Gondwana Research 25 (2014) 896909

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Gondwana Research
journal homepage: www.elsevier.com/locate/gr

GR Focus Review

Triggers for the Cambrian explosion: Hypotheses and problems

Xingliang Zhang , Degan Shu, Jian Han, Zhifei Zhang, Jianni Liu, Dongjing Fu
Early Life Institute and State Key Laboratory for Continental Dynamics, Department of Geology, Northwest University, Xian 710069, China

a r t i c l e

i n f o

Article history:
Received 30 August 2012
Received in revised form 9 May 2013
Accepted 2 June 2013
Available online 19 June 2013
Keywords:
Animal evolution
Ecology
Genetics
Environment
Cambrian explosion

a b s t r a c t
Abrupt appearance of major bilaterian clades in the fossil record during the rst three stages of the Cambrian Period
has puzzled the scientic world since 1830s. Many proposed causes including environmental, developmental, and
ecological hypotheses, are reviewed. Nutrient availability, oxygenation, and change of seawater composition are
commonly supposed to be environmental triggers. The nutrient input, e.g. the enrichment of phosphorus in an environment, would cause excess primary production, but it is neither directly linked with diversity nor disparity.
Fluctuating abiotic conditions during the Snowball Earth and the associated oxygenation event may have stimulated the diversication of complex multicellular organisms including diverse of macroscopic and morphologically
differentiated algae in the early Ediacaran, but did not lead to the ecological success of metazoan or bilaterian lineages. Further increase of oxygen level and change of seawater composition just before and during early Cambrian
are suggested by the high weathering rate of the trans-Gondwana mountains, Great Unconformity, and decline
of oceanic salinity. These are potential candidates of environmental triggers for the Cambrian explosion but require
future more detailed geochemical studies to conrm. The molecular phylogeny calibrated with the molecular clock
data suggested that the developmental system of bilaterians was established before their divergence. This, in turn,
suggests that the Cambrian explosion require environmental triggers. However, there still exists the contention
between deep or shallow divergence of bilaterian clades, which remains to be solved in the future. The deep
divergence model is supported by a majority of molecular clock studies, but is challenged by the paucity of
bilaterian fossils before and during the Ediacaran Period. The shallow model is generally consistent with the fossil
record, but has to explain the rapidity of increase in diversity, disparity, morphological complexity, acquisition of
biomineralized shells, etc. Regardless of deep or shallow model, the conservation of lineage-specic kernels
within the gene regulatory networks (GRNs) provides an explanation for the long-term stability of body plans
after the Cambrian explosion, and continuous addition of microRNAs into the GRNs seems to correspond well
to the increase in morphological complexity. As for ecological causes, some hypotheses (e.g. adaptive radiation
after mass extinction, cropping, and geospherebiosphere feedbacks) cannot explain the uniqueness of the
event, some others (such as Cambrian substrate revolution, predatorprey pressure, evolution of zooplankton,
and roughening of tness landscapes) fall into the trap of chicken-and-egg problem because of considering
the consequence as a cause. Expansion of ecosystem engineering in the early Cambrian might also be caused
by the Cambrian explosion. However, ecosystem engineering associated with Ediacaran ecosystems is likely a
pivotal ecological prerequisite for the later ecological success of bilaterian clades, particularly the engineering
effect by Ediacaran sponges that ventilated seawater by sponge pumping and removing organic material from
the water column. However, the ecological abundance of Ediacaran sponges needs to be further investigated.
Finally, a working plan is proposed for future research. For paleontologists, searching for ancestors of early
Cambrian faunas is crucial to testify the earlier divergence of bilaterian lineages. Environmentally, precise values
on the oxygen level and seawater composition are required during the EdiacaranCambrian transition.
2013 International Association for Gondwana Research. Published by Elsevier B.V. All rights reserved.

Contents
1.
2.

Introduction . . . . . . . . . . . . . .
Hypothetical triggers . . . . . . . . . .
2.1.
Environmental triggers . . . . .
2.1.1.
Tectonic backdrop . . .
2.1.2.
Aftermath of the Snowball

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Corresponding author. Tel.: +86 29 88303200; fax: +86 29 88304789.

E-mail address: xzhang69@nwu.edu.cn (X. Zhang).
1342-937X/$ see front matter 2013 International Association for Gondwana Research. Published by Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.gr.2013.06.001

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X. Zhang et al. / Gondwana Research 25 (2014) 896909

2.1.3.
True polar wander . . . . . . . . . . . . .
2.1.4.
Seawater composition . . . . . . . . . . .
2.1.5.
Rise of oxygen levels . . . . . . . . . . . .
2.2.
Developmental genes and molecular clock . . . . . .
2.2.1.
Early hypothesis: evolutionary addition of Hox
2.2.2.
Gene regulatory networks and microRNAs . .
2.2.3.
Deep or shallow divergence? . . . . . . . .
2.3.
Ecological causes . . . . . . . . . . . . . . . . . .
2.3.1.
Extinction of Ediacaran biotas . . . . . . . .
2.3.2.
Cropping . . . . . . . . . . . . . . . . . .
2.3.3.
Phytoplanktonzooplankton diversication .
2.3.4.
Bioturbation . . . . . . . . . . . . . . . .
2.3.5.
Advent of macrophagous predation . . . . .
2.3.6.
Roughening of tness landscapes . . . . . .
2.3.7.
Geospherebiosphere feedbacks . . . . . . .
2.3.8.
Ecosystem engineering . . . . . . . . . . .
3.
Conclusions . . . . . . . . . . . . . . . . . . . . . . . .
4.
Outlook for future research . . . . . . . . . . . . . . . . .
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . .

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1. Introduction
The Cambrian explosion is a long standing macroevolutionary
issue, which has been puzzling paleontologists and evolutionary biologists since 1830s as Conway Morris (2000, p. 4426) stated William
Buckland knew about it, Charles Darwin characteristically agonized
over it, and still we do not fully understand it. It is generally accepted
that essentially all of the readily fossilizable animal body plans (about
half of living animal phyla) made their rst appearance in the fossil
record within a few tens of millions of years during the early Cambrian
(Valentine, 2002; Erwin et al., 2011). Therefore, the Cambrian explosion
has been widely realized as the most signicant evolutionary event in
the history of life on Earth (Conway Morris, 2006; Marshall, 2006; Shu,
2008; Maruyama et al., 2013; Santosh et al., 2013).
Fossil rst appearances of animal phyla are obviously diachronous,
but relatively abrupt in a short time span during the late Ediacaran to
the early Cambrian (Shu et al., 2014-in this issue). The fossil record of
basal animals (sponges and cnidarians) is extended to a period of
time signicantly before the beginning of the Cambrian. Thus, the Cambrian explosion itself seems to represent the arrival of the bilaterians
(Budd, 2008). Analyses of early Cambrian faunas revealed that the
divergence of bilaterian clades are episodic: lophotrochozoans were diversied during the Terreneuvian Epoch, mainly the Fortunian Age;
ecdysozoans become diverse at the beginning of the Cambrian Stage 3
despite the fact that their fossil rst appearance can be traced back to
the Terreneuvian Epoch (e.g. arthropod traces and grasping spines of
chaetognaths); divergence of deuterostomes started from the middle
of Cambrian Stage 3 (Shu, 2008; Shu et al., 2009; Maloof et al., 2010;
Kouchinsky et al., 2012), but the appearance of remains and traces of
bilaterian animals remains abrupt (Erwin et al., 2011; Shu et al.,
2014-in this issue). Apparently, the Cambrian faunas show that diverse
animal phyla were already established during early Cambrian and have
given us plenty of information about the diversity, disparity and morphological complexity of animal life at that time (Nielsen, 2001).
Unfortunately, the fossil record tells very little about the origin of animal
phyla because early ancestors might be small and/or soft-bodied, with
little or no preservation and/or recognizable potential. Therefore, it is
likely that a period of animal evolution preceded the Cambrian explosion
we see in the early Cambrian. This is also indicated by studies of molecular diversication and comparative developmental data (Wray et al.,
1996; Bromham et al., 1998; Aris-Brosou and Yang, 2003; Peterson
et al., 2004, 2008; Blair, 2009), evolution of oxygen transport proteins
(Decker and van Holde, 2011), and phylogenic analyses of Cambrian
fossils and biogeography (Fortey et al., 1996; Lieberman, 2002), all

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developmental genes
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897

