Biological Journal of the Linnean Society (1996), 57: 13-33. With 5 figures
The Cambrian evolutionary cexplosion’:
decoupling cladogenesis from morphological
disparity
R.A. FORTEY
Department of Paleontology, 7he Natural Histo9 Museum, Cromwell Road, South Km’ngton,
London, SW7 5BD
D.E.G. BRIGGS
Department of Geology, Wills Mmorial Building, UniversiQ of Bristol, Queen’s Road, Bristol,
BS8 1RJ
AND
M.A. WILLS
Department of Paleobiology, Smithonian Institution, Wmhington D.C., USA
Rtceived 13 December 1994, acceptedfor publication I6 F e b w y I995
The origin and differentiation of major clades is often assumed to have occurred in tandem with the
‘explosion’of fossil evidence of diverse morphologies (‘disparity’) at the base of the Cambrian. Evidence
is presented that this was not the case. Biogeographical and morphological differentiation among the
earliest trilobites reveals incompleteness in the known early Cambrian record; similar evidence can be
accrued for other major groups. Phylogenetic analysis proves the likelihood of ‘ghost’ lineages extending
into the Precambrian. The important events in the generation of clades were earlier than the Cambrian
‘explosion’, at which time the groups become manifest in the fossil record. It is likely that the important
phylogenetic changes happened in animals of small size; sister taxa of major groups are shown to be
small animals. Decoupling cladogenesis from the Cambrian ‘explosion’ removes the necessity of
invoking unknown evolutionary mechanisms at the base of the Phanerozoic. Genes controlling
development may have played a role in generating new morphologies, through heterochrony for
example, in the early differentiation of metazoan body plans.
01996 ‘Thc Linnean Smicty of London
ADDITIONAL KEY WORDS: - metazoan phylogeny
Vendozoa adaptive radiation.
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cladistics - ghost ranges - basal Cambrian -
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CONTENTS
Introduction . . . . . . . . . . . . . . . . . . . .
The ‘explosion’ scenario . . . . . . . . . . . . . . . .
Arthropod phylogeny and the completeness of the phylogenetic record
Other phyla . . . . . . . . . . . . . . . . . . . .
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01996 The Linnean Society of London
R. A. FORTEY E T A .
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Molecular evidence . . . . . .
Trees under the ‘explosion’ scenario
The paradox . . . . . . . .
Tiny sister groups . . . . . .
Evolutionary mechanisms . . . .
Conclusions . . . . . . . .
Acknowledgements . . . . . .
References . . . . . . . . .
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INTRODUCTION
The Cambrian evolutionary ‘explosion’ has been the subject of much recent
attention (Gould, 1993; Ridley, 1993) and there has been a tendency to conflate it
with the origin of the marine fauna (McMenamin & McMenamin, 1990). Nobody
seriously doubts that the sudden appearance in the fossil record of numerous marine
animal groups of both familiar and enigmatic type close to the base of the Cambrian
reflects one of the important events in the history of the biosphere. Two major
aspects of this ‘explosion’, however, remain the subject of controversy.
fiparip
The question of variety of fundamental designs-what Gould (1989) termed
‘disparity’-has proven particularly contentious. Were there more bauplane in the
Cambrian than subsequently, such that post-Cambrian evolutionary history
operated upon an ostensibly randomly ‘weeded’ fauna? Alternatively, do most of the
Cambrian forms fit into schemes of relationship in which animals still living are
intimately intertwined? The former view claims that the concept of the ‘tree of life’
branching ever outwards and upwards can even be turned upside down (the inverted
cone: Gould 1989). Although claims about numerous additional and different
Cambrian animal phyla seem to have been downplayed more recently (e.g. Gould,
1991) the notion of greater Cambrian disparity has continued to be championed
(Foote & Gould, 1992). This is a difficult idea to test but analyses of the Arthropoda,
the group that provides by far the most extensive data base, indicate that disparity
has not increased markedly since the Cambrian (Briggs & Fortey, 1989; Briggs,
Fortey & Wills, 1992a,b; Wills, Briggs & Fortey, 1994). This conclusion is based on
various quantitative measures, both cladistic and phenetic (reviewed in Wills et al.,
1994).Disparity among Cambrian arthropods is close to that of the Recent (taking
a representative selection of morphologies from the Recent fauna for comparison),
implying, at the least, that ‘hypervolume’ of morphological space equivalent to that
occupied by Recent Arthropoda was already filled by Cambrian time. Thus there
was rapid early differentiation into, and occupation of, morphospace. Nonetheless,
cladistic analyses revealed that many of the early and allegedly strange arthropods
provide connections between known groups rather than occupying clades of their
own (Briggs & Fortey, 1989; Briggs et al., 1992, 1993; Wills et al., 1994).
Timing
Often wrongly conflated with the idea of maximum disparity is the idea that the
‘explosion’ happened with astonishing rapidity (indeed, the ‘explosion’ metaphor
implies chain reaction at speed). As radiometric estimates for the base of the
Cambrian are revised upwards (e.g. Bowring et al., 1993) “the speed of explosion and
the intrigue and mystery of the result” (Gould, 1993: 523) are heightened. As a
CAMBRIAN EVOLUTIONARY ‘EXPLOSION
15
separate issue, it is widely held that the cladogenesis of new major bodyplans
(equivalent to classes and phyla) happened in concert with the visible, fossilized
‘explosion’ (McShea, 1993; Ridley, 1993). Thus according to this interpretation the
fossil record provides a true narrative of events, both in terms of phylogenesis and
morphological disparity, which run in tandem. The explosive explanation may have
utility, however, even if (as argued by Wills et al., 1994) Cambrian disparity did not
vastly exceed that of the Recent.
