The quality of the fossil record through time

Does the fossil record tell the true story of the history of life? This has been a long-running debate that surfaces from time to time, but which has so far proved impossible to resolve. The debate goes back over 200 years, and it has figured prominently in considerations of much wider issues in geology and in evolutionary biology. In a new study, published in Nature today (3rd February), we believe we have resolved the issue.

The significance of the fossil record in documenting evolution worried Charles Darwin. He devoted two of the fourteen chapters of his On the origin of species (1859) to the fossil record, and one of them was specifically 'On the imperfection of the geological record.' Darwin wrote:

That our palaeontological collections are very imperfect, is admitted by every one. ...numbers of our fossil species are known and named from single and often broken specimens, or from a few specimens collected on some one spot. Only a small portion of the surface of the earth has been geologically explored, and no part with sufficient care, as the important discoveries made every year in Europe prove. No organism wholly soft can be preserved. Shells and bones will decay and disappear when left on the bottom of the sea, where sediment is not accumulating.

This rather negative view seems self-evident. And yet, in the to-and-fro of the controversy, no clear resolution has emerged. The protagonists on both sides have to resort to qualitative arguments and wild assertions.

The critics, following Darwin's rather cautious lead, declare that fossils are only fragmentary remains of whole organisms, that many living plants, animals and microbes are unlikely ever to leave fossil remains of any kind, and that the chances of finding more than 1% of all the species that ever lived are remote.

In answer to this rather bleak view, the fossil apologists claim that, despite all the huge efforts of palaeontologists around the world, we have really not learnt much since 1859. Since Darwin's day, fossils have been collected intensively from Greenland to Antarctica, and from Australia to Argentina. These have not changed the broad picture of the history of life one whit. We still record in our textbooks, as was done in the 1850s, that marine invertebrates became abundant during the Cambrian period, that fishes became abundant in the Silurian and Devonian, that dinosaurs existed through the Mesozoic, that Mesozoic mammals were small, and only flourished after the demise of the dinosaurs, from the beginning of the Tertiary.

The debate has exploded again in the past five years. Molecular biologists have claimed that the first half of the fossil record of many major groups is missing. As an example, molecular analyses of phylogeny (reconstructions of branching evolutionary patterns based on comparisons of the DNA and RNA of living forms) have projected the point of origin of modern bird and mammal groups deep into the Cretaceous, to a time some 100-120 million years ago when dinosaurs like Iguanodon and Polacanthus stalked the lush forests of southern England. The oldest fossils of modern bird and mammal groups are known, somewhat doubtfully from the very end of the Cretaceous, and then in abundance from the beginning of the Tertiary, 65 million years ago.

This is a major challenge to palaeontology. The claim is that the first half of the fossil record of these groups is missing. Perhaps the early ancestors of modern birds and mammals were so rare as not to be fossilized, or perhaps they lived in some region that has not yet been excavated. Nonetheless, my mind boggled at the thought of parrots and bats flitting through the steaming Mesozoic jungles, penguins skipping along the shores, and monkeys looking down quizzically at Tyrannosaurus rex. I am convinced, as are many molecular sequencers, that the calibration of the calculations is wrong. And yet the point has been accepted unquestioningly by many. This I find startling.

In our new work, we have taken advantage of the fact that there are several independent ways of looking at the history of life. The fossil record is one source of information - the order of fossils in the rocks. Independent approaches are now available, cladistics and molecular phylogenies. Cladistics is a set of methods for reconstructing tree-like patterns of relationships among living, or a mix of living and fossil, organisms, using only numerical scoring of their unique morphological characters. There is no recourse to the age of the fossils: the emerging pattern depends solely on records of shared characters. Molecular phylogenies are even more clearly independent of the fossil record. Comparison of the DNA and RNA sequences of living species allows the construction of a tree of relationships.

Cladistic and molecular trees give information on relationships and on the order of branching, and the order of branching points in the trees can be compared with the order of fossils in the rocks. Over the past few years, we have devised a number of metrics for effecting the comparison, and for assessing the significance of the claims for congruence. There is no claim that the fossil record, the cladistic trees, or the molecular trees are the standard of truth against which the other evidence is assessed. Any of the three approaches is equally likely to be wrong. However, we would assert that if any two, or all three, tell the same story, then that is probably the correct story. It is hard to see how the order of the fossils and a molecular tree could be biased in the same erroneous direction since the sources of data on which the results are based are so different.

The group in Bristol working on this problem consisted of Matthew Wills, now at the Oxford University Museum of Natural History, Becky Hitchin, and myself. Our earlier findings confirmed that (thank goodness) the majority of fossil records and trees were congruent, indicating that palaeontological methods and tree-making methods were working, and giving the correct story. In our latest study, we assessed 1000 published cladistic and molecular trees from all kinds of organisms - microbes, plants, and animals - and collated the results. For all three metrics, we found no change in the quality of the fossil record through time. In other words, the sample of several hundred trees based on groups that originated in early geological times, the Palaeozoic, gave congruence values which were just as good as those originating in the Mesozoic and Cenozoic.

How can this be? How can we claim, as we do, that the Palaeozoic fossil record is just as good as the Mesozoic and Cenozoic? This seems nonsensical when any geologist can tell you that the ancient rocks of the Cambrian have been folded, heated, buried, and eroded much more than the more recent rocks of the Jurassic. If you visit a Cambrian fossil locality, on the whole it is hard to collect fossils, and they are often damaged, whereas Jurassic localities yield undamaged shells and other fossils in abundance. The solution to the dilemma depends on the scale of observation. Close up, the Cambrian fossil record is obviously worse than the Jurassic. But step back, and look on a global scale at the broad outlines of evolution, and there is no difference in the quality of documentation.

Up to now, the fossil apologists and the critics have been talking at cross purposes. The apologists have been concentrating on the big picture, and they have been right: the fossil record does give the correct story of the history of life. The critics have also been right, but only at a fine, local scale, and they are wrong to assume that sparse and scrappy fossils in the Cambrian mean that palaeontologists can say nothing about what was going on 500 million years ago.

Michael J. Benton

Many thanks to the Leverhulme Trust and to NERC for funding. More information at http://palaeo.gly.bris.ac.uk/cladestrat/cladestrat.html