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Caste differences in the mushroom bodies of swarm-founding paper wasps: implications for brain plasticity and brain evolution (Vespidae, Epiponini)

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Abstract

Eusocial insect reproductive castes (in Hymenoptera, female reproductive queens and sterile workers) differ dramatically in behavior. Castes may differ in the cognitive demands that affect patterns of brain tissue investment. Queens and workers diverge most strongly in the advanced eusocial, or swarm-founding species, where queens do not forage and rarely leave their nests. We asked whether reproductive castes of swarm-founding paper wasps in the tribe Epiponini differed in the relative sizes of their mushroom bodies (MB), a key brain region involved in sensory integration, and in learning and memory. We measured brain-size corrected volumes of the MB dendritic-field neuropils (calyces) and the MB axonal bundles (peducles and lobes) for queens and workers from 16 species of 10 genera of the tribe Epiponini. The subject species spanned much of the epiponine phylogeny, differing in colony size and degree of caste differentiation. Queens had significantly higher relative MB investment than workers, both for the MB in toto and for the MB calyces. The magnitude of queen-worker MB size differences did not covary significantly with body size, but species with larger colonies had stronger caste differences in MB size. A review of caste differences in MB volume across a wide range of social Hymenoptera taxa suggested a positive association of MB investment with social dominance is widespread.

Significance statement

Social insect castes (reproducing queens and sterile workers) differ strongly in behavior, particularly in swarm-founding species where queens are largely nest-bound. Caste comparisons are a powerful model for understanding brain/behavior relationships. We measured the relative size of a key insect brain region, the mushroom bodies (MB), in 16 swarm-founding wasp species. MB are involved in sensory integration, and in learning and memory. Queens had relatively larger MB than workers, and the magnitude of the queen-worker differences increased with species average colony size. We suggest the reproductive dominance and social contact of nest-bound queens promotes greater mushroom body investment.

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References

  • Anderson C, McShea DW (2001) Individual versus social complexity, with particular reference to ant colonies. Biol Rev Camb Philos Soc 76:211–237

    Article  CAS  PubMed  Google Scholar 

  • Barron AB, Maleszka R, Helliwell PG, Robinson GE (2009) Effects of cocaine on honey bee dance behaviour. J Exp Biol 212:163–168

    Article  PubMed  Google Scholar 

  • Barton RA, Purvis A, Harvey PH (1995) Evolutionary radiation of visual and olfactory brain systems in primates, bats and insectivores. Philos Trans R Soc B 348:381–392

    Article  CAS  Google Scholar 

  • Carpenter JM (2004) Synonymy of the genus Marimbonda Richards, 1978, with Leipomeles Möbius, 1856 (Hymenoptera: Vespidae; Polistinae), and a new key to the genera of paper wasps of the New World. Am Mus Novit 3465:1–16

  • Carpenter JM, Kojima JI, Wenzel JW (2000) Polybia, paraphyly, and polistine phylogeny. Am Mus Novit 3298:1–24

    Article  Google Scholar 

  • Davis RL (2005) Olfactory memory formation in Drosophila: from molecular to systems neuroscience. An Rev Neurosci 28:275–302

    Article  CAS  Google Scholar 

  • Eberhard MJW (1975) The evolution of social behavior by kin selection. Q Rev Biol 50:1–33

    Google Scholar 

  • Ehmer B, Gronenberg W (2004) Mushroom body volumes and visual interneurons in ants: comparison between sexes and castes. J Comp Neurol 469:198–213

    Article  PubMed  Google Scholar 

  • Ehmer B, Reeve HK, Hoy RR (2001) Comparison of brain volumes between single and multiple foundresses in the paperwasp Polistes dominulus. Brain Behav Evol 57:161–168

    Article  CAS  PubMed  Google Scholar 

  • Fahrbach SE (2006) Organization of the mushroom bodies of the insect brain. Annu Rev Entomol 51:209–232

    Article  CAS  PubMed  Google Scholar 

  • Fahrbach SE, Dobrin S (2009) The how and why of structural plasticity in the honey bee brain. In: Dukas R, Ratcliffe J (eds) Cognitive ecology II. University of Chicago Press, Chicago

    Google Scholar 

  • Farris SM (2008) Structural, functional and developmental convergence of the insect mushroom bodies with higher brain centers of vertebrates. Brain Behav Evol 72:1–15

    Article  PubMed  Google Scholar 

  • Farris SM (2013) Evolution of complex higher brain centers and behaviors: behavioral correlates of mushroom body elaboration in insects. Brain Behav Evol 82:9–18

