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

Abstract

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 FST 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 (FST) 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.

Queen execution in a monogynous ant

“…Workers began to expel and kill the queens one to six weeks after colony collection in early spring. Contrary to previous observations in polygynous Argentine ants, in which queen executions apparently serve to increase the relatedness among workers (Inoue et al., 2015), aggression in T . crassispinus was not preferentially directed toward unrelated queens, which had usurped a colony and replaced the resident queen.…”

“…Queens of monogynous ants may live for several years (Keller, 1998; Keller & Genoud, 1997; Plateaux, 1971), and it is therefore not expected that workers kill the only individual in the nest that is capable of producing female offspring. Queen killing in societies of perennial social insects has so far been reported only from polygynous ants and stingless bees, where surplus young queens are eliminated (Balas, 2005; Inoue et al., 2015; Keller et al., 1989; Wenseleers et al., 2004), when new colonies of monogynous species are cooperatively initiated by several foundresses (Bernasconi & Strassmann, 1999; Forsyth, 1980; Heinze, 1993), or when matched‐mated queens produce large numbers of diploid males instead of workers (Vollet‐Neto et al., 2019). Furthermore, in the raider ant Ooceraea biroi workers, which produce female offspring via thelytokous parthenogenesis out of synchrony with other reproductives, may be attacked and killed by their nestmates (Teseo et al., 2013).…”

Factors triggering queen executions in the Argentine ant

“…That said, Inoue et al . 22 showed that genetic diversity in Argentine ant workers significantly decreased from May to September and suggested that queen executions are a contributing factor.…”

Complete mitochondrial genome of the H3 haplotype Argentine ant Linepithema humile (Mayr, 1868) (Formicidae; Hymenoptera)

“…Mating occurs within colonies and new colonies are made when small fractions of the mother colony bud out forming smaller colonies (Keller and Passera 1992). While these supercolonies remained insignificant in native ranges, genetic bottleneck of initial introduction and following 'genetic cleansing' presumably by annual queen executions (Keller et al 1989;Inoue et al 2015) caused extreme relatedness within introduced populations which allowed massive supercolonies distributed over multiple continents (Tsutsui et al 2003). In Korea, Argentine ants have just arrived in southern ports of Busan and Kwangyang (Lee et al 2020).…”