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899
899
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suggesting that the major animal clades diverged many tens of millions
of years before their rst appearance in fossil record. Any inference on
earlier divergence of bilaterian phyla was unavoidably challenged by
the paucity of fossils of bilaterian clades during the Ediacaran period.
Provisionally, the conundrum of the Cambrian explosion seems to
be conquered by the combination of present paleontological and molecular data: the major animal clades, at least stem lineages, diverged
during the late Cryogenian to early Ediacaran, and did not become
ecologically important until the late Ediacaran to early Cambrian
(Erwin et al., 2011). This solution still implies a long history of cryptic
evolution not present in the fossil record. Therefore, the Cambrian explosion is largely an ecological phenomenon, including the increasing
of body size and morphological complexity, and widespread biomineralization among animals.
However, the exact causality has not yet been established, although there are many hypotheses as to what triggered the Cambrian
explosion, ranging from environmental, developmental to ecological
causes. Since 2005, a joint project by Chinese and Japanese scientists
have worked on paleontological and environmental issues of the
Cambrian explosion, with preliminary research progress published in
a special issue of Gondwana Research 14 (12) 2008 and this volume.
The cooperative project will be continued in the next ve years. Therefore, here we give a review on available triggering mechanisms of the
Cambrian explosion, to identify the shortcomings of each hypothesis,
particularly with regard to paleontological data, and nally explicate
our future research on this topic.
2. Hypothetical triggers
It seems obvious that something must have changed or reached a
critical level favorable for the building of large, complex bodies and
the construction of hard skeletal material. The hypotheses of what
such evolutionary triggers can be split into extrinsic or external environment factors (e.g. tectonic settings, climatic conditions, nutrient
availability, oxygen level, oceanic salinity), intrinsic or internal biotic
factors (genetical and developmental innovations), and ecological
causes (Fig. 1).
2.1. Environmental triggers
Many environmental triggers have been proposed but the oxygenation and change of seawater composition are most relevant factors.
Some others, e.g. tectonic background and deglaciation of the Snowball
Earth, merely provide mechanisms for the rise of oxygen level and the

898

X. Zhang et al. / Gondwana Research 25 (2014) 896909

Fig. 1. Timeline of environmental, molecular and ecological events that were proposed as triggers of the Cambrian explosion. The phylogenetic tree for metazoans scaled against
the molecular dates of lineage splitting (Erwin et al., 2011). Note that each node is characterized by the addition of at least one new microRNA gene family, indicated in numbers
(Peterson et al., 2009). Three instances of high rate of microRNA acquisition are recognized, once at the base of protostomes and deuterostomes, once at the base of vertebrates, and
once at the base of primates (not indicated). Numbers 14 in the age column representing the rst four stages of the Cambrian System; HSP, heat shock protein; PDA, protostome
deuterostome ancestor.

uctuation of seawater chemistry. Of course, there are other environmental factors (e.g. atmospheric CO2 level, seawater pH, and trace
metals) that are potentially important for animal evolution, but the
lack of data that are specically relevant to the Cambrian explosion
does not allow a further discussion on these issues.
2.1.1. Tectonic backdrop
The assembly of Gondwanaland is more or less viewed as a polyphase accretion of formerly disparate blocks, which is accomplished
along three major orogenic belts known as the East African Orogen
(750620 Ma), the BrasilinaDamara Orogen (630520), and Kuungan
Orogen (570530 Ma) (Li and Powell, 2001; Meert, 2003; Rogers and
Santosh, 2004; Campbell and Squire, 2010; Meert, 2011). The latter two
orogens took place just before and during the Cambrian explosion.
More recent paleomagnetic and geochronological data also suggested
that the closure of the Clymene ocean was in the early Cambrian
(Tohver et al., 2010, 2012). And around the same period, the Iapetus
Ocean opened (Grunow et al., 1996), followed by the closure of Mawson
and Brasiliano Oceans (Meert and Lieberman, 2008). The hypothetical
short-lived supercontinent Pannotia, formed at the latest Neoproterozoic,
just before the Cambrian radiations (Dalziel, 1997), comprised Gondwana plus Laurentia adjacent to Amazonia (Li and Powell, 2001). No matter
the exact model of Gondwanaland assembly and the debate on the

existence of Pannotia, the formation of the supercontinents was just

prior to or nearly synchronous with the Cambrian explosion. Therefore,
it is reasonable to link biological changes that occurred at this time with
tectonic events that resulted in the assembly of supercontinents and the
opening of oceans. Each collisional orogen within the Gondwana extended for several kilometers (Dalziel, 1997; Campbell and Squire,
2010). The uplift and erosion of the huge trans-Gondwana mountains
would have a signicant inuence on the seawater composition and
global climate, providing nutrients (e.g. phosphorus) to the oceanic
realm (Brasier and Lindsay, 2001; Squire et al., 2006) and increasing
the burial rate of organic carbon that is believed to have triggered a critical rise in the availability of atmospheric oxygen (Knoll and Walter,
1992; Campbell and Allen, 2008; Campbell and Squire, 2010).
Of course, both oxygen and nutrient like P are necessary for animal
life. The enrichment of P or other limited nutrients like N in an environment may lead to the increase of primary production (Howarth,
1988; Tyrrell, 1999), but neither directly linked with the increased
biodiversity (number of species) nor with increased disparity (number
of phyla) as was embodied by the Cambrian explosion. On the contrary,
the biodiversity may decrease during the assembly of continents according to Valentine and Moores' (1970) model. Additionally, the worldwide
phosphate deposition during the EdiacaranCambrian transition
might aid in fossil preservation at this time, e.g. the phosphatized

X. Zhang et al. / Gondwana Research 25 (2014) 896909

Ediacaran biotas in South China and the Terreneuvian Small Shelly

Fossils worldwide (Meert and Lieberman, 2008). The case of oxygen
is more complicated (see below). Supercontinental amalgamation
and fragmentation are not unique during the PrecambrianCambrian
transition (Dalziel, 1997), and there is no evidence that the oceanic P
concentration is insufcient for animal diversication. Hence, the assembly of Gondwana merely provides a tectonic backdrop (Meert and
Lieberman, 2008) and it alone cannot be a driving force to the Cambrian
explosion. On the contrary, a study suggested that the Neoproterozoic
marine dissolved phosphate concentrations were signicantly higher
than Cambrian levels (Planavsky et al., 2010).
2.1.2. Aftermath of the Snowball Earth
Growing evidence indicated that the Earth experienced an extremely cold climate during the Neoproterozoic, which resulted in
two or three episodes of global glaciations during which ice sheets extend to equatorial latitudes, i.e. the Snowball Earth (Kirschvink, 1992;
Hoffman et al., 1998; Hoffman and Schrag, 2002). The duration of
the Snowball Earth is now constrained between 780 and 635 Ma,
interrupted by two interglacial warm periods. The Snowball Earth itself is catastrophic for biological world, causing the collapse of biological productivity in the surface ocean for millions of years (Hoffman
et al., 1998), but may have in fact played a role in triggering the
evolutionary bursts that followed (Fedonkin, 2003). However, many
researchers argued that it ultimately resulted in signicant leaps in
biological evolution, e.g. the Ediacaran radiation and the Cambrian
explosion (Kirschvink, 1992; Hoffman et al., 1998; Maruyama and
Santosh, 2008; Planavsky et al., 2010; Papineau, 2010). Again, it is nutrient P and oxygen that tie the Snowball Earth to biological evolution.
These two factors are intimately linked because a glacially induced
phosphorus surplus would have led to an increase in atmospheric oxygen (Planavsky et al., 2010). It has been argued that erosion of glaciations and high chemical weathering rates during the retreat of ice
sheets must have led to higher riverine delivery of phosphorus to seawater, which would have increased rates of primary productivity and
organic carbon burial that produced signicant quantities of atmospheric oxygen. As a result, the accumulation of atmospheric oxygen
paved the way for the rise of macroscopic oxygen-breathing organisms
and led to the emergence of animals in the NeoproterozoicCambrian
interval (Planavsky et al., 2010; Papineau, 2010).
On the other hand, the harsh and uctuating abiotic conditions
like the Snowball Earth may temporarily increase the degree of altruism that was adaptive and promoted an increasing degree of terminal
(irreversible) differentiation. This is thought to be of particular relevance to animal multicellularity because irreversible differentiation
(highly altruistic in that it imposes a high tness cost on the individual cell) is more prevalent than in other multicellular eukaryotes
(Boyler et al., 2007). Furthermore, the Snowball Earth may increase
the expression of genetic diversity in animals due to the effect of
extreme climatic stress on heat shock protein 90 (HSP90), which results
in pre-existing mutant signal transduction proteins and developmental
pathways were expressed in animals (Baker, 2006). Up to now, it seems
that the aftermath of the Snowball Earth on biological radiation become
increasingly evident, although it is still hard to see how a cold catastrophe could have lead to fundamentally new levels of developmental and
morphological organization (Marshall, 2006).
However, the Snowball Earth ended at 635 Ma, about 100 Ma before the Cambrian explosion. What happened with the Earth's surface
environment during this 100 Ma may be the crucial point. The steep
rise in seawater 87Sr/86Sr from the Ediacaran to early Cambrian is
attributed to elevated weathering rates that could lead to increased
nutrient availability, organic burial and to the further oxygenation of surface environments (e.g. Shields, 2007). The end of the Snowball Earth
was followed by the evolution of complex macroscopic multicellular organisms, revealed by the early Ediacaran Lantian biota (Yuan et al., 2011)
that occurs immediately above the Marinoan-aged glaciation, and many