It has recently become clear that much metazoan ‘disparity’ had appeared already
in the Lower Cambrian. The discovery of Konservat-Lagerstatten of this age in
Greenland (Sirius Passet faunas: see Conway Morris & Peel, 1990; Budd, 1993) and
China (Chengjiang fauna: see references in Hou, Ramskold & Bergstrom, 1991;
Chen, Ramskold & Hou, 1994) has revealed a variety of animals, including
arthropods, comparable to those in the celebrated Burgess Shale (Briggs, Erwin &
Collier, 1994), thus pushing back the timing of the ‘explosion’ nearer and nearer to
the base of the Cambrian System. While there is clear evidence of the appearance of
hard skeletal structures at about this horizon (Qian & Bengtson, 1989), whether or
not this ‘explosion’of revealed diversity coincides with the evolution of fundamental
designs is a different question (Erwin, 1991). The evidence bearing on whether the
origin of clades might be decoupled from the ‘explosion’ that dominates the narrative
provided by the fossil record is reviewed here.
THE ‘EXPLOSION’SCENARIO
A number of arguments have been advanced in support of a literal interpretation
of the geological record as an accurate narrative of both the origin of clades and the
growth of disparity. These are reviewed briefly here to emphasize the distinction
between what is fact and what is inference. Fuller reviews can be found in Lipps and
Signor (1992) and Bengtson (1995).
l’he Ediacaran biota
The Ediacaran biota is now known from numerous localities in the late Vendian.
The affinities of these animals have been the subject of controversy. Glaessner (1 984)
regarded them as metazoans, many with close afFinities to modern groups. Seilacher
(1985, 1989, 1992) by contrast, emphasized certain differences between the
construction of virtually all the Ediacaran animals (Vendobionta) and later forms. He
and a limited number of others have preferred to regard vendobionts as
representatives of an extinct clade which did not give rise to any major later group.
A few workers envisage a merent marine ecology in the Vendian (the ‘Garden of
Ediacara’; McMenamin & McMenamin, 1990) in which the vendobionts (with an
allegedly unique metabolism) fill all the niches later occupied by large Phanerozoic
metazoans. More recently, Buss & Seilacher (1994) argued that the Vendiobionta is
the immediate sister group to the rest of the Metazoa. However, there is a growing
body of evidence that many so-called vendobionts may actually belong to established
metazoan phyla, although debates about the proper assignment of individual taxa
continue. At the very least, we consider that there are strong arguments against the
application of the vendobiont hypothesis to all the Ediacaran taxa (Gehling, 1991).
The Cnidaria is almost certainly represented in the Precambrian (Conway Morris,
1993b). Amongst Ediacaran genera Spriggina has been interpreted as an annelid
16
R. A. FORTEY E T A L
(Jenkins, 1992), Arkarua as an echinoderm (Gehling, 1987), and Parvancorim
(considered again below) and Raecambridium (Jenkins, 1992) as arthropods. Other
taxa have attracted more diverse speculation, Dickimonia being variously interpreted
as cnidarian, flatworm or annelid (see discussion in Valentine, 1992).
Tracefossils
There is much debate about what constitutes an early trace fossil but a diverse
assemblage of ichnogenera, including some relatively large forms, is known from the
Vendian (Crimes, 1992;Jenkins, 1994).There is a significant increase in abundance,
diversity and complexity in the Tommotian and Atdabanian in tandem with the
appearance of post-Ediacaran body fossils (Crimes, 1992). Thus an increase in the
diversity of soft-bodied infaunal animals, as revealed by their activities in sediments,
is paralleled in the record of the body fossils. Valentine (1989) attributed this to the
appearance of truly coelomic animals capable of burrowing.
Basal Cambrian appearances
The base of the Cambrian is dated at the base of the Manykaian ( = NemakitDaldyn) stage (Bowringet al., 1993)containing a relatively sparse, small shelly fauna.
Correlations with the Newfoundland stratotype are uncertain (e.g. Vidal &
Moczydlowska, 1992),although Landing (1994) and Isachsen et al., (1994) considered
that the lowest Cambrian is an interval of trace fossil development extending from
the Phycodespedum zone, up to the base of the Tommotian. Crimes (1992) discussed
the increase in trace fossil diversity throughout the Nemakit-Daldyn and into the
Tommotian, suggesting a radiation in parallel to that of the body fossils. The crucial
Cambrian ‘explosion’ of metazoans can be considered as confined to this last stage
plus the succeeding Atdabanian stage (yielding the new and rich Chinese and
Greenland Konservat-Lagerstatten) along with just the base of the Botomian
( = Qiongzuhusian) Stage. Moreover, acritarchs demonstrate a radiation with a
similar pattern to the trace and body fossils (Paliacos & Vidal, 1992; Vidal &
Moczydlowska, 1993). Thus the post-Vendian biota must, in the ‘explosive model’,
become established over a very short period of time.Just how short is not certain, but
recent estimates propose as little as five million years. Even those who would extend
the Manykaian (Landing, 1994)posit an extended interval of trace, rather than body
fossils. In any case, the postulated scenaiio generally involves the differentiation of
the familiar phyla and classes, and many additional ‘problematica’, during the
Manykaian and Tommotian, reflected in a progressively rapid diversification of trace
and ‘small shelly’ fossils. Conway Morris and Peel (1995) proposed that halkeriids
may represent the common ancestral morphology of molluscs and brachiopods. By
the late Lower Cambrian both disparity and the range of taxa match, or even exceed
(Gould, 1989), those of the Recent oceans. In sum, there is an ‘explosion’, allegedly
the greatest in the history of life, with morphological disparity tracking the
evolutionary generation of new clades.
