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J. Seckbach and M. Walsh (eds.), From Fossils to Astrobiology, 211-229. © Springer Science + Business Media B. V. 2009

DECIPHERING FOSSIL EVIDENCE FOR THE ORIGIN OF LIFE AND THE ORIGIN OF ANIMALS: Common Challenges in Different Worlds

JONATHAN ANTCLIFFE1 AND NICOLA MCLOUGHLIN2

'Department of Earth Sciences, University of Oxford, Parks Road, Oxford, OX' 3PR, UK

2Department of Earth Sciences and Centre for Excellence in Geobiology, the University of Bergen, Allegaten 4', N-5007, Bergen, Norway

Abstract The origins of major biological groups contain a series of questions that engage all the natural sciences. Too often the different 'origin' case studies, such as the origins of animals and of life, are treated as separate entities, independent of one another. Viewing 'origin' questions as a whole helps the scientist to appreciate common challenges and then to share possible stratagems. We propose, specifically, that the palaeontologist working on Precambrian fossils should follow a series of nested questions that are outlined within, to guide what questions are valid and how to attain substantial answers to them. Two case studies are used to illustrate this approach: fossil stromatolites and the origins of life; and the Ediacara biota and the origins of animals.

1. Introduction

The deciphering of ancient fossil morphologies can be likened to the poem Jabberwocky from Through the Looking-Glass and What Alice Found There (Carroll, 1871) that treads a fine line between being understandable and being incomprehensible. Jabberwocky is littered with nonsense words, arguably, chosen for their sound and metre rather than their definitions. The mind invites us to attach the meanings of words they resemble and then suddenly the whole poem seems to make sense. So as the hunter, having killed the Jabberwocky, exclaims, 'O frabjous day! Callooh! CallayV we are invited to translate "O fabulous day! Hooray! Hooray!' but this is clearly not what is said. This is a simple interpretation, though it seems appropriate in context. Alice on reading this poem observes:

It seems very pretty, but it's rather hard to understand!" (You see she didn't like to confess even to herself, that she couldn't make it out at all.) "Somehow it seems to fill my head with ideas-only I don't exactly know what they are!

So it is when considering Precambrian palaeontology and, in particular, attempting to decipher the origins of life on earth in the Archean and the origins of the major animal groups in the Proterozoic. Other interpretations are always possible. Like Jabberwocky, the great strength of Precambrian palaeontology is that there is always the invitation of a different solution, a different approach; this keeps old fossils alive and vigorous. The enigmatic forms of such fossils may be as inviting to us as the words that comprise Jabberwocky, giving the appearance of a sensible and coherent whole waiting to be unearthed. Sometimes enigmatic fossils will be esoteric and incomparable to modern forms e.g. Tribrachidium from the Ediacara biota 580-543 Ma ago with its unusual three fold radial symmetry that is difficult to match in modern organisms. While at other times, fossil forms will be reassuringly familiar, for example, stromatolite morphology that is largely conserved over geological time. In the Precambrian however, where the majority of planetary processes operated significantly differently, for example: the composition and interaction of the atmosphere and hydrosphere; tectonic rates; the level of meteorite bombardment; and nature of long term solar cycles - just how uniformitarian can we be about our interpretations of these fossils?

We are faced with multiple hypotheses for the affinity of each candidate 'fossil'. To make matters worse these fossils should form a story that is a coherent whole with, for instance, single celled eukaryotes appearing before animals (one type of multi-celled eukaryotes), but this is not always the case. Some scientists would argue that there is no definitive evidence of eukaryotes until c.700 Ma, and they believe there are good theoretical reasons for believing in such a late arrival (Cavalier-Smith, 2006). Whereas, others would argue for the presence of animals as early as 1,500 Ma based on evidence of bilaterian animal trace fossils from the Vindhyan deposits of northern India (Seilacher et al., 1998) and predictions from molecular clocks that have placed divergence time for the Protostome-Deuterostome divergence as far as 1,200 Ma ago with the origin of all animals some time before this (Wray et al., 1996). Clearly these hypotheses are incompatible, but as they deal with separate fields, the origin of eukaryotes and animals respectively, the incon-gruence rarely meets at close quarters. So what are we to believe?