899

more late Ediacaran macrobiotas following the Gaskiers (McCall, 2006;

Fedonkin et al., 2007). In terms of the Cambrian explosion, it is, perhaps,
the continued post-glacial rise of atmospheric oxygen paving the way for
the later diversication of animals during the early Cambrian.
2.1.3. True polar wander
The EdiacaranCambrian interval is characterized by paleomagnetic
data that imply anomalously high rates of apparent plate motion, the
rotation or translation rates for each paleocontinent equivalent to or exceeding 10 to 20 cm per year (see Mitchell et al., 2011 and references),
in marked contrast to more typical continental moving rates of a few cm
per year (Meert et al., 1993). Therefore, true polar wander (TPW) was
invoked to explain the rapid motions of paleocontinents during the
EdiacaranCambrian transition (Kirschvink et al., 1997; Evans, 1998,
2003). It has been suggested that an episode of rapid true polar wander
occurred during the Cambrian explosion of animal life (Mitchell et al.,
2010). Kirschvink et al. (1997) argued that wholesale rotation of the
lithosphere was likely to have effected major changes in oceanic circulation and, hence, regional climates, and the repeated reorganizations in global climatic patterns during a TPW event would have
fragmented any large-scale ecosystems that were established, generating smaller, more isolated populations and leading to a higher
evolutionary branching rate among existing groups. Kirschvink and
Raub (2003) proposed more explicit relationships between a succession
of TPW events and Cambrian explosion. The argument is that, rst, tropical continental margins and shelf-slopes which formed due to the fragmentation of the Rodinia accumulated massive quantities of organic
carbon during Late Neoproterozoic time; second, an initial phase of
Ediacaran TPW moved these organic-rich deposits to high latitude,
where these and additionally added organic material were trapped as
methane hydrate or permafrost and stabilized until the geothermal gradient moved them out of the clathrate stability eld; nally, a burst of
TPW brought these deposits back to the Tropics, where they gradually
warmed and released to the atmosphere, and thus induced pulses of
global warming. Since the Earth's surface temperature correlates powerfully with biodiversity, Kirschvink and Raub (2003) suggested that the
Cambrian explosion could have been driven by global warming forced
by methane clathrate decomposition, induced by an inertial interchange
true polar wander event. In this hypothesis, the bridge between the
Cambrian explosion and TPW is largely the increase of biodiversity due
to elevation of temperature, but the nature of Cambrian explosion is far
more than a dramatic change in biodiversity. As noted by Marshall
(2006), this hypothesis offered no explanation as to why an increase in
biodiversity, per se, should have led to new levels of disparity. In addition, the global warming during early Cambrian is currently not testied
by geological and geochemical data, regardless of the likelihood that the
methane hydrates were brought from high latitude to tropics without
collapse. Furthermore, rapid climate uctuations might suppress
diversication owing to physiological stress. The other problem is
that the TPW hypothesis contradicts with phylogenetic analyses of
early Cambrian biogeography. Early Cambrian faunas show well
established endemism (Lieberman, 2002), which unlikely arose in
the rapidly changing geography required by the TPW hypothesis
(Meert and Lieberman, 2004, 2008).
2.1.4. Seawater composition
Salinity is an environmental factor of considerable importance for
organisms, which controls and limits the nature of biologic activity.
Salinity can also have a strong effect on the solubility of atmospheric
gases, especially oxygen. The salinity history of sea water is thus crucial
for life evolution. It was estimated that initial salinity of the oceans was
1.52 times (52.570) that of the modern value (~35), or even
higher, and it did not decline signicantly until the latest Neoproterozoic
when enormous amounts of salt and brine were sequestered in giant
Neoproterozoic evaporite basins (Knauth, 1998, 2005). Most forms of
modern macroscopic life, including metazoans, cannot tolerate salinities

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X. Zhang et al. / Gondwana Research 25 (2014) 896909

above 50 because high osmolarity in hypersaline conditions can be

deleterious to cells since water is lost to the external medium until
osmotic equilibrium is achieved. Therefore, Knauth (1998, 2005) speculated that the delayed decline of ocean salinity may have been a factor in the Cambrian explosion of life. The ocean salinity modeling
(developed using maximal and minimal estimates of the volumes of
existing evaporite deposits, and using constant and declining volumes
of ocean water through the Phanerozoic) also suggests that there was
a major salinity decline from the late Neoproterozoic to the Cambrian
(Hay et al., 2006). However, the late Neoproterozoic salt deposits of
the Hormuz region cannot be precisely dated, and the apparent sharp
decline before the Cambrian may be an artifact of the lack of better information (Hay et al., 2006). In addition, the presence of abundant
and diverse eukaryotic life during the Neoproterozoic also challenges
the high salinity hypothesis.
On the other hand, analyses of primary uid inclusions from
terminal Proterozoic (ca. 544 Ma) and Early Cambrian (ca. 515 Ma)
marine halites indicate that seawater Ca2+ concentrations increased
approximately threefold during the early Cambrian (Brennan et al.,
2004; Berner, 2004). The timing of this shift in seawater chemistry
broadly coincides with the Cambrian explosion, thus it was suggested
that the dramatic early Cambrian rise in the absolute concentration of
Ca2+ may have facilitated the pervasive biocalcication at this time
by promoting intracellular Ca2+ concentrations that were toxic to
some animals (Brennan et al., 2004; Petrychenko et al., 2005; Hay
et al., 2006). Furthermore, an experimental study of sponge cells indicated that the elevation of Ca2 + concentration could increase binding
forces between their calcium-dependent cell adhesion molecules.
This, together with the advent of self-/non-self-recognition systems
(assumed to have evolved gradually before the Cambrian period)
could have unleashed the rise of multicellular animals. Therefore, it
was proposed that the Cambrian explosion might have been triggered
by the coincidence in time of primitive animals endowed with self-/
non-self-recognition and of a surge in seawater calcium during the
early Cambrian (Fernndez-Busquets et al., 2009). However, rapid
Ca2+ increase in early Cambrian seas is accompanied by a decrease of
sulfate concentrations more than twofold (Brennan et al., 2004). This
is in conict with the paleontological data that bioturbation intensity
increased substantially (McIlroy and Logan, 1999) and matgrounds
evolved to mixgrounds (Seilacher, 2007) during the early Cambrian
because sediment mixing by bioturbating organisms resulted in a
severalfold increase in seawater sulfate concentration (Caneld and
Farquhar, 2009).
In the course of writing this paper, a seemingly new hypothesis
links the Great Unconformity (which separates Precambrian continental crystalline basement rock from much younger Cambrian shallow marine sedimentary deposits in several paleocontinents) to the
Cambrian explosion (Peters and Gaines, 2012). It argued that, the
formation of the Great Unconformity involved the widespread continental denudation followed by extensive physical reworking of soil,
regolith and basement rock, and enhanced chemical weathering of
continental crust during the rst continental-scale marine transgression of the Phanerozoic; these processes would affect seawater chemistry, e.g. increase of Ca2+ concentrations in seawater, and thus triggered
biomineralization in multiple clades, thereby promoting the Cambrian
explosion of marine animals (Peters and Gaines, 2012). This hypothesis
merely provided a possible mechanism for the increase in seawater
Ca2+. Neither new data of Ca2+ concentrations is offered, nor is new
explanation as to why an increase in sea water Ca2+, per se, should
have led to such a major diversication or biomineralization among
metazoans.
2.1.5. Rise of oxygen levels
Oxygen has long been proposed as a prerequisite to early animal
evolution (Nursall, 1959; Caneld and Teske, 1996). Increasing atmospheric oxygen levels have, for example, been implicated in the

rise of late pre-Cambrian and Cambrian marine faunas (Cloud, 1976;

