Behavioral Ecology and Sociobiology

, Volume 68, Issue 4, pp 529–536 | Cite as

A test of neuroecological predictions using paperwasp caste differences in brain structure (Hymenoptera: Vespidae)

  • Sean O’Donnell
  • Marie R. Clifford
  • Susan J. Bulova
  • Sara DeLeon
  • Christopher Papa
  • Nazaneen Zahedi
Original Paper


Adaptive brain architecture hypotheses predict brain region investment matches the cognitive and sensory demands an individual confronts. Social hymenopteran queen and worker castes differ categorically in behavior and physiology leading to divergent sensory experiences. Queens in mature colonies are largely nest-bound while workers depart nests to forage. We predicted social paperwasp castes would differ in tissue allocation among brain regions. We expected workers to invest relatively more than queens in neural tissues that process visual input. As predicted, we found workers invested more in visual relative to antennal processing than queens both in peripheral sensory lobes and in central processing brain regions (mushroom bodies). Although we did not measure individual brain development changes, our comparative data provide a preliminary test of mechanisms of caste differences. Paperwasp species differ in the degree of caste differentiation (monomorphic versus polymorphic castes) and in colony structure (independent- versus swarm-founding); these differences could correspond to the magnitude of caste brain divergence. If caste differences resulted from divergent developmental programs (experience-expectant brain growth), we predicted species with morphologically distinct queens, and/or swarm-founders, would show greater caste divergence of brain architecture. Alternatively, if adult experience affected brain plasticity (experience-dependent brain growth), we predicted independent-founding species would show greater caste divergence of brain architecture. Caste polymorphism was not related to the magnitude of queen-worker brain differences, and independent-founder caste brain differences were greater than swarm-founder caste differences. Greater caste separation in independent-founder brain structure suggests a role for adult experience in the development of caste-specific brain anatomy.


