In order to develop models which appropriately reflect microsatellite evolution, more knowledge is required about the processes by which these simple sequences evolve. In this study, historical mutation events in three avian microsatellite loci belonging to distinct classes of repeat types (one perfect di-, one compound di-, and one perfect tetranucleotide repeat) were examined by sequence analysis of 76 alleles in 39 species spanning the avian phylogeny. The mode and tempo of evolution varied greatly between loci. For the perfect dinucleotide repeat, intraspecific length polymorphism was detected when alleles contained as few as six or seven repeat units, and size expansion over evolutionary timescales was demonstrated for repeats as short as (AG)2. A remarkable level of fragment stability was found for the compound dinucleotide repeat, even in species thought to have diverged over 60 MYA, coinciding with a high level of primer sequence conservation at this locus. In contrast, a hypervariable (AAAG)n locus revealed extraordinary instability and structural heterogeneity in the repeat region, including long arrays of derivative repeat motifs such as (AG)n, (AAGG)n, (AAAAG)n, and even (AAAGAGAG)n. Often, several motifs could be found within the same allele. A large number of cases of allele size homoplasy were detected for all three loci. These findings reinforce the fact that greater attention should be paid to the repeat type and the mutational characteristics of a marker before use in phylogenetic studies.