Associative learning of non-nestmate cues improves enemy recognition in ants.

Abstract

Recognition protects biological systems at all scales, from cells to societies. Social insects recognize their nestmates by colony-specific olfactory labels that individuals store as neural templates in their memory. Throughout an ant's life, learning continuously shapes the nestmate recognition template to keep up with the constant changes in colony labels.^1,2,3,4 Most explanations for template update rely on non-associative learning.⁵ Indeed, we know that ants become habituated to their colony's label: their reaction to the omnipresent chemical cues typical of their own nest fades.^3,6,7,8 However, non-associative habituation cannot explain the enormous variation in nestmate recognition behavior. For example, some ant species are more aggressive toward neighboring colonies than toward unfamiliar colonies (nasty neighbor effect^9,10,11,12). Social insects can learn associatively, for example, by associating an odor cue with a food reward.¹³ A recent model proposes that associative learning of non-nestmate odors leads to variation in the recognition templates among individuals, which then improves recognition at the group level.¹⁴ Here, we test whether associative learning of non-nestmate colony odors is possible.¹¹ Our results show that associative learning plays a crucial role in the formation of both nestmate and non-nestmate recognition templates and that the aggression received by an ant acts as an unconditioned stimulus that the ant likely associates with the odor label of its enemy. This type of template learning can help explain different patterns of variation in nestmate recognition, from nasty neighbor effects to task- and age-specific variation in aggression.^15,16.