Summaly
The evidence for an explosive radiation may seem overwhelming, but it does
depend on the geological record providing a true narrative of events. Such a true
narrative is not axiomatic, although it is sometimes treated as such (McMenamin &
McMenamin, 1990). At the outset, it is critical to distinguish what is fact from what
is inference. The lack of late Vendian fossils easily attributed to known groups of
CAMBRIAN EVOLUTIONARY ‘EXPLOSION’
17
Metazoa is fact, but the complete absence of ancestors of ‘modern’ groups at the
same time is inference. The rarity of Precambrian infaunal traces is fact, but the
absence of coelomic animals which could have made them is inference. Most
important, the coincidence of cladogenesis with the temporal narrative (i.e. the
assumption that as groups originate they appear without delay in the fossil record)
through the Manykaian-Tommotian is entirely inference.
Before the narrative provided by the fossil record can be accepted as a true
historical account it should be tested against independent evidence. Is there evidence
that the record is incomplete? Does the rapid diversification revealed by the fossil
record necessarily track phylogeny? Evidence bearing on these questions is accessible
both from the fossil record and from phylogenetics.
ARTHROPOD PHYLOGENY AND THE COMPLETENESS OF THE PHYLOGENETIC RECORD
The arthropods are the most informative group, having the most diverse
representatives in the Cambrian faunas (40% of the Burgess Shale fauna by genus:
Whittington 1985), and they provide sufficient characters to allow them to be
analysed in quantitative and cladistic ways (Briggs & Fortey, 1989; Briggs et al.,
1992a; Wills et al., 1994). Previous analyses of the Cambrian arthropods have
revealed shortcomings in the ‘explosion’ hypothesis.
Ear4 trilobite histov
The Trilobita consistently form a clade in cladistic analyses of the Arthropoda (see
Wills et al., 1994, for review). Calcification of the cuticle is an important apomorphy
of the group. In their earliest (Atdabanian) history trilobites are already geographically differentiated (Fig. 1) (Fortey & Owens, 1990; Signor, 1991) into regions
characterized by endemic genera or families referred to separate faunal provinces;
two or three such provinces having been distinguished. The functional morphology
of early trilobites indicates that they were vagrant benthos, not plankton, and there
does not seem to have been any special distributional factor at work with these
animals (Bergstrom, 1973). Even ifthere was a short-lived planktonic larval stage the
dispersal and endemic speciation of the group suggest that there was a phase of
vicariance prior to the appearance of the first body fossils (Signor, 1991). Whether or
not the first trilobites were calcified the early fossil record of this, the best known of
the Cambrian arthropod groups, must be inadequate.
Naraoiid c u e
The primitive sister group of calcified trilobites is the family Naraoiidae which
lacks a biomineralized exoskeleton (see Fortey & Theron, 1995). The genus Naraoia
is known from both the major faunal ‘provinces’ in the Cambrian, admittedly at
slightly different times. Such a distribution is consistent with a phylogenetic
argument based upon vicariance biogeography. There was a late Precambrian
‘supercontinent’ prior to the breakup into separate palaeocontinents near the
beginning of the Phanerozoic. Thus, animal groups which had already come into
existence by this time would be anticipated to have been widely distributed,
especially compared with those later distributions that were a reflection of
subsequent vicariant evolution attendant upon continental break-up. On this
argument, the distribution of an early clade including Naraoia is related to the relict
R.A. FORTEY mAL.
18
Figure 1. Early Cambrian geographic differentiation of trilobite faunas (Olenellid and Redlichiid
‘provincea’),proving earlier phase of vicariance unrecorded in the fossil record. After Fortey and Owens,
1990. Some authors further divide into three ‘provinces’. The symbols are emblematic; the taxa are
known h m many more individual localities than indicated.
Precambrian palaeogeography prior to the vicariant differentiation of the higher
members of the trilobite clade in the Ediacaran or later. However, because there is
no fossil record known bridging the gap between the ‘pandemic’, precalciiied stage
and the geographically differentiated, calcified stage this is also consistent with an
important hiatus in the preserved evidence. The argument is akin to a more familiar
one which relates the distribution of the late Palaeozoic tree Glossopteris-currently
dispersed through southern Afiica, South America, India and Antarctica- to a
previous Gondwanan distribution.
lh arthropod tree
Cladistic analysis of arthropod relationships,using both living and Cambrian taxa,
has shown consistently that Trilobita occupies a rather ‘high’ position in the
hypothesis of descent (Wills et al., 1994). This is something of a surprise (Briggs &
Fortey, 1989) given the historic role of the Trilobita as a kind of de fact0 arthropod
ancestor. Although the consistency indices of such trees are’low, their topologies
share many features no matter what animals are added and subtracted. Furthermore, it is possible to obtain higher values for CI ( > 0.5) by omitting animals
with marked reversals or ambiguous combinations of characters (see Fortey &
Theron, 1995, Fig. 8, for example). Thus there is somejustification for hypothesizing
a series of evolutionary steps between an annelid, mollusc or lobopod-like outgroup
taxon and the higher arthropods, trilobites among them. Yet the arthropod groups
appear in the record all together, low in the Cambrian. Even the primitive lobopod
Xenurion is of similar age (Dzik & Krumbeigel, 1989).
CAMBRIAN EVOLUTIONARY ‘EXPLOSION’
19
The arrangement of arthropods on the cladogram represents a hypothesis of their
descent (Briggs et al., 1992; Wills et al., 1994) and the degree of correspondence
between this and their order of appearance in the fossil record provides a test of
completeness (see Smith, 1994).The ‘lace crab’ Muwellu, for example, falls among the
most primitive arthropods on most analyses, yet its sole and earliest representative is
Middle Cambrian. Its absence in Lower Cambrian faunas, however, is not regarded
as sufficient evidence to m o w the hypothesis of relationships. Rather it seems likely
that earlier Cambrian representatives existed, even though they have left no fossil
record. More strikingly, if the low insertion of Uniramia below most of the Burgess
Shale arthropods in our cladograms is correct, this reveals a more fundamental
stratigraphic mismatch; apart from one disputed example (Robison, 1990), all the
uniramians are post-Ordovician. Thus, in this case, a ‘ghost’ (Novacek & Wheeler,
1992) lineage extends through more than two geological systems.