Runnegar, 1982a,b; McMenamin and McMenamin, 1990; Gilbert,
1996; Caneld et al., 2007). Oxygen is absolutely essential for metazoans maintaining many metabolic and physiological processes, which
allows for effective aerobic respiration, mobility, body size increase,
skeletonization, and synthesis of collagen (holding cells in a metazoan
together) and cholesterin (making cell membranes rigid). However,
an excess of oxygen leads to accumulation of toxic reactive oxygen species (ROS), which can be dangerous for all organisms. To cope with ROS,
animals have evolved sophisticated mechanisms which they used for
defense (Decker and van Holde, 2011). Two defense strategies deserve
to be mentioned here. The rst one is cell aggregation, with surface cells
protecting interior members from ROS. Therefore, it is likely that the
protection against ROS is one of the evolutionary driving forces towards
multicellularity and oxygen plays an even larger role in evolution than
hitherto suspected. The other one is melanization, which might have
occurred on the dermal cells of primitive metazoans. It could offer protection and might also form a defensive cuticle against predation. Once
the principle of cell specialization was established, the way was open for
almost innite pathways of development of special organs, functions
and animal diversity (Decker and van Holde, 2011). Moreover, it is proposed that the prevailing atmospheric oxygen concentrations may have
played a role in shaping the evolution of oxygen sensing mechanisms
(Taylor and McElwain, 2010), which is mediated by hypoxia inducible
transcription factor (HIF) and acted by prolyl hydroxylases (PHDs).
The HIF/PHD system has been found in basal metazoan and further rened in bilaterians, but is not present in choanoagellates and other
protists, suggesting that it is unique to metazoans (Leonarz et al.,
2011; Rytknen and Storz, 2011). Rising oxygen levels in the atmosphere and oceans could also have had an indirect effect on biological
innovation by increasing the availability of bioessential trace elements
(Anbar and Knoll, 2002).
As for the rise of oxygen level as an environmental trigger for the
Cambrian explosion, the major problem is the lack of precise values
of oxygen levels before and during the diversication of animal
phyla. Geochemical evidence for the rise of oxygen levels during
late Neoproterozoic has accumulated over the past quarter century,
but it is still hard to distinguish atmospheric from oceanic and global
from local redox changes (Shields-Zhou and Och, 2011). According
to sulfur isotope discrimination values, Caneld and Teske (1996) argued that the atmospheric oxygen rose above the 5% present atmospheric level (PAL) during the PrecambrianCambrian transition.
But it is still difcult to determine whether the increase in 34S is
related to higher oxygen levels or instead to intensive bioturbation
(Caneld and Farquhar, 2009). The iron content of sediments shows
that shallow waters were typically well-oxygenated throughout the
later Neoproterozoic(b742 6 Ma) (Caneld et al., 2008), long before
the Cambrian explosion, whereas the deep ocean was anoxic and ferruginous before and during the Gaskiers Glaciation 580 million years ago
and that it became oxic afterward (Caneld et al., 2007; Li et al., 2010). A
more recent study suggested a very late oxygenation of deep seas, since
Cambrian Stage 3 (Wang et al., 2012). The oxygenation of deep sea requires atmospheric oxygen levels above 15% of PAL (Caneld et al.,
2007), while persistent anoxia of the oceans in the Neoproterozoic is argued to require atmospheric oxygen levels below 40% of PAL (Caneld,
2005; Kump, 2008). Therefore, the atmospheric oxygen level was
constrained between 15 and 40% of PAL by late Ediacaran. However,
such estimation based on uniformitarian principles was questioned by
Buttereld (2009). He argued that Precambrian oceans (stratied, turbid anoxic water column dominated by cyanobecteria) were quite
unlike the Phanerozoic counterparts (well-mixed, clear-water system
dominated by eukaryotic algae), and thus deep-sea geochemical signatures were unable to be used as a direct proxy for atmospheric oxygen
levels under such nonuniformitarian conditions (Buttereld, 2009).
It was suggested that erosion of the Gondwanan supermountains
produced more free-oxygen than earlier supercontinent amalgamations

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because the maximum height of the Gondwanan supermountains was

greater (Campbell and Squire, 2010). The advents of large, mobile, and
skeletal animals in early Cambrian may have been contemporaneous
with the further oxygenation of the surface environment (Shields-Zhou
and Och, 2011), but there is a geochemical study showing that the oxygen
content signicantly decreased during early Cambrian (Komiya et al.,
2008). On the other hand, the minimum oxygen requirements for metazoans to support their aerobic metabolism are loosely constrained.
Catling et al. (2005) suggested a quite broad range from 5% to 50% PAL.
The absolute minimum dissolved oxygen content able to support aerobic
metazoans varies from species to species, and is probably impossible to
know for the rst animals of diverse metazoan phyla. Extant marine infaunal and epifaunal metazoans can accommodate dissolved oxygen
dropping to the tens of micromolar in concentration. If these concentrations are extrapolated to equilibrium of the atmosphere with well
mixed cold surface water, they correspond to ~25% PAL (Petsch, 2004).
However, we do not know when oxygen rising above this level, nor do
we have geochemical evidence for a stepwise rise of oxygen levels corresponding to the episodic appearances of bilaterian clades during early
Cambrian. Additionally, we need to know whether a given level of oxygen
might select for a given type of physiology or morphology and whether
such effects might inuence morphological origins, ancestral form, etc.
Therefore, it is difcult to determine whether oxygen is a key threshold
that needs to be crossed for the Cambrian explosion.
Finally, just to be clear, we are sure that oxygen plays important
role in the development of complex, multicellular organisms. But
the widespread distribution of anaerobic biochemistry and anaerobic
mitochondria (mitochondria that are not dependent upon the nal
mediator of an electron transfer to O2) in most eukaryotic supergroups
(including Metazoa), combined with the presence of enzymes with
clear evolutionary links to an anaerobic past, suggests that eukaryotic ancestors evolved in a more anoxic past (see van der Giezen and Lenton,
2012 and references therein). Many extant animals are found to be facultative anaerobes and so are able to live in hypoxic or anoxic conditions
(Budd, 2008). It is amazing that some loriciferans have been found living
in permanently anoxic sediments (Danovaro et al., 2010). The widespread anaerobic pathways across metazoan phylogeny (Mentel and
Martin, 2010) somewhat undermine the claim that rising oxygen levels
were a prerequisite for animal evolution.
2.2. Developmental genes and molecular clock
Development of the animal body plan is controlled by large gene
regulatory networks (GRNs), and the evolution of the body plan depends
on change in the architecture of developmental GRNs over deep time
(Davidson and Erwin, 2006; Davidson, 2010). Therefore, the composition
and structural organization of the GRNs, and their functions and evolutionary changes are fundamental genetic issues to understand the development and evolution of animals (Carroll et al., 2001; Davidson and
Erwin, 2006, 2009; Davidson, 2010). With regard to the Cambrian explosion in this context, key questions are what developmental genes dene
ancestral bilaterians and whether the genes for building morphological
complexity of bilaterian clades were in place before and during the Cambrian explosion. If developmental system of bilaterians was established
before their divergence in the early Cambrian, what account for the
great differences between major metazoan lineages and the long period
of stasis in phylum- and class-level body plans since the early Cambrian?
Of course, it is impossible to directly identify genes of fossil animals, but
we can infer the presence of a specic gene according to the phylogenetic
distribution of developmental genes in animal clades. The analysis requires a robust metazoan phylogeny.
2.2.1. Early hypothesis: evolutionary addition of Hox genes and other
developmental genes
Whole-genome sequences of dozens of metazoans have demonstrated that only a small fraction of all genes in any given animal