The traditional scientific approach advocates that in such situations, parsimony must rule. In this methodology, also known as Occam's Razor, the 'simplest solution' is the best and other hypotheses are effectively discarded. This is the 'Phanerozoic' method for distinguishing between hypotheses but should we expect to know what the simplest solution is in a Precambrian world? For instance, when considering the Ediacara biota, is it simpler to place many fossils in separate modern groups, as recently argued by Gehling et al. (2005), or is it simpler for all Ediacaran forms to be fundamentally similar to each other and be placed in one extinct group as advocated by Seilacher (1989); Brasier and Antcliffe (2004)?

The second hypothesis is more epistemologically parsimonious in terms of the number of groups the fossils belong to; i.e. one as opposed to ten or more. However, the first hypothesis invents no groups while the second must invent one, so the first hypothesis is more ontologically parsimonious (in terms of degrees of inference). For parsimony to help us with this problem we must decide whether it is simpler to invent one group or to shoehorn fossils in to ten existing groups. The answer to this question is not known, and perhaps it is irresolvable. When the guiding principle of parsimony can no longer be applied, what are we to do?

Thus, one of the biggest challenges facing Precambrian palaeontology is not a lack of valid, challenging and exciting hypotheses, but a method for distinguishing between them. From the earliest evidence of possible life to the origin of animals, the scientific literature is littered with disputes and controversy. In the following section we discuss common tools and approaches for deciphering Precambrian fossil evidence for the rise of life and the rise of animals on earth. We advocate using a hierarchy of "starting questions" for dealing with fossils from these earliest rocks. This approach will be illustrated using the case studies of fossil stromatolites and the Ediacara biota.

2. Null Hypotheses for Palaeobiologists

Enigmatic fossil groups and the challenge of deciphering their morphology is not uniquely a Precambrian problem, but it certainly predominates in this interval of earth history. Throughout Precambrian time there is a general trend of increasing morphological complexity of the fossils, and this arguably leads to increased confidence when deciphering their biological affinities. This confidence may be misplaced in many instances, however, and we propose that all fossil remains should be treated with equal doubt, from the earliest putative cells to claims of Ediacaran animals. Modern equivalents can be very informative for interpreting much about fossils but we caution that the Cambrian - Precambrian boundary represents the limit to 'biological uniformitarianism' beyond which modern equivalents are of limited use when used in direct analogy. Instead, we emphasise the importance of adopting an abiogenic "starting question" where the burden of proof is towards proving life. If an abiogenic origin can first be rejected, then a prokaryotic affinity becomes the working model, with efforts potentially focused towards demonstrating a higher (eukaryotic) affinity or in the very latest Precambrian possibly meta-zoan affinity (see Fig. 1). These hypotheses can be viewed as hierarchical, each being carefully refuted before adoption of the next, and thus they are shown in Fig. 1 as nested cones encompassing the expanding biosphere through geological time.

It follows that if we are to accept arguments for early prokaryotic life then the likely abiological mechanism that could have produced the candidate structures must first be rejected - see for instance, the stromatolite case study below. To then accept claims for a eukaryotic affinity we must first reject plausible

Figure 1. (overleaf) A series of nested cones that represent the starting points for exploring enigmatic fossil morphologies within an expanding biosphere. The outer yellow cone represents the abiotic mor-phospace, the inner orange cone the expanding prokaryotic morphospace and the central red cone the eukaryotic morphospace. Please note that each layer of the cone represents the likely times that the starting question is valid not the origination of a particular group. Thus the prokaryotic cone appearing at 2.5 Ga does not mean that is when we believe prokaryotes originated but the approximate time that it becomes reasonable to start asking if the fossils present are higher than prokaryotic in affinity. It does mean, consequently, that we would view claims of eukaryotes before 2.5 Ga as highly questionable. The reader could choose their own dates. The important point is that at any given time the outer cone is the starting point and progress is made by working inwards progressively rejecting hypotheses until an affinity is reached, and no higher claim can be satisfied. (This conical representation was inspired by a diagram of chemical evolution from Williams and Frausto da Silva, 2006.)

