Socially induced brain development in a facultatively eusocial sweat bee Megalopta genalis (Hailctidae)

Proceedings of the Royal Society B: Biological Sciences

Volumn 277, Issue 1691, 2010, Pages 2157-2163

  Smith, Adam R ^a,b   Seid, Marc A ^a,b   Jiménez, Lissette C ^a,b   Wcislo, William T ^a,b  

^a SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

^b Box 0948   (United States)

Author keywords

Brain organization; Machiavellian intelligence; Mushroom bodies; Neural plasticity; Social brain; Social evolution

Indexed keywords

BEE; BIOLOGICAL DEVELOPMENT; BODY SHAPE; BRAIN; COGNITION; EUSOCIALITY; HISTOLOGY; MORPHOLOGY; PHENOTYPIC PLASTICITY; SOCIAL INSECT; SOCIAL ORGANIZATION; WORKER CASTE;

EID: 77955391863     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2010.0269     Document Type: Article

References (61)

1. Adolphs, R. 2001 The neurobiology of social cognition. Curr. Opin. Neurobiol. 11, 231-239. (doi:10.1016/S09594388(00)00202-6)
2. Arneson, L. & Wcislo, W. T. 2003 Dominant-subordinate relationships in a facultatively social, nocturnal bee, Megalopta genalis (Hymenoptera: Halictidae). J. Kans. Entomol Soc. 76, 183-193. (Festschrift Supplement).
3. Bernays, E. A. & Wcislo, W. T. 1994 Sensory capabilities, information processing, and resource specialization. Q. Rev. Biol. 69, 187-204. (doi:10.1086/418539)
4. Bhadra, A. & Gadagkar, R. 2008 We know that the wasps 'know': cryptic successors to the queen in Ropalidia marginata. Biol. Lett. 4, 634-637. (doi:10.1098/rsbl. 2008.0455)
5. Byrne, R. W. & Bates, L. A. 2007a Sociality, evolution, and cognition. Curr. Biol. 17, R714-R723. (doi:10.1016/ j.cub.2007.05.069)
6. Byrne, R. W. & Bates, L. A. 2007e When is a group not a group? Curr. Biol. 17, R883-R884. (doi:10.1016/j.cub. 2007.08.018)
7. Cane, J. H. 1987 Estimation of bee size using intertegular span (Apoidea). J. Kansas Entomol. Soc. 60, 145-147.
8. Capaldi, E. A. et al 2000 Ontogeny of orientation flight in the honeybee revealed by harmonic radar. Nature 403, 537-540. (doi:10.1038/35000564)
9. D'Ettorre, P. & Heinze, J. 2005 Individual recognition in ant queens. Curr. Biol. 15, 2170-2174. (doi:10.1016/j.cub. 2005.10.067)
10. de Waal, F. B. M. & Tyack, P. L. (eds) 2003 Animal social complexity: intelligence, culture, and individualized societies. Cambridge, MA: Harvard University Press.
11. Dunbar, R. I. M. & Shultz, S. 2007 Evolution in the social brain. Science 317, 1344-1347. (doi:10.1126/science. 1145463)
12. Durst, C., Eichmuller, S. & Menzel, R. 1994 Development and experience lead to increased volume of subcompartments of the honeybee mushroom body. Behav. Neural Biol. 62, 259-263. (doi:10.1016/S0163-1047(05)80025-1)
13. Eberhard, W. G. 2007 Miniaturized orb-weaving spiders: behavioural precision is not limited by small size. Proc. R Soc. B 274, 2203-2209. (doi:10.1098/rspb.2007.0675)
14. Edelman, G. M. & Changeux, J. P. (eds) 2001 The brain. New Brunswick, NJ: Transaction Publishers.
15. Ehmer, B., Reeve, H. K. & Hoy, R. R. 2001 Comparison of brain volumes between single and multiple foundresses in the paper wasp Polistes dominulus. Brain Behav. Evol. 57, 161-168. (doi:10.1159/000047234)
16. Fahrbach, S. E. 2006 Organization of the mushroom bodies of the insect brain. Ann. Rev. Entomol. 51, 209-232. (doi:10.1146/annurev.ento.51.110104. 150954)
17. Fahrbach, S. E., Giray, T. & Robinson, G. E. 1995 Volume changes in the mushroom bodies of adult honey bee queens. Neurobiol. Learn. Mem. 63, 181-191. (doi:10. 1006/nlme.1995.1019)
18. Fahrbach, S. E., Moore, D., Capaldi, E. A., Farris, S. M. & Robinson, G. E. 1998 Experience-expectant plasticity in the mushroom bodies of the honeybee. Learn. Mem. 5, 115-123.
19. Farris, S. M. & Roberts, N. S. 2005 Coevolution of generalist feeding ecologies and gyrencephalic mushroom bodies in insects. Proc. Natl Acad. Sci. USA 102, 17 393-17 399. (doi:10.1073/pnas.0508430102)
20. Farris, S. M., Robinson, G. E. & Fahrbach, S. E. 2001 Experience- and age-related outgrowth of intrinsic neurons in the mushroom bodies of the adult worker honeybee. J. Neurosci. 21, 6395-6404.
