Molecular evolution of repetitive sequences: The histone genes of Drosophila virilis

A large fraction of the eukaryotic genome consists of repetitive sequences. Many times repetitive sequences undergo an evolutionary process known as concerted evolution. Concerted evolution is a non-independent evolution that results in greater similarity between paralogs as compared to orthologs of even closely related species. For example, the histone repeats of Drosophila virilis are a concertedly evolving gene family. This study elucidates the molecular evolution of the D. virilis historic repeats. The D. virilis histone repeats consist of quintets (consists of divergently transcribed H2A:H2B and divergently transcribed H3:H4 histone genes as well as an H1 histone gene) and quartets (same histone gene geometry as quintets minus H1). Both quintets and quartets exhibit extensive length variations, allowing for easy identification. Also, these repeats are in tandem at two non-allelic positions, the major locus and the minor locus. The major locus consists of approximately 30 repeats and the minor locus has 6 repeats. Using the advantages of the D. virilis histone gene family we show the following: First, low resolution sequence analysis of repeats from both loci look very similar. However, high resolution analysis determined that the major and minor loci are evolving on different trajectories. Second, there is a hypothesis of an inverse relationship between the size of an array and the amount of variation. We show this is not the case with this gene family. Third, the minor locus does not show a correlation between repeat distance and variation. That is, neighboring repeats are not more alike than distant repeats. Fourth, the minor locus is the ancestral locus. Fifth, the evolution of two loci and length variations are not a recent event specific to D. virilis, but common to at least five other species of the virilis group.