Brain-behavioural olfactory asymmetries in Apoidea

Lateralization of the nervous system enhances optimization of neural circuitry and parallel processing in individual organisms. Over groups of individuals, brain-behavioural asymmetries might present a direction in the occurrence of the bias (the majority of the individuals showing the same direction at the population level) that has been mathematically demonstrated to be an evolutionarily stable strategy in social groups, thus optimizing coordination and cooperation. The superfamily Apoidea represents a group in which both the study of the appearance of population-level asymmetries and advantages in individual organisms (e.g., in the A. mellifera model) can be exploited. Here I described a study on olfactory lateralization in a primitively eusocial species of Apoidea, B. terrestris. I reported here that this species showed a direction in the behavioural asymmetry of short-term odour memory, but only individual-level differences in odour detection at the periphery of the nervous system. Moreover, B. terrestris showed a morphological difference at the level of the population in the number of structures where olfactory neurons are housed. In the same subfamily Apoidea, the perennial eusocial honeybee, A. mellifera, is a good candidate for assessing neural correlates of odour asymmetries. Lateralization in olfactory memory was reported in this species in the past; here I performed for the first time a study of anatomical and functional asymmetries within the brain, in the first olfactory neuropils, the antennal lobes. I measured a subset of glomeruli in naïve individuals and found symmetrical volumes between the sides for those glomeruli that are mainly activated by odours that show lateralization in behvaiour. Furthermore, I performed single-antenna recall tests, conditioning bees to extend their proboscis (in the so-called PER paradigm) in association with those odours that more strongly activated functional responses in the selected glomerular subset. The behavioural tests showed an odour dependency in the capacity of bees to recall compounds with the two antennae. A broader subset of glomeruli was measured after long-term memory formation and symmetrical volumes were confirmed in all glomerular classes revealing also memory-dependent shrinkage effect. At the functional level, I performed in vivo calcium imaging data of the bee antennal lobes. Odor-evoked activity maps were recorded with two-photon microscopy allowing for better spatial and temporal resolution compared to conventional fluorescence microscopy. A first comparison between sides from wide-field fluorescence microscopy data showed a left/right difference in distance between odour representations and different mixture interactions within each lobe. In the same social species, A.mellifera, I reported the results of experiments measuring social interactions between pairs of bees with only one antenna in use, revealing that animals tested with only their right antenna in use exhibited better social context-dependent behaviours. Overall, these results provide new evidence for the occurrence of behavioural lateralizations at the population level, and identify some of their possible anatomical and functional correlates. Finally, in relation to previous studies these results tighten the link between the occurrence of population-level asymmetries and their evolution in a social context.