Variation in queen phenotype and reproductive role in the fire ant Sol
enopsis invicta has been shown to have a simple genetic basis in a sin
gle introduced population in the United States. The evidence consists
of an association between this variation and queen genotype at Pgm-3,
a phosphoglucomutase-encoding gene. In the present study, we surveyed
Pgm-3 allele and genotype frequencies in diverse populations from the
native and introduced ranges of this ant to learn whether this simple
genetic basis for reproductive traits is a general feature of the spec
ies or a genetic anomaly in introduced ants stemming from a recent bot
tleneck or the invasion of novel habitats. No egg-laying queens living
in polygyne (multiple-queen) nests possessed the homozygous genotype
Pgm-3(a/a) in any of the study populations, yet nonreproductive female
s from such nests (workers as well as queens that had not yet initiate
d oogenesis) possessed this genotype at moderate frequencies. Remarkab
ly, Pgm-3(a/a) was the most common genotype among all classes of femal
es, including egg-laying queens, in monogyne (single-queen) nests from
all populations studied. Genotype proportions at Pgm-3 in polygyne po
pulations typically departed strongly from the proportions expected un
der Hardy-Weinberg equilibrium, whereas those in monogyne populations
did not. These patterns establish that a single mendelian gene influen
ces queen reproductive role in S. invicta and that this gene uniformly
is under strong directional selection in the polygyne social form onl
y. Moreover, the perfect association of Pgm-3 genotype and reproductiv
e role in all populations, combined with the known function of phospho
glucomutase in insect metabolism, suggest that this gene may directly
influence queen phenotypes rather than merely serving as a marker for
a linked gene that causes the effects.