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Isolation disrupts social interactions and destabilizes brain development in bumblebees

Z Yan Wang, Grace C. McKenzie-Smith, Weijie Liu, Hyo Jin Cho, Talmo Pereira, Zahra Dhanerawala, Joshua W. Shaevitz, Sarah D. Kocher

Preprint posted on December 17, 2021 https://www.biorxiv.org/content/10.1101/2021.12.16.472962v1.full

Socialize more for a better brain! Social isolation in bumblebees affects brain development and behavior

Selected by Niveda Udaykumar

Background

Social animals such as ants, wasps, and bees rely on social interactions with their conspecifics for survival, fitness, and longevity. Isolation of such animals from their groups during early development leads to poor fitness outcomes1-4. In addition, the isolated members have decreased adaptive behavior to different social surroundings. However, many reports that social isolation affects the physiology and behavior of social animals, especially bees5. In this preprint, Wang et.al., have investigated the molecular, behavioral, and neuroanatomical changes associated with social isolation in the bumblebee species, Bombus impatiens. They show that the social isolation of bumblebees leads to increased social interactions with disrupting gene expression, and brain development.

Key findings

Bumblebees live in a social colony consisting of a queen and approximately 100-200 female worker bees6. Over developmental time and context, as the bumblebee brain is developing rapidly, the members of the colony display different behavioral patterns by pairwise or spatial interactions7-10. To study the impact of social isolation on behavior, the authors altered the early life environment of the worker bees, followed by assaying for behavioral changes either alone or with a social partner. For this, newly eclosed females were split into three groups and placed in a modular housing that isolated residents from external visual, auditory, and olfactory cues. The three groups were as follows:

  1. Isolation (Iso) – consisting of single bees in complete social isolation
  2. Group- housed (Grp) – consisting of four nestmates outside the colony
  3. Colony- housed (Col)- individual bee is immediately returned to her natal colony

The bees were kept in these groups for 9 consecutive days. On post-eclosion day 10, behavioral assays and transcriptomics were performed for downstream analysis(Fig 1A).

Behavioral analyses

The behavior of experimental bees was captured either by themselves (solo) or with another social partner (paired) by recording their behavior in a petri dish with infrared illumination.  For the paired interactions, same treatment pair interactions (Iso+Iso, Grp+Grp, Col+Col) and combinations (Iso+Grp, Iso+Col, Grp+Col, and Grp bees from separate groups) were assayed.

With software, such as MotionMapper, SLEAP, and t-SNE, the behavior of the different groups of bees was categorized into five discrete states based on video clips: idle (no movement), antennal movement, grooming, locomotion, and fast locomotion behavior. The results suggested that colony-reared bees spend a longer time in an idle state compared to group-reared/ isolated bees. Additionally, group-reared bees show fast locomotion behavior compared to colony-reared/isolated bees, suggesting altered behavior due to altered social environments (Fig 1B).

Fig1: A – Experimental strategy for behavioral analyses. B- Changes in social behavior between isolated and group-housed bumblebees. (Adapted from Fig1  Wang et.al., 2021)

Next, the behavioral analyses were performed in the presence/absence of a social partner across the three treatment groups. In the absence of a social partner, observations suggested that colony-reared bees spend less time in an idle state compared to isolated and group-reared bees. Additionally, group-reared bees showed fast locomotion behavior than antennal behaviors, the primary mode of communication of bees, indicating that the absence of a social partner impacts early life behavior in bees across the three treatment groups.

Finally, the behavioral profiles were studied across the three treatment groups in the presence of a social partner, as these interactions form the foundation of the behavior dynamics of the colony. The proximity between the bees was measured by the difference in the inter-thorax distance between the same treatment pairs. The results suggested that all treatment groups showed an inter-thorax distance less than 2 cm. To investigate if the distance of a social partner affects the behavioral profile of a bee, the distances between the paired bees were quantified by using the Jensen-Shannon divergences. The results suggest that the behavior of the paired bees changes when the partner is less than 2cm over large distances. The behavioral change associated at less than 2cm is termed affiliated while the behavior over large distances is termed as unaffiliated, corroborating with previous studies on similar distance ranges. Moreover, the results showed that isolated bees were mostly affiliated with social partners while the behavior of the other treatment groups was unaffected. In summary, the behavioral analyses of the bumblebees show that the presence of a social partner and the early social environment of a bee determines the key behavior features of a bee’s later stage. Moreover, isolated bees show perturbed social behavior in the presence of a partner when compared to the other treatment groups.

