Monitoring the Mode and Tempo of Concerted Evolution in the Drosophila Melanogaster rDNA Locus

By Averbeck, Karin Tetzlaff; Eickbush, Thomas H. | Genetics, December 2005 | Go to article overview

Monitoring the Mode and Tempo of Concerted Evolution in the Drosophila Melanogaster rDNA Locus


Averbeck, Karin Tetzlaff, Eickbush, Thomas H., Genetics


ABSTRACT

Non-LTR retrotransposons R1 and R2 have persisted in rRNA gene loci (rDNA) since the origin of arthropods despite their continued elimination by the recombinational mechanisms of concerted evolution. This study evaluated the short-term evolutionary dynamics of the rDNA locus by measuring the divergence among replicate Drosophila melanogaster lines after 400 generations. The total number of rDNA units on the X chromosome of each line varied from 140 to 310, while the fraction of units inserted with R1 and R2 retrotransposons ranged from 37 to 65%. This level of variation is comparable to that found in natural population surveys. Variation in locus size and retrotransposon load was correlated with large changes in the number of uninserted and R1-inserted units, yet the numbers of R2-inserted units were relatively unchanged. Intergenic spacer (IGS) region length variants were also used to evaluate changes in the rDNA loci. All IGS length variants present in the lines showed significant increases and decreases of copy number. These studies, combined with previous data following specific R1 and R2 insertions in these lines, help to define the type and distribution, both within the locus and within the individual units, of recombinational events that give rise to the concerted evolution of the rDNA locus.

TANDEMLY repeated multigene families frequently undergo concerted evolution, a phenomenon in which genes in a gene family show more sequence homogeneity within a species than between species. It has been suggested that homogenization occurs most rapidly within a chromosome (SCHLOTTERER and TAUTZ 1994) by recombinational mechanisms such as gene conversion, intrachromosomal loop deletions, and unequal crossovers between sister chromatids (DOVER 1994; ELDER and TURNER 1995; LIAO 1999). New sequence variants within an array can also increase in frequency and spread through a population by segregation and recombination between homologs and can eventually become fixed in the species by natural selection, molecular drive, or drift.

The ribosomal RNA gene locus (rDNA) is of particular interest for the study of concerted evolution. In eukaryotes, the rDNA locus is composed of hundreds to thousands of tandemly repeated rRNA genes interspersed with noncoding, intergenic spacer (IGS) regions (LONG and DAWID 1980). High redundancy of rRNA genes is critical for fitness because the ribosomal translational machinery of the cell is necessary in large quantities for growth and the RNA components of the ribosome structure do not benefit from translational amplification. Homogenization of the repeats within species is thought to be beneficial to the organism by ensuring that all ribosomal subunits are equally compatible with other components of the translational machinery. On the basis of population genetic studies, various recombinational models for explaining the homogeneity of the tandemly repeated rRNA genes have been proposed (CoEN et al. 1982; LYCKEGAARD and CLARK 1991; SCHLOTTERER and TAUTZ 1994; POLANCO etal. 1998, 2000).

An added complexity to understanding the evolution of the rDNA loci is that in many animal phyla these loci are home to specialized transposable elements (EiCKBUSH 2002; BURKE et al. 2003; KOJIMA and FUJIWARA 2004; PENTON and CREASE 2004). Best studied are the Rl and R2 non-LTR retrotransposable elements of arthropods. These elements insert into the 28S gene and render the inserted genes nonfunctional (LONG and DAWID 1979; KIDD and GLOVER 1981; EICKBUSH and EICKBUSH 2003). Rl and R2 have persisted via vertical descent in arthropods since the origin of the phylum, suggesting that occasional retrotransposition has been an effective strategy to evade elimination from the rDNA locus by the recombinational mechanisms of concerted evolution (BURKE et al. 1998; MALIK et al. 1999; GENTILE et al. 2001).

To derive a comprehensive population genetics model for the evolution of the rDNA locus and its Rl and R2 inhabitants, one must measure changes in multiple properties of the locus over time. …

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Monitoring the Mode and Tempo of Concerted Evolution in the Drosophila Melanogaster rDNA Locus
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