In a world without fossils, we might never have known about the event commonly known as the Cambrian explosion. This perplexing episode in evolutionary history has been known since early geologists and palaeontologists first started piecing together the history of life on our planet; what they found was that the oldest rocks contained no fossils, overlain by rocks containing complex fossils. A lack of precursors for complex fossils, such as trilobites, did not fit the evolutionary narrative gaining traction at the time. Charles Darwin’s explanation for this puzzle was that the fossil record was incomplete; these ancestral forms had existed, but had either not been preserved or not been found. Since then, more fossils have been found, including a large variety in Precambrian rocks, and the timescale has been constantly refined, allowing for a better understanding of the timing of key events. The questions raised by Darwin’s ideas have not quite gone away: is the Cambrian fossil record a true representation of the emergence of major animal groups? or is it an illusion caused by the paucity of the fossil record?
Many palaeontologists would like to read the fossil record literally and support the idea that the Cambrian explosion was a real event, however, there is a story in the genes which is somewhat different. Geneticists can estimate the divergence times between lineages using molecular clocks, a technique which uses mutation rates to count back to the time when two species or higher groups split. When applied to the origins of major animal groups, these estimates have varied widely and have been constantly refined. One consistent theme is that these dates are always substantially before the Cambrian, including the origins of phylum-level groups. It is always to be expected that a group or species would have evolved earlier than they appear in the fossil record, but not to the degree shown by molecular clocks for the Cambrian. If the story of the genes is read literally, then there is a lot of cryptic evolution in the fossil record, making the Cambrian explosion either an illusion caused by an absence of fossils, or by an increase in preservation potential due to the origin of hard parts and/or increased size across multiple groups. The conclusions of a recent molecular clock study appear to support the idea that the Cambrian explosion is a preservation event, not the rapid appearance of major animal groups.
In a paper titled Uncertainty in the Timing of Origin of Animals and the Limits of Precision in Molecular Timescales, dos Reis et al. present some robust new data and provide an excellent overview of the limits of molecular clock studies. Their estimates vary widely depending on certain assumptions, which are addressed in detail, but all of them do support an early divergence of major animal clades. They conclude:
This is the long-standing conundrum of the Cambrian—whether the first animal fossils faithfully reflect an explosion in animal biodiversity or merely an explosion of fossils. The results of our study—which integrates fossil and molecular evidence to establish an evolutionary timescale—suggest that the Cambrian explosion is a phenomenon of fossilization, while biological diversity was established in the Neoproterozoic. Integrating all of the sources of uncertainty that we explore (Figure 6, Table 1) allows us to conclude that crown Metazoa originated 833–650 Ma, fully within the Cryogenian, while the component clades of crown Eumetazoa (746–626 Ma), crown Bilateria (688–596) Ma, crown Deuterostomia (662–587 Ma), and crown Protostomia (653–578 Ma) all diverged within a Cryogenian to early- or mid-Ediacaran interval.
The results of our analyses leads us to reject the hypothesis that metazoans, eumetazoans, bilaterians, protostomes, deuterostomes, ecdysozoans, lophotrochozoans, or, for that matter, any of the component phylum-level total groups, originated in the Cambrian.
The conclusion that the fossil record is not accurate for the Cambrian may seem dismissive, just as many palaeontologists dismiss molecular clocks as inaccurate when they ostensibly contradict fossil data. This incongruence between the two datasets might itself be an illusion. Might there be reasons to think that both are accurate, but that we are mistakenly expecting them to answer the same questions?
It is relatively easy to picture a number of scenarios which could create the illusion of a surprising increase in complexity when really we just do not have the fossils. The Cambrian fossil record clearly does show that there was a dramatic increase in fossilisable hard parts, as we see a handful of shells at the end of the Ediacaran, through the increasing diversity and complexity in the Small Shelly Fossils (SSFs); soft tissues do not preserve well, so it might be a case that hard parts evolved in animals which had been milling around for millions of years prior. Or could it be the case that they simply were not big enough to be preserved? An impression of a soft-bodied animal in sand cannot be smaller than the individual sand grains. The meiofauna live in those sorts of surroundings, in between the grains of loose sediment, where oxygen levels are often low; animals too small to see without a microscope, complex yet only found fossilised in exceptional circumstances. And maybe it is the case that we have fossils of them but are looking with the wrong expectations? In these scenarios, the genes are right and it is the fossils which do not give enough of the true picture.
