Gondwana Research 25 (2014) 896–909

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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 a b s t r a c t

Article history: Abrupt appearance of major bilaterian clades in the fossil record during the first three stages of the Cambrian Period
Received 30 August 2012 has puzzled the scientific world since 1830s. Many proposed causes including environmental, developmental, and
Received in revised form 9 May 2013 ecological hypotheses, are reviewed. Nutrient availability, oxygenation, and change of seawater composition are
Accepted 2 June 2013
commonly supposed to be environmental triggers. The nutrient input, e.g. the enrichment of phosphorus in an en-
Available online 19 June 2013
vironment, would cause excess primary production, but it is neither directly linked with diversity nor disparity.
Keywords:
Fluctuating abiotic conditions during the Snowball Earth and the associated oxygenation event may have stimulat-
Animal evolution ed the diversification of complex multicellular organisms including diverse of macroscopic and morphologically
Ecology differentiated algae in the early Ediacaran, but did not lead to the ecological success of metazoan or bilaterian line-
Genetics ages. Further increase of oxygen level and change of seawater composition just before and during early Cambrian
Environment are suggested by the high weathering rate of the trans-Gondwana mountains, Great Unconformity, and decline
Cambrian explosion of oceanic salinity. These are potential candidates of environmental triggers for the Cambrian explosion but require
future more detailed geochemical studies to confirm. 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-specific 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 geosphere–biosphere feedbacks) cannot explain the uniqueness of the
event, some others (such as Cambrian substrate revolution, predator–prey pressure, evolution of zooplankton,
and roughening of fitness 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 Ediacaran–Cambrian transition.
© 2013 International Association for Gondwana Research. Published by Elsevier B.V. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 897
2. Hypothetical triggers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 897
2.1. Environmental triggers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 897
2.1.1. Tectonic backdrop . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 898
2.1.2. Aftermath of the Snowball Earth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 899

⁎ 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
 X. Zhang et al. / Gondwana Research 25 (2014) 896–909 897

2.1.3. True polar wander . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 899

2.1.4. Seawater composition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 899
2.1.5. Rise of oxygen levels . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 900
2.2. Developmental genes and molecular clock . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 901
2.2.1. Early hypothesis: evolutionary addition of Hox genes and other developmental genes . . . . . . . . . . . . . . . . . . . . 901
2.2.2. Gene regulatory networks and microRNAs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 901
2.2.3. Deep or shallow divergence? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 903
2.3. Ecological causes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 904
2.3.1. Extinction of Ediacaran biotas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 904
2.3.2. Cropping . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 904
2.3.3. Phytoplankton–zooplankton diversification . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 904
2.3.4. Bioturbation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 904
2.3.5. Advent of macrophagous predation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 905
2.3.6. Roughening of fitness landscapes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 905
2.3.7. Geosphere–biosphere feedbacks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 905
2.3.8. Ecosystem engineering . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 905
3. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 906
4. Outlook for future research . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 906
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 907
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 907

1. Introduction
The Cambrian explosion is a long standing macroevolutionary
issue, which has been puzzling paleontologists and evolutionary biol-
ogists 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 first 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 significant 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 first 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 significantly before the beginning of the Cambrian. Thus, the Cam-
brian 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 di-
versified 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 first 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 morpho-
logical 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 molec-
ular diversification 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
suggesting that the major animal clades diverged many tens of millions
of years before their first 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 mo-
lecular 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 ex-
plosion is largely an ecological phenomenon, including the increasing
of body size and morphological complexity, and widespread biomin-
eralization among animals.
However, the exact causality has not yet been established, al-
though 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 (1–2) 2008 and this volume.
The cooperative project will be continued in the next five years. There-
fore, 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 finally 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 envi-
ronment 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 oxygen-
ation 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) 896–909

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 1–4 in the age column representing the first four stages of the Cambrian System; HSP, heat shock protein; PDA, protostome–
deuterostome ancestor.

