Telling the Evolutionary Time: Molecular Clocks and the Fossil Record

Chapter 1

Molecular clocks: whence and whither?

Francisco Rodríguez-Trelles, Rosa Tarrío and Francisco J.Ayala

ABSTRACT

The neutrality theory of molecular evolution predicts that the rate of molecular

evolution is constant over time, and thus that there is a molecular clock that can be

used for timing evolutionary events. Experimental data have shown that the

variance of the rate of evolution is generally larger than expected according to the

neutrality theory. This raises the question of how reliable the molecular clock is or,

indeed, whether there is a molecular clock. We have carried out an extensive

investigation of nine proteins in organisms belonging to the three multicellular

kingdoms, namely ADH, AMD, DDC, GPDH, G6PD, PGD, SOD, TPI, and XDH.

We observe that the nine proteins evolve erratically through time and across

lineages. The observations are inconsistent with the neutrality theory and also with

various subsidiary hypotheses proposed to account for the overdispersion of the

molecular clock.

Introduction: the hypothesis of a molecular clock

Biological evolution is a time-dependent process, by and large unidirectional. Some
degree of correlation is, therefore, expected between the biological differentiation of two
organisms and the time elapsed since their separation, by the comparison between an
organism and its ancestor, or between two organisms sharing a common ancestor. The
correlation, however, need not be exact, if only because organisms evolve in response to
the vagaries of environmental change in time and space. It is well known that some
organisms have evolved fast morphologically, at least with respect to some traits, whereas
others have changed but little over millions of years (see, e.g. Dobzhansky et al. 1977, pp.
327–31). Zuckerkandl and Pauling (1962, 1965; see also Margoliash, 1963) proposed
that the time-change correlation might be more approximately precise if change were
measured in the protein and nucleic acid components of organisms, indeed that there
might be a molecular clock of evolution.
The hypothesis of the molecular clock was advanced on the grounds that most amino acid
substitutions in a protein (or nucleotides in a gene) occur between functionally equivalent
residues, so that their replacement along evolving lineages would be determined by
mutation rate and time elapsed, rather than by natural selection (Zuckerkandl and Pauling