    Article  PubMed  Google Scholar 

  • 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 21:6395–6404

    CAS  PubMed  Google Scholar 

  • Feinerman O, Traniello JFA (2016) Social complexity, diet, and brain evolution: modeling the effects of colony size, worker size, brain size, and foraging behavior on colony fitness in ants. Behav Ecol Sociobiol 70:1063–1074

    Article  Google Scholar 

  • Giurfa M (2003) Cognitive neuroethology: dissecting non-elemental learning in a honeybee brain. Curr Opin Neurobiol 13:726–735

    Article  CAS  PubMed  Google Scholar 

  • Gronenberg W (2001) Subdivisions of hymenopteran mushroom body calyces by their afferent supply. J Comp Neurol 435:474–489

    Article  CAS  PubMed  Google Scholar 

  • Gronenberg W, Liebig J (1999) Smaller brains and optic lobes in reproductive workers of the ant Harpegnathos. Naturwissenschaften 86:343–345

    Article  CAS  Google Scholar 

  • 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 377–401

    Google Scholar 

  • Hampton RR, Shettleworth SJ (1996) Hippocampal lesions impair memory for location but not color in passerine birds. Behav Neurosci 110:831

    Article  CAS  PubMed  Google Scholar 

  • Heisenberg M, Heusipp M, Wanke C (1995) Structural plasticity in the Drosophila brain. J Neurosci 15:1951–1960

    CAS  PubMed  Google Scholar 

  • Holbrook CT, Barden PM, Fewell JH (2011) Division of labor increases with colony size in the harvester ant Pogonomyrmex californicus. Behav Ecol 22:960–966

    Article  Google Scholar 

  • Holldobler B, Wilson EO (2009) The superorganism. WW Norton, NY, 522 pp

    Google Scholar 

  • 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 94:555–562

    Article  Google Scholar 

  • Jeanne RL (1991) The swarm-founding Polistinae. In: Ross KG, Matthews RW (eds) The social biology of wasps. Comstock Publishing Associates, Ithaca, pp 191–231

    Google Scholar 

  • 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, Japan, pp 81–131

    Google Scholar 

  • Jeanne RL, Suryanarayanan S (2011) A new model for caste development in social wasps. Comm Integr Biol 4:373–377

    Article  Google Scholar 

  • Jones TA, Donlan NA, O’Donnell S (2009) Growth and pruning of mushroom body Kenyon cell dendrites during worker behavioral development in the paperwasp, Polybia aequatorialis (Hymenoptera: Vespidae). Neurobiol Learn Mem 92:485–495

    Article  PubMed  Google Scholar 

  • Julian GE, Gronenberg W (2002) Reduction of brain volume correlates with behavioral changes in queen ants. Brain Behav Evol 60:152–164

    Article  PubMed  Google Scholar 

  • Kamhi JF, Gronenberg W, Robson SK, Traniello JFA (2016) Social complexity influences brain investment and neural operation costs in ants. Proc R Soc B 283:20161949

    Article  PubMed  Google Scholar 

  • Lee YA, Goto Y (2013) The effects of prenatal and postnatal environmental interaction: prenatal environmental adaptation hypothesis. J Physiol Paris 107:483–492

    Article  PubMed  Google Scholar 

  • Lozano V, Armengaud C, Gauthier M (2001) Memory impairment induced by cholinergic antagonists injected into the mushroom bodies of the honeybee. J Comp Physiol A 187:249–254

    Article  CAS  PubMed  Google Scholar 

  • Markiewicz DA, O'Donnell S (2001) Social dominance, task performance and nutrition: implications for reproduction in eusocial wasps. J Comp Physiol A 187:327–333

    Article  CAS  PubMed  Google Scholar 

  • Martins EP (2004) COMPARE, version 4.6b. Computer programs for the statistical analysis of comparative data. Distributed by the author at http://compare.bio.indiana.edu/. Department of Biology, Indiana University, Bloomington IN

  • Martins EP, Hansen TF (1997) Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. Am Nat 149:646–667

    Article  Google Scholar 

  • McNeill MS, Kapheim KM, Brockmann A, McGill TA, Robinson GE (2016) Brain regions and molecular pathways responding to food reward type and value in honey bees. Genes Brain Behav 15:305–317

