© 2005 Society of Systematic Biologists
Telling the Evolutionary Time: Molecular Clocks and the Fossil Record.—Philip C. J. Donoghue and M. Paul Smith, editors.
Henry Wellcome Ancient Biomolecules Centre, Department of Zoology, University of Oxford OX1 3PS, UK
Telling the Evolutionary Time: Molecular Clocks and the Fossil Record.—Philip C. J. Donoghue and M. Paul Smith, editors. (Systematics Association Special Volumes, v. 66). 2003. CRC Press, Boca Raton, Florida. 296 pp. ISBN 0–4152–7524–5. $109.95.
Telling the Evolutionary Time: Molecular Clocks and the Fossil Record.—Philip C. J. Donoghue and M. Paul Smith, editors. (Systematics Association Special Volumes, v. 66). 2003. CRC Press, Boca Raton, Florida. 296 pp. ISBN 0-4152-7524-5. $109.95.
Determining the temporal scale of biological evolution has traditionally been the preserve of paleontology, with the timing of species originations and major diversifications all being read from the fossil record. However, the ages of the earliest (correctly identified) records will underestimate actual origins due to the incomplete nature of the fossil record and the necessity for lineages to have evolved sufficiently divergent morphologies in order to be distinguished. The possibility of inferring divergence times more accurately has been promoted by the idea that the accumulation of genetic change between modern lineages can be used as a molecular clock (Zuckerkandl and Pauling, 1965). In practice, though, molecular dates have often been so old as to be incongruent even with liberal readings of the fossil record. Prominent examples include inferred diversifications of metazoan phyla hundreds of millions of years before their Cambrian fossil record appearances (e.g., Nei et al., 2001) and a basal split between modern birds (Neoaves) that is almost double the age of their earliest recognizable fossils (e.g., Cooper and Penny, 1997).
Proponents of molecular dates typically explain the absence of older fossil records as a consequence of low preservation potential (e.g., small, planktonic Precambrian animals without hard parts) or origins in areas without (known) appropriate fossiliferous sediments. For example, molecular studies predict Cretaceous origins for some avian groups in the Australian region (Cracraft, 2001), but there are no land vertebrate fossil sites in Australia dated between 55 and 105 million years old). On the other hand, advocates of fossil-based divergence estimates suggest that molecular-based range extensions result from variation in substitution rates among lineages that invalidate the assumption of a molecular clock (see Bromham et al., 2000). The possibility that molecular rates could change uniformly across different groups is of particular concern, because such rate variation is difficult to detect. If rate deceleration postdates calibration points, then dates for deeper nodes can be overestimated.
In September 2001 a joint Palaeontological Association/ Systematics Association symposium at the Third Biennial Meeting of the Systematics Association was held in London with the primary aim of addressing discrepancies between molecular and paleontological estimates, particularly for the timing of major taxonomic radiations. The book Telling the Evolutionary Time: Molecular Clocks and the Fossil Record, edited by Philip C. J. Donoghue and M. Paul Smith, stems from that meeting. The 12 papers in this book demonstrate that the perspectives of molecular biologists and paleontologists are not as irrevocably polarized as the impassioned debates and commentaries in major journals often imply.
An important result of the increased interaction between paleontologists and molecular biologists is clarification of just what events each is measuring. No less than 10 of the papers stress the importance of distinguishing the concepts of crown-group (the extant taxa of the group, their last common ancestor, and all extinct taxa nested within) and total-group (the crown-group plus taxa on or diverging from its stem lineage). This understanding reduces apparent conflict when, for example, a molecular biologist (thinking of the total-group) proclaims Chiroptera (bats) to have originated before the Cretaceous–Tertiary boundary, which a paleontologist (thinking of the crown-group) might consider inconceivable.
For nonspecialist readers this book is a useful primer on the potential pitfalls of both molecular and paleontological dating estimates. In the first paper, Rodríguez-Trelles, Tarrío, and Ayala consider that the extent of rate variation among nine genes and across plant, fungi, and animal taxa undermines the neutrality assumption that underpins the idea of a universal stochastic molecular clock. Fortey, Jackson, and Strugnell attempt to account for such variation by allowing substitution rates to vary in different groups, though they still recover a protostome/deuterostome divergence that predates the Cambrian by more than 100 million years. Furthermore, Pawlowski and Berney show that erroneous relationships and divergence date estimates among a eukaryote data set could be linked to an extreme rate speed-up along the Foraminifera stem-lineage.
Concern among the paleontology papers centers on the relative importance of "true" biotic signal and sampling artifacts for interpreting the fossil record. Of particular interest here are confidence interval (e.g., Marshall, 1990) and group sampling (Foote and Raup, 1996) methods, which can be used to infer how much of a group's fossil record may reasonably be expected to be missing. Problematic issues relating to these methods, such as geographical/niche-dependent biases and nonrandom distribution of fossil-bearing sediments across time are explained well in the Benton paper and the Donoghue, Smith and Sansom paper. Other papers illustrate the potential for biases relating to preservation and identification. Wellman uses the example of land plants, for which the hardy pollen record begins in the early Ordovician, but it is not until 50 million years later that megafossils appear in the fossil record, apparently coinciding with the evolution of lignified cell walls. Additionally, Ruta and Coates use phylogenetic inference to show that the absence of identifiable lissamphibians before the early Triassic, but presence of sister group taxa early in the Permian, implies a ghost range for lissamphibians of about 60 million years.