Antennal lobe Brain evolution Mushroom body Neural plasticity Optic lobe 


  1. Anderson C, McShea DW (2001) Individual versus social complexity, with particular reference to ant colonies. Biol Rev 76:211–237PubMedCrossRefGoogle Scholar
  2. Arenas A, Giurfa M, Sandoz JC, Hourcade B, Devaud JM, Farina WM (2012) Early olfactory experience induces structural changes in the primary olfactory center of an insect brain. Eur J Neurosci 35:682–690PubMedCrossRefGoogle Scholar
  3. Arrenberg AB, Driever W (2013) Integrating anatomy and function for zebrafish circuit analysis. Front Neural Circ 7:74Google Scholar
  4. Barth M, Hirsch HVB, Meinertzhagen IA, Heisenberg M (1997) Experience-dependent developmental plasticity in the optic lobe of Drosophila melanogaster. J Neurosci 17:1493–1504PubMedGoogle Scholar
  5. Barton RA, Purvis A, Harvey PH (1995) Evolutionary radiation of visual and olfactory brain systems in primates, bats, and insectivores. Phil Trans Biol Sci 348:381–392CrossRefGoogle Scholar
  6. Bourke AFG (1999) Colony size, social complexity and reproductive conflict in social insects. J Evol Biol 12:245–257CrossRefGoogle Scholar
  7. Brown ER, Piscopo S (2013) Synaptic plasticity in cephalopods; more than just learning and memory? Invert Neurosci 13:35–44PubMedCrossRefGoogle Scholar
  8. Bruyndonckx N, Kardile SP, Gadagkar R (2006) Dominance behaviour and regulation of foraging in the primitively eusocial wasp Ropalidia marginata (Lep.) (Hymenoptera: Vespidae). Behav Proc 72:100–103CrossRefGoogle Scholar
  9. Carpenter JM (2004) Synonymy of the genus Marimbonda Richards, 1978, with Leipomeles Mobius, 1856 (Hymenoptera: Vespidae; Polistinae), and a new key to the genera of paper wasps of the new world. Am Mus Novit 3465:1–16CrossRefGoogle Scholar
  10. Carpenter JM, Kojima J-I, Wenzel JW (2000) Polybia, paraphyly, and polistine phylogeny. Am Mus Novit 3298:1–24CrossRefGoogle Scholar
  11. Catania KC (2005) Evolution of sensory specializations in insectivores. Anat Rec A: Discov Mol Cell Evol Biol 287:1038–1050CrossRefGoogle Scholar
  12. Chavarria-Pizarro L, West-Eberhard MJ (2010) The behavior and natural history of Chartergellus, a little-known genus of neotropical social wasps (Vespidae Polistinae Epiponini). Ethol Ecol Evol 22:317–343CrossRefGoogle Scholar
  13. Chen X, Hu Y, Zheng HQ, Cao LF, Niu DF, Yu DL, Sun YQ, Hu SN, Hu FL (2012) Transcriptome comparison between honey bee queen- and worker-destined larvae. Insect Biochem Mol Biol 42:665–673PubMedCrossRefGoogle Scholar
  14. Chittka L, Niven J (2009) Are bigger brains better? Curr Biol 19:995–1008CrossRefGoogle Scholar
  15. Cooper HM, Herbin M, Nevo E (1993) Visual system of a naturally microphthalmic mammal: the blind mole rat, Spalax ehrenbergi. J Comp Neurol 328:313–350PubMedCrossRefGoogle Scholar
  16. De Souza AR, Prezoto F (2012) Regulation of worker activity in the social wasp Polistes versicolor. Insect Soc 59:193–199CrossRefGoogle Scholar
  17. Durst C, Eichmueller S, Menzel R (1994) Development and experience lead to increased volume of subcompartments of the honeybee mushroom body. Behav Neural Biol 62:259–263PubMedCrossRefGoogle Scholar
  18. Ehmer B, Hoy R (2000) Mushroom bodies of vespid wasps. J Comp Neurol 416:93–100PubMedCrossRefGoogle Scholar
  19. Eickhoff R, Lorbeer R-A, Sheiblich H, Heisterkamp A, Meyer HS, MichaelBicker G (2012) Scanning laser optical tomography resolves structural plasticity during regeneration in an insect brain. PLOS ONE 7:e41236PubMedCentralPubMedCrossRefGoogle Scholar
  20. Fahrbach SE (2006) Structure of the mushroom bodies of the insect brain. Annu Rev Entomol 51:209–232PubMedCrossRefGoogle Scholar
  21. Fahrbach SE, Moore D, Capaldi EA, Farris SM, Robinson GE (1998) Experience-expectant plasticity in the mushroom bodies of the honeybee. Learn Mem 5:115–123PubMedCentralPubMedGoogle Scholar
  22. Farris SM, Robinson GE, Fahrbach SE (2001) Experience- and age-related outgrowth of intrinsic neurons in the mushroom bodies of the adult worker honeybee. J Neurosci 21:6395–6404PubMedGoogle Scholar
  23. Farris SM, Pettrey C, Daly KC (2011) A subpopulation of mushroom body intrinsic neurons is generated by protocerebral neuroblasts in the tobacco hornworm moth, Manduca sexta (Sphingidae, Lepidoptera). Arthropod Struct Dev 40:395–408PubMedCentralPubMedCrossRefGoogle Scholar