Such indications of imperfections are plausible, and this type of approach is
becoming widely applied (Norrell & Novacek, 1992; Smith, 1994). Strauss and
Sadler (1989) and Marshall (1990, 1992) demonstrated that the confidence intervals
applying to stratigraphic ranges relate directly to the number of occurrences of a
taxon within this range. Thus although it is not surprising that sparsely represented
sister lineages in the Cambrian imply long ghost ranges, these ranges nonetheless
reflect the nature of the Palaeozoic record. Yet an extension of such arguments to
infer ghost ranges in the Precambrian is apparently not considered by those who
favour a Cambrian ‘explosion’ model of cladogenesis (e.g. McMenamin &
McMenamin, 1990). The acquisition of derived characters (in the arthropod
example: a dorsal carapace, sclerotized labrum, compound lateral eyes, and
‘arthropodized’limbs with their associated musculature) is regarded, by implication,
as simultaneous rather than stepwise. In addition, the steps higher in the arthropod
tree -leading, for example, to geographically differentiated trilobites -are products of the same rapid event. The compressed timescale is a direct consequence of the
lack of appropriate Precambrian precursors. A literal reading of the fossil record
makes the Cambrian ‘explosion’ a logical necessity, however much it seems to
require abrogation of normal evolutionary modes. However, the possibility of
accommodating all the facts within an actualistic framework has yet to be eliminated.
It is not adequate to interpret the distinctive Cambrian animals as a random
selection of hopeful monsters from the aftermath of the ‘explosion’. The arthropods
are just arthropods for all their peculiarities; even the type example of the
bizarre -Anomalocm6- has been brought into the same broad fold (Chen et al.,
1994).
irhe timing ofclade dichotomies
Accommodating even one fossil from the Precambrian in a clade can calibrate the
tree by placing a minimum time of origin on a branch within the ‘ghost’ part.
Recently described possible ‘protaspides’ (larvae) of Naraoiu from the Lower
Cambrian of China (Hou et al., 1991) differ from those of other trilobites in their
enormous size. This is consistent with an idea (Fortey & Theron, 1995)that naraoiids
were derived from a ‘normal’ ontogeny by the heterochronic process known as
hypermorphosis. Thus Naraoiu resembled a gigantic larva. Could the Ediacaran fossil
Parvancorina, which has usually been considered as an arthropod (Glaessner, 1984;
Gehling, 1991) be similarly explained? The morphological evidence provided by
both Parvancorina and Naraoiu is sparse (Fig. 2) although the single shield, mode of
20
R. A. FORTEY ETAL
Figure 2. Similarity between the Ediacaran organism P a m m i n u (left, X 5) from the Pound Quartzite,
and the possible giant ‘protaspis’larva of the Lower Cambrian arthropod Nuraoia (right, X 16), specimen
from the Chengjiang fauna of China refigured from Hou ct a/., (1991).
growth, and cephalic outline may be similar enough to encourage speculation that
both belong to the trilobite clade. But ifthis relationship were true, it alone would be
sufficient to extend the range of the clade Trilobita (s.1.) back into Vendian ‘preexplosion’ times, and hence to fals;rt this model in general. An alternative to a
trilobite afhity for Palvanconnu is the possibility of a relationship to Burgessiu (Jenkins,
1992).Additional evidence for Ediacaran arthropods is the occurrence of Dip1ichnite.s
trackways (Gehling, 1991) and other scratch marks (Jenkins, 1992). A trilobite-like
soft animal has recently been reported from the Ediacara Member of the Rawnsley
Quartzite (Jenkins, 1992).The Trilobita occupy a high position on the tree; hence if
any or all of these Ediacaran identifications were correct, the major steps in the
radiation of the arthropods must have taken place in the Precambrian.
OTHER PHYLA
The kind of arguments rehearsed for the arthropods can be repeated for other
phyla, but robust cladistic analyses of relationships are arguably more diacult to
construct (Runnegar, 1994).We briefly review the evidence for other well-skeletised
phyla with a Cambrian fossil record. A more eclectic review of these groups can be
found in Valentine & Erwin (1987) and Erwin (199 1).
Mollusca
Although the relationships of molluscs are still controversial, most authors consider
that the shell-bearingforms constitute a clade, the Conchifera (whichincludes clams,
gastropods, scaphopods, chitons, cephalopods, monoplacophorans and rostroconchs,
as well as sundry early Cambrian shells, such as Pelagiellida) (Stasek, 1972; see
Runnegar, 1996, for a recent review). Most modern views favour the chitons as the
sister group to other conchiferans. Cephalopods originate higher in both time and
cladogram, and are not relevant to the current discussion. Other conchiferan groups
do have early Cambrian representatives, and gastropods, pelagiellids, mono-
CAMBRIAN EVOLUTIONARY 'EXPLOSION'
21
placophorans (which may be paraphyletic or polyphyletic) and chitons extend into
the Tommotian. Thus, like the calcified trilobites, the shelled molluscs appear
'instantly' (but see Conway Morris and Peel 1995). Their morphological compass
may be as great as that in trilobites although the time available to 'explode' is even
shorter since the earliest records of shelled forms are older than those of
trilobites -Tommotian as opposed to Atdabanian. If the shell is a synapomorphic
feature of Conchifera, the cladogram (Fig. 3A) reveals a gap in the fossil narrative
representing the important evolutionary steps from the first acquisition of shells to
the differentiation of the major groups as they appear at the base of the Cambrian.
