Origins of animals

The fossil record of the earliest animals has been enlivened in recent years by a series of spectacular discoveries, including embryos, from the Ediacaran to the Cambrian, but many issues, not least of dat- ing and interpretation, remain controversial. In particular, aspects of the taphonomy of the earli- est fossils require careful consideration before pro- nouncements about their affinities. Nevertheless, a reasonable case can be now made for the extension of the fossil record of at least basal animals (sponges and perhaps cnidarians) to a period of time signifi- cantly before the beginning of the Cambrian. The Cambrian explosion itself still seems to represent the arrival of the bilaterians, and many new fos- sils in recent years have added significant data on the origin of the three major bilaterian clades. Why animals appear so late in the fossil record is still unclear, but the recent trend to embrace ris- ing oxygen levels as being the proximate cause remains unproven and may even involve a degree of circularity.

1.1 Introduction

The ‘Cambrian explosion’ is a popular term that refers to the period of profound evolutionary and environmental change that took place at the open- ing of the Phanerozoic some 540 million years ago (Ma). Although this set of events is multifaceted, it is associated primarily with the origin of animals in the fossil record. For over 150 years, an argu- ment has raged about the reality of this event. Is it a genuine evolutionary event, or merely a sudden manifestation in the fossil record of evolutionary

processes that took place long before? Even if the fossil record of that time is accurately recording the unfolding of events in real time, the question of why the events took place then—and what the potential trigger was—has continued to be prob- lematic. The Cambrian explosion itself has been much discussed (Gould, 1989; Conway Morris,

1998a, 2003a; Knoll and Carroll, 1999; Budd and Jensen, 2000; Knoll, 2003). Here I want to focus on three issues: the age of the earliest animal fossils, the continuing debate about their affinities, and finally, a critical examination of the most popu- lar candidate for ‘triggering’ the explosion; the concentration of atmospheric oxygen.

Geologists as long ago as William Buckland (1784–1856) realized that a dramatic step change in the fossil record occurred at the base of what we now call the Cambrian. The apparent appearance in the fossil record of many animal groups with few or no antecedents caused Charles Darwin great trouble—indeed he devoted a substantial chapter of the Origin to this problem. Further insights were provided by the remarkable amount of work on North American faunas by Charles D. Walcott, who proposed that an interval of time, or the ‘Lipalian’, was not represented in the fossil record and/or did not preserve fossils and that the forms ances- tral to the Cambrian taxa evolved during this time. However, the intense modern interest in the subject was probably sparked by the work of Whittington and colleagues in their redescriptions of the Burgess Shale (see below), together with Stephen Jay Gould’s popular account of this work, Wonderful Life, published in 1989. In recent years, the attention

paid to the youngest part of the Precambrian has led to the erection of the formal Ediacaran Period of c. 630–542 Ma (Knoll et al., 2006), an interval that has been intensely scrutinized for its bearing on the origin of the animals.

1.2 Fossil evidence for the origin of animals: the state of play

The classical fossil evidence for the early evolu- tion of animals consists of several sources: trace fossils, the Ediacaran biota from just before the beginning of the Cambrian (Narbonne, 2005), the conventional Cambrian fossil record (Bengtson,

1992), and the Burgess Shale fauna (Briggs et al.,

1995). In recent years these data sources have been

enriched by further important discoveries, espe-

cially new Cambrian exceptional faunas such as

the Chengjiang fauna (Hou et al., 2004) and indeed

very substantial new discoveries from the Burgess

Shale itself (Caron et al., 2006; Conway Morris

and Caron, 2007); the Doushantuo fossils from

the Ediacaran period of the latest Precambrian

(Xiao and Knoll 2000; Xiao et al., 2007a; Yin et al.,

2007), and more Ediacaran discoveries, such as

from Namibia, Newfoundland, and the White Sea

(Grazhdankin and Seilacher, 2002; Narbonne, 2004).

Outside the Cambrian, the Silurian Herefordshire

fauna has also yielded some remarkable fossils

that have had significant bearing on the origins of

various animal clades (e.g. Sutton et al., 2001a, 2002;

Siveter et al., 2007). The volume of data that the fos-

sil record has brought to bear on the issue of the

origin of the animals has thus notably increased

in recent years, explaining the exciting dynamism

that currently characterizes the field. Nevertheless,

even a casual observer would note that few of these

new inputs have been without controversy; with

high-profile publications regularly attracting pub-

lished responses or critical reviews. The undeni-

able difficulties surrounding these data can be

attributed to several causes: (1) an often incomplete

understanding of the taphonomy (i.e. the complete

set of preservational processes surrounding the

production of the final fossil), a lack that has often

led to interpretation of ambiguous fossils in a pre-

conceived manner; (2) the continuing discussion

of how Cambrian taxa should be classified; and

(3) various dating problems.

1.2.1 The Doushantuo Formation and its taphonomy

The processes that convert a living organism into a mineralized or organically preserved fossil are far from being fully understood; nevertheless, at least some understanding of them is essential if fossils are to be successfully interpreted (Butterfield et al.,

2007). Nowhere has this been more important than the evaluation of the various exceptional faunas around the Precambrian/Cambrian boundary. Of particular recent interest has been the Doushantou Formation (Fm) of South China. This c. 250-m thick sequence of siliciclastic, phosphatic, and carbonate rocks has yielded exceptionally preserved puta- tive examples of algae, acritarchs, and metazoan embryos and adults including sponges and a bila- terian (Chen et al., 2000; Xiao and Knoll 2000; Yin et al., 2001, 2007; Chen and Chi 2005; Dornbos et al.,

2006; P. J. Liu et al., 2006; Tang et al., 2006; Xiao et al.,

2007a). However, nearly all of these fossils have

proved highly controversial. One reason for this is

clear: the Doushantuo Fm has been dated to well

before the beginning of the Cambrian, and thus

these fossils would undoubtedly include the oldest

animals in the record (but see below).