  24. Fujun X, Hu K, Zhu T, Racey P, Wang X, Sun Y (2012) Behavioral evidence for cone-based ultraviolet vision in divergent bat species and implications for its evolution. Zoologia 29:109–114Google Scholar
  25. Groh C, Roessler W (2008) Caste-specific postembryonic development of primary and secondary olfactory centers in the female honeybee brain. Arthropod Struct Devel 37:459–468CrossRefGoogle Scholar
  26. Groh C, Ahrens D, Rossler W (2006) Environment- and age-dependent plasticity of synaptic complexes in the mushroom bodies of honeybee queens. Brain Behav Evol 68:1–14PubMedCrossRefGoogle Scholar
  27. Gronenberg W (1999) Modality-specific segregation of input to ant mushroom bodies. Brain Behav Evol 54:85–95PubMedCrossRefGoogle Scholar
  28. Gronenberg W, Liebig J (1999) Smaller brains and optic lobes in reproductive workers of the ant Harpegnathos. Naturwissenschaften 86:343–345CrossRefGoogle Scholar
  29. Gronenberg W, Riveros AJ (2009) Social brains and behavior—past and present. In: Gadau J, Fewell J (eds) Organization of insect societies: from genome to sociocomplexity. Harvard University Press, Cambridge, pp 377–401Google Scholar
  30. Gronenberg W, Heeren S, Hölldobler 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
  31. Hansson BS, Stensmyr M (2011) Evolution of insect olfaction. Neuron 72:698–711PubMedCrossRefGoogle Scholar
  32. Herman RA, Queller DC, Strassmann JE (2000) The role of queens in colonies of the swarm-founding wasp Parachartergus colobopterus. Anim Behav 59:841–848PubMedCrossRefGoogle Scholar
  33. Hunt JH, O’Donnell S, Chernoff N, Brownie C (2001) Observations on two Neotropical swarm-founding wasps, Agelaia yepocapa and A. panamaensis (Hymenoptera: Vespidae). Ann Entomol Soc Am 98:555–562CrossRefGoogle Scholar
  34. Hunt JH, Kensinger BJ, Kossuth JA, Henshaw MT, Norberg K, Wolschin F, Amdam GV (2007) A diapause pathway underlies the gyne phenotype in Polistes wasps, revealing an evolutionary route to caste-containing insect societies. Proc Natl Acad Sci U S A 104:14020–14025PubMedCentralPubMedCrossRefGoogle Scholar
  35. Jeanne RL (2003) Social complexity in the Hymenoptera, with special attention to wasps. In: Kitkuchi T, Azuma N, Higashi S (eds) Genes, behaviors and evolution of social insects. Hokkaido University Press, Sapporo, pp 81–131Google Scholar
  36. Jones TA, Donlan NA, O’Donnell S (2009) Growth and pruning of mushroom body Kenyon cell dendrites during worker behavioral development in the paper wasp, Polybia aequatorialis (Hymenoptera: Vespidae). Neurobiol Learn Mem 92:485–495PubMedCrossRefGoogle Scholar
  37. Julian GE, Gronenberg W (2002) Reduction of brain volume correlates with behavioral changes in queen ants. Brain Behav Evol 60:152–164PubMedCrossRefGoogle Scholar
  38. Kuhn-Buhlmann S, Wehner R (2006) Age-dependent and task-related volume changes in the mushroom bodies of visually guided desert ants, Cataglyphis bicolor. J Neurobiol 66:511–521PubMedCrossRefGoogle Scholar
  39. Laughlin SB (2001) Energy as a constraint on the coding and processing of sensory information. Curr Opin Neurobiol 11:475–480PubMedCrossRefGoogle Scholar
  40. Linsey TJ, Bennett MB, Collin SP (2007) Volumetric analysis of sensory brain areas indicates ontogenetic shifts in the relative importance of sensory systems in elasmobranchs. Raffles Bull Zool 14:7–15Google Scholar
  41. Mantini D, Corbetta M, Romani GL, Orban, Vanduffel WJ (2013) Evolutionarily novel functional networks in the human brain? J Neurosci 33:3259–3275PubMedCrossRefGoogle Scholar
  42. Martins JR, Nunes FMF, Cristino AS, Simoes ZP, Bitondi MMG (2010) The four hexamerin genes in the honey bee: structure, molecular evolution and function deduced from expression patterns in queens, workers and drones. BMC Mol Biol 11:23PubMedCentralPubMedCrossRefGoogle Scholar
  43. Molina Y, O’Donnell S (2008) A developmental test of the dominance-nutrition hypothesis: linking adult feeding, aggression, and reproductive potential in the paperwasp Mischocyttarus mastigophorus. Ethol Ecol Evol 20:125–139CrossRefGoogle Scholar
  44. Muscedere ML, Traniello JFA (2012) Division of labor in the hyperdiverse ant genus Pheidole is associated with distinct patterns of worker brain organization. PLoS One 7:e31618PubMedCentralPubMedCrossRefGoogle Scholar
  45. Navarrete A, van Schaik CP, Isler K (2011) Energetics and the evolution of human brain size. Nature 480:91–93PubMedCrossRefGoogle Scholar