    Article  CAS  PubMed  Google Scholar 

  • 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 70:137–144

    Article  PubMed  Google Scholar 

  • Molina Y, O'Donnell S (2008) Age, sex, and dominance-related mushroom body plasticity in the paperwasp Mischocyttarus mastigophorus. Dev Neurobiol 68:950–959

    Article  PubMed  Google Scholar 

  • Muscedere ML, Traniello JFA (2012) Division of labor in the hyperdiverse ant genus Pheidole is associated with distinct subcaste-and age-related patterns of worker brain organization. PLoS One 7:e31618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nascimento FD, Tannure-Nascimento IC, Zucchi R (2004) Behavioral mediators of cyclical oligogyny in the Amazonian swarm-founding wasp Asteloeca ujhelyii (Vespidae, Polistinae, Epiponini). Ins Soc 51:17–23

    Article  Google Scholar 

  • Niven JE, Laughlin SB (2008) Energy limitation as a selective pressure on the evolution of sensory systems. J Exp Biol 211:1792–1804

    Article  CAS  PubMed  Google Scholar 

  • Noll FB, Wenzel JW, Zucchi R (2004) Evolution of caste in Neotropical swarm-founding wasps (Hymenoptera: Vespidae; Epiponini). Am Mus Novit 3467:1–24

    Article  Google Scholar 

  • Noll FB, Zucchi R (2002) Castes and the influence of the colony cycle in swarm-founding polistine wasps (Hymenoptera, Vespidae, Epiponini). Ins Soc 49:62–74

    Article  Google Scholar 

  • O'Donnell S (1996) Reproductive potential and division of labor in wasps: are queen and worker behavior alternative strategies? Ethol Ecol Evol 8:305–308

    Article  Google Scholar 

  • O'Donnell S (1998) Reproductive caste determination in eusocial wasps (Hymenoptera: Vespidae). Annu Rev Entomol 43:323–346

    Article  PubMed  Google Scholar 

  • O’Donnell S, Bulova SJ (2017) Development and evolution of brain allometry in wasps (Vespidae): size, ecology and sociality. Curr Opin Insect Sci 22:54–61

    Article  Google Scholar 

  • O'Donnell S, Clifford MR, DeLeon S, Papa C, Zahedi N, Bulova SJ (2013) Brain size and visual environment predict species differences in paperwasp sensory processing brain regions (hymenoptera: vespidae, polistinae). Brain Behav Evol 82:177–184

    Article  PubMed  Google Scholar 

  • O’Donnell S, Clifford MR, Bulova SJ, DeLeon S, Papa C, Zahedi N (2014) A test of neuroecological predictions using paperwasp caste differences in brain structure (Hymenoptera: Vespidae). Behav Ecol Sociobiol 68:529–536

    Article  Google Scholar 

  • O'Donnell S, Clifford M, Molina Y (2011) Comparative analysis of constraints and caste differences in brain investment among social paperwasps. Proc Natl Acad Sci 108:7107–7112

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Donnell S, Donlan NA, Jones TA (2004) Mushroom body structural plasticity is associated with temporal polyethism in eusocial wasp workers. Neurosci Lett 356:159–162

    Article  PubMed  Google Scholar 

  • O'Donnell S, Donlan N, Jones T (2007) Developmental and dominance-associated differences in mushroom body structure in the paperwasp Mischocyttarus mastigophorus. Dev Neurobiol 67:39–46

    Article  PubMed  Google Scholar 

  • Pascual A, Preat T (2001) Localization of long-term memory within the Drosophila mushroom body. Science 294:1115–1117

    Article  CAS  PubMed  Google Scholar 

  • Platt TG, Queller DC, Strassmann JE (2004) Aggression and worker control of caste fate in a multiple-queen wasp, Parachartergus colobopterus. Anim Behav 67:1–10

    Article  Google Scholar 

  • 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 85:117–124

    Article  PubMed  Google Scholar 

  • Revell LJ (2012) Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223

    Article  Google Scholar 

  • Richards OW (1978) The social wasps of the Americas. Br. Mus. Nat. Hist, London

    Google Scholar 

  • Richards OW, Richards MJ (1951) Observations on the social wasps of South America (Hymenoptera Vespidae). Trans R Ent Soc Lond 102:1–169

    Article  Google Scholar 

  • Richter MR (2000) Social wasp (Hymenoptera: Vespidae) foraging behavior. Annu Rev Entomol 45:121–150

    Article  CAS  PubMed  Google Scholar 

  • Riveros AJ, Gronenberg W (2010) Brain allometry and neural plasticity in the bumblebee Bombus occidentalis. Brain Behav Evol 75:138–148