901

constitute the toolkit (about 20,000 protein-coding genes) that is devoted to the formation and patterning of body plan and body parts
(Carroll et al., 2001; Erwin, 2009). Among them, Hox genes (anterior/posterior patterning) are the earlier characterized developmental
regulatory genes within and between metazoan phyla (Carroll et al.,
2001). It has been recognized that cnidarians have two denitive Hox
genes and all three major bilaterian lineages (Lophotrochozoa, the
Ecdysozoa, and the Deuterostoma) have seven or eight Hox genes (de
Rosa et al., 1999; Balavoine et al., 2002). Accordingly, it can be inferred
that the common ancestor of Cnidaria and Bilateria most likely has only
two Hox genes, and the last common ancestor of bilaterians (Urbilateria)
possesses at least seven Hox genes (Carroll et al., 2001). Apparently,
several new Hox genes arose before the radiation of bilaterian phyla. It
has also been recognized that the Hox gene cluster is just a small part of
an upstream-downstream cluster of genetically determined interactions
that specify morphology (Carroll et al., 2001; Levinton, 2001; a more
complete list in Erwin, 2009). Therefore, many workers suggested that
the establishment of the bilaterian developmental system, including the
expansion of Hox genes, is a primary cause of the Cambrian explosion
(e.g., Valentine et al., 1996; Peterson and Davidson, 2000; Valentine,
2001; Erwin and Davidson, 2002). However, the increase in the number
of Hox genes and other genes is not necessary to increase morphological
complexity. The evolution of form is not so much about what genes you
have, but about how you use them, because the genetic toolkit may be
untapped for a considerable length of time (Carroll, 2005). On the other
hand, the analyses of sponge gene repertoire show that the genomic
complexity of the common ancestor of bilaterians, at least in terms of
gene content, was already present in the common ancestor of all metazoans (Harcet et al., 2010; Adamska et al., 2011). Therefore, it is likely
that the establishment of animal GRNs coincided with the origin of animal multicellularity, and hence is long before the fossil diversication of
bilaterian lineages in the early Cambrian (see discussion below).
2.2.2. Gene regulatory networks and microRNAs
A great advance in developmental biology relevant to our discussion
here is the discovery that developmental regulatory genes (including a
variety of transcription factor genes, the components of the big ve
signaling pathways, as well as cell adhesion molecules) are not only
present across the animal kingdom, but the regulatory networks they
form appear conserved between animals as distantly related as fruit
ies and vertebrates. A variety of transcription factors (that regulate
the expression of many other genes), signaling pathway genes (that mediate short- and long-range interactions between cells) and other regulatory elements once thought to be characteristic of bilaterians, have
been documented in basal metazoans (sponges, cnidarians, placozoans)
and choanoagellates (nearest sister group to the Metazoa) (Larroux
et al., 2006; Erwin, 2009; Adamska et al., 2011). In fact, virtually all of
the bilaterian developmental regulatory genes are also present in
sponges and cnidarians. Therefore, the last common ancestor of all metazoans was strikingly complex in genetic composition (Harcet et al., 2010;
Adamska et al., 2011), albeit its morphology might be as simple as the
earliest branching metazoans, e.g. sponges. The morphological complexity of the Urbilateria (the common ancestor of bilaterians) is contentious
(Bagu and Riutort, 2004), in a large part, due to different phylogenetic
placement of the acoels, varying from basal bilaterians (Bagu and
Riutort, 2004; Bagu et al., 2008; Hejnol and Martindale, 2008) to
secondarily simplied lophotrochozoans (Adoutte et al., 2000) or deuterostomes (Philippe et al., 2007, 2011). In the more complex scenarios
(e.g. Carroll et al., 2001; Balavoine and Adoutte, 2003), the Urbilateria
not only possessed the developmental systems, but the complex morphologies that they produce in modern organisms (Fig. 2), minimally
including the following: anterior/posterior patterning (seven or eight
Hox genes and associated microRNAs, the ParaHox and NK cluster
genes), dorsal/ventral patterning (sog/chordindpp/BMP2/4 system),
a tripartite brain (specic anterior patterning genes ems/Emx and
otd/Otx), segmentation (engrailed and Delta-Notch), eyes (Pax6 and ey),

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X. Zhang et al. / Gondwana Research 25 (2014) 896909

Fig. 2. Deep and shallow models for the divergence of bilaterian lineages. In the deep divergence model (left), the Acoelomorpha is considered as secondarily simplied deuterostomes or lophotrochozoans, and thus the Urbilateria, corresponding to the protostomedeuterostome ancestor (PDA), is morphologically complex. Shown in dark color is the
known fossil record of each of the three bilaterian lineages. In the shallow divergence model (right), many of developmental toolkit genes and regulatory networks may have
remained untapped for a considerable length of time, and the Acoelomorpha is placed in the basal bilaterians, and thus the Urbilateria is far simpler than the PDA. Numbers 14
in the age column representing the rst four stages of the Cambrian System.

endoderm and regionalized gut (GATA transcription factors, brachyury

and goosecoid), heart (Nkx2.5/tinman), appendages (distal-less) (Carroll
et al., 2001; Hejnol and Martindale, 2008; Erwin, 2009). In the alternative
scenario, the Urbilateria resembling acoelomorph atworms was likely to
be a small, unsegmented, planula-like organism with blind digestive
system, far simpler morphologically than the protostomedeuterostome
ancestor (PDA) despite possessing a nearly complete eubilaterian genome (Hejnol and Martindale, 2008) (Fig. 2), but anterior/posterior and
dorsal/ventral patterning inescapable.
Another advance important for our understanding the Cambrian
explosion is the recognition that developmental GRNs have a modular
and hierarchical organization (Davidson and Erwin, 2006). They consist
of assemblies of multigenic subciruits of various forms. The subcircuits
that perform essential upstream functions in building a given body
part, termed the kernels of the GRN, are evolutionarily conserved in
all descendants of the lineages. It was argued that there should exist
clade-specic kernels that dene the body plan of each clade at different
high-rank taxonomic levels, i.e. superphylum, phylum, and class levels
(Davidson and Erwin, 2006, 2009; Davidson, 2010). The conservation
of the clade-specic kernels results in developmental or phylogenetic
constraints, and hence provides a developmental explanation for the
long-term stability of phylum- and superphylum-level body plans since
the Cambrian explosion (Davidson and Erwin, 2006, 2009). Because
major metazoan body plans occurred during the early Cambrian and almost all innovations thereafter have been at subphylum level (Shu et al.,
2014-in this issue), phylum- and superphylum-level kernels must have
originated before or during the Cambrian explosion (Davidson and
Erwin, 2006, 2009).
Since the basic developmental genes are broadly shared among all
metazoans, the marked morphological differences between metazoan

lineages does not depend on the absence or presence of certain genes

but on differences in the temporal and spatial deployment of these
genes and their regulation (Erwin, 2007; Erwin et al., 2011). The evolution of the developmental GRNs is largely the process of assembly,
reassembly, and redeployment of subcircuits (Davidson, 2010). If
the developmental GRNs required to build bilaterian body plans was
established before their divergence (see below), what mechanisms account for the increasing morphological complexity during the metazoan
evolution. It has been assumed that the morphologic complexity corresponds to the number, depth, and subcircuit diversity of the developmental GRNs. Early metazoans may have been associated with developmental
GRNs of less complexity, shallower depth, and fewer subcircuits, and
with a less hierarchically structured regulatory network (Davidson
and Erwin, 2009), and hence were less complex. Subsequently, developmental genes providing spatial, temporal, and homeostatic control
were continuously inserted into preexisting simpler dGRN subcircuits
(Davidson and Erwin, 2010).
For example, the continual evolutionary addition of microRNAs
tracks increasing morphological complexity. MicroRNAs affect the
translation of target messenger RNAs, ultimately contributing to the
maintenance of cellular homeostasis and cellular identity and to the
robustness of developmental programs. Much of the messenger RNA
toolkit was acquired before the evolution of bilaterians, whereas
microRNAs were continuously added to metazoan genomes through
time with very little secondary loss in most clades. Losses and gains
of microRNAs are respectively corresponding to secondary simplications and increases of complexity in morphology (Philippe et al., 2011).
It is, therefore, likely that the increasing morphological complexity during the evolution of bilaterian lineages resulted from an accumulation
in the number and diversity of dGRN subcircuits through time, including

