Colony personalities and the importance of behavioral variance for insect societies

Résumé

Social insect colonies - also called superorganisms - may exhibit personalities, similar to other animals, in which individuals consistently differ in behavior. However, insect societies can not only vary in the mean, but also in the variance of a behavior. Our recent studies on ants demonstrate that ecological factors select for different colony personalities and for different degrees of behavioral variance or specialization. Temnothorax longispinosus ant colonies vary in behavior and certain behavioral types are associated with environmental factors such as competition or parasitism. Ant colonies in high density areas are more aggressive and these behavioral differences persist under standardized lab conditions and with the emergence of a new worker generation. Colonies with more aggressive behavioral types did better in the field against the invasion of Protomognathus slavemaker queens, their most important social parasite. Moreover, aggressive colonies better fend of slave raids, suggesting that parasite pressure selects for host aggression. Indeed, a comparison of 17 host populations showed that host colony aggression and flight behavior co-varies with parasite pressure over large geographic scales. Division of labor, a key trait of social insects, relies on intracolonial behavioral variation, but fitness benefits of behavioral variation are largely unexplored. By testing individual workers of T. longispinosus, we demonstrated that colonies with higher behavioral variance are more productive under field and lab conditions. However, under variable environments and early in colony development, colonies with less specialized workers do better. In an experimental approach, using artificially composed colonies of specialists and / or generalists with the same behavioral mean, we could show fitness benefits of generalists. Finally, in a recent transcriptome study we revealed typical gene expression patterns of different behavioral worker castes and the queen. Genes overexpressed in workers were more derived than queen-specific genes, suggesting more recent evolutionary changes in genes controlling worker behavior.