J Mol Evol (1994) 39:160-173
Journal
of Molecular
Evolution
© Springer-Verlag New YorkInc. 1994
Analysis of Directional Mutation Pressure and Nucleotide Content in
Mitochondrial Cytochrome b Genes
Lars S. Jermiin, Dan Graur,* Roger M. Lowe, Ross H. Crozier
School of Genetics and Human Variation, La Trobe University, Bundoora, Victoria 3083, Australia
Received and accepted: 23 February 1994
Abstract. We present a new approach for analyzing
directional mutation pressure and nucleotide content in
protein-coding genes. Directional mutation pressure,
the heterogeneity in the likelihood of different nucleo-
tide substitutions, is used to explain the increasing or de-
creasing guanine-cytosine content (GC%) in DNA and
is represented by ~D, in agreement with Sueoka (1962,
Proc Natl Acad Sci USA 48:582-592). The new method
uses simulation to facilitate identification of significant
A + T or G + C pressure as well as the comparison of
directional mutation pressure among genes, even when
they are translated by different genetic codes. We use the
method to analyze the evolution of directional mutation
pressure and nucleotide content of mitochondrial cy-
tochrome b genes. Results from a survey of 110 taxa in-
dicate that the cytochrome b genes of most taxa are
subjected to significant directional mutation pressure
and that the gene is subject to A + T pressure in most
cases. Only in the anseriform bird Cairina moschata is
the cytochrome b gene subject to significant G + C pres-
sure. The GC% at nonsynonymous codon sites decreases
proportionately with increasing A + T pressure, and
with a slope less than one, indicating a presence of se-
lective constraints. The cytochrome b genes of insects,
nematodes, and eumycotes are subject to extreme A +
T pressures (#D = 0.123, 0.224, and 0.130) and, in par-
allel, the GC% of the nonsynonymous codon sites has
decreased from about 0.44 in organisms that are not
subjected to A + T or G + C pressure to about 0.332,
* Permanent address: Department of Zoology, George S. Wise Fac-
ulty of Life Science, Tel Aviv University, Ramat Aviv 69978, Israel
Correspondence to: L.S. Jermiin
0.323, and 0.367, respectively. The distribution of taxa
according to the GC% at nonsynonymous codon sites
and directional mutation pressure supports the notion
that variation in these parameters is a phylogenetic com-
ponent.
Key words: Directional mutation pressure -- A + T
pressure -- G + C pressure -- Synonymous codon sites
-- Nonsynonymous codon sites -- Mitochondrial cy-
tochrome b gene -- Metazoa -- Magnoliophyta --
Chlorophyta -- Eumycota
Introduction
More than 30 years age Freese (1962) and Sueoka (1962)
formulated a quantitative theory of directional muta-
tion pressure and used it to explain wide interspecific
(Lee et al. 1956; Belozersky and Spirin 1958) and nar-
row intragenomic (Sueoka 1959; Sueoka et al. 1959;
Rolfe and Meselson 1959) heterogeneities in the base
composition of bacterial DNA. The theory is based on
the assumption that all nucleotide substitutions in DNA
are not equiprobable, but can have an overall direc-
tionality toward higher or lower GC%. The theory pre-
dicts that the GC% is determined by selective con-
straints and two antagonistic mutation rates u and v; u
being the mutation rate from an A:T or a T:A nucleotide
pair (cx pairs) to a G:C or a C:G nucleotide pair (y pairs),
with v being the reverse mutation rate. Mathematically,
directional mutation pressure is defined as occurring
when gi) v~ 0.5, where FtD = v/(v + u), and is equal to
the GC% in those nucleotide sites that are selectively
neutral and in equilibrium (Sueoka 1962, 1988, 1992).