GENETIC ORIGIN OF MALE DIPLOIDY IN THE FIRE ANT, SOLENOPSIS INVICTA (HYMENOPTERA: FORMICIDAE), AND ITS EVOLUTIONARY SIGNIFICANCE.

Abstract

Male diploidy was studied in natural populations of the fire ant, Solenopsis invicta, in order to find an explanation from population genetics for the apparently common occurrence of this phenomenon in some North American populations. The association of male diploidy with polygyne (more than one queen per colony) populations in this species led us to expect that the two phenomena are causally linked. We proposed three hypotheses, based on current knowledge of sex-determining mechanisms in the Hymenoptera, to explain the loss of genetic diversity associated with high rates of diploid male production in S. invicta: a) allelic diversity was reduced during colonization of North America by a small founder group; b) allelic diversity was reduced during subsequent subfounding of the several polygyne populations; and c) genetic structuring of polygyne populations due to local inbreeding caused reduced allelic diversity and/or increased homozygosity. An extensive survey revealed that diploid males are common in all four polygyne (P) populations studied, and that none occur in the monogyne (M) population in north-central Georgia. On the other hand, newly mated (i.e., colony-founding) queens from this same M population produced diploid males in the laboratory, and in the Georgia M and P populations, the frequencies of queens that produce diploid males were shown to be similar. We conclude that the frequent production of diploid males in S. invicta has resulted from a loss of allelic diversity during colonization of North America rather than from any special genetic attribute of P populations. We found no evidence for genetic structuring of the Georgia P population or for decreased allelic diversity relative to the Georgia M population. Thus, the exclusive occurrence of diploid males in P populations does not reflect a fundamental difference between P and M populations in the genetic determinants of male diploidy but is, rather, the result of differential mortality of diploid-male-producing colonies of the two forms. In view of these results, the common occurrence of male diploidy in the P form of S. invicta cannot be taken as evidence of a role for kin selection in the evolution of polygyny. (In this paper, "polygyny" is used to refer to a multiple-queen society.) Studies of the progeny of single queens with allozyme markers demonstrated that diploid male S. invicta are produced biparentally, as in other hymenopteran species. Diploid males were found to take part in the normal summer mating flights in the Georgia P population, although the significance of this behavior is unknown. Males sampled from two P populations exhibited bimodal size distributions, with the diploid males consistently larger than haploids. Assuming a single locus sex determinant, we estimate 15 alleles at this locus for both forms of the ant in North America.