Advertisement

The Science of Nature

, 106:49 | Cite as

Brain differences between social castes precede group formation in a primitively eusocial bee

  • Sarah Pahlke
  • Sarah Jaumann
  • Marc A. Seid
  • Adam R. SmithEmail author
Short Communication

Abstract

Social interactions may shape brain development. In primitively eusocial insects, the mushroom body (MB), an area of the brain associated with sensory integration and learning, is larger in queens than in workers. This may reflect a strategy of neural investment in queens or it may be a plastic response to social interactions in the nest. Here, we show that nest foundresses—the reproductive females who will become queens but are solitary until their first workers are born—have larger MBs than workers in the primitively eusocial sweat bee Augochlorella aurata. Whole brain size and optic lobe size do not differ between the two groups, but foundresses also have larger antennal lobes than workers. This shows that increased neural investment in MBs precedes social group formation. Larger MBs among foundresses may reflect the increased larval nutrition provisioned to future queens and the lack of social aggression from a dominant queen upon adult emergence.

Keywords

Social evolution Social brain hypothesis Neural plasticity Dominance Mushroom body 

Notes

Funding information

This work was supported by NSF grant #17-1028536545 to ARS and MAS.

Compliance with ethical standards

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

References

  1. Brand N, Chapuisat M (2012) Born to be bee, fed to be worker? The caste system of a primitively eusocial insect. Front Zool 9:35CrossRefGoogle Scholar
  2. Fahrbach SE (2006) Structure of the mushroom bodies of the insect brain. Annu Rev Entomol 51:209–232CrossRefGoogle Scholar
  3. Fahrbach SE, Farris SM, Sullivan JP, Robinson G (2003) Limits on volume changes in the mushroom bodies of the honey bee brain. J Neurobiol 57:141–151CrossRefGoogle Scholar
  4. Grob R, Fleischmann PN, Grübel K, Wehner R, Rössler W (2017) The role of celestial compass information in Cataglyphis ants during learning walks and for neuroplasticity in the central complex and mushroom bodies. Front Behav Neurosci 11:226CrossRefGoogle Scholar
  5. Gronenberg W, Heeren S, Holldobler B (1996) Age-dependent and task-related morphological changes in the brain and the mushroom bodies of the ant Camponotus floridanus. J Exp Biol 199:2011–2019PubMedGoogle Scholar
  6. Heisenberg M, Heusipp M, Wanke C (1995) Structural plasticity in the Drosophila brain. J Neurosci 15:1951–1960CrossRefGoogle Scholar
  7. Kapheim KM (2017) Nutritional, endocrine, and social influences on reproductive physiology at the origins of social behavior. Curr Opin Insect Sci 22:62–70CrossRefGoogle Scholar
  8. Kapheim KM, Chan T, Smith A, Wcislo WT, Nonacs P (2016) Ontogeny of division of labor in a facultatively eusocial sweat bee Megalopta genalis. Insect Soc 63:185–191CrossRefGoogle Scholar
  9. Michener CD (1974) The social behavior of the bees: a comparative study. Harvard University Press, CambridgeGoogle Scholar
  10. Michener C, Brothers D (1974) Were workers of eusocial hymenoptera initially altruistic or oppressed. Proc Natl Acad Sci U S A 71:671–674.  https://doi.org/10.1073/pnas.71.3.671 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Moda LM, Vieira J, Freire ACG, Bonatti V, Bomtorin AD, Barchuk AR, Simoes ZLP (2013) Nutritionally driven differential gene expression leads to heterochronic brain development in honeybee castes. PLoS One 8:e64815CrossRefGoogle Scholar
  12. Molina Y, O’Donnell S (2007) Mushroom body volume is related to social aggression and ovary development in the paperwasp Polistes instabilis. Brain Behav Evol 70:137–144CrossRefGoogle Scholar
  13. Molina Y, O’Donnell S (2008) Age, sex, and dominance-related mushroom body plasticity in the paperwasp Mischocyttarus mastigophorus. Devol Neurobiol 68:950–959CrossRefGoogle Scholar
  14. Mueller UG (1996) Life history and social evolution of the primitively eusocial bee Augochlorella striata (Hymenoptera: Halictidae). J Kansas Entomol Soc 69:116–138Google Scholar
  15. O’Donnell S, Donlan N, Jones T (2007) Developmental and dominance-associated differences in mushroom body structure in the paper wasp Mischocyttarus mastigophorus. Dev Neurobiol 67:39–46PubMedGoogle Scholar
  16. O’Donnell S, Bulova SJ, DeLeon S, Barrett M, Fiocca K (2017) Caste differences in the mushroom bodies of swarm-founding paper wasps: implications for brain plasticity and brain evolution (Vespidae, epiponini). Behav Ecol Sociobiol 71:116CrossRefGoogle Scholar
  17. Rehan SM, Bulova SJ, O’Donnell S (2015) Cumulative effects of foraging behavior and social dominance on brain development in a facultatively social bee (Ceratina australensis). Brain Behav Evol 85:117–124CrossRefGoogle Scholar
  18. Roat TC, da Cruz Landim C (2008) Temporal and morphological differences in post-embryonic differentiation of the mushroom bodies in the brain of workers, queens, and drones of Apis mellifera (Hymenoptera, Apidae). Micron 39:1171–1178CrossRefGoogle Scholar
  19. Seid MA, Junge E (2016) Social isolation and brain development in the ant Camponotus floridanus. Sci Nat 103:42CrossRefGoogle Scholar
  20. Smith AR, Seid MA, Jimenez LC, Wcislo WT (2010) Socially induced brain development in a facultatively eusocial sweat bee Megalopta genalis (Halictidae). Proc Biol Sci 277:2157–2163CrossRefGoogle Scholar
  21. Steijven K, Spaethe J, Steffan-Dewenter I, Härtel S (2017) Learning performance and brain structure of artificially-reared honey bees fed with different quantities of food. PeerJ 5:e3858CrossRefGoogle Scholar
  22. Tibbetts EA, Injaian A, Sheehan MJ, Desjardins N (2018) Intraspecific variation in learning: worker wasps are less able to learn and remember individual conspecific faces than queen wasps. Am Nat 191:595–603CrossRefGoogle Scholar
  23. Withers GS, Fahrbach SE, Robinson GE (1993) Selective neuroanatomical plasticity and division of labour in the honeybee. Nature 364:238–240CrossRefGoogle Scholar
  24. Withers GS, Day NF, Talbot EF, Dobson HE, Wallace CS (2008) Experience-dependent plasticity in the mushroom bodies of the solitary bee Osmia lignaria (Megachilidae). 68:73–82Google Scholar
  25. Wittwer B, Hefetz A, Simon T, Murphy LEK, Elgar MA, Pierce NE, Kocher SD (2017) Solitary bees reduce investment in communication compared with their social relatives. Proc Natl Acad Sci U S A 114:6569–6574CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.George Washington UniversityWashingtonUSA
  2. 2.Program in NeurobiologyUniversity of ScrantonScrantonUSA

Personalised recommendations