(HEFTAPLACOTA) +
PLACOPHORA
= POLYPLACOPHORA'
Acsnthochitonida
I
TRYBLIDIA
= MONOPLACOPHORA*
A
GASTROPODA*
D
SPHONOPODA
= CEPHALOPODA
SCAPHOPODA
D
BNALVIA'
Figure 3. A, relationships among molluscs (after Runnegar, 1996); B, brachiopods (after Popov et al.,
1993) showing how taxa are already differentiated at the early Cambrian (asterisked taxa are known from
Cambrian strata) implying an earlier history of cladogenesis. The molluscan groups Caudofoveata and
Solenogastres are wo groups of small size and lacking shells formerly united withiin the Aplacophora.
22
R. A. FORTEY E T A
There may even be further ‘provincial’ differentiation like that in the trilobites,
because Cambrian molluscs, other than pelagiellids, are localized in distribution. In
any case, as with arthropods, the tree is truncated at its base at the time when
important changes were taking place.
Brachiopoda
Valentine and Erwin (1987) argued strongly that the evolution of the brachiopod
shell must have occurred in tandem with the development of an internalized,
lamellar feeding current around the stiffened lophophore. This suggests that the
capacity to secrete a shell is a brachiopod character, which provides evidence for an
early history unrepresented by fossils, like that of the Mollusca or Trilobita. A recent
cladistic analysis of the brachiopods (Popov et al., 1993; Bassett et al., 1994),however,
using a phoronid outgroup, concluded that the monophyletic clade Brachiopoda can
be divided into two broad groups, Lingulata and Calciata (Fig. 3B). Since the shell
composition is phosphatic in one clade, and calcareous in the other (“consistently
separated shell chemistries from early in phylogenetic history”, Popov et al., 1993: 1)
it is possible that the different shell types evolved independently. In this case, their
appearance in the Tommotian could be interpreted as the moment when shells were
acquired, implying a more complete record than that of the molluscs. Carlson (1994),
however, disputed the concept of Lingulata and Calciata, arguing that the
inarticulate brachiopods form a clade including both calcareous and phosphatic
forms. In either case, the record of soft-bodied, ‘pre-brachiopods’ is lacking.
Echinodermah
Echinodermata and Chordata have a comparatively poor Cambrian record,
particularly in the early part. They are regarded as sister taxa by most authorities.
The Burgess Shale pikaia is usually regarded as a chordate, while true echinoderms
are known from the Tommotian, and hence, as in the case of Marrella discussed
above, early Cambrian chordates must have existed even though they are not
preserved in the fossil record. If the Vendian Arkurua is correctly interpreted as an
echinoderm (Gehling, 1987), the important events in their phylogenesis must have
occurred in the Precambrian, regardless of the lack of preserved fossils. Paul and
Smith (1984) considered it likely that all echinoderm groups have their roots in an
early Cambrian stem lineage. However, such a hypothetical stem group left no
record, and would still need to be related satisfactorily to the chordates.
Implications
Phylogenetics provides the most rigorous approach to analysing the Cambrian
radiation. A testable analytical approach, even if limited, is preferable to simply
making assertions (e.g. “as many as 100 phyla may have existed during the
Cambrian, and only 5 percent or less of this number show evidence of a Precambrian
ancestry”; McMenamin & McMenamin, 1990: 168). The record of the arthropods,
molluscs, and to a lesser extent echinoderms and brachiopods provide direct
evidence of ghost ranges extending into the Precambrian for these well supported,
major lineages. The evidence is more indirect for other groups of animals.
Hemichordates, for example, are known in the Middle Cambrian (Durman &
Sennikov, 1993), but since,they are thought likely to be a sister group of either
chordates or echinoderms (e.g. Wada & Satoh, 1994; Peterson, 1994), and the latter
occur in rocks as old as Lower Cambrian, the hemichordates must have originated
CAMBRIAN EVOLUTIONARY ‘EXPLOSION
23
even earlier. A species attributed to Paleolina from the late Vendian Jinshan
Formation, Anhui Province, China (assigned to Vermes by Wang et aL, 1984, plate
7, figs 1,2) bears a remarkable resemblance to Rhabdophra and, if this were
substantiated, would provide the earliest hemichordate record. Similarly, inferred
relationships between lophophorate phyla (Nielsen, 1994) suggest that phoronids
must have pre-dated the Tommotian, which yields the earliest brachiopods, even
though the first phoronid record is doubtfully Pennsylvanian (Benton, 1993). This
suggests that the origination of these clades occurred significantly earlier than the
‘explosion’ of fossils filling morphological space (i.e. providing direct evidence of
disparity). Increases in recorded disparity and the generation of clades may have
been decoupled in time.
Valentine and Erwin (1988) argued for the divergence of metazoan phyla and
classes over time periods significantly less than a million years. Only a strictly
stratophenetic approach, however, can deny the existence of substantial unpreserved
ranges. The present discussion indicates that numerous metazoan lineages extended
back into the Precambrian without preservation. The question of calibrating rates of
evolution within these groups or determining how far back in time they originated or
diverged is a separate issue.
The preferred model becomes similar to the history of the mammals, with a long
Mesozoic prehistory that witnessed much phylogenetic groundwork before the rapid
deployment into vaned terrestrial habitats in the Palaeocene, with an accompanying
increase in size and disparity. If this model is correct, no special dispensation waiving
evolutionary rules need be invoked. It remains an interesting and important question
why the changes in skeletization and expression of clades are evident at the base of
the Cambrian, but it is a question with no necessuy connection to the cladogenesis.
MOLECULAR EVIDENCE
Evidence derived from molecules is a potentially powerfd tool in unravelling the
relationships between classes and phyla of living animal groups. Indeed, neontological and molecular studies are just as important as fossils for tackling this problem
because the majority of higher taxa are revealed, ready made, in the Cambrian.