Transcriptomic profiling

The authors hypothesized that the differences in the social behavior across the three groups might stem from neurobiological molecular changes across the treatment groups. To test this, brain transcriptomics of the bees of the three treatment groups was performed by tagmentation 3’ RNA-sequencing approach. This approach gave a set of differentially expressed genes across treatment groups. The results showed a strong differential gene expression (DEG) between isolated and colony-housed bees while there were slight differences between isolated and group-housed bees, while there was no differential gene expression between group-housed and colony-housed bees. Additionally, the differential gene expression was mostly downregulated in the isolated bees when compared to the other two treatment groups. The GO enrichment of the DEGs revealed that the genes belonged to social communication and signaling processes, implying that social isolation impacts the social behavior of the bees, in agreement with the behavioral analyses performed earlier in this study(Fig 2A).

Fig 2: A- Differentially expressed across the treatment groups. B- Annotated template of a worker bee. C and D- Variances in volume fraction across the treatment groups on the antennal and mushroom bodies of the bumblebee brain. (Adapted from Fig 3 and 4 of Wang et.al.,2021)

Lastly, the authors investigated whether changes in social behavior affected the brain development of the bees. The early brain of the bees is measured by the change in neuropil volume, which reaches the adult state 9 days post eclosion. Maturation of the brain involves processes such as experience, hormone signaling, and learning. To study the impact of social isolation on the bumblebee brain, an annotated brain template of a worker bee was prepared by confocal imaging. This was followed by stacking the brain of the bees across the three treatment groups and fitting them into the annotated template for volumetric analysis. The analysis showed that while mean volume fractions were similar across the three treatment groups, the variances of volume fractions were different. The variances of volume fractions were highest in the isolated bees in comparison to the other treatment groups, thereby suggesting that social isolation affects brain development (Fig 2B-D). The authors’ reason that the differences in variation may arise due to the destabilization of the developmental trajectory of the bumblebee brain in the complete absence of social cues.

Why I chose to highlight this preprint

I chose to highlight this preprint as the authors have very precisely demonstrated the impact of social isolation using behavioral and transcriptomics assays, thereby paving way for research on the impact of social isolation and human behavior in the future.

Questions to authors

  1. Considering that humans are social beings too, can the results of the study be extrapolated to human brain development and behavior as well?
  2. What do you speculate to be the potential causes for social isolation?
  3. Do you speculate that social isolation in an adult bee can alter the neurogenic landscape?

References

  1. Boulay, R., Soroker, V., Godzkinska, E.J., Hefetz, A., and Lenoir, A. (2000). Octopamine reverses social deprivation effects. The Journal of Experimental Biology, 513–520.
  2. Boulay, R., and Lenoir, A. (2001). Social isolation of mature workers affects nestmate recognition in the ant Camponotus fellah. Behavioural Processes 55, 67–73.
  3. Koto, A., Mersch, D., Hollis, B., and Keller, L. (2015). Social isolation causes mortality by disrupting energy homeostasis in ants. Behav Ecol Sociobiol 69, 583–591.
  4. Seid, M.A., and Junge, E. (2016). Social isolation and brain development in the ant Camponotus floridanus. Sci Nat 103, 42.
  5. Breed, M.D., Silverman, J.M., and Bell, W.J. (1978). Agonistic behavior, social interactions, and behavioral specialization in a primitively eusocial bee. Ins. Soc 25, 351–364.
  6. Goulson, D. (2010). Bumblebees: Behaviour, Ecology, and Conservation (OUP Oxford).
  7. Jandt, J.M., and Dornhaus, A. (2009). Spatial organization and division of labour in the bumblebee Bombus impatiens. Animal Behaviour 77, 641–651.
  8. Jandt, J.M., and Dornhaus, A. (2011). Competition and cooperation: bumblebee spatial 695 organization and division of labor may affect worker reproduction late in life. Behav Ecol 696 Sociobiol 65, 2341–2349.
  9. Jandt, J.M., Huang, E., and Dornhaus, A. (2009). Weak specialization of workers inside a 698 bumblebee (Bombus impatiens) nest. Behav Ecol Sociobiol 63, 1829–1836.
  10. 10.Crall, J.D., Switzer, C.M., Oppenheimer, R.L., Ford Versypt, A.N., Dey, B., Brown, A., Eyster, M., Guérin, C., Pierce, N.E., Combes, S.A., et al. (2018). Neonicotinoid exposure disrupts bumblebee nest behavior, social networks, and thermoregulation. Science 362, 683–686.

Tags: bees, behavior, brain development

Posted on: 13th January 2022

doi: https://doi.org/10.1242/prelights.31265

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