Multilocus evolution in fire ants: effects of selection, gene flow and recombination.

The reproductive success of individual fire ant queens (Solenopsis invicta) previously has been shown to be strongly influenced by their genotype at a single enzyme-encoding gene, designated Pgm-3. This paper presents evidence that a second, tightly linked gene, designated Gp-9, is under similarly strong selection in these ants. Selection appears to act independently on the two genes and is detectable in only one of the two social forms of this species (the "polygyne" social form in which nests contain multiple fertile queens). Strong directional selection on Pgm-3 in this form, involves worker destruction of all queens with genotype Pgm-3AA before they reproduce. Selection on Gp-9 is more complex, involving both lethality of all Gp-9bb females and a strong or even complete survival advantage to reproductive queens with the heterozygous genotype Gp-9Bb. Pgm-3 and Gp-9 are tightly linked (rf = 0.0016) and exhibit strong gametic phase disequilibrium in introduced populations in the U.S. This disequilibrium seems not to have stemmed from the founder event associated with the introduction, because the same associations of alleles found in the U.S. apparently occur also in two native populations in Argentina. Rather, selection acting independently on Pgm-3 and Gp-9, in conjunction with gene flow from the alternate, "monogyne" social form (in which nests contain a single fertile queen), may explain the origin of disequilibrium between the two loci in polygyne fire ants.