Figure 1. (overleaf) A series of nested cones that represent the starting points for exploring enigmatic fossil morphologies within an expanding biosphere. The outer yellow cone represents the abiotic mor-phospace, the inner orange cone the expanding prokaryotic morphospace and the central red cone the eukaryotic morphospace. Please note that each layer of the cone represents the likely times that the starting question is valid not the origination of a particular group. Thus the prokaryotic cone appearing at 2.5 Ga does not mean that is when we believe prokaryotes originated but the approximate time that it becomes reasonable to start asking if the fossils present are higher than prokaryotic in affinity. It does mean, consequently, that we would view claims of eukaryotes before 2.5 Ga as highly questionable. The reader could choose their own dates. The important point is that at any given time the outer cone is the starting point and progress is made by working inwards progressively rejecting hypotheses until an affinity is reached, and no higher claim can be satisfied. (This conical representation was inspired by a diagram of chemical evolution from Williams and Frausto da Silva, 2006.)

abiological mechanisms and demonstrate additional features that could not have been produced by any Prokaryotes (see Brasier et al., 2002). To accept claims of animals we must go one step further, first rejecting an abiogenic origin, then a prokaryote affinity, followed by rejection of single-celled eukaryote affinity before seeking features consistent with a multicelled-Eukarya. Even then the possibility of fungal and plant affinities must still be entertained - see for example the discussion of the Ediacara biota below. This may seem like overkill, but in many instances it may be rather easy to demonstrate biogenicity, as well as a prokaryote affinity. Take for instance the Ediacaran fossil Dickinsonia known from sections in Australia and Russia. It is clearly not abiogenic; the consistency and control of its morphology across a variety of facies, environments and taphonomic regimes speaks against this. The maximum size that Dickinsonia can achieve (in excess of a metre in several known specimens) quickly makes a prokaryote affinity very unlikely indeed. Add to this a growth program more complex than anything a prokaryote is known to achieve and we are quickly onto the single celled Eukarya hypothesis. However, not all Ediacaran fossils that have been described as some type of animal can run through this sequence so quickly. For instance the erstwhile Ediacaran/Cambrian chondrophorine hydrozoan Kullingia (Foyn and Glaessner, 1979; Narbonne et al., 1991) was recently reinterpreted as a scratch mark (Jensen et al., 2002). Thus the creature is not a body fossil and is now thought to have an entirely abiogenic origin. In this way we propose a series of nested cones (Fig. 1) as a theoretical structure within which to consider fossil morphology - this represents the exploration of doubt, in addition to trying to seek confirmation of successive hypotheses for the origins and affinities of a particular fossil.

A large number of criteria have been proposed by many different studies to distinguish between these multiple hypotheses. Table 1 provides a brief summary of these and subsequent case studies. Explore how these have been applied to the origins of life (e.g. stromatolites) and the Ediacara biota.

3. The Origin of Life: The Stromatolite Question

Stromatolites provide the earliest macro-fossil evidence for microbial life on earth. We here adopt a non-genetic definition of a stromatolite "an attached, laminated, lithified sedimentary growth structure, accretionary away from a point or limited surface of initiation" (Semikhatov et al., 1979). This definition encapsulates the key morphological and textural characteristics of a stromatolite as seen in outcrop or hand specimen and, crucially, it implies nothing about the relative importance of biotic and abiotic processes in their formation. We have chosen not to adopt a genetic definition of a stromatolite here (e.g. Kalkowsky, 1908; Walter, 1976), because it can be difficult to demonstrate active biological participation in their growth, especially in the early rock record. This challenge has long been recognized, as first explained in the somewhat paradoxical, genetic definition of stromatolites given by Kalkowsky (1908), namely that they are "organogenic, laminated calcareous rock structures, the origins of which is clearly related to microscopic life, which in itself must not be fossilized" (translated in Krumbein, 1983). Stromatolites therefore provide an excellent case study to illustrate the application and testing of the "nested cones," outlined above, when examining some of the earliest candidate fossils on earth.

Trends in stromatolite abundance and morphology through time record a complex and changing interplay of physical, chemical and biological processes

Table 1. compilations of key features that have been proposed for distinguishing eukaryotic and prokaryotic fossil morphologies from abiotic artefacts. Criteria marked with a (*) are consistent with biology, but care must be taken that reasoning does not become circular and that biogenicity is not inferred on the basis of these criteria alone.

Question

Abiotic

Prokarya Eukarya

Notes

Environment conducive to life? Are structures discrete? i.e. do not grade into matrix Are structures hollow? Are there bifurcations or branchings? Do chambers expand with growth? Is there evidence of nuclei?

*What are the growth curves or stages?

*What is the size of the "fossil?"

*Can individuals amalgamate during growth?

*Morphological differentiation consistent with bio-genic tiering within laminae or aggregates *Is there evidence for phototaxis? *Is there evidence for chemotaxis?

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