Learning Distinct Chemical Labels of Nestmates in Ants

Abstract

Colony coherence is essential for eusocial insects because it supports the inclusive fitness of colony members. Ants quickly and reliably recognize who belongs to the colony (nestmates) and who is an outsider (non-nestmates) based on chemical recognition cues (cuticular hydrocarbons: CHCs) which as a whole constitute a chemical label. The process of nestmate recognition often is described as matching a neural template with the label. In this study, we tested the prevailing view that ants use commonalities in the colony odor that are present in the CHC profile of all individuals of a colony or whether different CHC profiles are learned independently. We created and manipulated sub-colonies by adding one or two different hydrocarbons that were not present in the original colony odor of our Camponotus floridanus colony and later tested workers of the sub-colonies in one-on-one encounters for aggressive responses. We found that workers adjust their nestmate recognition by learning novel, manipulated CHC profiles, but still accept workers with the previous CHC profile. Workers from a sub-colony with two additional components showed aggression against workers with only one of the two components added to their CHC profile. Thus, additional components as well as the lack of a component can alter a label as “non-nestmate.” Our results suggest that ants have multiple-templates to recognize nestmates carrying distinct labels. This finding is in contrast to what previously has been proposed, i.e., a widening of the acceptance range of one template. We conclude that nestmate recognition in ants is a partitioned (multiple-template) process of the olfactory system that allows discrimination and categorization of nestmates by differences in their CHC profiles. Our findings have strong implications for our understanding of the underlying mechanisms of colony coherence and task allocation because they illustrate the importance of individual experience and task associated differences in the CHC profiles that can be instructive for the organization of insect societies.

Odor Coding of Nestmate Recognition in the Eusocial AntCamponotus floridanus

“…In contrast, ants with bilateral antennal ablations displayed a significant and indeed near-complete reduction in aggression against nNMs. These data are consistent with the widely reported ability of C. floridanus workers to robustly discriminate between nNMs and NMs and supports the hypothesis that their chemosensory apparatus is required to recognize and trigger aggression against nNMs (2, 6, 13, 16, 19, 20, 38, 39, 42-44).…”

“…Among these social behaviors, nestmate (NM) recognition is especially important for establishing and maintaining discrete societal boundaries for C. floridanus and many other species of ant (2). NM recognition is a dynamic behavior that has been postulated to occur when an individual ant compares chemically encoded “labels” that it encounters with potentially multiple neural-encoded “templates” that represent its own particular global colony chemosensory signature whereby a mismatch between a foreign label and the recognition templates leads to aggression between nNMs (13-15). The foreign label is derived, at least in part, from subtle variations in the profile of cuticular hydrocarbons (CHCs) that distinguish nNMs from NMs (6, 13, 16).…”

“…These have been broadly organized into two categories: the gestalt model, in which label sharing between individuals yields a distinct template based on a blend; and individualistic models, which include requiring the exact matching of the label to the template (“genotype matching”), rejection of any labels containing cues not found in the template (“foreign-label rejection”), and the acceptance of labels that overlap with the template (“habituated-label acceptance”). Similarly, there have been efforts to elucidate the rules governing template-label matching within a phenotypic context (13, 16, 18). These models suggest that ants discriminate between friends and foes based on the presence and/or absence of NM (“desirable”) cues or nNM (“undesirable”) cues.…”

“…While it was initially proposed that ants accept individuals if they possess desirable cues (D-present) or if they lack undesirable cues (U-absent) to the exclusion of all others (18), more recent evidence suggests that ants actively detect foes but not friends through the detection of nNM odor cues (simple U-present model) (16). Importantly however, discrimination may also occur when critical components of the CHC profile are missing (13). These studies suggest that there are multiple templates being used to assess different labels, and that there is variability in the importance of a given component of the label, whether in absence or in abundance, when determining nNM or NM status.…”

“…While the importance of CHCs in mediating NM recognition among ants is well established, several alternative hypotheses have been proposed for the neuronal and molecular mechanisms required for ants to distinguish friends from foes (13, 16-21). In all of these models, CHCs and other semiochemicals are initially detected by the peripheral olfactory sensory system which relies on three major classes of peripheral chemosensory receptors–odorant receptors (ORs), gustatory receptors, and ionotropic receptors.…”