaving at least some trace in the fossil record. As a result, hypothetical Proterozoic bilaterians are usually thought to be some combination of tiny (planktonic or meiofaunal), immobile in sediment (e.g. sessile or planktonic) and without hard parts. In theory, such hypotheses can be tested by phylogenetic reconstruction of the morphology of the most basal bilaterians. However, this has proven to be fraught with difficulty. They seem at least to have possessed a through-gut and striated musculature – neither of which are compatible with a minute size. Some Proterozoic fossils have been interpreted as coprolites (fossilized faeces), and excreting solid waste requires a through-gut; others have been interpreted as tunnels or burrows, which requires a muscular body with a tube-like shape (which also suggests a through-gut).

Proterozoic predecessors
The hunt for Precambrian metazoans has intensified as the Cambrian debate has continued. Over the last decades, a rich and diverse prokaryotic and eukaryotic biota has been documented from Proterozoic rocks around the world. However, larger, more obviously animal-like fossils have been much harder to detect, although some disputed carbonaceous tubes have sometimes been described as annelid- or pogonophoran-like.

The Ediacaran Period, immediately preceding the Cambrian, is host not only to the trace fossils and tubes previously mentioned, but also the highly enigmatic Ediacaran biota, which — despite decades of study and a flurry of recent intense interest — remains very hard to place in the context of animal evolution. Some taxa such as Kimberella are thought by some to represent bilaterians or even more derived forms such as molluscs, but these assignations are by no means generally accepted.

Perhaps the most promising area for study is the Doushantuo Formation of China, spectacular fossils from which are probably around 580 million years old or younger. They preserve a variety of fossils in shales, phosphorites and cherts. Of these, the best known are those from the phosphorites. The Doushantuo fossils include algae, giant acritarchs, and, spectacularly, phosphatised embryos that may represent non-bilaterian animals such as sponge or cnidarian grade organisms. Other bilateran embryos have also been described, along with a possible adult bilaterian, Vernanimalcula. However, these assignments have been criticised on the grounds that they fail to take into proper account the preservational processes that gave rise to the fossils. For example, it has been suggested on the basis of the mode of preservation of Doushantuo fossils, that Vernanimalcula is largely an artefact created by rock-forming processes. As a result, opinion is split about the age of the first convincing bilaterian fossil: the first universally accepted bilaterian fossils are probably not known until the Cambrian. Clearly, further research is required to clarify the many problematic aspects of Doushantuo diversity.

Early trace fossils
It is fair to say that no convincing trace fossils before the end of the Ediacaran are currently accepted: most of these have turned out to be pseudofossils. A few have been reported, including one from approximately one billion year-old sandstones from India, and some even older structures from the Stirling quartzite in Australia. Of these, the biogenicity of the former has now been abandoned by the original authors, and doubts have been cast on the latter in the literature.

The sum of the evidence, then, suggests that neither large bilateral animals (which would probably have been capable of leaving a body or trace fossil record) nor tiny ones (which would perhaps be expected to be found in the Doushantuo Formation) existed before close to the end of the Proterozoic. While this viewpoint is by no means generally accepted, it is also somewhat supported by revised molecular clock estimates, which tend to converge towards a much later bilaterian divergence date, and close to that suggested by the fossil record.

Evolutionary significance
The rapidity of the Cambrian explosion, the lack of precursors in the fossil record, the lack of discovered "new" post-Cambrian species, and the apparent bewildering diversity of the forms displayed by the exceptional faunas, has generated much interest from many students of evolution, including most recently from the field of evolutionary developmental biology ("Evo-Devo"). Stephen Jay Gould's promulgation of the view that the Cambrian represented an unprecedented riot of disparity, of which only a very few managed to survive until the present day, still represents the most widespread view of the event. However, recent taxonomic and dating revisions also allow a more sober view to be taken.

