William Buckland knew about it, Charles Darwin
characteristically agonized over it, and still we do not fully
understand it. “It,” of course, is the seemingly abrupt
appearance of animals in the Cambrian “explosion.” The crux of
this evolutionary problem can be posed as a series of interrelated
questions. Is it a real event or simply an artifact of changing
fossilization potential? If the former, how rapidly did it happen and
what are its consequences for understanding evolutionary processes? The
Cambrian explosion addresses problems of biology as diverse as the
origin of metazoan bodyplans, the role of developmental genetics, the
validity of molecular clocks, and the influence of extrinsic factors
such as ocean chemistry and atmospheric oxygen. The Framework. Stratigraphic sections spanning the Vendian-Cambrian boundary show a
broadly similar pattern whereby the key events are bracketed by the
≈600-million-year (Myr)-old Neoproterozoic glacial deposits
(tillites) and in the succeeding Cambrian diverse metazoan assemblages,
typified by abundant skeletons, diverse trace fossils, and Burgess
Shale-type faunas (Fig. 1). One key
development is a series of accurate radiometric determinations ( 1). The
Vendian-Cambrian boundary is now placed at ≈543 Myr, and the duration
(≈45 Myr) of the Cambrian is substantially shorter than once thought.
The preceding Ediacaran faunas have an approximate age range of
565–545 Myr. Accordingly, the overall time-scale for discussion is a
relatively protracted 65 Myr, although the principal events of
evolutionary interest are probably more tightly bracketed (550–530
Myr) between the diverse Ediacaran faunas of latest Neoproterozoic age
( 2) and the Chengjiang Burgess Shale-type faunas ( 3). Correlations are
also assisted by emerging schemes of chemostratigraphy ( 2, 4), notably
with reference to strontium (δ 87Sr) and carbon
(δ 13C).
| Figure 1Principal events across the Vendian-Cambrian boundary, spanning an
interval of approximately 60 Myr (570–510 Myr), in the context of the
early evolution of metazoans. On the left are denoted a series of
important fossil assemblages, e.g., Burgess (more ...) |
The First Metazoans. Ediacaran assemblages ( 2, 5) are presumably integral to understanding
the roots of the Cambrian “explosion,” and this approach assumes
that the fossil record is historically valid. It is markedly at odds,
however, with an alternative view, based on molecular data. These posit
metazoan divergences hundreds of millions of years earlier ( 6, 7). As
such, the origination of animals would be more or less coincident with
the postulated “Big Bang” of eukaryote diversification ≈1,000
Myr ago ( 8). The existence of some sort of pre-Ediacaran metazoan
history is a reasonable assumption ( 9), but such animals must have been
minute because anything larger than about one millimeter would leave a
sedimentary imprint as a trace fossil. The literature is littered with
claims for pre-Ediacaran traces, but the history of research has been
one of continuous rebuttal. Will the most recent candidates avoid the
same fate? If such examples as the ≈1,000-Myr-old structures from
India are genuine ( 10), it is strange that there was not a rapid and
global colonization of marine sediments. A failed adventure in metazoan
history? Motility and hence the potential for sediment disturbance are
not, moreover, automatically a prerogative of the metazoans.
Conceivably, simple traces could be produced by strolling protistan
“slugs,” analogous to slime-mold
Dictyostelium. The Way Forward. The key element in deciphering the Cambrian explosion ( 11) is to
integrate the expanding insights of molecular phylogeny ( 12) and
developmental biology with the totality of paleontological evidence,
including the Ediacaran assemblages. Somewhere, and this is the tricky
point, in the Ediacaran assemblages are animals that may throw
particular light on key transitions. Of these, the most significant are
those between sponges and diploblasts, cnidarians and triploblasts, as
well as the early evolution of the three superclades of triploblast
(deuterostomes, ecdysozoans, and lophotrochozoans) (Fig. 1). The
overall framework of early metazoan evolution comes from molecular
data, but they cannot provide insights into the anatomical changes and
associated changes in ecology that accompanied the emergence of
bodyplans during the Cambrian explosion. The fossil record
provides, therefore, a unique historical perspective. Only those aspects of the Ediacaran record relevant to the Cambrian
diversification are noted here. Sponges, anthozoan cnidarians, and
stem-group triploblasts can all be identified with reasonable
confidence. Anthozoans, which are perhaps best known from such animals
as sea anemones, are represented by frond-like fossils. These types
persisted into the Cambrian (Fig.