fluctuation of seawater chemistry. Of course, there are other environ-
mental 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 specifically 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 poly-
phase accretion of formerly disparate blocks, which is accomplished
along three major orogenic belts known as the East African Orogen
(750–620 Ma), the Brasilina–Damara Orogen (630–520), and Kuungan
Orogen (570–530 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 Gondwa-
na 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 ex-
tended for several kilometers (Dalziel, 1997; Campbell and Squire,
2010). The uplift and erosion of the huge trans-Gondwana mountains
would have a significant influence 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 crit-
ical 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 envi-
ronment 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 accord-
ing to Valentine and Moores' (1970) model. Additionally, the worldwide
phosphate deposition during the Ediacaran–Cambrian transition
might aid in fossil preservation at this time, e.g. the phosphatized
 X. Zhang et al. / Gondwana Research 25 (2014) 896–909
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 Precambrian–Cambrian
transition (Dalziel, 1997), and there is no evidence that the oceanic P
concentration is insufficient for animal diversification. Hence, the as-
sembly 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 significantly higher
than Cambrian levels (Planavsky et al., 2010).
2.1.2. Aftermath of the Snowball Earth
Growing evidence indicated that the Earth experienced an ex-
tremely cold climate during the Neoproterozoic, which resulted in
two or three episodes of global glaciations during which ice sheets ex-
tend 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 it-
self is catastrophic for biological world, causing the collapse of biolog-
ical 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 significant 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 nutri-
ent 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 oxy-
gen (Planavsky et al., 2010). It has been argued that erosion of glacia-
tions and high chemical weathering rates during the retreat of ice
sheets must have led to higher riverine delivery of phosphorus to sea-
water, which would have increased rates of primary productivity and
organic carbon burial that produced significant quantities of atmo-
spheric 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 Neoproterozoic–Cambrian
interval (Planavsky et al., 2010; Papineau, 2010).
On the other hand, the harsh and fluctuating abiotic conditions
like the Snowball Earth may temporarily increase the degree of altru-
ism that was adaptive and promoted an increasing degree of terminal
(irreversible) differentiation. This is thought to be of particular rele-
vance to animal multicellularity because irreversible differentiation
(highly altruistic in that it imposes a high fitness cost on the individ-
ual 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 catastro-
phe 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 be-
fore 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 sur-
face environments (e.g. Shields, 2007). The end of the Snowball Earth
was followed by the evolution of complex macroscopic multicellular or-
ganisms, 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 diversification of animals during the early Cambrian.
2.1.3. True polar wander
The Ediacaran–Cambrian 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 ex-
ceeding 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
Ediacaran–Cambrian 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 cir-
culation and, hence, regional climates, and the repeated reorganiza-
tions in global climatic patterns during a TPW event would have
fragmented any large-scale ecosystems that were established, gen-
erating 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, first, trop-
ical continental margins and shelf-slopes which formed due to the frag-
mentation 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 gra-
dient moved them out of the clathrate stability field; finally, 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 power-
fully 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 addi-
tion, the global warming during early Cambrian is currently not testified
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 fluctuations might suppress
diversification 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
1.5–2 times (52.5–70‰) that of the modern value (~35‰), or even
higher, and it did not decline significantly 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
900 X. Zhang et al. / Gondwana Research 25 (2014) 896–909
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) spec-
ulated that the “delayed” decline of ocean salinity may have been a fac-
tor 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 in-
formation (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 fluid 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 biocalcification 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 indi-
cated 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 (Fernàndez-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 conflict 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 (Canfield and
Farquhar, 2009).
In the course of writing this paper, a seemingly new hypothesis
links the Great Unconformity (which separates Precambrian conti-
nental crystalline basement rock from much younger Cambrian shal-
low 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 conti-
nental denudation followed by extensive physical reworking of soil,
regolith and basement rock, and enhanced chemical weathering of
continental crust during the first continental-scale marine transgres-
sion of the Phanerozoic; these processes would affect seawater chemis-
try, 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 diversification 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; Canfield and Teske, 1996). Increasing at-
