Mutation and Evolution of Microsatellite Loci in Neurospora

By Dettman, Jeremy R.; Taylor, John W. | Genetics, November 2004 | Go to article overview

Mutation and Evolution of Microsatellite Loci in Neurospora


Dettman, Jeremy R., Taylor, John W., Genetics


ABSTRACT

The patterns of mutation and evolution at 13 microsatellite loci were studied in the filamentous fungal genus Neurospora. First, a detailed investigation was performed on five microsatellite loci by sequencing each microsatellite, together with its nonrepetitive flanking regions, from a set of 147 individuals from eight species of Neurospora. To elucidate the genealogical relationships among microsatellite alleles, repeat number was mapped onto trees constructed from flanking-sequence data. This approach allowed the potentially convergent microsatellite mutations to be placed in the evolutionary context of the less rapidly evolving flanking regions, revealing the complexities of the mutational processes that have generated the allelic diversity conventionally assessed in population genetic studies. In addition to changes in repeat number, frequent substitution mutations within the microsatellites were detected, as were substitutions and insertion/deletions within the flanking regions. By comparing microsatellite and flankingsequence divergence, clear evidence of interspecific allele length homoplasy and microsatellite mutational saturation was observed, suggesting that these loci are not appropriate for inferring phylogenetic relationships among species. In contrast, little evidence of intraspecific mutational saturation was observed, confirming the utility of these loci for population-level analyses. Frequency distributions of alleles within species were generally consistent with the stepwise mutational model. By comparing variation within species at the microsatellites and the flanking-sequence, estimated microsatellite mutation rates were ~2500 times greater than mutation rates of flanking DNA and were consistent with estimates from yeast and fruit flies. A positive relationship between repeat number and variance in repeat number was significant across three genealogical depths, suggesting that longer microsatellite alleles are more mutable than shorter alleles. To test if the observed patterns of microsatellite variation and mutation could be generalized, an additional eight microsatellite loci were characterized and sequenced from a subset of the same Neurospora individuals.

MICROSATELLITES are composed of tandemly repeated, simple DNA sequence motifs of as many as six nucleotides in length. These loci are commonly found throughout both prokaryotic and eukaryotic genomes and typically are highly polymorphic within species and populations. In addition, these codominant genetic markers are relatively easy to score and have high reproducibility and specificity. As such, microsatelgelites have become one of the most popular classes of molecular markers and are commonly employed to investigate the population genetics of a diverse range of organisms (BRUFORD and WAYNE 1993; GOLDSTEIN and SCHLÖTTERER 1999). Although fewer studies have addressed the evolutionary dynamics and mutational processes of microsatellite loci, an understanding of these topics is beginning to develop (see ESTOUP and CORNUET 1999; SCHLÖTTERER 2000).

This study of microsatellite evolution in the model microbial eukaryote Neurospora had three main objectives:

1. To describe the patterns of mutation and evolution at multiple microsatellite loci: Are these patterns similar across loci and across species? Are these patterns consistent with accepted theories of microsatellite mutation and evolution?

2. To determine if microsatellites are appropriate genetic markers for inferring the phylogenetic relationships among species of Neurospora: At what level of phylogenetic divergence does microsatellite mutational saturation occur? Are the amounts of allelic homoplasy large enough to render interspecific comdressed parisons meaningless?

3. To determine if microsatellites would be useful for answering population genetic questions: What are the relative rates of microsatellite mutation, and how variable are these genetic markers within a single species? …

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