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. We have previously 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. Here, we extend our 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.

Traditionally, only humans were thought to exhibit brain and behavioural asymmetries, but several studies have revealed that most vertebrates are also lateralized. Recently, evidence of left-right asymmetries in invertebrates has begun to emerge, suggesting that lateralization of the nervous system may be a feature of simpler brains as well as more complex ones. Here I present some examples in invertebrates of sensory and motor asymmetries, as well as asymmetries in the nervous system. I illustrate two cases where an asymmetric brain is crucial for the development of some cognitive abilities. The first case is the nematode C. elegans, which has asymmetric odour sensory neurons and taste perception neurons. In this worm left/right asymmetries are responsible for the sensing of a substantial number of salt ions, and lateralized responses to salt allow the worm to discriminate between distinct salt ions. The second case is the fruit fly D. melanogaster, where the presence of asymmetry in a particular structure of the brain is important in the formation or retrieval of long-term memory. Moreover, I distinguish two distinct patterns of lateralization that occur in both vertebrates and invertebrates: individual-level and population-level lateralization. Theoretical models on the evolution of lateralization suggest that the alignment of lateralization at the population level may have evolved as an evolutionary stable strategy in which individually-asymmetrical organisms must coordinate their behaviour with that of other asymmetrical organisms. This implies that lateralization at the population-level is more likely to have evolved in social rather than in solitary species. I evaluate this new hypothesis with specific focus on insects showing different level of sociality. In particular, I present a series of studies on antennal asymmetries in honeybees and other related species of bees, showing how insects may be extremely useful to test evolutionary hypothesis.

Lateralization, i.e., the different functional roles played by the left and right sides of the brain, is expressed in two main ways: (1) in single individuals, regardless of a common direction (bias) in the population (aka individual-level lateralization); or (2) in single individuals and in the same direction in most of them, so that the population is biased (aka population-level lateralization). Indeed, lateralization often occurs at the population-level, with 60–90% of individuals showing the same direction (right or left) of bias, depending on species and tasks. It is usually maintained that lateralization can increase the brain’s efficiency. However, this may explain individual-level lateralization, but not population-level lateralization, for individual brain efficiency is unrelated to the direction of the asymmetry in other individuals. From a theoretical point of view, a possible explanation for population-level lateralization is that it may reflect an evolutionarily stable strategy (ESS) that can develop when individually asymmetrical organisms are under specific selective pressures to coordinate their behavior with that of other asymmetrical organisms. This prediction has been sometimes misunderstood as it is equated with the idea that population-level lateralization should only be present in social species. However, population-level asymmetries have been observed in aggressive and mating displays in so-called “solitary” insects, suggesting that engagement in specific inter-individual interactions rather than “sociality” per se may promote population-level lateralization. Here, we clarify that the nature of inter-individuals interaction can generate evolutionarily stable strategies of lateralization at the individual- or population-level, depending on ecological contexts, showing that individual-level and population-level lateralization should be considered as two aspects of the same continuum.

Sophisticated cognitive abilities have been documented in honeybees, possibly an aspect of their complex sociality. In vertebrates brain asymmetry enhances cognition and directional biases of brain function are a putative adaptation to social behaviour. Here we show that honeybees display a strong lateral preference to use their right antenna in social interactions. Dyads of bees tested using only their right antennae (RA) contacted after shorter latency and were significantly more likely to interact positively (proboscis extension) than were dyads of bees using only their left antennae (LA). The latter were more likely to interact negatively (C-responses) even though they were from the same hive. In dyads from different hives C-responses were higher in RA than LA dyads. Hence, RA controls social behaviour appropriate to context. Therefore, in invertebrates, as well as vertebrates, lateral biases in behaviour appear to be associated with requirements of social life.