Brain size and visual environment predict species differences in paper wasp sensory processing brain regions (Hymenoptera: Vespidae, Polistinae)

Brain, Behavior and Evolution

Volumn 82, Issue 3, 2013, Pages 177-184

  O'Donnell, Sean ^a   Clifford, Marie R ^b   Deleon, Sara ^a   Papa, Christopher ^a   Zahedi, Nazaneen ^a   Bulova, Susan J ^a  

^a DREXEL UNIVERSITY   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Antennal lobe; Mosaic evolution; Mushroom body; Optic lobe; Paper wasp; Vespidae

Indexed keywords

APOICA; BASIDIOMYCOTA; HYMENOPTERA; MAMMALIA; POLISTINAE; VESPIDAE;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BRAIN; CLASSIFICATION; ECOLOGY; ENVIRONMENT; EVOLUTION; HISTOLOGY; LIGHT; ORGAN SIZE; PHOTOSTIMULATION; PHYSIOLOGY; SPECIES DIFFERENCE; WASP;

ANIMALS; BEHAVIOR, ANIMAL; BIOLOGICAL EVOLUTION; BRAIN; ECOLOGY; ENVIRONMENT; LIGHT; ORGAN SIZE; PHOTIC STIMULATION; SPECIES SPECIFICITY; WASPS;

EID: 84886742633     PISSN: 00068977     EISSN: None     Source Type: Journal    
DOI: 10.1159/000354968     Document Type: Article

References (49)

