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Evolution of Repeated Sequences in the Ribosomal DNA Intergenic Spacer of 32 Arthropod Species

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Abstract

The evolution of a multigene family (MGF) is affected by the structure and function of its regulatory elements, specifically by the link between recombination and DNA transcription and/or replication. The ribosomal DNA (rDNA) MGF is often hierarchically repetitive, combining function with repetition in a single genic system. Its tandemly repeated operons contain the transcription unit of the 45S ribosomal RNA precursor alternating with an intergenic spacer (IGS) that commonly includes repeated transcription regulatory elements. To study the evolution of repeated sequences and the influence of repeat characteristics on their sequence divergence, we sequenced and characterized a single complete IGS from 11 daphniid species and analyzed their repeat arrays along with those from an additional 21 species of arthropods. We tested the hypotheses that sequence similarity is higher among tandemly arrayed repeats than among interleaved or dispersed repeats, and that the homogeneity of repeat arrays is affected by the number and the length of repeats, as well as by the presence of putative regulatory elements. We found that both tandem repeat organization and the presence of a TATA motif are significantly correlated with increased sequence similarity among homologous IGS repeats. We also observed that some repeat types are only found in a single species, while others appear to have persisted for >100 MY, with evidence for homologous repeat types in sister species. Taken together, these data suggest that both drift and natural selection influence repeat evolution within the IGS.

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Acknowledgments

This work was supported by a grant from the Natural Sciences and Engineering Research Council of Canada to TJC. CDA was supported by Ontario Graduate Scholarships. We thank A. Holliss for assistance with the DNA sequencing. D. Irwin, R. Danzmann, L. Weider, S. McTaggart, and two anonymous reviewers provided helpful comments on the manuscript.

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Correspondence to Teresa J. Crease.

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Ambrose, C.D., Crease, T.J. Evolution of Repeated Sequences in the Ribosomal DNA Intergenic Spacer of 32 Arthropod Species. J Mol Evol 70, 247–259 (2010). https://doi.org/10.1007/s00239-010-9324-4

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