  46. Niven JE, Laughlin SB (2008) Energy limitation as a selective pressure on the evolution of sensory systems. J Exp Biol 211:1792–1804PubMedCrossRefGoogle Scholar
  47. Noll FB, Zucchi R (2000) Increasing caste differences related to life cycle progression in some Neotropical swarm-founding polygynic polistine wasps (Hymenoptera: Vespidae; Epiponini). Ethol Ecol Evol 12:43–65CrossRefGoogle Scholar
  48. Noll FB, Wenzel JW, Zucchi R (2004) Evolution of caste in Neotropical swarm-founding wasps (Hymenoptera: Vespidae; Epiponini). Am Mus Novit 3467:1–24CrossRefGoogle Scholar
  49. O’Donnell S (1998a) Reproductive caste determination in eusocial wasps (Hymenoptera: Vespidae). Annu Rev Entomol 43:323–346PubMedCrossRefGoogle Scholar
  50. O’Donnell S (1998b) Effects of experimental forager removals on division of labour in the primitively eusocial wasp Polistes instabilis (Hymenoptera: Vespidae). Behaviour 135:173–193CrossRefGoogle Scholar
  51. O’Donnell S (2006) Polybia wasp biting interactions recruit foragers following experimental worker removals. Anim Behav 71:709–715CrossRefGoogle Scholar
  52. O’Donnell S, Donlan NA, Jones TA (2004) Mushroom body structural plasticity is associated with temporal polyethism in eusocial wasp workers. Neurosci Lett 356:159–162PubMedCrossRefGoogle Scholar
  53. O’Donnell S, Donlan NA, Jones TA (2007) Developmental and dominance-associated differences in mushroom body structure in the paper wasp Mischocyttarus mastigophorus. Dev Neurobiol 67:39–46PubMedGoogle Scholar
  54. O’Donnell S, Clifford M, Molina Y (2011) Comparative analysis of constraints and caste differences in brain investment among social paper wasps. Proc Natl Acad Sci U S A 108:7107–7112PubMedCentralPubMedCrossRefGoogle Scholar
  55. Roat TC, da Cruz-Landim C (2011) Differentiation of the honey bee (Apis mellifera L.) antennal lobes during metamorphosis: a comparative study among castes and sexes. Anim Biol 61:153–161CrossRefGoogle Scholar
  56. Shi YY, Yan WY, Huang ZY, Wang ZL, Wu XB, Zeng ZJ (2013) Genomewide analysis indicates that queen larvae have lower methylation levels in the honey bee (Apis mellifera). Naturwissenschaften 100:193–197PubMedCrossRefGoogle Scholar
  57. Shima SN, Yamane S, Zucchi R (1994) Morphological caste differences in some Neotropical swarm-founding polistine wasps I. Apoica flavissima (Hymenoptera, Vespidae). Jap J Entomol 62:811–822Google Scholar
  58. Shima SN, Yamane S, Zucchi R (1996) Morphological caste differences in some Neotropical swarm-founding polistine wasps II. Polybia dimidiata (Hymenoptera, Vespidae). Jpn J Entomol 64:131–144Google Scholar
  59. Shultz S, Dunbar RIM (2010) Species differences in executive function correlate with hippocampus volume and neocortex ratio across nonhuman primates. J Comp Psychol 124:252–260PubMedCrossRefGoogle Scholar
  60. Strausfeld NJ, Hansen L, Li Y, Gomez RS, Ito K (1998) Evolution, discovery, and interpretation of arthropod mushroom bodies. Learn Mem 5:11–37PubMedCentralPubMedGoogle Scholar
  61. Tanaka NK, Endo K, Ito K (2012) Organization of antennal lobe-associated neurons in adult Drosophila melanogaster brain. J Comp Neurol 520:4067–4130PubMedCrossRefGoogle Scholar
  62. Toth AL, Bilof KBJ, Henshaw MT, Hunt JH, Robinson GE (2009) Lipid stores, ovary development, and brain gene expression in Polistes metricus females. Insect Soc 56:77–84CrossRefGoogle Scholar
  63. Wenzel JW, Carpenter JM (1994) Comparing methods: adaptive traits and tests of adaptation. In: Eggleton P, Vane-Wright RI (eds) Phylogenetics and ecology. Academic Press, London, pp 79–101Google Scholar
  64. West-Eberhard MJ (1978) Temporary queens in Metapolybia wasps: nonreproductive helpers without altruism? Science 200:441–443PubMedCrossRefGoogle Scholar
  65. West-Eberhard MJ (1981) Intragroup selection and the evolution of insect societies. In: Alexander RD, Tinkle DW (eds) Natural selection and social behavior. Chiron, New York, pp 3–17Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Sean O’Donnell
    • 1
  • Marie R. Clifford
    • 2
  • Susan J. Bulova
    • 1
  • Sara DeLeon
    • 1
  • Christopher Papa
    • 1
  • Nazaneen Zahedi
    • 1
  1. 1.Department of Biodiversity, Earth & Environmental ScienceDrexel UniversityPhiladelphiaUSA
  2. 2.Department of BiologyUniversity of WashingtonSeattleUSA

Personalised recommendations