1. Barton RA, Harvey PH (2000): Mosaic evolution of brain structure in mammals. Nature 405: 1055-1058.
2. Barton RA, Purvis A, Harvey PH (1995): Evolutionary radiation of visual and olfactory brain systems in primates, bats, and insectivores. Philos Trans R Soc Lond B Biol Sci 348: 381-392.
3. Borowsky R (2008): Restoring sight in blind cavefish. Curr Biol 18:R23-R24.
4. 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: 1-16.
5. Carpenter JM, Kojima J-I, Wenzel JW (2000): Polybia, paraphyly, and polistine phylogeny. Am Mus Novit 3298: 1-24.
6. Catania KC (2005): Evolution of sensory specializations in insectivores. Anat Rec A Discov Mol Cell Evol Biol 287: 1038-1050.
7. Chittka L, Niven J (2009): Are bigger brains better Curr Biol 19: 995-1008.
8. Cooper HM, Herbin M, Nevo E (1993): Visual system of a naturally microphthalmic mammal: the blind mole rat, Spalax ehrenbergi. J Comp Neurol 328: 313-350.
9. Ehmer B, Hoy R (2000): Mushroom bodies of vespid wasps. J Comp Neurol 416: 93-100.
10. Fahrbach SE (2006): Structure of the mushroom bodies of the insect brain. Annu Rev Entomol 51: 209-232.
11. Farris SM (2008): Evolutionary convergence of higher order brain centers spanning the protostome deuterostome boundary. Brain Behav Evol 72: 106-122.
12. Felsenstein J (1985): Phylogenies and the comparative method. Am Nat 125: 1-15.
13. Gatenby RA, Gillies RJ, Brown JS (2011): Of cancer and cave fish. Nat Rev Cancer 11: 237-238.
14. Greiner B (2006): Visual adaptations in the nightactive wasp Apoica pallens. J Comp Neurol 495: 255-262.
15. Groh C, Lu Z, Meinertzhagen IA, Roessler W (2012): Age-related plasticity in the synaptic ultrastructure of neurons in the mushroom body calyx of the adult honeybee Apis mellifera. J Comp Neurol 520: 3509-3527.
16. Gronenberg W (1999): Modality-specific segregation of input to ant mushroom bodies. Brain Behav Evol 54: 85-95.
17. Gronenberg W (2001): Subdivisions of Hymenopteran mushroom body calyces by their afferent supply. J Comp Neurol 436: 474-489.
18. Gronenberg W, Hölldobler B (1999): Morphologic representation of visual and antennal information in the ant brain. J Comp Neurol 412: 229-240.
19. Gunter H, Meyer A (2013): Trade-offs in cavefish sensory capacity. BMC Biol 11: 5.
20. Hager R, Lu L, Rosen GD, Williams RW (2012): Genetic architecture supports mosaic brain evolution and independent brain-body size regulation. Nat Commun 3: 1079.
21. Herculano-Houzel S (2011): Not all brains are made the same: new views on brain scaling in evolution. Brain Behav Evol 78: 22-36.
22. Jeffery WR (2009): Regressive evolution in Astyanax cavefish. Annu Rev Genet 43: 25-47.
23. Jones TA, Donlan NA, O'Donnell S (2009): Growth and pruning of mushroom body Ken yon cell dendrites during worker behavioral development in the paper wasp, Polybia aequatorialis (Hymenoptera: Vespidae). Neurobiol Learn Mem 92: 485-495.
24. Kaskan PM, Franco ECS, Yamada ES, Silveira LC, Darlington RB, Finlay BL (2005): Peripheral variability and central constancy in mammalian visual system evolution. Proc Biol Sci 272: 91-100.
25. Kelber A, Jonsson F, Wallen R, Warrant E, Kornfeldt T, et al (2011): Hornets can fly at night without obvious adaptations of eyes and ocelli. PLoS One 6:e21892.
26. Kolb EM, Rezende EL, Holness, Radtke A, Lee SK, Obenaus A, Garland T Jr (2013): Mice selectively bred for high voluntary wheel running have larger midbrains: support for the mosaic model of brain evolution. J Exp Biol 216: 515-523.
27. Laughlin SB (2001): Energy as a constraint on the coding and processing of sensory information. Curr Opin Neurobiol 11: 475-480.
28. 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 Suppl 14: 7-15.
29. Martins EP (2004): COMPARE, version 4.6b-computer programs for the statistical analysis of comparative data. http://compare.bio.indiana. edu/. Bloomington, Department of Biology, Indiana University.
30. Merabet LB, Pascual-Leone A (2010): Neural reorganization following sensory loss: the opportunity of change. Nat Rev Neurosci 11: 44-52.
31. Navarrete A, van Schaik CP, Isler K (2011): Energetics and the evolution of human brain size. Nature 480: 91-93.
32. Niven JE, Laughlin SB (2008): Energy limitation as a selective pressure on the evolution of sensory systems. J Exp Biol 211: 1792-1804.
33. 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 USA 108: 7107-7112.
34. O'Donnell S, Jeanne RL (1992): Life-long patterns of forager behaviour in a tropical swarmfounding wasp: effects of specialization and activity level on longevity. Anim Behav 44: 1021-1027.
35. Pfeiffer K, Kinoshita M (2012): Segregation of visual inputs from different regions of the compound eye in two parallel pathways through the anterior optic tubercle of the bumblebee (Bombus ignitus). J Comp Neurol 520: 212-229.
36. Powell BJ, Leal M (2012): Brain evolution across the Puerto Rican anole radiation. Brain Behav Evol 80: 170-180.
37. Rössler W, Zube C (2011): Dual olfactory pathway in Hymenoptera: evolutionary insights from comparative studies. Arthropod Struct Dev 40: 349-357.
38. Shultz S, Dunbar RIM (2010): Species differences in executive function correlate with hippocampus volume and neocortex ratio across nonhuman primates. J Comp Psychol 124: 252-260.
39. Smaers JB, Soligo C (2013): Brain reorganization, not relative brain size, primarily characterizes anthropoid brain evolution. Proc Biol Sci 280: 20130269.
40. Strausfeld NJ, Hansen L, Li Y, Gomez RS, Ito K (1998): Evolution, discovery, and interpretation of arthropod mushroom bodies. Learn Mem 5: 11-37.
41. Warrant EJ (2008): Seeing in the dark: vision and visual behaviour in nocturnal bees and wasps. J Exp Biol 211: 1737-1746.
42. Warrant EJ, Kelber A, Gislen A, Greiner B, Ribi W, Wcislo WT (2004): Nocturnal vision and landmark orientation in a tropical halictid bee. Curr Biol 14: 1309-1318.
43. Warren DL, Iglesias TL (2012): No evidence for the 'expensive tissue hypothesis' from an interspecific study in a highly variable species. J Evol Biol 25: 1226-1231.
44. Wenzel JW (1991): Evolution of nest architecture; in Ross KG, Matthews RW (eds): The Social Biology of Wasps. Ithaca, Cornell University Press, p 678.
45. Wenzel JW, Carpenter JM (1994): Comparing methods: adaptive traits and tests of adaptation; in Eggleton P, Vane-Wright RI (eds): Phylogenetics and Ecology. London, Academic Press, pp 79-101.
46. Wilczynski W (1984): Central neural systems subserving a homoplasous periphery. Am Zool 24: 755-763.
47. Xuan F, 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: 109-114.
48. Yoshizawa M, Yamamoto Y, O'Quin KE, Jeffery WR (2012): Evolution of an adaptive behavior and its sensory receptors promotes eye regression in blind cavefish. BMC Biol 10: 108.
49. Zhao H, Rossiter SJ, Teeling EC, Li C, Cotton JA, Zhang S (2009): The evolution of color vision in nocturnal mammals. Proc Natl Acad Sci USA 106: 8980-8985.