The preservation in phosphate of many

Doushantuo fossils leads to problems of disen-

tangling primary morphology from subsequent

taphonomic overprints (Bengtson and Budd, 2004;

Xiao et al., 2000). As a result of such concerns,

some of the more extravagant claims, such as that

the Doushantuo biota includes representatives of

bilaterians and deuterostomes, do not currently

stand up to scrutiny. Nevertheless, and not with-

standing attempts to provide alternative bacterial-

affinity explanations (Bailey et al., 2007a,b; Xiao

et al., 2007b), the Doushantuo fossils remain as

convincing embryos. Even if the presence of phos-

phatized embryos is accepted though, a significant

amount of disagreement over their precise dating

remains, which, in its extreme, would extend the

range of animals down to close to the opening

of the Ediacaran at around 630 Ma, while at the

E A RL IES T F OSS IL RE C O RD O F T H E A N IM A L S 5

other extreme the Doushantuo fossils may not sig- nificantly pre-date the oldest Ediacaran fossils at around 565 Ma.

1.2.2 Towards a chronology of the latest

Precambrian

The later stages of the Precambrian are marked by glaciations of global extent that show up in the record as, for example, a series of tillites (lithi- fied glacial sedimentary rocks of mixed compos- ition that are formed as the result of movement by ice). These glaciations have been suggested to be evidence for the so-called ‘snowball earth’, i.e. intervals of time when the earth was effect- ively deep-frozen. The amelioration of conditions after these glaciations has been suggested to be a key factor in the rise of the animals (Runnegar,

2000), although the mechanism for such a direct causality remains largely obscure. The interval of time known informally as the ‘Cryogenian’, from approximately 850–630 Ma is marked in the Australian record by two distinct ice intervals: the

‘Sturtian’ and the ‘Marinoan’ (Kennedy et al., 1998). These glacial intervals can be correlated with gla- cial deposits elsewhere in the world, such as in China (Zhou et al., 2004). In addition, a further short-lived glacial interval, the ‘Gaskiers’, known primarily from Newfoundland (Eyles and Eyles,

1989), has been dated to be c. 580 Ma. Correlating Precambrian glacial intervals worldwide is diffi- cult at best, largely because of the lack of accurate biostratigraphical control, and the task is compli- cated by the technical problems associated with the various types of absolute radiometric dating. As a result, a number of minority views exist, such as that the Marinoan and Gaskiers glaciations are identical (based on dating in Tasmania; Calver et al., 2004). As far as the dating of the Doushantuo Fm goes, the glacial rocks below can be dated to close to 635 Ma, and the base of the overlying Dengying Fm, has been dated to 551 Ma (Condon et al., 2005). A complicating factor is that the well- preserved fossils of the Doushantuo Fm are known not from its type locality but from the Weng’an locality, which consists of a much shorter (c. 40 m thick) section made up largely of two phosphoritic units (Dornbos et al., 2006).

An additional aid to dating comes in the form of chemostratigraphy, especially using GC13, which suggests that the Doushantuo Fm is marked by three negative GC13 excursions: one at the base, associated with the so-called ‘cap carbonates’ that directly overlay the glacial deposits; one in the middle, and one near the top (Condon et al., 2005). It has often been thought that the excursion towards the top is associated with the Gaskiers glaciation, in which case the age of the Doushantuo Fm would range from about 580–635 Ma. The significance of these dates is that all of the Doushantuo fossils would pre-date the oldest of the famous Ediacaran fossils such as Dickinsonia etc., and thus would provide an independent record of animal life during a period of time for which no large-body fossils or trace fos- sils are known. Indeed, the overlying Dengying Fm does yield Ediacaran-type fossils, which could be said to support this contention. However, some recent work has questioned this view, suggesting that it is the middle GC13 in the Doushantuo Fm that corresponds to the Gaskiers Fm (despite the lack of other evidence for glaciation in the type area; in the Weng’an section, a definite break in the sequence at this point could be correlated with gla- cially related drop in sea-level). This would con- strain the age of the upper Doushantuo Fm units to lie within about 551 and 580 Ma (Dornbos et al.,

2006), and, as it is this interval that is thought to yield the animal fossils, these fossils could plaus- ibly be regarded as being of a similar age to the Ediacaran assemblages. In order for this model to be correct, some of the published radiometric dates for the Doushantuo Fm would have to be incorrect (Barfod et al., 2002), but given the care required to interpret whole-rock radiometric dates, this possi- bility cannot simply be ruled out.

More recently, the claim has been made that at least one of the enigmatic acanthomorphic (i.e. spinose) acritarchs (see Figure 1.2), which are nor- mally assigned to protist groups such as the green algae and dinoflagellates, are actually the hulls of diapause animal eggs (Yin et al., 2004, 2007). Although the fossil in question, Tianzhushania, is known to contain embryos only in the upper part of the Doushantuo Fm, it ranges down to very close to the base, and thus to 630 Ma or so. The claim would be that the oldest animal fossils of

the Doushantuo Fm, dating back to just after the Nantuo glaciation (i.e. the Chinese glacial deposits normally correlated with the Marinoan) are of this age, a time that pre-dates the first Ediacaran fossils by some 60 million years, as well as the more con- servative molecular clock estimates for the diver- gence of the bilaterians.

Despite the obvious uncertainties, the most reasonable interpretation of the data is thus that embryo-forming animals of some sort had evolved by just after Marinoan time; that sponges and presumed other animals had started to emerge by 580 Ma at the latest; and that the Ediacaran biotas are likely to be a little younger than the Doushantuo embryos. The upshot of the new data is that much more convincing evidence exists in