Olfactory System Morphology Suggests Colony Size Drives Trait Evolution in Odorous Ants (Formicidae: Dolichoderinae)

Abstract

In social insects colony fitness is determined in part by individual worker phenotypes. Across ant species, colony size varies greatly and is thought to affect worker trait variation in both proximate and ultimate ways. Little is known about the relationship between colony size and worker trait evolution, but hypotheses addressing the role of social structure in brain evolution suggest workers of small-colony species may have larger brains or larger brain regions necessary for complex behaviors. In previous work on odorous ants (Formicidae: Dolichoderinae) we found no correlation between colony size and these brain properties, but found that relative antennal lobe size scaled negatively with colony size. Therefore, we now test whether sensory systems scale with colony size, with particular attention to olfactory components thought to be involved in nestmate recognition. Across three species of odorous ants, Forelius mccooki, Dorymyrmex insanus, and D. bicolor, which overlap in habitat and foraging ecology but vary in colony size, we compare olfactory sensory structures, comparing those thought to be involved in nestmate recognition. We use the visual system, a sensory modality not as important in social communication in ants, as a control comparison. We find that body size scaling largely explains differences in eye size, antennal length, antennal sensilla density, and total number of olfactory glomeruli across these species. However, sensilla basiconica and olfactory glomeruli in the T6 cluster of the antennal lobe, structures known to be involved in nestmate recognition, do not follow body size scaling observed for other structures. Instead, we find evidence from the closely related Dorymyrmex species that the larger colony species, D. bicolor, invests more in structures implicated in nestmate recognition. To test for functional consequences, we compare nestmate and non-nestmate interactions between these two species and find D. bicolor pairs of either type engage in more interactions than D. insaus pairs. Thus, we do not find evidence supporting a universal pattern of sensory system scaling associated with changes in colony size, but hypothesize that observed differences in the olfactory components in two closely related Dorymyrmex species are evidence of a link between colony size and sensory trait evolution.

Evolution of neural circuitry and cognition

“…For example, antennal lobe glomeruli are close proxies of underlying olfactory receptor function, and subspecialization of this system reflects olfactory adaptation [77]. Volumes of each glomerulus as well as glomeruli number thus closely mirror investment in synaptic numbers and receptor diversity, making volume and number accurate proxies [78][79][80]. However, even in this case, any investment in increased glomerulus size or overall number needs to be placed into the context of the overall olfactory circuit.…”

Evolution of the neuronal substrate for kin recognition in social Hymenoptera

“…Secondly, it has been demonstrated that functional ORs are necessary for non‐nestmates discrimination in Camponotus floridanus (Ferguson et al ., 2020). Accordingly, the transition to higher social complexity may be associated with expansions of brain regions supporting olfactory communication, as has been observed between ant species with different colony sizes (Riveros, Seid & Wcislo, 2012; Godfrey et al ., 2021). This idea is also supported by observations made in Halictidae (sweat bees), in which a higher investment in chemosensory structures on the antennae has been observed in social bees compared to solitary ones, at both species and population levels (Wittwer et al ., 2017; Wenseleers & van Zweden, 2017; Boulton & Field, 2022).…”

“…In social Hymenoptera, previous research has intensively documented the chemical signals involved in recognition and how they might reflect attributes of the signaller, but the features ensuring adequate reception of the signals and how it is enabled by receptor organs of the receiver have received much less consideration. So far, the BaS and the 9‐exon ORs have emerged as key elements of CHC detection, and they are considered as components of the nestmate recognition system in the current literature (Nishikawa et al ., 2012; Zhou et al ., 2015; McKenzie et al ., 2016; Godfrey et al ., 2021; Gellert et al ., 2022). The apparent dichotomy of the BaS subsystem with the general olfactory system conveniently allows the study of recognition at the neuronal level with little interference from the general odour‐detection system.…”