There are hardly any fossils which suggest links between phyla. Budd (1993) claimed
that Kqpachela from the Lower Cambrian of Greenland may link the lobopods and
arthropods, a substantially similar claim to that made for Xenusion by Dzik and
Krumbeigel (1989). Molecular trees at this high phylogenetic level have been based
mainly on small subunit rRNA sequences, and they have not yet reached a state
where they could be described as stable (compare Ballard et aL, 1992; Lake, 1987,
1990; Turbeville et aL, 1991; Eernisse, Albert & Anderson, 1992; Raf€, Marshall &
Turbeville 1994; see Erwin, 1992; Conway Morris, 1993a). Significant homology in
sequences along branches of great antiquity may be concealed by changes that have
accumulated since the ancient dichotomy (the so-called ‘long branch problem’).
Large internode distances may be the result of relatively slow changes over long
periods, rather than the rapid changes postulated for an explosive event. The
coherence of the Arthropoda as a clade was not supported by some earlier molecular
studies, although subsequent investigations have re-established the monophyly of the
group (Turbeville et ul., 1991; Wheeler, Cartwright & Hayashi, 1993).
The absence of a clear signal in the molecular data says nothing about the speed
24
R. A. FORTEY ETAL.
CAMBRIAN EVOLUTIONARY ‘EXPLOSION’
25
Acoelomate “PLATYHELMINTHES”
C
Figure 4. Similar topologies of trees under ‘explosion’ scenario. A, Stormer’s phylogenetic ‘lawn’ after
Whittington (1979, 1981), where no connection between taxa are proposed. B, after Bergstrom (1989),
where all major taxa originate rapidly from a paraphyletic ‘Procoelomata’. C, after Willmer (1 990), where
all major higher taxa derive from (unspecified) platyhelminths.
of the radiation, but does suggest the accumulation of numerous, overwritten
changes in sister lineages. Molecular phylogenetic trees of the Metazoa have yet to
supply a critical test of the Cambrian ‘explosion’. Nonetheless, the separation of the
deuterostome echinoderm-chordate clade from one that includes the metamerically
segmented animals (molluscs, arthropods, annelids and lobopods among them) has
been confirmed by the molecular studies on small subunit rRNA. Whatever the
outcome of the debate about the mutual relationships within these groups the major
split must have preceded all the branching events discussed above. Thus it follows
that the ‘ghost’ lineages extend still further, at least where the echinoderm/chordate
and arthropod/mollusc/annelid clades are concerned.
TREES UNDER THE ‘EXPLOSION SCENARIO
Most of the trees which attempt to portray an ‘explosive’ origination for major
groups display many topological similarities (Fig. 4).The precursor of the others,
based upon such papers as Whittington (1979, 1981))shows the various major taxa
(phyla, classes, problematica) emerging as a kind of phylogenetic lawn (to use
St~rmer’s
phrase, quoted in Manton & Anderson, 1979: 281) from the Precambrian
(Fig. 4A). In this version no attempt is made to suggest interrelationships, and the
taxa emerge ‘ready made’. This diagram is little more than formalization of
uncertainty: problems of phylogeny are pushed backwards into a time when they
need not be addressed. This model was developed further after the notion of a
phylogenetic ‘explosion’ gained currency. “Thus, the genesis of most animal phyla
26
R. A. FORTEY ETAL.
must date back to the Cambrian and not before then” (McMenamin & McMenamin,
1990: 168) because of the lack of known Precambrian ancestors: the timing of
phylogenesis and the Cambrian ‘explosion’ are effectively conflated. Bergstrsm
(1989) derived both protostome and deuterostome phyla from a ‘new’ phylum
Procoelomata, to which he assigned various Cambrian sclerite-bearing shelly fossils,
with differing degrees of certainty (Fig. 4B). The Procoelomata is essentially a
massively paraphyletic ancestral stock from which advanced animal phyla arose.
These diagrams invite comparison with that taken from Willmer (1990) as a
summary of metazoan phylogeny, and based largely on classical comparative
anatomy, without primary reference to Cambrian fossils (Fig. 4C). The topology of
the tree and the derivation of the advanced animal phyla shows an obvious similarity
to those described previously. In this case, an extant group, Platyhelminthes,
provides the matrix from which the higher phyla originate.
It should be noted that adherence to an explosion scenario and the ‘formalisation
of uncertainty’ represented in the above diagrams have no logical relationship to
each other. Clearly, for example, it is possible to hold that the metazoan radiation
occurred within a relatively short time (e.g. 5-10 million years), and yet still pursue
the recovery of phyletic branching patterns. However, in achli& these two issues
have frequently been conflated (even in more recent writings). The absence of a clear
pattern of relationships between phyla and classes invites scenarios of chaotic and
presumably rapid divergence, which conveniently finds expression in the appearance
of groups in the fossil record.
The similarity of these topologies is consistent with the diaculties of relating phyla,
and determining the afiinities of Cambrian Problematica. But it is not apparent how
the explanatory power of having ‘explosion’ at the base of metazoan phylogeny is
either better or worse than having ‘platyhelminths’ or ‘Procoelomata’, nor, from the
published studies, how any one hypothesis is capable of being falsified. While it might
be possible to suggest, for example, that one platyhelminth taxon rather than another
is more closely related to a derived group, this kind of specific hypothesis has not
been made. Certainly, such trees do nothing to contradict the possibility of
cladogenesis being a separate issue from the acquisition of hard parts and overt
expression of the radiation at the base of the Cambrian.