mospheric 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; Canfield et al., 2007). Oxygen is absolutely essential for meta-
zoans 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 spe-
cies (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 first 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 pro-
tection and might also form a defensive cuticle against predation. Once
the principle of cell specialization was established, the way was open for
almost infinite pathways of development of special organs, functions
and animal diversity (Decker and van Holde, 2011). Moreover, it is pro-
posed 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 re-
fined in bilaterians, but is not present in choanoflagellates and other
protists, suggesting that it is unique to metazoans (Leonarz et al.,
2011; Rytkönen and Storz, 2011). Rising oxygen levels in the atmo-
sphere 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 diversification 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, Canfield and Teske (1996) ar-
gued that the atmospheric oxygen rose above the 5% present atmo-
spheric level (PAL) during the Precambrian–Cambrian transition.
But it is still difficult to determine whether the increase in Δ34S is
related to higher oxygen levels or instead to intensive bioturbation
(Canfield and Farquhar, 2009). The iron content of sediments shows
that shallow waters were typically well-oxygenated throughout the
later Neoproterozoic(b742 ± 6 Ma) (Canfield et al., 2008), long before
the Cambrian explosion, whereas the deep ocean was anoxic and ferru-
ginous before and during the Gaskiers Glaciation 580 million years ago
and that it became oxic afterward (Canfield 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 re-
quires atmospheric oxygen levels above 15% of PAL (Canfield et al.,
2007), while persistent anoxia of the oceans in the Neoproterozoic is ar-
gued to require atmospheric oxygen levels below 40% of PAL (Canfield,
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
Butterfield (2009). He argued that Precambrian oceans (stratified, tur-
bid 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 signa-
tures were unable to be used as a direct proxy for atmospheric oxygen
levels under such nonuniformitarian conditions (Butterfield, 2009).
It was suggested that erosion of the Gondwanan supermountains
produced more free-oxygen than earlier supercontinent amalgamations
 X. Zhang et al. / Gondwana Research 25 (2014) 896–909
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 significantly decreased during early Cambrian (Komiya et al.,
2008). On the other hand, the minimum oxygen requirements for meta-
zoans 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 first animals of diverse metazoan phyla. Extant marine in-
faunal and epifaunal metazoans can accommodate dissolved oxygen
dropping to the tens of micromolar in concentration. If these concentra-
tions 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 corre-
sponding 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 influence morphological origins, ancestral form, etc.
Therefore, it is difficult 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 final
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 an-
cestors evolved in a more anoxic past (see van der Giezen and Lenton,
2012 and references therein). Many extant animals are found to be facul-
tative 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 wide-
spread 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 evolu-
tionary changes are fundamental genetic issues to understand the devel-
opment and evolution of animals (Carroll et al., 2001; Davidson and
Erwin, 2006, 2009; Davidson, 2010). With regard to the Cambrian explo-
sion in this context, key questions are what developmental genes define
ancestral bilaterians and whether the genes for building morphological
complexity of bilaterian clades were in place before and during the Cam-
brian 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 specific gene according to the phylogenetic
distribution of developmental genes in animal clades. The analysis re-
quires 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 demon-
strated that only a small fraction of all genes in any given animal
901
constitute the toolkit (about 20,000 protein-coding genes) that is de-
voted to the formation and patterning of body plan and body parts
(Carroll et al., 2001; Erwin, 2009). Among them, Hox genes (anteri-
or/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 definitive 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 meta-
zoans (Harcet et al., 2010; Adamska et al., 2011). Therefore, it is likely
that the establishment of animal GRNs coincided with the origin of ani-
mal multicellularity, and hence is long before the fossil diversification 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 five”
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
flies and vertebrates. A variety of transcription factors (that regulate
the expression of many other genes), signaling pathway genes (that me-
diate short- and long-range interactions between cells) and other regu-
latory elements once thought to be characteristic of bilaterians, have
been documented in basal metazoans (sponges, cnidarians, placozoans)
and choanoflagellates (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 meta-
zoans 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 complex-
ity of the Urbilateria (the common ancestor of bilaterians) is contentious
(Baguñà and Riutort, 2004), in a large part, due to different phylogenetic
placement of the acoels, varying from basal bilaterians (Baguñà and
Riutort, 2004; Baguñà et al., 2008; Hejnol and Martindale, 2008) to
secondarily simplified lophotrochozoans (Adoutte et al., 2000) or deu-
terostomes (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 mor-
phologies 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 (specific anterior patterning genes ems/Emx and
otd/Otx), segmentation (engrailed and Delta-Notch), eyes (Pax6 and ey),
902 X. Zhang et al. / Gondwana Research 25 (2014) 896–909

