Queen execution increases relatedness among workers of the invasive Argentine ant, Linepithema humile

Polygyny in social insects can greatly reduce within-nest genetic relatedness. In polygynous ant species, potential rival queens in colonies with multiple queens are often executed by other queens, workers, or both. The Argentine ant, Linepithema humile, native to South America, forms a "supercolony" that is composed of a large number of nests and is considered to contribute to the ant's invasion success. Currently, four mutually antagonistic supercolonies are contiguously distributed within a small area of Japan. Here, we analyzed the genetic structure and relatedness within and among the four supercolonies using microsatellite markers to clarify how L. humile maintains its supercoloniality. The results of AMOVA and BASP, the F ST values, and the existence of several private alleles indicated that the L. humile population in the Kobe area had a characteristic genetic structure. Within a given supercolony, there was significant genetic differentiation (F ST) among workers collected in May and those collected in September. The significant deviation from Hardy-Weinberg equilibrium increased, and the relatedness among workers significantly increased from May to September in all supercolonies. This result suggested that the supercolonies replaced old queens with new ones during the reproductive season, thus supporting the plausibility of queen execution. From the perspective of kin selection, workers collectively eliminate queens, thereby increasing their own inclusive fitness. Restricted gene flow among supercolonies, together with mating with sib and queen execution, could help to maintain the unique social structure of L. humile, the distribution of which is expanding worldwide.