A limited record
First, as mentioned above, the diversity seen in all other major exceptional faunas is a sample of life well after the beginning of the Cambrian explosion — in the case of the Burgess Shale, which may be as young as 507 million years or so, some 35 million years after the beginning of the Cambrian, as defined by trace fossil proliferation, and even longer after the first reasonable trace fossils. Nevertheless, the older Chengjiang and Sirius Passet faunas both represent a period of time perhaps more than 10 million years earlier. Clearly, animal life had diversified greatly during the Nemakit-Daldynian and Tommotian, periods of time that, crucially, lack exceptionally preserved faunas of Burgess Shale type. The fossil record is thus currently almost silent on one of the most critical periods of animal evolution. In the gap are found instead the largely enigmatic "small shelly fossils", poorly understood taxa upon which much more work is required.

Appearance of phyla
While the general rapidity of the Cambrian explosion thus seems to remain a reality, attempts have been made to downplay the “amount” of evolution that was required to generate the taxa actually seen in the Cambrian. In particular, the distinction between “crown” and “stem” groups has been applied to claim that many or even most lower-middle Cambrian taxa fall outside the crown groups of the modern phyla. This in some cases somewhat legalistic argument allows the origins of many of the phyla as we see them today to be pushed up into the succeeding Ordovician Period, or even later. Thus, the view that all modern phyla essentially suddenly appear at the base of the Cambrian has come under assault. One aspect of this reassessment is that many or most of the problematic Cambrian fossils have begun to be seen in the light of a stem-group placement to modern phyla or groups of phyla. Rather than being seen as one-off oddities, they can in this view be seen as representing the progressive adaptive stages of the assembly of modern day body plans, albeit ones with their own particular adaptations. An analogy can be drawn with the origin of the tetrapods or mammals, which have also been sequentially mapped out in the fossil record. Of course, many problematica remain, but in at least some of these cases, such as Odontogriphus, not enough has been known until recently about their morphology in order to come to a reasonable conclusion. Williamson (2006) contends (1) that there were no true larvae until after the establishment of classes in the respective phyla, (2) that early animals hybridized to produce chimeras of parts of dissimilar species, (3) that the Cambrian explosion resulted from many such hybridizations, and (4) that modern animal phyla and classes were produced by such early hybridizations, rather than by the gradual accumulation of specific differences. (Williamson, D.I. 2006.  Hybridization in the evolution of animal form and life-cycle.  Zoological Journal of  the Linnean Society 148: 585-602)

Mechanistic basis
If this viewpoint is correct, then unusual genetic or other evolutionary mechanisms might not be needed to explain what the Cambrian fossil record reveals. As added evidence for this viewpoint, most attempts to quantify morphospace occupancy - that is, the proportion of possible modes of life that are exercised - in the Cambrian have suggested that it is certainly not greater than today, and most studies have suggested it to be considerably lesser. However, this area remains a topic of considerable controversy.

Causes of the Cambrian explosion
Understanding why the Cambrian explosion happened when it did revolves around three major themes: i) extrinsic forcing events such as environmental change; ii) intrinsic mechanisms such as the acquisition of complex genomes; and iii) intrinsic mechanisms such as the natural consequences of metazoan ecology.

The role of oxygen
Of the first class of explanation, by far the most popular, dating back at least to the 1950s, is that animals did not evolve before the beginning of the Cambrian because of low atmospheric oxygen. Low oxygen levels could prevent the synthesis of collagen, present in metazoans (and now also known in other eukaryotes) which requires at least 1% of present atmospheric levels (the “Towe limit”); however, it would be more likely to provide a physiological constraint. Animals living in low oxygen environments today tend to have low diversity, thin shells and low metabolic activity. Whilst oxygen levels thus do certainly have an effect on animal life, it is not currently clear what atmospheric levels of oxygen were during the close of the Proterozoic, to what extent available oxygen was sequestered away by reduced mineral compounds, and what adaptations purported Proterozoic animals had to low oxygen conditions (presumably, they, like many living animals, possessed effective anaerobic metabolic pathways).