    Article  PubMed  PubMed Central  Google Scholar 

  • Roat TC, da Cruz Landim C (2010) Differences in mushroom bodies morphogenesis in workers, queens and drones of Apis mellifera: neuroblasts proliferation and death. Micron 41:382–389

    Article  PubMed  Google Scholar 

  • Sale A, Berardi N, Maffei L (2014) Environment and brain plasticity: towards an endogenous pharmacotherapy. Physiol Rev 94:189–234

    Article  CAS  PubMed  Google Scholar 

  • Seid MA, Harris KM, Traniello JFA (2005) Age-related changes in the number and structure of synapses in the lip region of the mushroom bodies in the ant Pheidole dentata. J Comp Neurol 488:269–277

    Article  PubMed  Google Scholar 

  • Seid MA, Junge E (2016) Social isolation and brain development in the ant Camponotus floridanus. Sci Nat 103(1-6):42

    Article  Google Scholar 

  • 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 62:811–822

    Google Scholar 

  • Shima SN, Yamane S, Zucchi R (1996) Morphological caste differences in some Neotropical swarm-founding polistine wasps II. Polybia dimidiata (Hymenoptera, Vespidae). Jap J Entomol 64:131–144

    Google Scholar 

  • Smith AR, Seid MA, Jiménez LC, Wcislo WT (2010) Socially induced brain development in a facultatively eusocial sweat bee Megalopta genalis (Halictidae). Proc R Soc B 277:2157–2163

    Article  PubMed  PubMed Central  Google Scholar 

  • Strassmann JE, Gastreich KR, Queller DC, Hughes CR (1992) Demographic and genetic evidence for cyclical changes in queen number in a neotropical wasp, Polybia emaciata. Am Nat 140:363–372

    Article  CAS  PubMed  Google Scholar 

  • Strassmann JE, Queller DC, Solis CR, Hughes CR (1991) Relatedness and queen number in the neotropical wasp, Parachartergus colobopterus. Anim Behav 42:461–470

    Article  Google Scholar 

  • Strausfeld NJ (2002) Organization of the honey bee mushroom body: representation of the calyx within the vertical and gamma lobes. J Comp Neurol 450:4–33

    Article  PubMed  Google Scholar 

  • Strausfeld NJ, Hansen L, Li Y, Gomez RS, Ito K (1998) Evolution, discovery, and interpretations of arthropod mushroom bodies. Learn Mem 5:11–37

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tindo M, Dejean A (2000) Dominance hierarchy in colonies of Belonogaster juncea juncea (Vespidae, Polistinae). Ins Soc 47:158–163

    Article  Google Scholar 

  • Toth AL, Varala K, Newman TC, Miguez FE, Hutchison SK, Willoughby DA, Robinson GE (2007) Wasp gene expression supports an evolutionary link between maternal behavior and eusociality. Science 318:441–444

    Article  CAS  PubMed  Google Scholar 

  • Wenzel JW, Carpenter JM (1994) Comparing methods: adaptive traits and tests of adaptation. In: Eggleton P, Vane-Wright R (eds) Phylogenetics in ecology. Harcourt Brace, London, pp 79–101

    Google Scholar 

  • West-Eberhard MJ (1977) The establishment of reproductive dominance in social wasp colonies. In: Proceedings of the 8th International Ethological Conference, Wageningen, pp. 223–227

  • West-Eberhard MJ (1986) Dominance relations in Polistes canadensis (L.), a tropical social wasp. Monit Zool Ital 20:263–281

    Google Scholar 

  • 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). Dev Neurobiol 68:73–82

    Article  PubMed  Google Scholar 

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Acknowledgements

Marie Clifford, Robin Harris, Emily Johnson, Paulina Khodak, Nola MacAloon, Skye Miller, Yamile Molina, Abigail Mudd, Christopher Papa, Elisabeth Sulger, Eve Swearingen, James Warren, and Nazaneen Zahedi assisted with histology and neuroanatomy. Specimen collections were made under research permits from the governments of Costa Rica and Ecuador. Research was supported by NSF grant IOS-1209072 and Drexel University start-up funds.

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O’Donnell, S., Bulova, S.J., DeLeon, S. et al. Caste differences in the mushroom bodies of swarm-founding paper wasps: implications for brain plasticity and brain evolution (Vespidae, Epiponini). Behav Ecol Sociobiol 71, 116 (2017). https://doi.org/10.1007/s00265-017-2344-y

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