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903

the continued and hierarchical incorporation of microRNAs into these

networks in a lineage specic manner (Peterson et al., 2009; Erwin
et al., 2011). MicroRNAs might be instrumental in the canalization of
development and ultimately allow for natural selection to elaborate
morphological complexity (Peterson et al., 2009; Berezikov, 2011).
Hence, microRNAs might play an important role in shaping metazoan
macroevolution, and might be part of the solution to the increasing morphological complexity of metazoan lineages during Cambrian explosion
(Peterson et al., 2009).
2.2.3. Deep or shallow divergence?
It is now clear that the developmental GRNs were established before the divergence of bilaterian clades. The presence of many developmental genes of bilaterians in morphologically simpler organisms
reinforces the suggestion that the original role of these genes and
regulatory networks was in the formation of specialized cell types
in specic regions of the body, not necessarily in producing complex
morphology (Erwin and Davidson, 2002). Therefore, the advent of
developmental genes was a necessary but not sufcient component
for the Cambrian radiation of bilaterian lineages (Erwin et al., 2011).
Then, what is the genetic basis underlying the morphological diversication of bilaterian forms? The key issue lies in the timing and level
of gene expression.
The earlier molecular estimates using hemoglobins suggest that
the initial radiation of the animal phyla occurred at least 9001000 Ma
ago (Runnegar, 1982c). Subsequent estimates of metazoan divergence
times based on molecular clock vary as new studies are reported, from
several hundred million years before the Cambrian explosion to close
to the base of the Cambrian (see Blair, 2009 for a complete review).
Some younger dates were thought to be affected by signicant methodological biases (Blair, 2009). The most recent molecular dating study
(Erwin et al., 2011) suggests that the common ancestor of all metazoans
arose about 800 Ma, the split between protostomes and deuterostomes
occurred at around 680 Ma, and stem lineages leading to most extant
bilaterian clades had evolved by the end of the Ediacaran. However,
most crown group bilaterian phyla were estimated to be diverged during
the late Ediacaran through the Cambrian period, largely consistent with
the fossil record (Erwin et al., 2011). The phylogenetic distribution of
different oxygen transport proteins (OTPs) (hemocyanin, globin and
hemerythrin), a prerequisite for development of shells or hard carapace,
also indicates an early divergence of bilaterian clades, with OTPs evolved
before the appearance of shelly fossils but after the divergence of phyla
(Decker and van Holde, 2011). The molluscan hemocyanin evolved
700 Ma ago (or earlier), and the origin of arthropod hemocyanin was
estimated between 600 and 700 Ma.
The deep divergence of bilaterian phyla, at least in stem lineages,
is supported by a majority of molecular clock studies, but it is suffering from a couple of challenges. First, the cold climate during late
Cryogenian was unfavorable for animal diversication. Second, it is
not clear whether oxygen content was sufcient for bilaterians by
the Cryogenian. The greatest challenge is the paucity of bilaterian fossils in this period, completely absent before the Gaskiers Glaciation.
Possible animal embryo fossils from the Ediacaran-aged Doushantuo
Formation (Fig. 3A) were recently reinterpreted as non-metazoan
Holozoa (Buttereld, 2011; Huldtgren et al., 2011). Most putative
metazoans from the Ediacara-type biotas are very likely within the
scope of cnidarian-grade organisms below the split of protostomes
and deuterostomes (Erwin, 2009), except for Kimberellomorpha,
which are possible molluscans commonly associated with radiating
trace fossils (Fedonkin, 2003). Trace fossils are widely accepted as
strong evidence for the presence of bilaterian animals in the Ediacaran,
whereas the bilaterian nature of early trace fossils has been questioned
by the nding that large amoeboid protists leave macroscopic traces at
the bottom of the deep ocean (Matz et al., 2008). The oldest putative
evidence of bioturbation by bilaterians is ca. 555 Ma in age (Rogov
et al., 2012), signicantly younger than most molecular clock ages. The

Fig. 3. A. An embryo fossil from the Ediacaran Doushantuo Formation of South China,
but recently reinterpreted as nonmetazoan holozoans; B. Kimberella, widely accepted
as a bilaterian in the Ediacaran.

only relatively convinced bilaterian body fossil is the Kimberellomorpha

(Fig. 3B), coeval with the oldest known bioturbation. However, a
small group makes neither diversity nor disparity. The most commonly attempted explanation is that early bilaterians were small
and soft-bodied, and thus escaped the fossil record, while microscopic fossils of protists and prokaryotes have been recognized
back to Archean and Lagersttten of macroscopic soft-bodied fossils
have been known since the Ediacaran. Another possibility is that
early bilaterians were ecologically insignicant and thus quite rare.
In any case, the deep divergence of bilaterians can only be testied
by the discovery of diverse bilaterian body fossils before and during
the Ediacaran period.
Alternatively, many genes and subcircuits of the GRNs that underlie the building of body plans may have remained untapped over hundreds of millions of years. Basal metazoan phyla morphologically
diverged during late Ediacaran and bilaterian phyla diversied during
early Cambrian, as is indicated by the fossil record (Shu et al., 2014-in
this issue). The Urbilateria might be complex in genetic makeup but
small and simple in morphology. This shallow divergence model
(Fig. 2) is, however, supported by a minority of molecular studies. Perhaps, till early Cambrian oxygen levels and other environmental factors (e.g. Ca2+ concentrations in seawater) crossed a critical threshold
and favorable ecosystems were well established, thereby causing widespread biomineralization and increase in morphological complexity,

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body size, diversity, and disparity among bilaterian lineages. This model
is approximately reconciled with the paleontological data, but unequivocal metazoan body fossils are still rare during the Ediacaran. There is
another challenge to this view. Early Cambrian animals were considerably diverse and complex in morphology. It is hard to imagine how all of
these could have sprung forth from a single ancestor in a brief period
from ca. 550 to 520 Ma.
Nevertheless, the bilaterian developmental GRNs were established
before the diversication of body plans. When Kimberella was accepted
as a true bilaterian (Fig. 3B), then the establishment of developmental
system predated the Cambrian explosion by at least 10 Ma. The developmental system, which enabled divergence of bilaterian body plans, is a
prerequisite but not sufcient for the Cambrian explosion (Marshall,
2006; Erwin et al., 2011). If the invention of toolkit genes per se was
not the trigger for the Cambrian explosion, then what was? It is becoming increasingly appreciated that the Cambrian explosion was an ecological phenomenon and environmental triggers are indispensable.
2.3. Ecological causes
Since environmental changes during the close of the Proterozoic
and opening of the Phanerozoic form the essential backdrop of the
Cambrian explosion, and the genetic complexity was very likely
established long before the construction of metazoan-dominated
ecosystem (see above discussion), ecological explanations are now
looking up (Carroll, 2005; Conway Morris, 2006; Budd, 2008; Erwin
et al., 2011; Erwin and Tweedt, 2012). Many workers considered the
Cambrian explosion as an ecological phenomenon, consisting largely
of a cascade of knock-on events that emerged from multicellularity
and mobility (e.g. Budd, 2008). Once the rst animal appeared the interactions between different types of organisms and with environments
would lead to more complex ecologies. The complex ecologies were
subject to both continuing expansion and feedback, thereby resulting
in the evolution of metazoan-dominated ecosystem since early Cambrian (Conway Morris, 2006). Many ecological hypotheses have been proposed as drivers, but none can satisfy geological, paleontological and
molecular records. Some theories are well suited to explaining why
there was a rapid increase in both disparity and diversity, but they
fail to explain why the explosion happened when it did (Marshall,
2006). Some even considered consequences as causes, e.g. increase in
bioturbation and advent of macrophagous predators, thus falling into
a trap of chicken-and-egg problem.
2.3.1. Extinction of Ediacaran biotas
In the history of metazoan evolution the most signicant episodes
of adaptive radiation often have been preceded by mass extinction
events. Extinction events can remove ecologically dominant species,
making the resources they had utilized available to surviving species.
Many clades diversied rapidly after mass extinction events, the most
famous case being the diversication of many mammal and bird clades
after the end-Cretaceous extinction event (Losos, 2010). Therefore, the
extinction of Ediacaran macrobiotas (Narbonne, 2005) and Cloudina
Namacalathus assemblage (Amthor et al., 2003) could open up new possibilities for metazoans in the same way the extinction of the dinosaurs
opened the way for mammals (Knoll and Carroll, 1999; Amthor et al.,
2003). However, as was noted by Marshall (2006) and Erwin et al.
(2011), standard models of adaptive radiation involved diversication
from pre-existing clades (e.g. the evolution of land vertebrates) and
cannot explain the polyphyletic nature, morphological and ecological
breath, or the extended duration of the Cambrian explosion.
2.3.2. Cropping
This ecological theory was developed by Stanley (1973, 1976). It
was argued that Precambrian systems were self-limiting in terms
of diversication because of systems in the absence of cropping by
herbivores; when advanced heterotrophy arose, it would initiate

