Reading the entrails of chickens: molecular timescales of evolution and the illusion of precision

doi:10.1016/j.tig.2003.12.003

Trends in Genetics

Volume 20, Issue 2, February 2004, Pages 80-86

https://doi.org/10.1016/j.tig.2003.12.003 Get rights and content

Abstract

For almost a decade now, a team of molecular evolutionists has produced a plethora of seemingly precise molecular clock estimates for divergence events ranging from the speciation of cats and dogs to lineage separations that might have occurred ∼4 billion years ago. Because the appearance of accuracy has an irresistible allure, non-specialists frequently treat these estimates as factual. In this article, we show that all of these divergence-time estimates were generated through improper methodology on the basis of a single calibration point that has been unjustly denuded of error. The illusion of precision was achieved mainly through the conversion of statistical estimates (which by definition possess standard errors, ranges and confidence intervals) into errorless numbers. By employing such techniques successively, the time estimates of even the most ancient divergence events were made to look deceptively precise. For example, on the basis of just 15 genes, the arthropod–nematode divergence event was ‘calculated’ to have occurred 1167±83 million years ago (i.e. within a 95% confidence interval of ∼350 million years). Were calibration and derivation uncertainties taken into proper consideration, the 95% confidence interval would have turned out to be at least 40 times larger (∼14.2 billion years).

Section snippets

Chapter 1: the origin of the primary 310±0 million-year calibration

The saga starts with ‘an accurate calibration point’ for obtaining ‘reliable estimates of divergence times from molecular data’ [1]. From among the many calibration points available in the paleontological literature, ‘the relatively well-constrained fossil divergence time between the ancestor of birds (diapsid reptiles) and mammals (synapsid reptiles)’ was selected [1]. This divergence time was said to be 310 million years ago (MYA). As a calibrating measurement, the 310-MYA value is treated as

Chapter 2: the origin of the secondary 110±0 million-year calibration

The second chapter purports to estimate ‘a molecular timescale for vertebrate evolution’ [3], although what are in fact estimated are divergence times between humans and other organisms. Because of a lack of sufficient molecular data from chicken, the primary calibration point can not be used for the vast majority of protein comparisons. Kumar and Hedges [3], thus, opted for a secondary calibration point. (Secondary calibration points are divergence-time estimates that have been derived from

Chapter 3: transubstantiation of a secondary calibration into a primary calibration

The reason for the transformation of the secondary calibration date into a primary one, which is equivalent to blood becoming Cabernet Sauvignon, is purportedly based on external evidence: ‘Fossil evidence (Archibald 1996) also supports an early divergence time (>90 Ma) for the primate-rodent split’ [4]. Unfortunately, the Science article by Archibald [48] is entitled Fossil Evidence for a Late Cretaceous Origin of “Hoofed” Mammals, and as such deals with neither rodents nor humans. Thus, the

Chapter 4: tautological comparison of the 310±0 versus 110±0 MYA calibrations

An important detour in the saga of assigning precise timescales to the evolution of everything is found in a paper in which the miracle of transubstantiation attains fulfillment [5]. In this paper, the 310±0 MYA and the 110±0 MYA dates are treated as ‘independent’ calibrations for purposes of dating avian divergence events. The results based on the 310±0 MYA calibration and the results based on the 110±0 MYA calibration are compared and discussed. Unsurprisingly, because one date was derived

Chapter 5: errorless molecular estimates substitute for fossil evidence

The fifth chapter in the saga marks the emergence of five tertiary calibration points [6]. That is, five estimates from Wang et al. [4] that were derived from the secondary 110±0 MYA calibration, which in turn was derived from the primary 310±0 MYA calibration, are turned into ‘errorless’ (±0) calibrations, from which further molecular-clock estimates are derived. The tertiary calibration pairs are: plants versus animals, animals versus fungi, plants versus fungi, nematodes versus arthropods

Chapter 6: dating Genesis

The continuation of the saga is as predictable as it is outlandish. By using tertiary, and possibly quaternary, quinary and senary derivations from the mythical 310±0 chicken–human calibration, five of the most ancient divergence events are dated [2]. The pinnacle is reached with an estimate of 3.97±0.25 billion years ago for the divergence between archaebacteria and eukaryotes. An illustrative example of the extrapolations involved in estimating ancient divergence events is shown in Figure 2.

Postscript: the 110±0 MYA calibration dies but its descendants survive

In what will surely not be the last chapter in this story, a recent review in Trends in Genetics [13] contains four blood-curdling innovations involving statistical methodology, taxonomy, physics of time reversal and logic. The statistical novelty concerns the primate–artiodactyl divergence time, which was 90±8 MYA in Hedges at al. [1], whereas in Ref. [13] it is quoted as ‘90–98 million years ago.’ This change turns the mean into the lower end of the range and reduces by 76% the

Conclusion and recommendation

Despite their allure, we must sadly conclude that all divergence estimates discussed here 1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13 are without merit. Our advice to the reader is: whenever you see a time estimate in the evolutionary literature, demand uncertainty!

Acknowledgements

We thank John H. Calder, Daniel A. Chamovitz, Or M. Graur, S. Blair Hedges, Michael S.-Y. Lee, Michael Ovadia, Robert R. Reisz and Shaul Shaul for information.

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Trends in Genetics

Reading the entrails of chickens: molecular timescales of evolution and the illusion of precision

Abstract

Section snippets

Chapter 1: the origin of the primary 310±0 million-year calibration

Chapter 2: the origin of the secondary 110±0 million-year calibration

Chapter 3: transubstantiation of a secondary calibration into a primary calibration

Chapter 4: tautological comparison of the 310±0 versus 110±0 MYA calibrations

Chapter 5: errorless molecular estimates substitute for fossil evidence

Chapter 6: dating Genesis

Postscript: the 110±0 MYA calibration dies but its descendants survive

Conclusion and recommendation

Acknowledgements

Gene

Gene

Trends Ecol. Evol.

Mol. Phylog. Evol.

Gene

Continental breakup and the ordinal divergence of birds and mammals

Nature

A molecular timescale for vertebrate evolution

Nature

Divergence time estimates for the early history of animal phyla and the origin of plants, animals and fungi

Proc. R. Soc. Lond. B. Biol. Sci.

Calibration of avian molecular clocks

Mol. Biol. Evol.

Molecular evidence for the early colonization of land by fungi and plants

Science

The origin and evolution of model organisms

Nat. Rev. Genet.

Vertebrate genomes compared

Science

Human and ape molecular clocks and constraints on paleontological hypotheses

J. Hered.

A molecular phylogeny of reptiles

Science

Genomic clocks and evolutionary timescales

Trends Genet.

The fossil record of North American mammals: evidence for a Paleocene evolutionary radiation

Syst. Biol.

Early origins of modern birds and mammals: molecules vs. morphology

BioEssays

Molecular clock calibrations and metazoan divergence dates

J. Mol. Evol.

The power of relative rates tests depends on the data

J. Mol. Evol.

Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach

Mol. Biol. Evol.

r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock

Bioinformatics

Perils of paralogy: Using HSP70 genes for inferring organismal phylogenies

Syst. Biol.

Dating the tree of life

Science