THE PARADOX
Three lines of evidence indicate that phylogenetic history was decoupled from the
‘explosive radiation’ recorded by fossils at the base of the Cambrian that led to
modern levels of disparity of design: (1) the fossil record of organisms with hard parts
(and in some cases their palaeogeography);(2) the inferred phylogenetic relationships
between major subdivisions of arthropods, molluscs, brachiopods and echinoderms
and (3)the molecular evidence, so far as it goes. Paradoxically, there is good evidence
of important cladogenesis prior to the Cambrian ‘explosion’, but the fossils have so
far provided a very poor documentation of these events. This paradox can be
explained if the important events in cladogenesis happened in animals of small size,
a possibility considered by Runnegar (1983), and briefly by Valentine and Erwin
(1987; see also Valentine et aL., 1991). Such tiny animals are not readily detected in
the fossil record. Furthermore, the high surface area:mass ratio in small organisms
dictates that they decay more rapidly. Small size would also account for the rarity of
CAMBRIAN EVOLUTIONARY ‘EXPLOSION’
27
large scale trace fossils before the late Vendian: the habits and habitats of the animals
were not appropriate. This scenario implies that numerous lineages increased in size
synchronously, almost certainly in response to some environmental or ecological
trigger. Evolutionary size increase is straightforwardly mediated via heterochronic
change (see McKinney & McNamara, 199l), a basic developmental mechanism that
would have been available to all of the parallel lineages.
The sudden appearance of metazoan phyla and classes in the Cambrian may
simply reflect a Simultaneous size-increase in numerous groups, which, while it had
profound implications for the subsequent history of life, may not have involved any
fundamental genetic change. This made manifest in the record what had previously
been achieved by normal evolutionary mechanisms over a much longer period. This
hypothesis (which is implicit in Glaessner, 1984)explains the decoupling of events in
the Cambrian from the long prior history implied by the phylogenetic and other
evidence. An organism does not have to be large to have all the defining characters
of, say, a mollusc or an arthropod. Runnegar (1983) and Haszprunar (1992))for
example, considered it most probable that the molluscs were primitively minute.
Whether or not the niches for ‘large animals’ in the late Precambrian were occupied
by Ediacaran vendobionts it does seem that the basal Cambrian triggered a release
from the constraints of small size.
TINY SISTER GROUPS
The hypothesis of small ancestral size is supported by relationships among living
organisms. Although the phylogenetic relationships among higher taxa are
frequently controversial (Willmer, 1990))a number of living organisms of the order
of a millimetre in size (and often obscure and little known) have been identified as
sister groups to familiar living classes that radiated during the Cambrian. These
living sister groups are often meiofaunal or interstitial in habit (Boaden, 1975, 1989).
There is the classic problem of whether small animals are secondarily simplified, and
therefore actually relatively advanced (e.g. by paedomorphosis), but in the cases cited
below the small animals are either widely accepted as sister groups or very plausibly
occupy that position.
Arthropoda
Tardigrades have been claimed as the sister group of the arthropods (e.g. Nielsen,
1994).Tardigrades are usually a millimetre or less in length, and the marine species
live interstitially or among algae. They may have a thickened dorsal cuticle (Dewel,
Nelson & Dewel, 1993). Among the uniramian clade the Collembola are often
regarded as the sister group of all higher hexapods (Brusca & Brusca, 1990). They,
too, are minute and include interstitial species (there is one fossil example, Rhyniella
from the Devonian Rhynie Chert, see Whalley & Jarzembowski, 1981). Although
Collembola are currently terrestrial, their earliest history may have been aquatic (a
transition from water to land is documented for other arthropods including
diplopods and scorpions, and also for onychophorans).
Mollusca
Early representatives of conchiferan molluscs are already known to be small
(Runnegar, 1983; Haszprunar, 1992). The sister group of shelled molluscs has been
28
R. A. FORTEY ET AL,
considered to be the relatively little known group Aplacophora (Salvini-Plauwen,
1985).These animals are diminutive and lack shells; they inhabit the meiofauna, or
live on marine algae. Although their status is somewhat controversial (they may
comprise more than one clade, for example) recent cladistic treatments concur in
placing them low in molluscan phylogeny (e.g. Runnegar, 1994).
Deuti?rostoms
High level relationships among deuterostomes axe a matter of debate, but it is
generally accepted that hemichordates insert at a basal level in the phylogeny of the
group (Neilsen, 1994).However, the balanoglossids may not be closely related to the
pterobranchs (Peterson, 1994). The pterobranchs display the more generalized
morphology and are assumed to be primitive. Among these, Cephalodkcus, which
forms loosely attached aggregations of small zooids rather than true colonies in the
manner of IUlabdophru (Bulman, 1970), is likely to be close to the basal
morphology.
hphophrates
The relationships between brachiopods, phoronids and bryozoans are not
resolved. Taking the order of their appearance as fossils as phylogenetic evidence
would imply that the brachiopods were the most primitive because of their early
Cambrian record (the first bryozoan fossils are early Ordovician, while Taylor (in
Benton, 1993) stated that a possible phoronid trace of Devonian age is known), but
none of the phylogenetic analyses seems to support such an idea. If phoronids are the
most primitive of lophophorates, as is usually stated, then it follows that there are
‘ghost’ lineages in this group, and probably also in the bryozoans. The
Phylactolaemata, which have been interpreted as the most primitive bryozoans
(Jebram, 1986), includes species with few zooids and organic walls, which are not
candidates for fossilization under normal conditions. Ctenostome bryozoans are
usually considered to be the sister group of more advanced calcified bryozoans, and
these, too, include small and delicate uncalcified encrusters; they are known fossilized
only as bio-immurations (Taylor, 1990). In any case, the colonial habit is derived,
and the ancestral bryozoan was almost certainly a small, solitary animal, with
organic walls.
Allowing for the likelihood that many ‘intermediate’ taxa have become extinct
since the Cambrian, it is remarkable how many small-sized primitive sister groups
remain in the extant fauna. Many of these seem to be interstital or cryptic in
habit.
