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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 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.

SUBMITTER: Inoue MN

PROVIDER: S-EPMC4588641 | biostudies-other | 2015 Sep

REPOSITORIES: biostudies-other

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Project description:BackgroundEfficient division of reproductive labor is a crucial characteristic of social insects and underlies their ecological and evolutionary success. Despite of the harmonious appearance of insect societies, nestmates may have different interests concerning the partitioning of reproduction among group members. This may lead to conflict about reproductive rights. As yet, few studies have investigated the allocation of reproduction among queens in multi - queen societies ("reproductive skew"). In the ant Leptothorax acervorum, reproductive skew varies considerably among populations. While reproduction is quite equally shared among nestmate queens in most populations from boreal Eurasia (low skew), colonies from populations at the edge of the species' range are characterized by "functional monogyny," i.e., high skew. The proximate mechanisms underlying high skew, in particular how workers influence which queen lays eggs, are not well understood. We investigated the behavior of queens and workers in functionally monogynous colonies of L. acervorum from two mountain ranges in central Spain.ResultsWe provide evidence for both queen and worker influence on the outcome of conflict over reproduction in colonies of L. acervorum from Spain. The patterns of queen - queen aggression and worker - queen grooming and feeding after hibernation allowed predicting, which queen later began to lay eggs. In contrast, worker aggression towards queens was not clearly associated with a queen's future reproductive success. Queen - queen and worker - queen aggression differed in quality: queens typically engaged in ritualized dominance behavior, such as antennal boxing, while workers also attacked queens by biting and prolonged pulling on their legs and antennae. In several cases, overt worker aggression led to the expulsion of queens from the nest or their death.ConclusionWe conclude that queens of L. acervorum from Spain establish rank orders by ritualized dominance interactions, such as antennal boxing. Workers may reinforce these hierarchies by preferentially feeding and grooming high ranking queens and attacking lower ranking queens. Aggressive worker policing may thus stabilize functional monogyny. Optimal skew models predict that high skew in ants is associated with high dispersal costs. In central Spain, L. acervorum is restricted to small patches at higher elevations, which presumably makes dispersal and colony founding difficult. Because of the ecological requirements of L. acervorum and the predicted large impact of global change on central Spain, the functionally monogynous populations of this ant must be considered as threatened.

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

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