Long Microsatellite Alleles in Drosophila melanogaster Have a Downward Mutation Bias and Short Persistence Times, Which Cause Their Genome-Wide Underrepresentation

Corresponding author: Christian Schlötterer, Institut für Tierzucht und Genetik, Veterinärplatz 1, 1210 Vienna, Austria., christian.schloetterer{at}vu-wien.ac.at (E-mail)

Communicating editor: Y.-X. FU

Microsatellites are short tandemly repeated DNA sequence motifs that are highly variable in most organisms. In contrast to mammals, long microsatellites (>15 repeats) are extremely rare in the Drosophila melanogaster genome. To investigate this paucity of long microsatellites in Drosophila, we studied 19 loci with exceptionally long microsatellite alleles. Inter- and intraspecific analysis showed that long microsatellite alleles arose in D. melanogaster only very recently. This lack of old alleles with many repeats indicated that long microsatellite alleles have short persistence times. The size distribution of microsatellite mutations in mutation-accumulation lines suggests that long alleles have a mutation bias toward a reduction in the number of repeat units. This bias causes the short persistence times of long microsatellite alleles. We propose that species-specific, size-dependent mutation spectra of microsatellite alleles may provide a general mechanism to account for the observed differences in microsatellite length between species.

This article has been cited by other articles:

				R. McConnell, S. Middlemist, C. Scala, J. E. Strassmann, and D. C. Queller An Unusually Low Microsatellite Mutation Rate in Dictyostelium discoideum, an Organism With Unusually Abundant Microsatellites Genetics, November 1, 2007; 177(3): 1499 - 1507. [Abstract] [Full Text] [PDF]

				W. Wang, J. Xu, L. Xu, B. Yue, and F. Zou The instability of (GpT)n and (ApC)n microsatellites induced by formaldehyde in Escherichia coli Mutagenesis, September 1, 2007; 22(5): 353 - 357. [Abstract] [Full Text] [PDF]

				J. Laidlaw, Y. Gelfand, K.-W. Ng, H. R. Garner, R. Ranganathan, G. Benson, and J. W. Fondon III Elevated Basal Slippage Mutation Rates among the Canidae J. Hered., August 3, 2007; (2007) esm017v2. [Abstract] [Full Text] [PDF]

				O. Paun and E. Horandl Evolution of Hypervariable Microsatellites in Apomictic Polyploid Lineages of Ranunculus carpaticola: Directional Bias at Dinucleotide Loci Genetics, September 1, 2006; 174(1): 387 - 398. [Abstract] [Full Text] [PDF]

				J. M. Marshall and R. E. Weiss A Bayesian Heterogeneous Analysis of Variance Approach to Inferring Recent Selective Sweeps Genetics, August 1, 2006; 173(4): 2357 - 2370. [Abstract] [Full Text] [PDF]

				E. J. Vowles and W. Amos Quantifying Ascertainment Bias and Species-Specific Length Differences in Human and Chimpanzee Microsatellites Using Genome Sequences Mol. Biol. Evol., March 1, 2006; 23(3): 598 - 607. [Abstract] [Full Text] [PDF]

				H. Karaoglu, C. M. Y. Lee, and W. Meyer Survey of Simple Sequence Repeats in Completed Fungal Genomes Mol. Biol. Evol., March 1, 2005; 22(3): 639 - 649. [Abstract] [Full Text] [PDF]

				M. Perez, F. Cruz, and P. Presa Distribution Properties of Polymononucleotide Repeats in Molluscan Genomes J. Hered., January 1, 2005; 96(1): 40 - 51. [Abstract] [Full Text] [PDF]

				M. D. Prasad, M. Muthulakshmi, M. Madhu, S. Archak, K. Mita, and J. Nagaraju Survey and Analysis of Microsatellites in the Silkworm, Bombyx mori: Frequency, Distribution, Mutations, Marker Potential and Their Conservation in Heterologous Species Genetics, January 1, 2005; 169(1): 197 - 214. [Abstract] [Full Text] [PDF]

				R. Sainudiin, R. T. Durrett, C. F. Aquadro, and R. Nielsen Microsatellite Mutation Models: Insights From a Comparison of Humans and Chimpanzees Genetics, September 1, 2004; 168(1): 383 - 395. [Abstract] [Full Text] [PDF]

				P. Almeida and C. Penha-Goncalves Long Perfect Dinucleotide Repeats Are Typical of Vertebrates, Show Motif Preferences and Size Convergence Mol. Biol. Evol., July 1, 2004; 21(7): 1226 - 1233. [Abstract] [Full Text] [PDF]

				Y. Lai and F. Sun The Relationship Between Microsatellite Slippage Mutation Rate and the Number of Repeat Units Mol. Biol. Evol., December 1, 2003; 20(12): 2123 - 2131. [Abstract] [Full Text] [PDF]