EVOLUTIONARY MECHANISMS
Evolutionary size increase is not dimcult to accomplish (e.g. Harvey & Read,
1988), although it does have interesting implications with regard to locomotion,
respiration and skeletal support. A common, and perhaps dominant mechanism for
changes in size involves heterochrony (reviewed by McKinney & McNamara, 1991).
Heterochronic changes may involve a mutation at a single locus, with a ‘cascade’
effect down through the ensuing ontogeny. Thus they provide a genetically
straightforward way of achieving fundamental modifications.
It is not a simple matter to demonstrate heterochronic change without an
CAMBRIAN EVOLUTIONARY ‘EXPLOSION
29
ancestor-descendant series of species, a condition unlikely to be fulfilled at the
Precambrian-Cambrian interface. There are, however, some instances where a
heterochronic explanation for the origin of particular morphologies is reasonable.
Larvae of crustaceans (nauplius), trilobites (protaspis) and primitive arachnomorphs (so-called ‘trilobite larva’ of Limulw) are all about 1mm long with single
dorsal shields, and thus conform in size to the small sister groups mentioned above.
During ontogeny segments are progressively released from the front of the telson (or
pygidium in trilobites) into the thoracic region. Thus heterochronic change may
operate either by inhibiting segmental release (paedomorphosis s m lato) or by
accelerating segmental release (peramorphosis), in relation to overall growth
trajectory. In the trilobite clade, two apparently highly different Lower Cambrian
morphologies may have arisen by opposite heterochronic processes. Naraoia, which
lacks free thoracic segments, is essentially an enormously inflated larval uncalcsed
trilobite; its morphology may be attributed to hypermorphosis (Fortey & Theron,
1995). The primitive trilobite Emuella (Pocock, 1970), on the other hand, shows the
greatest proliferation of thoracic segments, attesting to a hyperactive process in their
release. Thus in spite of the striking differences between these two animals they could
have descended from a small, common ancestor by the differential operation of
heterochrony. Similar processes operating upon a number of small arthropodous
animals with differing bauplane might go some way towards explaining the ‘explosion’
of new, large forms near the base of the Cambrian, without recourse to novel
evolutionary mechanisms (Valentine, 1994).
HOM/Hox homeobox genes are present in different arthropod clades (e.g. insects
and crustaceans: Averof & h a m , 1993; Limulus: Cartwright, Dick & BUSS,1993). It
seems likely that the differential expression of these controlling genes is responsible
for maintaining differences in body plans between groups. In the Lower Cambrian
the timing of developmental changes -or the ‘fixing’ of particular expressions of
these genes -may reflect the operation of heterochronic change accompanying a
rapid increase in body size. This is not inconsistent with the views of Valentine and
Erwin (1987) on the comparative lability of Cambrian genetic programs and their
subsequent ‘fixing’ in Phanerozoic history.
CONCLUSIONS
The case that the origin of clades may be decoupled from the increase in disparity
at the base of the Cambrian has not received the consideration that it deserves. Yet
a period of metazoan evolution within the Vendian (Fig. 5) is supported by evidence
from phylogenetic trees, from the taxonomic differentiation within clades already
present at the base of the Cambrian, the geographic distribution of some of these
early taxa, and from molecular studies on living animals. This positive evidence must
be weighed against essentially negative evidence for an ‘explosion’: the lack of known
fossils of the right kind from strata in the latest Precambrian. This does have the
unfortunate consequence of providing a poor constraint for the timing of the onset,
and thus the rate of radiation (Valentine et al., 1991).
The hypothesis that the crucial phase of evolution in bauplane happened in animals
of small size may explain the apparent paradox of the mismatch between the fossil
record, and the evidence for Vendian cladogenesis. The search for the fossils of such
animals should be directed at sediments suitable for the preservation of interstitial or
R.A. FORTEY E T A
30
ij %
I
I
-oI-
"Phanerozoic"
Metazoa
Figure 5. Possible model for cladogenesisduring the Vendian and basal Cambrian, adopting the scenario
described in this paper. Lineages comprising large animals in habitats readily capable of fossilization are
represented by thickened lies, while smaller forms which may have lived in meiofaunal or planktonic
niches are shown in thinner lines.
possibly planktic animals. Fragmentary organic remains of arthropods are already
known in Cambrian rocks (Mount Cap Formation: Buttefield, 1994: Devonian
Gilboa Formation: Shear et al., 1984). In particular, sites where bio-immured fossils
(Taylor, 1990) might occur should be investigated, because these have proved to
record small, soft-bodied taxa. The normal agents for bio-immuration, such as
cementing clams, were obviously not available at this time, but calcareous mats
formed by algae and bacteria are a possibility 0. Todd, pers. comm.).
Too literal an adoption of the 'explosion' hypothesis may discourage attempts to
place Cambrian animals into phylogenetic hypotheses, but reasonable phylogenetic
trees can and have been proposed for several phyla. As far as arthropods are
concerned, fossils reveal character combinations long since lost which help to reveal
branching events such as those leading to living groups. Some far-reaching changes
may have involved heterochrony in particular. The genetic basis for such changes,
perhaps through the operation of homeobox genes, is potentially a subject for
experiment.
ACKNOWLEDGEMENTS
We thank Andrew B. Smith, Douglas Erwin, Geoffrey Levinton, Colin Patterson
and an anonymous referee for reading and suggesting improvements to the
manuscript.Jan Bergstrom and Richard J.Jenkins proGded photographs. We thank
Mike Foote, Michael h a m , Adrian Friday and Richard Jenkins for discussion.
MAW was funded by a University of Bristol postgraduate scholarship. DEGB's
contribution was written while he was a Distinguished Visiting Scholar at the
University of Adelaide.
CAMBRIAN EVOLUTIONARY ‘EXPLOSION’
31
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