Fig. 2. Deep and shallow models for the divergence of bilaterian lineages. In the deep divergence model (left), the Acoelomorpha is considered as secondarily simplified deutero-
stomes or lophotrochozoans, and thus the Urbilateria, corresponding to the protostome–deuterostome 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 1–4
in the age column representing the first 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 flatworms was likely to
be a small, unsegmented, planula-like organism with blind digestive
system, far simpler morphologically than the protostome–deuterostome
ancestor (PDA) despite possessing a nearly complete eubilaterian ge-
nome (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-specific kernels that define 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-specific 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 al-
most 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 evo-
lution 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 ac-
count for the increasing morphological complexity during the metazoan
evolution. It has been assumed that the morphologic complexity corre-
sponds to the number, depth, and subcircuit diversity of the developmen-
tal 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, devel-
opmental 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 simplifica-
tions and increases of complexity in morphology (Philippe et al., 2011).
It is, therefore, likely that the increasing morphological complexity dur-
ing the evolution of bilaterian lineages resulted from an accumulation
in the number and diversity of dGRN subcircuits through time, including
 X. Zhang et al. / Gondwana Research 25 (2014) 896–909 903

the continued and hierarchical incorporation of microRNAs into these

networks in a lineage specific 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 mor-
phological 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 be-
fore the divergence of bilaterian clades. The presence of many devel-
opmental 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 specific 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 sufficient component
for the Cambrian radiation of bilaterian lineages (Erwin et al., 2011).
Then, what is the genetic basis underlying the morphological diversi-
fication 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 900–1000 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 significant method-
ological 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 Fig. 3. A. An “embryo” fossil from the Ediacaran Doushantuo Formation of South China,
but recently reinterpreted as nonmetazoan holozoans; B. Kimberella, widely accepted
hemerythrin), a prerequisite for development of shells or hard carapace,
as a bilaterian in the Ediacaran.
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 only relatively convinced bilaterian body fossil is the Kimberellomorpha
700 Ma ago (or earlier), and the origin of arthropod hemocyanin was (Fig. 3B), coeval with the oldest known bioturbation. However, a
estimated between 600 and 700 Ma. small group makes neither diversity nor disparity. The most com-
The deep divergence of bilaterian phyla, at least in stem lineages, monly attempted explanation is that early bilaterians were small
is supported by a majority of molecular clock studies, but it is suffer- and soft-bodied, and thus escaped the fossil record, while micro-
ing from a couple of challenges. First, the cold climate during late scopic fossils of protists and prokaryotes have been recognized
Cryogenian was unfavorable for animal diversification. Second, it is back to Archean and Lagerstätten of macroscopic soft-bodied fossils
not clear whether oxygen content was sufficient for bilaterians by have been known since the Ediacaran. Another possibility is that
the Cryogenian. The greatest challenge is the paucity of bilaterian fos- early bilaterians were ecologically insignificant and thus quite rare.
sils in this period, completely absent before the Gaskiers Glaciation. In any case, the deep divergence of bilaterians can only be testified
Possible animal embryo fossils from the Ediacaran-aged Doushantuo by the discovery of diverse bilaterian body fossils before and during
Formation (Fig. 3A) were recently reinterpreted as non-metazoan the Ediacaran period.
Holozoa (Butterfield, 2011; Huldtgren et al., 2011). Most putative Alternatively, many genes and subcircuits of the GRNs that under-
metazoans from the Ediacara-type biotas are very likely within the lie the building of body plans may have remained untapped over hun-
scope of cnidarian-grade organisms below the split of protostomes dreds of millions of years. Basal metazoan phyla morphologically
and deuterostomes (Erwin, 2009), except for Kimberellomorpha, diverged during late Ediacaran and bilaterian phyla diversified during
which are possible molluscans commonly associated with radiating early Cambrian, as is indicated by the fossil record (Shu et al., 2014-in
trace fossils (Fedonkin, 2003). Trace fossils are widely accepted as this issue). The Urbilateria might be complex in genetic makeup but
strong evidence for the presence of bilaterian animals in the Ediacaran, small and simple in morphology. This shallow divergence model
whereas the bilaterian nature of early trace fossils has been questioned (Fig. 2) is, however, supported by a minority of molecular studies. Per-
by the finding that large amoeboid protists leave macroscopic traces at haps, till early Cambrian oxygen levels and other environmental fac-
the bottom of the deep ocean (Matz et al., 2008). The oldest putative tors (e.g. Ca2+ concentrations in seawater) crossed a critical threshold
evidence of bioturbation by bilaterians is ca. 555 Ma in age (Rogov and favorable ecosystems were well established, thereby causing wide-
et al., 2012), significantly younger than most molecular clock ages. The spread biomineralization and increase in morphological complexity,
904 X. Zhang et al. / Gondwana Research 25 (2014) 896–909
body size, diversity, and disparity among bilaterian lineages. This model
is approximately reconciled with the paleontological data, but unequiv-
ocal metazoan body fossils are still rare during the Ediacaran. There is
another challenge to this view. Early Cambrian animals were consider-
ably 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 diversification 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 develop-
mental system, which enabled divergence of bilaterian body plans, is a
prerequisite but not sufficient 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 becom-
ing increasingly appreciated that the Cambrian explosion was an ecolog-
ical 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 first animal appeared the inter-
actions 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 Cambri-
an (Conway Morris, 2006). Many ecological hypotheses have been pro-
posed 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 significant 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 diversified rapidly after mass extinction events, the most
famous case being the diversification 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 pos-
sibilities 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 diversification
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 diversification because of systems in the absence of cropping by
