Highly efficient concerted evolution in the ribosomal DNA repeats: Total rDNA repeat variation revealed by whole-genome shotgun sequence data

Abstract

Repeat families within genomes are often maintained with similar sequences. Traditionally, this has been explained by concerted evolution, where repeats in an array evolve "in concert" with the same sequence via continual turnover of repeats by recombination. Another form of evolution, birth-and-death evolution, can also explain this pattern, although in this case selection is the critical force maintaining the repeats. The level of intragenomic variation is the key difference between these two forms of evolution. The prohibitive size and repetitive nature of large repeat arrays have made determination of the absolute level of intragenomic repeat variability difficult, thus there is little evidence to support concerted evolution over birth-and-death evolution for many large repeat arrays. Here we use whole-genome shotgun sequence data from the genome projects of five fungal species to reveal absolute levels of sequence variation within the ribosomal RNA gene repeats (rDNA). The level of sequence variation is remarkably low. Furthermore, the polymorphisms that are detected are not functionally constrained and seem to exist beneath the level of selection. These results suggest the rDNA is evolving via concerted evolution. Comparisons with a repeat array undergoing birth-and-death evolution provide a clear contrast in the level of repeat array variation between these two forms of evolution, confirming that the rDNA indeed does evolve via concerted evolution. These low levels of intra-genomic variation are consistent with a model of concerted evolution in which homogenization is very rapid and efficiently maintains highly similar repeat arrays.[Supplemental material is available online at www.genome.org.]Repetitive elements are an abundant feature of genomes (Britten and Kohne 1968) and play critical roles in cell biology, genome structure, and adaptive evolution (Andersson et al. 1998;Shapiro and von Sternberg 2005). In many cases, repeats from a repeat family are highly similar to one another within a genome, a pattern that persists through evolutionary time even though sequence differences are apparent between species (Brown et al. 1972). Thus, the repeats seem to be maintained as a coherent family. This pattern is contrary to the expectations of conventional evolution, where repeats are expected to evolve independently ( Fig. 1) and diverge with time. This unusual mode of evolution, where repeats within a genome are more similar to each other than they are to "orthologous" repeats in a related species, is defined as concerted evolution (Zimmer et al. 1980). The molecular process responsible for concerted evolution is known as homogenization (Dover 1982), and although not fully elucidated, is thought to involve continual turnover of repeat copies by unequal recombination (e.g., Smith 1973;Szostak and Wu 1980;Kobayashi et al. 1998). However, recent studies have shown that several repeat families previously thought to evolve by concerted evolution actually evolve via a different evolutionary process known as birth-...

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