Abstract
BackgroundAnimal societies are diverse, ranging from small family-based groups to extraordinarily large social networks in which many unrelated individuals interact. At the extreme of this continuum, some ant species form unicolonial populations in which workers and queens can move among multiple interconnected nests without eliciting aggression. Although unicoloniality has been mostly studied in invasive ants, it also occurs in some native non-invasive species. Unicoloniality is commonly associated with very high queen number, which may result in levels of relatedness among nestmates being so low as to raise the question of the maintenance of altruism by kin selection in such systems. However, the actual relatedness among cooperating individuals critically depends on effective dispersal and the ensuing pattern of genetic structuring. In order to better understand the evolution of unicoloniality in native non-invasive ants, we investigated the fine-scale population genetic structure and gene flow in three unicolonial populations of the wood ant F. paralugubris.ResultsThe analysis of geo-referenced microsatellite genotypes and mitochondrial haplotypes revealed the presence of cryptic clusters of genetically-differentiated nests in the three populations of F. paralugubris. Because of this spatial genetic heterogeneity, members of the same clusters were moderately but significantly related. The comparison of nuclear (microsatellite) and mitochondrial differentiation indicated that effective gene flow was male-biased in all populations.ConclusionThe three unicolonial populations exhibited male-biased and mostly local gene flow. The high number of queens per nest, exchanges among neighbouring nests and restricted long-distance gene flow resulted in large clusters of genetically similar nests. The positive relatedness among clustermates suggests that kin selection may still contribute to the maintenance of altruism in unicolonial populations if competition occurs among clusters.
Highlights
Animal societies are diverse, ranging from small family-based groups to extraordinarily large social networks in which many unrelated individuals interact
Many social animals live in small family groups of closely related individuals, and the role of kinship in promoting the evolution of reproductive altruism and eusociality by kin selection has long been recognized [1,2,3,4]
If workers help completely unrelated individuals, selection should favour selfish females that develop into queens or produce males, and adaptive altruistic worker behaviour cannot be maintained by kin selection [6]
Summary
Animal societies are diverse, ranging from small family-based groups to extraordinarily large social networks in which many unrelated individuals interact. The evolution and maintenance of unicolonial populations constitutes one of the enduring major challenges for kin selection, and more generally for modern, gene-centred evolutionary theory [6,7,8,9]. This is because high queen number and mixing of individuals among nests can lead to extremely low relatedness among nestmates [6,8,10,11]. It is of considerable interest to study the breeding system, dispersal pattern and genetic structuring in unicolonial populations
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