herbivores; when advanced heterotrophy arose, it would initiate
self-propagating feedback systems of diversification; thus, the nearly
simultaneous origin and explosive radiations of heterotrophic pro-
tists, metaphytes, and metazoans were inevitable. This theory could
explain the increase in diversity under the influence of cropping,
but it was not directed against the uniqueness of the Cambrian explo-
sion in terms of timing and nature. The Cambrian explosion is far
more than the increase in biodiversity. Furthermore, heterotrophic pro-
tists 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. Phytoplankton–zooplankton diversification
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 (2–200 μm). It is the zooplank-
ton 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 10–100 times as large.
Therefore, repackaging effected by herbivorous mesozooplankton
(0.2–20 mm) represents a key link in marine metazoan food chains
(Butterfield, 1997, 2001). The phytoplankton (acritach) underwent a
major diversification 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
(0.2–2 μm) (Butterfield, 2009). This sudden diversification might
have stimulated the diversification of zooplankton, which in turn
might stimulate the evolution of large metazoans through food sup-
ply. However, the ecological significance of zooplankton during early
Cambrian is unclear because zooplankton fossils of this age are quite
sparse (Butterfield, 1997, 2001; Vannier et al., 2007). In addition, as a
component of the Cambrian explosion, the diversification of acritarchs
may also require a trigger. It was suggested that the early Cambrian ex-
pansion of animals into the water column might have been responsible
for driving the evolution of large net-phytoplankton (Butterfield, 2009).
So a chicken–egg problem arises. Did the diversification of phytoplank-
ton 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 diver-
sification 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 radi-
ation of bilaterian phyla in the early Cambrian but also exhibited by
substrate revolution during the Ediacaran–Cambrian transition, which
resulted from advents of burrowing bioturbation penetrating into the
depths of sediments (Seilacher and Pflüger, 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 seafloor
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 seafloor sediments, referred to as mixgrounds,
were heavily bioturbated by burrowing organisms, resulted in ventila-
tion of the sediments, and a change in redox gradients. This substrate
revolution was suggested to have significant 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 pro-
found (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) 896–909
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 diversifica-
tion 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 predator–prey pressure is the most commonly proposed eco-
logical 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 capa-
bilities 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 ap-
pearance of biomineralized skeletons in protists ca. 750 Ma ago
(Porter, 2011), but it surely did not trigger the widespread biominer-
alization 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 stimu-
lated 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, first 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 definite large predators,
e.g. anomalocaridids (Fig. 4E, F) made their first appearance in the
Cambrian Stage 3 (ca. 520 Ma), significantly postdating the metazo-
an 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 feed-
ing strategy (Erwin et al., 2011). Again, the advent of macrophagous
predators still requires a trigger. Since predators stand high above prima-
ry consumers in the trophic level, it is reasonable to assume that their in-
vasion lagged behind. Apparently, the establishment of predator–prey
relationships is an essential component of the Cambrian explosion but
not an ecological trigger.
2.3.6. Roughening of fitness landscapes
This hypothesis applied the concept of fitness landscapes from ge-
netics to the morphogenesis (Marshall, 2003, 2006). Computer simu-
lations demonstrated that the roughening of fitness landscapes could
led to increases in diversity and disparity of land plants, not necessar-
ily 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 fitness landscapes
(Kauffman, 1993). However, the organisms' needs are often frustrated,
which lead to conflicting 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 fitness landscape (corresponding to diversity and dispar-
ity), i.e. the fitness landscapes are roughening as the number of frustrat-
ed needs is increasing. The Ediacaran biotas had very few bilaterians,
showing rather smooth fitness landscapes (Marshall, 2006, fig. 3). On
the contrary, the Early Cambrian faunas contained some 20 bilaterian
body plans, showing very rough landscapes (Marshall, 2006, fig. 3). Ac-
cordingly, Marshall (2006) suggested that roughening was the primary
905
driver of the Cambrian explosion. This theory nicely depicted the
Ediacaran–Cambrian evolutionary transition and provided a good
explanation of body plan diversification without invoking the inven-
tion of toolkit genes. However, it invoked ecological interactions be-
tween 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 predator–prey
hypothesis (see above). Simply, the roughening of fitness landscapes
in the early Cambrian is a consequence of evolution.
2.3.7. Geosphere–biosphere feedbacks
This hypothesis is based on Earth system model for the long-term
carbon cycle by introducing three different types of biosphere: pro-
karyotes, eukaryotes, and complex multicellular life, each are charac-
terized by different global temperature tolerance windows. It argued
that the nonlinear feedback between temperature dependent produc-
tivity of complex multicellular life and their biotic enhancement of
silicate weathering could led to the temperature drops to the opti-
mum 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 sug-
gested 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 modification of the abiotic environ-
ment by a species that strongly affects other organisms by creating, mod-
ifying or destroying the niches of other species (Jones et al., 1994, 1997;
Wright and Jones, 2006; Erwin and Tweedt, 2012). Ecosystem engineer-
ing organisms interact nonlinearly and generate positive feedbacks that
enhance diversity (Altieri et al., 2010). Erwin and Tweedt (2012) ana-
lyzed the role of positive ecological feedbacks during the Ediacaran–
Cambrian transition based on the first 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 ecosys-
tem engineering (Erwin et al., 2011; Erwin and Tweedt, 2012). However,
as was noted by the authors, it is presently difficult to determine whether
the expansion of ecosystem engineering was merely a component of the
establishment of metazoan-dominated marine ecosystems or it was a
significant 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 struc-
ture 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 definitely appeared in the
Ediacaran period (Fig. 4A–C) (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 ecolog-
ical feedbacks need abundance.
906 X. Zhang et al. / Gondwana Research 25 (2014) 896–909