2e) ( 13, 14) and are similar
to the living sea-pens (pennatulaceans). Despite the widespread onset
of biomineralization, it is curious that an authenticated record of
Cambrian cnidarians is relatively sparse but does include some
primitive corals. Jellyfish, which belong to the scyphozoans, are
virtually unknown. A benthic scyphozoan shows, however, an
astonishingly complete ontogenetic sequence that can be traced from the
early embryo ( 15). Remarkably, given their very delicate and gelatinous
construction, representatives of the sea gooseberries (ctenophores) are
also known (Fig. 2b).
| Figure 2Representative Cambrian animals from Burgess Shale-type deposits
(all except d) and an example of early phosphatization
(d). (a) The agnathan chordate
Myllokunmingia fengjiao from the Lower Cambrian (lower
Botomian) Chengjiang lagerstätte, (more ...) |
Lophotrochozoans. The ancestral lophotrochozoan may have looked slug-like, creeping
across the seafloor on a muscular foot. The Ediacaran
Kimberella may be an early representative ( 16), and the
armored halkieriids (Fig. 2c) from the Lower Cambrian are
possibly a subsequent development ( 17). A surprising discovery is
fossil embryos (Fig. 2d), from the Lower Cambrian of
Siberia, that are reasonably attributed to the halkieriids ( 18). From a
halkieriid-like stock, it may be possible to derive not only the
molluscs, but more surprisingly two more bodyplans, specifically in the
form of the brachiopods and annelids ( 17) (Fig. 1). Although molecular data define the lophotrochozoans, with some
exceptions ( 19) internal resolution of the phylogeny is limited. This
makes the Cambrian fossil record of potentially key importance.
Nevertheless, several phyla remain “floating,” arising from
unresolved polychotomies. Most surprising, perhaps, is a changed status
for the platyhelminthes (free-living flatworms and various parasitic
groups) ( 12). Classically regarded as primitive triploblasts, the
flatworms appear now to be anatomically degenerate, dispensing with
such features as an anus. Ecdysozoans. If the concept of the Lophotrochozoa overthrows some
long-cherished beliefs, it remains consistent with some earlier lines
of evolutionary thinking and is at least partly congruent with the
Cambrian fossil record. In contrast, the notion of the ecdysozoans ( 20)
is much more revolutionary. Its principal phyla are the arthropods,
nematodes and priapulids, all of which molt (or ecdyse) their cuticle
(or exoskeleton) at some point in their life cycle. The unusual
nematode bodyplan, based on a hydrostatic “skeleton,” and the
reduced complement of Hox genes ( 12) suggest these worms, of
central importance in molecular science in the form of
Caenorhabditis elegans, are highly derived.
Nematode origins, however, remain unresolved, although possible
connections between some Cambrian priapulid-like fossils and the group
of “nemathelminthes” (which includes the nematodes) have been
made ( 21). The priapulids (Fig. 2h) are a diverse and prominent group
in the Cambrian ( 11). As a group newly recruited to the ecdysozoans,
can we find a link with the arthropods? One interesting proposal ( 22)
looks to a distinctive group of priapulids with an armored cuticle,
known as the palaeoscolecidans, as potential precursors. The key step
is to affect a functional transition from the peristaltic burrowing
action of priapulids to a walking cycle based on the leg-like lobopods
(Fig. 2f) that are found in the first arthropods.
Functional interpretations of the subsequent evolution of early
arthropods can be put in a context of changing ecology, linked to
defense and shifts in feeding style. In this scenario ( 23), a number of
hitherto enigmatic taxa, notably Kerygmachela (24, Fig.