self-propagating feedback systems of diversication; thus, the nearly

simultaneous origin and explosive radiations of heterotrophic protists, metaphytes, and metazoans were inevitable. This theory could
explain the increase in diversity under the inuence of cropping,
but it was not directed against the uniqueness of the Cambrian explosion in terms of timing and nature. The Cambrian explosion is far
more than the increase in biodiversity. Furthermore, heterotrophic protists evolved much earlier (Porter, 2011), and herbivorous metazoan
fossils (e.g. Kimberella) were present in Ediacaran biotas (ca. 555 Ma).
Why were occurrences of bilaterian clades delayed?
2.3.3. Phytoplanktonzooplankton diversication
Phytoplankton comprises the vast majority of production in modern
marine ecosystems. Most large animals are unable to graze directly on
even relatively large net phytoplankton (2200 m). It is the zooplankton that links the microscopic world of marine primary productivity to
the macroscopic world of large animals by repackaging unicellular
phytoplankton as nutrient-rich particles some 10100 times as large.
Therefore, repackaging effected by herbivorous mesozooplankton
(0.220 mm) represents a key link in marine metazoan food chains
(Buttereld, 1997, 2001). The phytoplankton (acritach) underwent a
major diversication in the early Cambrian, in marked parallel with
the Cambrian radiation of metazoans. Prior to the evolution of planktic
metazoans, oceans would have been dominated by picoplankton
(0.22 m) (Buttereld, 2009). This sudden diversication might
have stimulated the diversication of zooplankton, which in turn
might stimulate the evolution of large metazoans through food supply. However, the ecological signicance of zooplankton during early
Cambrian is unclear because zooplankton fossils of this age are quite
sparse (Buttereld, 1997, 2001; Vannier et al., 2007). In addition, as a
component of the Cambrian explosion, the diversication of acritarchs
may also require a trigger. It was suggested that the early Cambrian expansion of animals into the water column might have been responsible
for driving the evolution of large net-phytoplankton (Buttereld, 2009).
So a chickenegg problem arises. Did the diversication of phytoplankton cause the evolution of zooplankton, which in turn stimulated the
radiation of animals? Or, alternatively, did the ecological expansion of
planktic metazoans cause the increase of net-phytoplankton in size
and diversity? We here adopt a simpler solution, considering the diversication of phytoplankton as a consequence, rather than a cause of the
Cambrian explosion.
2.3.4. Bioturbation
The Cambrian explosion is not only manifested by explosive radiation of bilaterian phyla in the early Cambrian but also exhibited by
substrate revolution during the EdiacaranCambrian transition, which
resulted from advents of burrowing bioturbation penetrating into the
depths of sediments (Seilacher and Pger, 1994; Bottjer et al., 2000).
It is, therefore, assumed that bioturbation had a key role in the evolution
of early metazoan life (Meysman et al., 2006). The Ediacaran seaoor
sediments had well-developed microbial mats and poorly developed
vertically oriented bioturbation. The microbially-bound substrates (also
known as matgrounds) produced a fairly stable and sharp water
sediment interface, and thus had little interaction with bottom water.
The early Cambrian seaoor sediments, referred to as mixgrounds,
were heavily bioturbated by burrowing organisms, resulted in ventilation of the sediments, and a change in redox gradients. This substrate
revolution was suggested to have signicant evolutionary and ecological
impact (Bottjer et al., 2000). Accordingly, it was assumed that benthic
faunas had to adapt to the newly emerging bioturbated mixgrounds,
thereby triggering the Cambrian explosion (Thayer, 1979; Bottjer et al.,
2000; Meysman et al., 2006). In contrast, it was also suggested that the
infaunal habits were a strategy to escape the new menace of predation
(Seilacher, 2007). No doubt the ecological effect of bioturbation is profound (Thayer, 1979; Meysman et al., 2006; Erwin and Tweedt, 2012).
However, the substrate revolution required infaunal bioturbators to

X. Zhang et al. / Gondwana Research 25 (2014) 896909

destruct the matgrounds. Therefore, the chicken-and-egg problem arises

again (Levinton, 2001). Did the Cambrian explosion cause the substrate
revolution or did the Cambrian substrate revolution drive the diversication of bilaterian clades (including bioturbators)? It is evident that the
advent of bilaterian bioturbators is a consequence rather than a cause.
2.3.5. Advent of macrophagous predation
The predatorprey pressure is the most commonly proposed ecological trigger for the Cambrian explosion (Evans, 1912; Hutchinson,
1961; Vermeij, 1990; Bengtson, 2002; Peterson et al., 2005; Erwin
et al., 2011). The rise of predation would cause rapid natural selection
for increasing body size, developing novel defensive mechanisms
such as biomineralized shells or developing new structures or capabilities that allowed movement into new habitats (Levinton, 2001;
Erwin et al., 2011). The rise of microphagous, single-celled predators
in the mid-Neoproterozoic might have been responsible for the appearance of biomineralized skeletons in protists ca. 750 Ma ago
(Porter, 2011), but it surely did not trigger the widespread biomineralization in metazoans, most likely because animals were not around
at this time. Therefore, it appears reasonable to assume that the advent
of macrophagous predators near the end of the Neoproterozoic stimulated the spectacular radiation of animals (Peterson et al., 2005),
while the fossil evidence for the presence of macrophagous predator
at this time is uncertain. The boring holes preserved in Cloudina (an
Ediacaran skeletonized tubular fossil) were commonly considered to
be predatory traces (Bengtson and Yue, 1992; Bengtson, 2002; Hua
et al., 2003), but they are also likely nonpredatory in origin because
many microbial borers are capable of drilling holes. Body fossils that
are likely macrophagous predators did not occurred until the early
Cambrian. The protoconodonts, rst appeared in the Fortunian Stage
(Kouchinsky et al., 2012), were interpreted as teeth and grasping spines
of chaetognaths (Szaniawski, 2002), hence representing the earliest
known candidates of bilaterian predators. The denite large predators,
e.g. anomalocaridids (Fig. 4E, F) made their rst appearance in the
Cambrian Stage 3 (ca. 520 Ma), signicantly postdating the metazoan biomineralization. At present there is no fossil evidence for
macrophagous predators prior to the early Cambrian. Therefore, it
was assumed that the origin of animal predation was driven by increased
oxygenation because the predation was a metabolically expensive feeding strategy (Erwin et al., 2011). Again, the advent of macrophagous
predators still requires a trigger. Since predators stand high above primary consumers in the trophic level, it is reasonable to assume that their invasion lagged behind. Apparently, the establishment of predatorprey
relationships is an essential component of the Cambrian explosion but
not an ecological trigger.
2.3.6. Roughening of tness landscapes
This hypothesis applied the concept of tness landscapes from genetics to the morphogenesis (Marshall, 2003, 2006). Computer simulations demonstrated that the roughening of tness landscapes could
led to increases in diversity and disparity of land plants, not necessarily requiring new developmental genes (Niklas, 2004). The roughness
is controlled by the number of needs the organism must satisfy
(Niklas, 1994, 1997, 2004) rather than the degree of interaction
between the genes, as is the case of the genetic tness landscapes
(Kauffman, 1993). However, the organisms' needs are often frustrated,
which lead to conicting solutions, so that the overall optimal design for
an organism is rarely achieved (the principle of frustration) (Marshall,
2006). Therefore, it is the degree of frustration that determines the
roughness of a tness landscape (corresponding to diversity and disparity), i.e. the tness landscapes are roughening as the number of frustrated needs is increasing. The Ediacaran biotas had very few bilaterians,
showing rather smooth tness landscapes (Marshall, 2006, g. 3). On
the contrary, the Early Cambrian faunas contained some 20 bilaterian
body plans, showing very rough landscapes (Marshall, 2006, g. 3). Accordingly, Marshall (2006) suggested that roughening was the primary

905

driver of the Cambrian explosion. This theory nicely depicted the

EdiacaranCambrian evolutionary transition and provided a good
explanation of body plan diversication without invoking the invention of toolkit genes. However, it invoked ecological interactions between organisms, especially the arm race (predation pressure), as a
roughening mechanism, which stated: there were myriad predators
to contend with, and a myriad number of ways to avoid them, which
in turn led to more specialized ways of predation as different
species developed different avoidance strategies, etc. Therefore,
this hypothesis suffers from the same problem as the predatorprey
hypothesis (see above). Simply, the roughening of tness landscapes
in the early Cambrian is a consequence of evolution.
2.3.7. Geospherebiosphere feedbacks
This hypothesis is based on Earth system model for the long-term
carbon cycle by introducing three different types of biosphere: prokaryotes, eukaryotes, and complex multicellular life, each are characterized by different global temperature tolerance windows. It argued
that the nonlinear feedback between temperature dependent productivity of complex multicellular life and their biotic enhancement of
silicate weathering could led to the temperature drops to the optimum value of 15 C for complex multicellular life productivity by
ca. 540 Ma ago. It was, therefore, assumed that the Neoproterozoic
Snowball Earth events might have initiated an earlier appearance
of complex multicellular life, and the Cambrian explosion might be
mainly driven by extrinsic environmental causes, i.e., a gradual cooling
of the Earth (von Bloh et al., 2003). Apparently, this hypothesis did not
touch the essence of the Cambrian explosion. In addition, there is no
geological evidence for such a cooling event. At least one study suggested that Earth's surface temperatures declined dramatically in the
Paleoproterozoic and values similar to those of the Phanerozoic were
reached by 1.2 Ga (Knauth, 2005).
2.3.8. Ecosystem engineering
Ecosystem engineering refers to modication of the abiotic environment by a species that strongly affects other organisms by creating, modifying or destroying the niches of other species (Jones et al., 1994, 1997;
Wright and Jones, 2006; Erwin and Tweedt, 2012). Ecosystem engineering organisms interact nonlinearly and generate positive feedbacks that
enhance diversity (Altieri et al., 2010). Erwin and Tweedt (2012) analyzed the role of positive ecological feedbacks during the Ediacaran
Cambrian transition based on the rst appearance and generic diversity
patterns of various metazoan clades, and their results revealed that the
feedback substantially increased during the early Cambrian, principally
through bioturbation (ventilating the sediment), sponge pumping
(modifying chemical condition of water column) and the appearance
of a number of structural engineers, e.g. archaeocyathid reefs (enhancing
the habitat complexity). Therefore, they suggested that the ecological
expansion during early Cambrian was driven, at least partly, by ecosystem engineering (Erwin et al., 2011; Erwin and Tweedt, 2012). However,
as was noted by the authors, it is presently difcult to determine whether
the expansion of ecosystem engineering was merely a component of the
establishment of metazoan-dominated marine ecosystems or it was a
signicant driver of this event (Erwin and Tweedt, 2012). Moreover,
the Cambrian explosion involves not only infaunas but also epifaunas.
The increase of bioturbation and the appearance of archaeocyathid structure engineers (Fig. 4D) in the early Cambrian are better understood as
consequences of the Cambrian explosion. But we agree with Erwin and
Tweedt (2012) that ecosystem engineering during Ediacaran, in spite
of small degree, might be crucial for the Cambrian explosion, particularly
engineering effects of sponges because they denitely appeared in the
Ediacaran period (Fig. 4AC) (Gehling and Rigby, 1996; Clites et al.,
2012). However, sponge fossils are actually rare in the Ediacaran period.
Their engineering effects are thus somewhat speculative because ecological feedbacks need abundance.