Fig. 4. A–C. 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 diversification 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 environ-
mental 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 diversifi-
cation 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 finally caused the Cambrian explosion.
The change of seawater composition, e.g. the increase in Ca2 + con-
centration, 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 feed-
back 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 Ediacaran–Cambrian
boundary and subsequently amplified 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 significant sine
 X. Zhang et al. / Gondwana Research 25 (2014) 896–909
Cenozoic but their ancestor appeared in Triassic and Jurassic. Ancestors
of early Cambrian faunas are most likely found in exceptional preserva-
tions in the late Ediacaran even if they were small or soft-bodied. In
China and other parts of the world, the Burgess Shale-type Lagerstätten
and phosphorous chert deposits are well known for exquisitely pre-
served 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, pre-
cise data are still lacking. The increase in atmospheric oxygen level dur-
ing the Ediacaran–Cambrian transition was suggested by the tectonic
events at this period, but yet to be confirmed 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 geo-
chemical colleagues.
Acknowledgments
We are grateful to Shigenori Maruyama and Yukio Isozaki for or-
ganizing 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 Author-
ity are greatly acknowledged.
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Taylor, C.T., McElwain, J.C., 2010. Ancient atmospheres and the evolution of oxygen in Northwest University, China before he finished one-
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Thayer, C.W., 1979. Biological bulldozers and the evolution of marine benthic commu- in Uppsala University, Sweden. He is interested in the evo-
nities. Science 203, 458–461. lution of Cambrian Burgess Shale type soft-bodied faunas.
Tohver, E., Trindade, R.I.F., Solum, J.G., Hall, C.M., Riccomini, C., Nogueira, A.C., 2010. His research is focused on exceptionally preserved bra-
Closing the Clymene ocean and bending a Brasiliano belt: evidence for the Cambrian chiopods and other lophotrochozoan fossils.
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Valentine, J.W., 2002. Prelude to the Cambrian explosion. Annual Review of Earth and versity, Germany. Her research interests center around the
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to oxic deep ocean during the Ediacaran–Cambrian transition and implications for research interests revolve around the so-called ‘Cambrian
bioradiation. Chemical Geology 306, 129–138. explosion’ of some 521 million years ago. Her studies on
Wray, G.A., Levinton, J.S., Shapiro, L.H., 1996. Molecular evidence for deep Precambrian the origin and early evolution of arthropods are largely
divergences among metazoan phyla. Science 274, 568–573. based on exceptionally preserved fossils from the Cambri-
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blage of macroscopic and morphologically differentiated eukaryotes. Nature 470,
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