Dynamics of concerted evolution of ribosomal DNA and histone gene families in the melanogaster species subgroup of Drosophila

Many multigene and non-coding families of DNA reveal unexpected high levels of sequence homogeneity (concerted evolution). In order to assess the rates and mechanisms of concerted evolution, we have analysed sequence variation in functionally diverse regions of the ribosomal DNA and histone gene families in seven sibling species of the Drosophila melanogaster species subgroup. Variant sequences of the non-transcribed and transcribed rDNA spacers have become fixed in both the X and Y chromosome rDNA clusters in a diagnostic manner for each species. Similarly, species-specific variants have become fixed in the spacer and coding regions of the histone cluster. Variation in non-transcribed spacer length, within and between species, is based on multiples of the periodicity of an internal region of repetition within the non-transcribed spacer. These observations, in conjunction with the genetic analysis of the extensive polymorphism in non-transcribed spacer length and copy-number in D. melanogaster (Coen et al., 1982) suggest that unequal exchange is a relatively rapid process and results in a turnover of sequences at several periodicities within the arrays. The rate of turnover can contribute substantially to the fixation of variants within an array and the stochastic process of drift can contribute to the fixation of an array in a population. However, the observation that regions of rDNA and histone repeats have become homogeneous for variants that can discriminate between the two most closely related and recently diverged species suggests that additional processes might be required to drive variants to complete fixation. Data on the distribution of the type I and type II introns of the rDNA implies a process of continual re-insertion into newly fixed rDNA variants during the homogenization process. Comparative data on the forces responsible for the evolutionary progression of variants in families of larger copy-number and wider karyotypic distribution in the same group of species are described in the accompanying paper (Strachan et al., 1982).