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X. Zhang et al. / Gondwana Research 25 (2014) 896909

Fig. 4. AC. An Ediacaran sponge as important ecosystem engineering organisms during the Ediacaran Period; A. Entire sponge body; B. Detail view of spicular impressions in the
rectangular region of A; C. Holdfast on the sole; D. Archaeocyathids of a bioherm from the lower Cambrian of South China, as a important structural engineer; E and F. Frontal
appendage (E) and gastric mills (F) of anamalocaridids from the Chengjiang biota, the most famous predators in early Cambrian.

3. Conclusions
Both the fossil record and molecular results suggest that the basic
developmental system of bilaterian animals was in place in the
Urbilateria at least 555 Ma ago, whether the Urbilateria was complex
or simple in morphology. The GRNs that control the development of
an animal are broadly shared among metazoan lineages. It may be
that the assembly, reassembly, and redeployment of subcircuits of
the GRNs are responsible for the morphological diversication of
bilaterian clades. Since the developmental prerequisites already
existed in the ancestral taxon, the Cambrian explosion still requires
environmental triggers (Gould, 2002). The oxygenation and change
of seawater composition are the most commonly proposed environmental triggers, particularly the oxygenation which allow the most
components of the Cambrian explosion, such as the increase in body
size, widespread biomineralization, and metabolically expensive
ecological strategies (e.g. burrowing and predation). The oxygenation
associated with the Snowball Earth may cause the explosive diversication of complex multicellular organisms as is exhibited by the early
Ediacaran macrobiotas, and the subsequent stepwise increase in
atmospheric oxygen levels that linked to the weathering of the
trans-Gondwana mountains nally caused the Cambrian explosion.

The change of seawater composition, e.g. the increase in Ca2 + concentration, may also contribute to widespread biomineralization in
metazoan lineages. The Cambrian explosion itself, at least in part,
is an ecological expansion of bilaterian lineages, thus the ecological
feedbacks initiated by this event cannot be invoked as ecological
triggers. However, the positive feedback of Ediacaran ecosystem,
particularly by the sponge engineering, may contribute to the formation
of well-mixed, clear-water system typical of Phanerozoic oceans, and
thus paved the way for the Cambrian explosion. But the potential feedback of sponges is challenged by the rarity of sponge fossils in the
Ediacaran period. In a ward, the Cambrian explosion may have been
triggered by environmental perturbation near the EdiacaranCambrian
boundary and subsequently amplied by ecological interactions within
reorganized ecosystems (Knoll and Carroll, 1999).
4. Outlook for future research
If the Cambrian explosion was the ecological expansion of bilaterian
clades, a number of bilaterian ancestral groups including Urbilateria may
have existed at least in the late Ediacaran, regardless of deep or shallow
divergence. This inference can be made by analogy with the evolution of
vertebrates: birds and mammals became ecologically signicant sine

X. Zhang et al. / Gondwana Research 25 (2014) 896909

Cenozoic but their ancestor appeared in Triassic and Jurassic. Ancestors

of early Cambrian faunas are most likely found in exceptional preservations in the late Ediacaran even if they were small or soft-bodied. In
China and other parts of the world, the Burgess Shale-type Lagersttten
and phosphorous chert deposits are well known for exquisitely preserved soft-bodied fossils and microorganisms. Therefore, searching
for ancestors of early Cambrian faunas in exceptionally preserved fossil
beds is a major task for our future paleontological work.
Environmentally, oxygenation and change of seawater composition
appear more closely relevant to the Cambrian explosion. However, precise data are still lacking. The increase in atmospheric oxygen level during the EdiacaranCambrian transition was suggested by the tectonic
events at this period, but yet to be conrmed by geochemical studies.
It is unclear when the oxygen level crossed the threshold that minimally
meets the demand of large animals. Changes of oceanic salinity and
concentrations of many important ions (e.g., Ca, Mg and trace metals)
during the critical time interval are also working targets of our geochemical colleagues.
Acknowledgments
We are grateful to Shigenori Maruyama and Yukio Isozaki for organizing this special issue and three anonymous reviewers for critical
comments. Financial supports by the Major Basic Research Project of the
Ministry of Science and Technology of China (Grant: 2013CB835002),
the Natural Science Foundation of China (NSFC, Grants: 40925005,
41272036), and the Sanqin Scholarship project of the Shaanxi Authority are greatly acknowledged.
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909
Xingliang Zhang is a professor at the Department of Geology,
Northwest University (NWU), and serves as Vice-Chairman of
the International Subcommission of Cambrian Stratigraphy,
ICS. He received his Ph.D. in Paleontology and Stratigraphy
from NWU. He also worked as a Humboldt Research
Fellow at University of Gttingen, Germany, and a postdoctoral research fellow at National Museum of Natural History,
Smithsonian Institution, USA. He is a section editor for Encyclopedia of Geobiology, and author of the textbook, Lecture
Notes of Geobiology. His current research interests include
the evolution of animals during the Cambrian explosion,
and microbial contributions to rocks and minerals.

Degan Shu is Distinguished Professor of Evolutionary Paleobiology at Northwest University, China. He received
his undergraduate training in Paleontology at Beijing University, and Ph.D. from China University of Geosciences
(Beijing). His research mainly focuses on evolution of early
deuterostomes. He discovered the rst sh in life history
and erected the Phyla Vetulicolian. As a member of Chinese Academy of Science and recipient of National First
Grade Award of Natural Science, he has authored a dozen
of publications in Nature and Science.

Jian Han is an associate professor at the Department of

Geology, Northwest University. Here he obtained his Ph.D.
He also worked as a visiting scholar at Gttingen University,
Germany. He has 17 years experience in the study of the
Cambrian Chengjiang fauna in Yunnan Province, China.
His main research interests include priapulid worms and
deuterstomes from the Chengjiang fauna. His recent work
centered on the fossil cnidarian embryos from the early
Cambrian Kuanchuanpu Formation, Shaanxi Province, China.

Zhifei Zhang is a Professor of Paleontology in the Department of Geology in Northwest University, Xi'an, China. He
received his Bachelor's from Life Science College and
Master's and Ph.D. from the Department of Geology, both
in Northwest University, China before he nished oneyear postdoctoral visiting study at faculty of Earth Science
in Uppsala University, Sweden. He is interested in the evolution of Cambrian Burgess Shale type soft-bodied faunas.
His research is focused on exceptionally preserved brachiopods and other lophotrochozoan fossils.

Jianni Liu is a professor at Northwest University, China.

She obtained her Ph.D. in Paleontology and Stratigraphy
from NWU. She worked as a Humboldt Fellow at Free University, Germany. Her research interests center around the
co-evolution of the Cambrian explosion and environments,
especially focus on the origin and diversication of the
lobopodians and arthropods from the early Cambrian
Chengjiang Lagersttte. She reported an armored lobopodian
walking cactus in Nature as a cover paper. This nding was
selected as Top ten Scientic Progress in Universities of
China in 2011, and the walking cactus was chosen as Top
ten new species award in 2012 by International Institute
for Species Exploration.

Dongjing Fu is a lecturer at the Department of Geology in

Northwest University, China, where she obtained her Ph.D.
in Paleontology and Stratigraphy. She also worked as a visiting scholar in Uppsala University, Sweden. Her principal
research interests revolve around the so-called Cambrian
explosion of some 521 million years ago. Her studies on
the origin and early evolution of arthropods are largely
based on exceptionally preserved fossils from the Cambrian Chengjiang, Sirius Passet, Emu Bay Shale and Burgess
Shale Lagersttten, etc.