The Ediacaran period is famous for its menageries of soft-bodied organisms, preserved as impressions in sand, or by volcanic ash smothering their soft forms; any organism large enough would surely have been preserved. Within this period of time, we also find the Doushantuo fossils, visible only through the use of high-powered microscopes. Preserved in phosphate, they are largely an assortment of little ball-shaped clusters, thought by some to be embryos, yet by others to be single-celled organisms in the process of division. During the Cambrian and later, phosphate deposits such as these contain the elusive meiofauna, yet they are absent from the Ediacaran. Instead, we see a finer degree of fossilisation. Preservation in the Precambrian is arguably better than the Cambrian and later – preservation has evolved, but not towards higher fidelity.
Geneticists can also shed light on this question of preservation potential. Animals have a number of microRNAs, which are regulatory RNA genes that can be used to track the evolution of complexity, put simply because more complex animals have more microRNAs than simpler organisms. When some of the simpler animals are analysed, such as acoel flatworms and rotifers, it is found that they have lost microRNAs and become less complex, so they cannot be used to work out what a simple bilaterian ancestor might have looked like. Instead, they seem to indicate that the common ancestor of bilaterians was relatively large and complex, and at the very least a persistent puzzle.
It is possible that we already have fossils of bilaterians from the Precambrian, but that we are not identifying them correctly. The Ediacaran form Kimberella is often considered to be a possible mollusc, whilst its contemporaries Spriggina and Parvancorina are sometimes linked to arthropods, yet all of these are questionable. Recently, the shelly Ediacaran organism Namacalathus has been identified as a lophophorate, placing it with animals like brachiopods and bryozoans, but this is undeniably controversial.
Bilaterians don’t often sit still. They wriggle around on the sea floor, they churn up the sediment in search of food and shelter, they swim around looking for food. Burrows and trails are abundant in the fossil record, often found alongside body fossils, but also in sediments where body fossils could not be preserved. They give us insight into the nature of the sediment, the life habits of animals, and the evolution of complexity. Trace fossils tell a similar story to the body fossils. The sediments in the Precambrian were quite hard and largely devoid of oxygen – not conducive to the existence of meiofauna – and lack any clear evidence of bilaterian activity, then animals began to wriggle about in the sediment in the Cambrian, allowing oxygen to reach greater depths. The first stage of the Cambrian shows a large increase in the ways animals interacted with the sediment, but it was not until the second stage of the Cambrian when they started to burrow up to a metre deep and ecosystems took on a new level of complexity. The trace fossil record suggests that the Cambrian explosion was a very real event, but that body-plan diversification happened before changes in ecological structure.
The data from trace fossils hints at how the record of body fossils and the information in the genes could both be telling the same story. It is possible that molecular clocks are right about major animal groups diversifying much earlier than the Cambrian, but the conclusion that the Cambrian explosion is an illusion caused by a poor fossil record is misguided. The fossil record does indeed appear to record an actual evolutionary event, but it might not be the origins of these major animal groups – it may instead be their ecological expansion, not least the widespread evolution of hard parts. Under this scenario, we are still lacking in key fossils, but that lack is not the explanation for the incredible diversification through the start of the Cambrian period. The Cambrian explosion would therefore not be a case of “animals or fossils” but an ecological restructuring which could not have been known without the fossil record.
dos Reis, M., Thawornwattana, Y., Angelis, K., Telford, M.J., Donoghue, P.C.J, and Yang, Z. 2015. Uncertainty in the timing of origin of animals and the limits of precision in molecular timescales. Current Biology. [Link]
Erwin, D.H., Laflamme, M., Tweedt, S.M., Sperling, E.A., Pisani, D., Peterson, K. 2011. The Cambrian conundrum: Early divergence and later ecological success in the early history of animals. Science 334: 1091-97. [Link]
Mangano M.G., Buatois L.A. 2014. Decoupling of body-plan diversification and ecological structuring during the Ediacaran – Cambrian transition: evolutionary and geobiological feedbacks. Proc. R. Soc. B 281: 2014003. [Link]