Transition-transversion bias is not universal: a counter example from grasshopper pseudogenes

Abstract

Comparisons of the DNA sequences of metazoa show an excess of transitional over transversional substitutions. Part of this bias is due to the relatively high rate of mutation of methylated cytosines to thymine. Postmutation processes also introduce a bias, particularly selection for codon-usage bias in coding regions. It is generally assumed, however, that there is a universal bias in favour of transitions over transversions, possibly as a result of the underlying chemistry of mutation. Surprisingly, this underlying trend has been evaluated only in two types of metazoan, namely Drosophila and the Mammalia. Here, we investigate a third group, and find no such bias. We characterize the point substitution spectrum in Podisma pedestris, a grasshopper species with a very large genome. The accumulation of mutations was surveyed in two pseudogene families, nuclear mitochondrial and ribosomal DNA sequences. The cytosine-guanine (CpG) dinucleotides exhibit the high transition frequencies expected of methylated sites. The transition rate at other cytosine residues is significantly lower. After accounting for this methylation effect, there is no significant difference between transition and transversion rates. These results contrast with reports from other taxa and lead us to reject the hypothesis of a universal transition/transversion bias. Instead we suggest fundamental interspecific differences in point substitution processes.

Figure 1. Neutral Point Substitution Patterns in Two Types of Grasshopper Pseudogenes

(A and B) Frequency of the different substitutions in rDNA pseudogenes (black) and Numts (grey) expressed as a percentage of the average substitution rate.

Figure 2. Neutral Point Substitution Pattern in Grasshopper Pseudogenes Accounting for Multiple Substitutions

Maximum likelihood estimates of the frequency (with associated standard errors) of the different substitutions in grasshopper pseudogenes expressed as a percentage of the average substitution rate (C:G → T:A substitutions at CpG sites are excluded) (light grey, transversions; dark grey, transitions).

Figure 3. Neutral Point Substitution Patterns in the Grasshopper Podisma and the Fruit Fly Drosophila

Frequency of the different point substitutions in Podisma (black) and Drosophila (grey) (data from Petrov and Hartl [9]) expressed as a percentage of the average substitution rate.