2g) and the large and active predator
Anomalocaris, are seen as key staging posts leading from the
primitive lobopodians (Fig. 2f) to the somewhat more
familiar clade of advanced arthropods (CCT =
crustacean-chelicerate-trilobite). Morphometric and phylogenetic
studies ( 25) have shown that the supposedly “bizarre” Burgess
Shale-type arthropods fall into a phylogenetic scheme that gives no
support to the idea that they are outliers in morphospace awaiting the
grim reaper of contingent extinction. Deuterostomes. Although there seems to be some congruence between the fossil record
and molecular phylogenies with respect to the ecdysozoans and
lophotrochozoans, in the case of the deuterostomes, matters are less
clear-cut. One difficulty is the extreme morphological distinction of
the component phyla, so that plausible functional intermediates between
echinoderms, hemichordates, and chordates remain effectively ad hoc
constructions ( 26). Molecular data are certainly yielding important
insights, most notably in terms of amphioxus ( 27) and the developmental
biology of ascidians ( 28). With the addition of the fossil record,
there may now be the glimmerings of a resolution (Fig. 1). Arguably the basal deuterostome bodyplan is best conceived as basically
consisting of two sections: a head with pharyngeal perforations
(gill-slits) and, to the posterior, a segmented unit. The most
primitive of living deuterostomes are taken to be the hemichordates,
although living representatives, such as the acorn-worms, are evidently
derived. Chengjiang fossils, such as Yunnanozoon ( 29) and
the almost identical Haikouella ( 30), possess a segmented
body, with incomplete cuticular rings, and an anterior section with
prominent gill slits. Although interpreted as advanced chordates, in
the artist's reconstruction ( 30) of Haikouella, the
supposed myotomes show a subtle “enhancement” of a
sigmoidal profile when compared with the illustrated fossils. The
supposed notochord is also in a biomechanically peculiar position,
inconsistent with its role as an antagonist to the purported myotomes.
These strange-looking taxa from Chengjiang may be our best glimpse of
the first deuterostomes. The first definite echinoderms do not appear until the Lower Cambrian.
The riot of ensuing forms has proved difficult to place in a coherent
phylogeny. Nevertheless, the classic five-fold symmetry is apparently a
derived feature and as such is consistent with marked redeployment of a
number of developmental genes ( 31). What then did the first echinoderms
look like? The concept of a basic deuterostome bipartite bodyplan of
head with gill slits and tail could reinvigorate the status of the
otherwise highly controversial fossils known as the
“calcichordates” ( 32), which show a puzzling combination of
echinoderm and chordate characters. The fossil record of the earliest chordates remains sporadic, but new
fossil discoveries are beginning to fill in the picture. From
Chengjiang, these include the cephalochordate Cathaymyrus
and, more sensationally, two types of agnathan fish ( 33) (Fig.
2a). The proposal ( 3) that Cathaymyrus is
synonymous with Yunnanozoon verges on the whimsical. The
more famous Pikaia, from the Burgess Shale ( 11), remains
more of a conundrum. It has myotomes and a notochord, but a peculiar
bilobed head. Neither Cathaymyrus nor Pikaia are
particularly similar to the living amphioxus, suggesting that, although
genomically primitive ( 27), this living representative is anatomically
derived. What Triggered the Cambrian Explosion? Isotopic and chemical indicators ( 2, 4), notably
δ 13C (Fig. 1), δ 32S,
δ 87Sr, and phosphogenesis, suggest substantial
changes in ocean chemistry and circulation on various time-scales.
Despite repeated speculation, the extent to which these changes in the
oceans influenced, let alone stimulated, the Cambrian explosion is
obscure. The motor of the Cambrian explosion was largely ecological,
notably with the rise of macroscopic predation (and defense) and
effective filter-feeding on the seafloor and in the pelagic zone.
Skeletal hard-parts, the most tangible expression of this event, seem
to have been largely protective, even though the proportion of animals
with robust hard-parts in the original communities was small ( 11). There is also continued interest in the role of genomic change,
especially with respect to the homeotic genes. Although they are
clearly of central importance in the definition of bodyplan
architecture, there is a risk of losing the overall evolutionary
context ( 34). It is evident that at least some components of a given
bodyplan are assembled by virtue of a genetic “toolbox.” This, in
turn, has provoked extensive discussions on definitions of homology,
but perhaps deflects the interesting question of how such toolboxes are
recruited. This is no trivial point because there is increasing
evidence for extensive co-option and redeployment of genes. Not only
that, but there are intriguing mismatches between genomic architecture
and bodyplan complexity. To complicate matters further, a substantial
proportion of the metazoan genome was probably available well before
the Cambrian explosion. Genes make bodies and bodyplans require a
corresponding genetic architecture, but we are still far from
understanding either their interconnections or evolution. To conclude: The Cambrian explosion is real and its consequences set in
motion a sea-change in evolutionary history. Although the pattern of
evolution is clearer, the underlying processes still remain
surprisingly elusive. |
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