We examined the evolution of the repeat regions of three noncoding microsat
ellite loci in 58 species of the Polistinae, a subfamily of wasps that dive
rged over 140 million years ago. A phylogenetic approach allows two new kin
ds of approaches to studying microsatellite evolution: character mapping an
d comparative analysis. The basic repeat structure of the loci was highly c
onserved, but was often punctuated with imperfections that appear to be phy
logenetically informative. Repeat numbers evolved more rapidly than other c
hanges in the repeat region. Changes in number of repeats among species see
m consistent with the stepwise mutation model, which is based on slippage d
uring replication as the main source of mutations. Changes in repeat number
s can occur even when there are very few tandem repeats but longer repeats,
especially perfect repeats led to greater rates of evolutionary change. Sp
ecies phylogenetically closer to the one from which we identified the loci
had longer stretches of uninterrupted repeats and more different motifs, bu
t not longer total repeat regions. The number of perfect repeats increased
more often than it decreased. However, there was no evidence that some spec
ies have consistently greater numbers of repeats across loci than other spe
cies have, once ascertainment bias is eliminated. We also found no evidence
for a population size effect posited by one form of the directionality hyp
othesis. Overall, phylogenetic variation in repeat regions can be explained
by adding neutral evolution to what is already known about the mutation pr
ocess. The life cycle of microsatellites appears to reflect a balance betwe
en growth by slippage and degradation by an essentially irreversible accumu
lation of imperfections.