				M. O. Kauer, D. Dieringer, and C. Schlotterer A Microsatellite Variability Screen for Positive Selection Associated With the "Out of Africa" Habitat Expansion of Drosophila melanogaster Genetics, November 1, 2003; 165(3): 1137 - 1148. [Abstract] [Full Text] [PDF]

				S. Souames, E. Bonnivard, C. Bazin, and D. Higuet High Mutation Rate of TPE Repeats: A Microsatellite in the Putative Transposase of the hobo Element in Drosophila melanogaster Mol. Biol. Evol., November 1, 2003; 20(11): 1826 - 1832. [Abstract] [Full Text] [PDF]

				D. Dieringer and C. Schlotterer Two Distinct Modes of Microsatellite Mutation Processes: Evidence From the Complete Genomic Sequences of Nine Species Genome Res., October 1, 2003; 13(10): 2242 - 2251. [Abstract] [Full Text] [PDF]

				C. L. Ross, K. A. Dyer, T. Erez, S. J. Miller, J. Jaenike, and T. A. Markow Rapid Divergence of Microsatellite Abundance Among Species of Drosophila Mol. Biol. Evol., July 1, 2003; 20(7): 1143 - 1157. [Abstract] [Full Text] [PDF]

				J. C. Whittaker, R. M. Harbord, N. Boxall, I. Mackay, G. Dawson, and R. M. Sibly Likelihood-Based Estimation of Microsatellite Mutation Rates Genetics, June 1, 2003; 164(2): 781 - 787. [Abstract] [Full Text] [PDF]

				P. Calabrese and R. Durrett Dinucleotide Repeats in the Drosophila and Human Genomes Have Complex, Length-Dependent Mutation Processes Mol. Biol. Evol., May 1, 2003; 20(5): 715 - 725. [Abstract] [Full Text] [PDF]

				M. T. Webster, N. G. C. Smith, and H. Ellegren Microsatellite evolution inferred from human- chimpanzee genomic sequence alignments PNAS, June 25, 2002; 99(13): 8748 - 8753. [Abstract] [Full Text] [PDF]

				J. Brohede, C. R. Primmer, A. Moller, and H. Ellegren Heterogeneity in the rate and pattern of germline mutation at individual microsatellite loci Nucleic Acids Res., May 1, 2002; 30(9): 1997 - 2003. [Abstract] [Full Text] [PDF]

				D. Metzgar, L. Liu, C. Hansen, K. Dybvig, and C. Wills Domain-Level Differences in Microsatellite Distribution and Content Result from Different Relative Rates of Insertion and Deletion Mutations Genome Res., March 1, 2002; 12(3): 408 - 413. [Abstract] [Full Text] [PDF]

				C. Schlotterer A Microsatellite-Based Multilocus Screen for the Identification of Local Selective Sweeps Genetics, February 1, 2002; 160(2): 753 - 763. [Abstract] [Full Text] [PDF]

				M. Kauer, B. Zangerl, D. Dieringer, and C. Schlotterer Chromosomal Patterns of Microsatellite Variability Contrast Sharply in African and Non-African Populations of Drosophila melanogaster Genetics, January 1, 2002; 160(1): 247 - 256. [Abstract] [Full Text] [PDF]

				G. Queney, N. Ferrand, S. Weiss, F. Mougel, and M. Monnerot Stationary Distributions of Microsatellite Loci Between Divergent Population Groups of the European Rabbit (Oryctolagus cuniculus) Mol. Biol. Evol., December 1, 2001; 18(4): 2169 - 2178. [Abstract] [Full Text]

				G. Queney, N. Ferrand, S. Weiss, F. Mougel, and M. Monnerot Stationary Distributions of Microsatellite Loci Between Divergent Population Groups of the European Rabbit (Oryctolagus cuniculus) Mol. Biol. Evol., December 1, 2001; 18(12): 2169 - 2178. [Abstract] [Full Text] [PDF]

				P. P. Calabrese, R. T. Durrett, and C. F. Aquadro Dynamics of Microsatellite Divergence Under Stepwise Mutation and Proportional Slippage/Point Mutation Models Genetics, October 1, 2001; 159(2): 839 - 852. [Abstract] [Full Text] [PDF]

				M. V. Katti, P. K. Ranjekar, and V. S. Gupta Differential Distribution of Simple Sequence Repeats in Eukaryotic Genome Sequences Mol. Biol. Evol., July 1, 2001; 18(7): 1161 - 1167. [Abstract] [Full Text] [PDF]

				M. P. H. Stumpf and D. B. Goldstein Genealogical and Evolutionary Inference with the Human Y Chromosome Science, March 2, 2001; 291(5509): 1738 - 1742. [Abstract] [Full Text]