21. Fiala, J. C. 2005 Reconstruct: a free editor for serial section microscopy. J. Microsc. 218, 52-61. (doi:10.1111/j.1365-2818.2005.01466.x)
22. Fletcher, D. J. C. & Michener, C. D. (eds) 1987 Kin recognition in animals. New York, NY: John Wiley & Sons.
23. Goodson, J. L., Evans, A. K., Lindberg, L. & Allen, C. D. 2005 Neuro-evolutionary patterning of sociality. Proc. R Soc. B 272, 227-235. (doi:10.1098/rspb.2004.2892)
24. Gronenberg, W & Riveras, A. J. 2009 Social brains and behavior-past and present. In Organization of insect societies from genome to sociocomplexity (eds J. Gadau & J. Fewell), pp. 377-401. Cambridge, MA: Harvard University Press.
25. Gronenberg, W., Heeren, S. & Hölldobler, B. 1996 Agedependent and task-related morphological changes in the brain and the mushroom bodies of the ant Camponotus fioridanus. J. Exp. Biol. 199, 2011-2019.
26. Gronenberg, W, Ash, L. E. & Tibbetts, E. A. 2007 Correlation between facial pattern recognition and brain composition in paper wasps. Brain Behav. Evol. 71, 1-14. (doi:10.1159/000108607)
27. Healy, S. D. & Rowe, C. 2007 A critique of comparative studies of brain size. Proc. R. Soc. B 274, 453-464. (doi:10.1098/rspb.2006.3748)
28. Heisenberg, M. 1998 What do the mushroom bodies do for the insect brain? An introduction. Learn. Mem. 5, 1-10.
29. Heisenberg, M., Heusipp, M. & Wanke, C. 1995 Structural plasticity in the Drosophila brain. J. Neurosd. 15, 1951-1960.
30. Howse, P. E. 1974 Design and function of the insect brain. In Experimental analysis of insect behavior (ed. L. B. Browne), pp. 180-195. Berlin, Germany: Springer.
31. Howse, P. E. & Williams, J. L. D. 1969 The brains of social insects in relation to behaviour. In Proc. of the Sixth Congress of the International Union for the Study of Social Insects, Bern, pp. 59-64.
32. Humphrey, N. K. 1976 The social function of intellect. In Growing points in ethology (eds P. P. G. Bateson & R. A. Hinde), pp. 303-317. Cambridge, UK: Cambridge University Press.
33. Ismail, N., Robinson, G. E. & Fahrbach, S. E. 2006 Stimulation of muscarinic receptors mimics experiencedependent plasticity in the honey bee brain. Proc. Nad Acad. Sci. USA 103, 207-211. (doi:10.1073/pnas. 0508318102)
34. Julian, G. E. & Gronenberg, W. 2002 Reduction of brain volume correlates with behavioural changes in queen ants. Brain Behav. Evol. 60, 152-164. (doi:10. 1159/000065936)
35. Kapheim, K. M., Bernai, S. V, Smith, A. R., Nonacs, P. & Wcislow, W T. Submitted. Support for maternal manipulation of developmental nutrition in a facultatively eusocial bee, Megabpta genalis (Halictidae).
36. Kelber, A., Warrant, E. J., Pfaff, M., Wallé, R., Theobald, J. C., Wcislo, W. T & Raguso, R. A. 2006 Light intensity limits foraging activity in nocturnal and crepuscular bees. Behav. Ecol. 17, 63-72. (doi:10.1093/beheco/ arj001)
37. Kühn-Bühlmann, 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, 511-521. (doi:10.1002/neu.20235)
38. Menzel, R. & Giurfa, M. 2001 Cognitive architecture of a mini-brain: The honeybee. Trends Cognit. Sci. 5, 62-71. (doi:10.1016/S1364-6613(00)01601-6)
39. Michener, C. D. 2007 The bees of the world, 2nd edn. Baltimore, MD: The John Hopkins University Press.
40. Molina, Y & O'Donnell, S. 2007 Mushroom body volume is related to social aggression and ovary development in the paperwasp Polistes instabais. Brain Behav. Evol. 70, 137-144. (doi:10.1159/000102975)
41. Molina, Y & O'Donnell, S. 2008 Age, sex, and dominancerelated mushroom body plasticity in the paperwasp Mischocyttarus mastigophorus. Dev. Neurobiol. 68, 950-959. (doi:10.1002/dneu.20633)
42. Molina, Y., Harris, R. M. & O'Donnell, S. 2009 Brain organization mirrors caste differences, colony founding and nest architecture in paper wasps (Hymenoptera: Vespidae). Proc. R. Soc. B 276, 3345-3351. (doi:10.1098/rspb. 2009.0817)
43. Niven, J. E. & Laughlin, S. B. 2008 Energy limitation as a selective pressure on the evolution of sensory systems. J. Exp. Biol. 211, 1792-1804. (doi:10.1242/jeb.017574)
