The study of the evolution of sociality is closely associated with the study of the evolution of sensory systems. Indeed, group life and sociality necessitate that individuals recognize each other and detect outsiders, as seen in eusocial insects such as Hymenoptera. While we know that antennal sense organs that are involved in olfactory perception are found in greater densities in social species of that group compared to solitary hymenopterans, whether this among-species correlation represents the consequence of social evolution leading to sensory evolution, or the opposite, is still questioned. Knowing more about how sociality and sensory abilities covary within a species would help us understand the evolutionary sequence. Studying a species that shows social plasticity, that is facultatively social, would further allow disentangling the cause and consequence of social evolution and sensory systems and the implication of plasticity in the process.

Boulton and Field (2022) studied a species of sweat bee that shows social plasticity, Halictus rubicundus. They studied populations at different latitudes in Great Britain: populations in the North are solitary, while populations in the south often show sociality, as they face a longer and warmer growing season, leading to the opportunity for two generations in a single year, a pre-condition for the presence of workers provisioning for the (second) brood. Using scanning electron microscope imaging, the authors compared the density of antennal sensilla types in these different populations (north, mid-latitude, south) to test for an association between sociality and olfactory perception capacities. They counted three distinct types of antennal sensilla: olfactory plates, olfactory hairs, and thermos/hygro-receptive pores, used to detect humidity, temperature and CO2. In addition, they took advantage of facultative sociality in this species by transplanting individuals from a northern population (solitary) to a southern location (where conditions favour sociality), to study how social plasticity is reflected (or not) in the density of antennal sensilla types. They tested the prediction that olfactory sensilla density is also developmentally plastic in this species.

Their results show that antennal sensilla counts differ between the 3 studied regions (north, mid-latitude, south), but not as predicted. Individuals in the southern population were not significantly different from the mid-latitude and northern ones in their count of olfactory plates and they had less, not more, thermos/hygro receptors than mid-latitude and northern individuals. Furthermore, mid-latitude individuals had more olfactory hairs than the ones from the northern population and did not differ from southern ones. The prediction was that the individuals expressing sociality would have the highest count of these olfactory hairs. This unpredicted pattern based on the latitude of sampling sites may be due to the effect of temperature during development, which was higher in the mid-latitude site than in the southern one. It could also be the result of a genotype-by-environment interaction, where the mid-latitude population has a different developmental response to temperature compared to the other populations, a difference that is genetically determined (a different “reaction norm”). Reciprocal transplant experiments coupled with temperature measurements directly on site would provide interesting information to help further dissect this intriguing pattern. 

Interestingly, where a sweat bee developed had a significant effect on their antennal sensilla counts: individuals originating from the North that developed in the south after transplantation had significantly more olfactory hairs on their antenna than individuals from the same Northern population that developed in the North. This is in accordance with the prediction that the characteristics of sensory organs can also be plastic. However, there was no difference in antennal characteristics depending on whether these transplanted bees became solitary or expressed the social phenotype (foundress or worker). This result further supports the hypothesis that temperature affects development in this species and that these sensory characteristics are also plastic, although independently of sociality. Overall, the work of Boulton and Field underscores the importance of including phenotypic plasticity in the study of the evolution of social behaviour and provides a robust and fruitful model system to explore this further.

References

Boulton RA, Field J (2022) Sensory plasticity in a socially plastic bee. bioRxiv, 2022.01.29.478030, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.01.29.478030