Abstract

Recent studies have revealed a variety of left–right asymmetries among vertebrates and invertebrates. In many species, left- and right-lateralized individuals coexist, but in unequal numbers (‘population-level’ lateralization). It has been argued that brain lateralization increases individual efficiency (e.g. avoiding unnecessary duplication of neural circuitry and reducing interference between functions), thus counteracting the ecological disadvantages of lateral biases in behaviour (making individual behaviour more predictable to other organisms). However, individual efficiency does not require a definite proportion of left- and right-lateralized individuals. Thus, such arguments do not explain population-level lateralization. It has been shown that, in the context of prey–predator interactions, population-level lateralization can arise as an evolutionarily stable strategy when individually asymmetrical organisms must coordinate their behaviour with that of other asymmetrical organisms. I extended the mathematical model showing that populations consisting of left- and right-lateralized individuals in unequal numbers can be evolutionarily stable, based solely on strategic factors arising from the balance between antagonistic (competitive) and synergistic (cooperative) interactions. I also provided empirical evidence to support the prediction from theoretical models suggesting that population-level lateralization is more likely to have evolved in social than in non-social species. I compared olfactory lateralization in two species of Hymenoptera Apoidea, the honeybee (Apis mellifera), a social species, and the mason bee (Osmia cornuta), a solitary species. Recall of the olfactory memory 1 h after training to associate an odour with a sugar reward, as revealed by the bee extending its proboscis when presented with the trained odour (Proboscis Extension Reflex – PER), was better in honeybees trained with their right than with their left antenna. No such asymmetry was observed in mason bees. Similarly, electroantennographic (EAG) responses to a floral volatile compound and to an alarm pheromone component were higher in the right than in the left antenna in honeybees but not in mason bees. Further experiments were conducted to test the lateralized recall of olfactory memory in honeybees, following conditioning of the PER, at 1 or 6 h after training, using a range of different odours. Results confirmed previous evidence that bees learn to associate a new odour of a positive stimulus mainly in neural circuits accessed via their right antenna, and that, after a period of a few hours, memory consolidation occurred accompanied by antennal asymmetry, with bees now being able to recall the odour mainly when using their left antenna. I showed that this peculiar dynamic of memory traces has severe consequences when odours are already known to the bees (either for a biological reason or as a result of previous experience) and are thus already present in the long-term memory store. Response competition arising from multiple memory traces could be observed, with bees showing unexpected lack of specificity in their longer-term olfactory memories. The behavioural finding that honeybees are better in learning to associate odours with a sugar reward when they are trained through their right antenna can been partially explained by the stronger responsiveness of the olfactory receptor neurons inside the right antenna, as shown in my experiments by EAG recordings. I checked whether this in turn might be associated due to a difference in the number of the olfactory sensilla present on the right and on the left antennae. I found that the number of olfactory sensilla is higher on the right antenna with respect to the left antenna. Surprisingly, I also observed for the first time that the number of non-olfactory sensilla was significantly higher on the left antenna than on the right antenna in all segments except the apex. I investigated the generality and phylogenetic origins of the antennal asymmetry found in the honeybee Apis mellifera by examining three species of Australian stingless social bees (Trigona carbonaria, Trigona hockingsi and Austroplebia australis). Meliponinae (stingless bees) are much older compared to Apidae, Bombinae and Euglossinae; thus, it is maintained that the honeybees did not evolve from the stingless bees but rather independently from some other (asocial) bee type and that any social features the two lines of evolution now share are the result of convergent rather than divergent evolution. I found that stingless bees (Meliponinae) have the same laterality as honeybees (Apinae). This evidence suggests that lateralization evolved prior to the evolutionary divergence of these groups or that it evolved separately in each line. Furthermore, since honeybees and stingless bees are the only highly social bees, it seems that lateralization at the population level was convergent and evolved in association with social behaviour, supporting the hypotheses of the theoretical models that population level lateralization is more likely to evolve in social rather than in non-social species.