Snowball Earth
A related and currently popular explanation is that of “Snowball Earth”, which ties the severe glaciations towards the end of the Proterozoic to profound changes in oxygen levels and ocean chemistry. The explanatory power of such a hypothesis depends on I) how convincing the evidence for Snowball Earth is and II) providing a clear mechanistic link between what would undoubtedly have been a severe global upheaval and the subsequent radiation of the animals. As well as global cooling, global warming — perhaps as the result of massive methane release into the atmosphere — has been posited, as well as variety of other less exotic mechanisms such as continental breakup together with increased shelf area. Another example is a facilitating change in oceanic chemistry that allowed the formation of hard parts for the first time, although this cannot, of course, explain why some organisms seem to start diversifying before the origin of hard parts.

Developmental mechanisms
Of the second class of explanation, interest has centred on the timing of acquisition of the homeotic genes that all animals seem to possess and use to a greater or lesser extent in laying out their body architecture during development. It has been argued that the radiation of animals could not take place before a certain minimum complexity of such genes had been acquired, to give them the necessary genetic toolbox for subsequent diversification. Clearly, the evolution of development is critical in the history of the animals. However, it is currently difficult to disentangle the origins of bilaterian genetic architectures from their morphological diversification. Recent studies seem to suggest that the genes responsible for bilaterian development were largely present before they radiated, although it is quite possible that they were performing somewhat differing tasks at this time, later being co-opted into the classical patterns of bilaterian development.

Ecological explanations
In addition, several recent examinations of the Cambrian explosion have suggested that ecological diversification is the primary motor for the Cambrian explosion: even that the Cambrian explosion represents nothing more than ecological diversification. Given the evolution of multicellularity in heterotrophic organisms, it could be argued, a dynamic would be set up that would inevitably lead to the familiar food webs consisting of primary and secondary consumers, parasites, and (especially with the advent of mobility) deposit feeding and trophic recuperation. While it has been claimed that certain “key innovations” — most notably the origin of sight, by Parker — were critical in driving the whole process decisively forward, most of these can themselves be seen as products of earlier ecological pressure. In this view, the Cambrian become the first and most spectacular “adaptive radiation” as posited for evolution in general by especially G.G. Simpson.

Timing of the Cambrian Explosion
Assuming that the Cambrian explosion was a real event that occurred broadly as outlined above, there still remains the question of why it occurred precisely when it did. Two broad possibilities exist.

The first is that the origin of heterotrophic multicellularity was prompted either by climatic change, or by some other trigger. A popular example of the latter would be a meteoritic impact (the Australian Acraman crater, dated to 578 million years old, has been seen as a potential suspect) or some sort of other disastrous ecological collapse. With analogy to the supposed “take-over” by mammals after the extinction of the non-avian dinosaurs at the K-T boundary, the destruction of previous ecological systems allowed the animals to gain the ecological advantage and radiate spectacularly. For a long time, such a view was broadly supported by the evidence that the Ediacaran organisms seemed to go extinct some distance before the base of the Cambrian. More recently, however, this gap has been closed, and indeed surviving Ediacaran taxa have now been reported from the Cambrian itself. Nevertheless, some taxa such as Namacalathus do seem to vanish at this point, and the idea of faunal replacement, as opposed to simple development, cannot be ruled out.

Secondly, there is the view that the Cambrian explosion took place when it did simply because many other events had to take place first. Butterfield, for example, has argued that the presence of animals, with their vigorous ability to move about and prey on other organisms, would have sped up general ecological evolution by a factor of about ten. Indeed, if one shrinks Proterozoic history by this factor, then the time from the origin of the eukaryotes to that of the bilaterian animals then looks like a simple radiation with no undue “delay”. In any event, evolution of complex multicellular heterotrophs clearly massively impacted the biosphere, and a strong, or perhaps even dominant purely ecological component cannot be ruled out in any attempt at explaining this remarkable period in the history of Earth.