44. O'Donnell, S., Donlan, N. A. & Jones, T. A. 2004 Mushroom body structural plasticity is associated with temporal polyethism in eusocial wasp workers. Neurosd. Lett. 356, 159-162. (doi:10.1016/j.neulet.2003.11.053)
45. O'Donnell, S., Donlan, N. A. & Jones, T. A. 2006 Organizational and dominance associated differences in mushroom body organization in the paper wasp, Mischocyttarus mastigophorus. J. Neurobiol. 67, 39-46. (doi: 10. 1002/neu.20324)
46. O'Neill, K. M. 2001 Solitary wasps: behavior and natural history. Ithaca, NY: Cornell University Press.
47. Pérez-Barbería, F. J., Shultz, S., Dunbar, R. I. M. & Janis, C. 2007 Evidence for coevolution of sociality and relative brain size in three orders of mammals. Evolution 61, 2811-2821. (doi:10.1111/j.1558-5646.2007. 00229.x)
48. Ricklefs, R. E. 2004 The cognitive face of avian life histories: The 2003 Margaret Morse Nice Lecture. Wilson Bull 116, 119-133. (doi:10.1676/04-054)
49. Seid, M. A. & Wehner, R. 2009 Delayed axonal pruning in the ant brain: a study of developmental trajectories. Dev. Neurobiol 69, 350-364. (doi:10.1002/dneu.20709)
50. Smith, A. R., Wcislo, W. T. & O'Donnell, S. 2007 Survival and productivity benefits to social nesting in the sweat bee Megabpta genalis (Hymenoptera: Halictidae). Behav. Ecol. Sociobiol 61, 1111-1120. (doi:10.1007/s00265006-0344-4)
51. Smith, A. R., Wcislo, W. T. & O'Donnell, S. 2008 Body size shapes caste expression, and cleptoparasitism reduces body size in the facultatively eusocial bees Megabpta (Hymenoptera: Halictidae). J. Insect Behav. 21, 394-406. (doi:10.1007/s10905-008-9136-l)
52. Smith, A. R., Kapheim, K. M., O'Donnell, S. & Wcislo, W T 2009 Social competition leads to a division of labour among totipotent females in the facultatively social sweat bee Megalopta genalis (Hymenoptera: Halictidae). Anim. Behav. 78, 1043-1050. (doi:10.1016/j. anbehav.2009.06.032)
53. Strausfeld, N. J., Sinakevitch, I., Brown, S. M. & Farris, S. M. 2009 Ground plan of the insect mushroom body: functional and evolutionary implications. J. Comp. Neurol. 513, 265-291. (doi:10.1002/cne.21948)
54. Tibbetts, E. A. 2002 Visual signals of individual identity in the paper wasp Polistes fuscatus. Proc. R. Soc. Lond. B 269, 1423-1428. (doi:10.1098/rspb.2002.2031)
55. Wcislo, W. T. 1997 Behavioural environments of sweat bees (Halictinae) in relation to variability in social organization. In Social behaviour in insects and arachnids (eds J. C. Choe & B. J. Crespi), pp. 316-332. Cambridge, UK: Cambridge University Press.
56. Wcislo, W. T & Gonzalez, V. H. 2006 Social and ecological contexts of trophallaxis in facultatively social sweat bees, Megalopta genalis and M. ecuadoria (Hymenoptera, Halictidae). Insect. Soc. 53, 220-225. (doi:10.1007/s00040005-0861-6)
57. Wcislo, W. T., Wille, A. & Orozco, E. 1993 Nesting biology of tropical solitary and social sweat bees, Lasioglossum (Dialictus) figueresi Wcislo and Lasioglossum (D.) aeneiventre (Friese). Insect. Soc. 40, 21-40. (doi:10.1007/ BF01338830)
58. Wcislo, W. T., Arneson, L., Roesch, K., Gonzalez, V. H., Smith, A. R. & Fernandez, H. 2004 The evolution of nocturnal behaviour in sweat bees, Megalopta genalis and M. ecuadoria (Hymenoptera: Halictidae): an escape from competitors and enemies? Biol. J. Linn. Soc. 83, 377-387. (doi:10.1111/j.1095- 8312.2004.00399.x)
59. Withers, G. S., Fahrbach, S. E. & Robinson, G. E. 1993 Selective neuroanatomical plasticity and division of labour in the honeybee. Nature 364, 238-240. (doi:10. 1038/364238a0)
60. Withers, G. S., Fahrbach, S. E. & Robinson, G. E. 1995 Effects of experience and juvenile hormone on the organization of the mushroom bodies of honey bees. J. Neurobiol. 26, 130-144. (doi:10.1002/neu.480260111)
61. Withers, G. S., Day, N. F., Talbot, F., Dobson, H. E. M. & Wallace, C. S. 2007 Experience-dependent plasticity in the mushroom bodies of the solitary bee Osmia lignaria (Megachilidae). Devebp. Neurobiol. 68, 73-82. (doi:10. 1002/dneu.20574)