Obviously a key aim of the symposium was to work at solutions to methodological shortcomings. The book reveals some progress here, particularly in the ability of fossil record analyses to incorporate sampling into fossil range estimates for specific groups. Important developments in tests that compare the order of fossil occurrences with the order of branching events on cladograms (see Benton et al., 1999) are also documented. These tests are employed as indicators of the reliability of the fossil record in papers by Benton, by Paul, and by Budd and Jensen. However, Ruta and Coates point out in their paper that the assumption in these tests that the phylogeny is independent of the stratigraphy is unlikely to be strictly true.
The direction of progress on the molecular front is showcased in papers by Fortey et al., by Pawlowski and Berney, and by Wikström, Savolainen, and Chase. Of particular note is the trend towards using relaxed clock methods in which a universal molecular clock need not be relied upon and also the realization that single calibration points are not ideal. Here, though, the time from symposium to publication renders the specifics (though not the concepts) of the methodologies obsolete. For recent methods that incorporate multiple calibration points (or bounds) and allow rate variation across the tree, one would do better to look towards the multidistribute (Thorne and Kishino, 2002) or r8s (Sanderson, 2002) packages.
Most of the major temporal discrepancies that are examined in this book are not resolved. For example, Wikström, Savolainen, and Chase use three genes to trace the angiosperm crown-group back to the Middle Jurassic, more than 50 million years before the oldest clearly identifiable fossils, whereas Budd and Jensen contend that the sediment record, inference on ancestral characters, and dispersal potential cannot explain the additional 100 million years of bilaterian crown-group fossil history required to fit molecular timescales. Unresolved incongruence is of course not in itself an indictment. However, I cannot help but feel that the search for solutions in this book (and in the primary literature) is not adventurous enough. One fundamental issue that is ignored is the potential for consistent molecular dating biases to result from branch-length estimation under models that neglect compositional nonstationarity and covarion evolution. Another is the restriction of tree reconstruction from morphological data to parsimony methods, which are only satisfied by minimizing homoplasy. This is hardly conducive to understanding the potential for parallel trends and convergence to allow for apparently plesiomorphic taxa to in fact be included within crown-groups. Probabilistic models for morphological evolution (see Lewis, 2001) aim to address such problems, which are regularly being exposed by comparison of molecular and morphological trees for modern taxa and importantly, would tend to have a shallowing effect on fossil-based estimates for crown-group origins.
Despite these frustrations, a number of papers in the book provide evidence that differences between molecular and fossil-based dating estimates are decreasing or at least becoming more explicable. Benton's example for placental mammals is a consequence of both a reduced molecular timescale and an improved understanding of the fossil record. Similarly encouraging are the findings of Donoghue et al. and Ruta and Coates that molecular and fossil-based estimates are more congruent when the fossil record is more complete.
The upshot of a cover-to-cover read of Telling the Evolutionary Time: Molecular Clocks and the Fossil Record will be a solid understanding of the potential uses and primary concerns for both molecular and fossil-based estimates of taxonomic origins/divergences, at least as they have been debated in the primary literature. Furthermore, the referencing provides plenty of scope for delving deeper. Along with the introspections and methodological justifications that make up much of the book, there are also interesting papers of more specific interest. Dyke provides possible internal points for the elusive task of calibrating avian evolution, whereas Hedges argues that molecular dates for early origins of terrestrial plants, fungi, and animals are consistent with biological explanations for both the Precambrian Snowball Earth and Cambrian explosion. This all adds up to a worthwhile read for students and other interested biologists with newly developed interests in inferring the timing of evolutionary events.
The long gestation of this book is unfortunate, though the significance of the papers is enhanced by their being representative of the changing nature of the field, for which apparent incongruence between alternative approaches is driving debate that is becoming less about polarization and more about scientific rigor. Specialists on molecular dating or the fossil record should not expect to find much inspiration with regard to their own discipline, but the book promotes an understanding of the perspectives of the alternative approaches, and this is of central importance in resolving the timescale of biological evolution.
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Acknowledgements |
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Matthew J. Phillips, Henry Wellcome Ancient Biomolecules Centre, Department of Zoology, University of Oxford, Oxford, OX1 3PS, UK.
Gonzalo Giribet, Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, 16 Divinity Avenue, Cambridge, Massachusetts 02138, USA; E-mail: ggiribet@oeb.harvard.edu
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Bromham L., Penny D., Rambaut A., Hendy M. D. The power of relative rates tests depends on the data. J. Mol. Evol. (2000) 50:296–301.[Web of Science][Medline]
Cracraft J. Avian evolution, Gondwana biogeography and the Cretaceous-Tertiary mass extinction event. Proc. Roy. Soc. Lond. B (2001) 268:459–469.[Medline]
Cooper A., Penny D. Mass survival of birds across the Cretaceous-Tertiary boundary: Molecular evidence. Science (1997) 275:1109–1113.
Foote M., Raup D. M. Fossil preservation and the stratigraphic ranges of taxa. Paleobiology (1996) 22:121–140.[Abstract]
Lewis P. O. A likelihood approach to estimating phylogeny from discrete morphological characte. data. Syst. Biol. (2001) 50:913–925.
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Nei M., Xu P., Glazko G. Estimation of divergence times from multiprotein sequences for a few mammalian species and several distantly related organisms. Proc. Natl Acad. Sci. USA (2001) 98:2497–2502.
Sanderson M. J. Estimating absolute rates of molecular evolution and divergence times: A penalized likelihood approach. Mol. Biol. Evol. (2002) 19:101–109.
Thorne J. L., Kishino H. Divergence time and evolutionary rate estimation with multilocus data. Syst. Biol. (2002) 51:689–702.
Zuckerkandl E., Pauling L. Evolutionary divergence and convergence in proteins. In: Evolving genes and proteins—Bryson V., Vogel H. J., eds. (1965) New York: Academic Press. 97–166.
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