Evolution of complex higher brain centers and behaviors: Behavioral correlates of mushroom body elaboration in insects

Brain, Behavior and Evolution

Volumn 82, Issue 1, 2013, Pages 9-18

  Farris, Sarah M ^a  

^a WEST VIRGINIA UNIVERSITY   (United States)

Author keywords

Behavior; Evolution; Higher brain center; Insect; Mushroom bodies

Indexed keywords

ANIMAL; ANIMAL BEHAVIOR; CONFERENCE PAPER; EVOLUTION; HISTOLOGY; INSECT; MUSHROOM BODY;

ANIMALS; BEHAVIOR, ANIMAL; BIOLOGICAL EVOLUTION; INSECTS; MUSHROOM BODIES;

BASIDIOMYCOTA; BILATERIA; HEXAPODA; PRIMATES; VERTEBRATA;

EID: 84883204410     PISSN: 00068977     EISSN: None     Source Type: Journal    
DOI: 10.1159/000352057     Document Type: Conference Paper

References (92)

1. Arendt D, Denes AS, Jékely G, Tessmar-Raible K (2008): The evolution of nervous system centralization. Philos Trans R Soc Lond B Biol Sci 363: 1523-1528.
2. Avarguès-Weber A, Deisig N, Giurfa M (2010): Visual cognition in social insects. Annu Rev Entomol 56: 423-443.
3. Bell WJ, Roth LM, Nalepa CA (2007): Cockroaches: Ecology, Behavior and Natural History. Baltimore, Johns Hopkins University Press.
4. Brown CR, Hatch MH (1929): Orientation and 'fright' reactions of whirligig beetles (Gyrinidae). J Comp Psychol 9: 159-189.
5. Brown S, Strausfeld N (2009): The effect of age on a visual learning task in the American cockroach. Learn Mem 16: 210-223.
6. Busto GU, Cervantes-Sandoval I, Davis RL (2010): Olfactory learning in Drosophila. Physiology 2010: 338-346.
7. Collett M, Collett TS (2007): Spatial aspects of foraging in ants and bees; in North G, Greenspan RJ (eds): Invertebrate Neurobiology. Cold Spring Harbor, Cold Spring Harbor Laboratory Press, pp 467-502.
8. Dujardin F (1850): Mémoire sur le système nerveux des insectes. Ann Sci Nat Zool 14: 195-206.
9. Dunbar RI (1998): The social brain hypothesis. Evol Anthropol 6: 178-190.
10. Dunbar RI, Shultz S (2007): Understanding primate brain evolution. Philos Trans R Soc Lond B Biol Sci 362: 649-658.
11. Eason PK, Switzer PV (2006): Spatial learning in dragonflies. Int J Comp Psychol 19: 268-281.
12. Eggleton P (2011): An introduction to termites: biology, taxonomy and functional morphology; in Bignell DE, Roisin Y, Lo N (eds): Biology of Termites: a Modern Synthesis. New York, Springer Science+Business Media, pp 1-26.
13. Farris SM (2005): Evolution of insect mushroom bodies: old clues, new insights. Arthropod Struct Dev 34: 211-234.
14. Farris SM (2008a): Structural, functional and developmental convergence of the insect mushroom bodies with higher brain centers of vertebrates. Brain Behav Evol 72: 1-15.
15. Farris SM (2008b): Tritocerebral tract input to the insect mushroom bodies. Arthropod Struct Dev 37: 492-503.
16. Farris SM, Roberts NS (2005): Coevolution of generalist feeding ecologies and gyrencephalic mushroom bodies in insects. Proc Natl Acad Sci USA 102: 17394-17399.
17. Farris SM, Robinson GE, Davis RL, Fahrbach SE (1999): Larval and pupal development of the mushroom bodies in the honey bee, Apis mellifera. J Comp Neurol 414: 97-113.
18. Farris SM, Robinson GE, Fahrbach SE (2001): Experience- and age-related outgrowth of intrinsic neurons in the mushroom bodies of the adult worker honey bee. J Neurosci 21: 6395-6404.
19. Farris SM, Schulmeister S (2011): Parasitoidism, not sociality, is associated with the evolution of elaborate mushroom bodies in the brains of hymenopteran insects. Proc Biol Sci 278: 940-951.
20. Farris SM, Strausfeld NJ (2001): Development of laminar organization in the mushroom bodies of the cockroach: Kenyon cell proliferation, outgrowth, and maturation. J Comp Neurol 439: 331-351.
21. Farris SM, Strausfeld NJ (2003): A Unique mushroom body substructure common to basal cockroaches and termites. J Comp Neurol 456: 305-320.
22. Gotz M, Huttner WB (2005): The cell biology of neurogenesis. Nat Rev Mol Cell Biol 6: 777-788.
23. Grimaldi DA, Engel MS (2005): Evolution of the Insects. New York, Cambridge University Press. Gronenberg W (2001): Subdivisions of hymenopteran mushroom body calyces by their afferent supply. J Comp Neurol 436: 474-489.
24. Grunewald B (1999): Morphology of feedback neurons in the mushroom body of the honey bee, Apis mellifera. J Comp Neurol 404: 114-126.
25. Hartenstein V (1993): Atlas of Drosophila Development. Cold Spring Harbor, Cold Spring Harbor Laboratory Press. Hirth F (2010): On the origin and evolution of the tripartite brain. Brain Behav Evol 76: 3-10.
26. Homberg U (1984): Processing of antennal information in extrinsic mushroom body neurons of the bee brain. J Comp Physiol A 154: 825-836.
27. Homberg U, Montague RA, Hildebrand JG (1988): Anatomy of antenno-cerebral pathways in the brain of the sphinx moth Manduca sexta. Cell Tissue Res 254: 255-281.
28. Hunt JH (1999): Trait mapping and salience in the evolution of eusocial vespid wasps. Evolution 53: 225-237.
29. Inward D, Beccaloni G, Eggleton P (2007): Death of an order: a comprehensive molecular phylogenetic study confirms that termites are eusocial cockroaches. Biol Lett 3: 331-335.
30. Ito K, Hotta Y (1992): Proliferation pattern of postembryonic neuroblasts in the brain of Drosophila melanogaster. Dev Biol 149: 134-148.
31. Ito K, Suzuki K, Estes P, Ramaswami M, Yamamoto D, Strausfeld NJ (1998): The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. Learn Mem 5: 52-77.
32. Jacobs LF (2012): From chemotaxis to the cognitive map: the function of olfaction. Proc Nat Acad Sci USA 109: 10693-10700.
33. Jawlowski H (1959): On the brain structure of the Ichneumonidae. B Acad Pol Sci Biol 8: 123- 125.
34. Jefferis GS, Potter CJ, Chan AM, Marin EC, Rohlfing T, Mauer CR Jr, Luo L (2007): Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 128: 1187-1203.
35. Kaas JH (1995): The evolution of isocortex. Brain Behav Evol 46: 187-196.
36. Kahsai L, Zars T (2011): Learning and memory in Drosophila: behavior, genetics, and neural systems. Int Rev Neurobiol 99: 139-167.
37. Kenyon FC (1896): The meaning and structure of the so-called 'mushroom bodies' of the Hexapod brain. Am Nat 30: 643-650.
38. Kirk EC (2006): Visual influences on primate encephalization. J Hum Evol 51: 76-90.
39. Kriegstein A, Noctor S, Martinez-Cerdeño V (2006): Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nat Rev Neurosci 7: 883-890.
40. Kwon HW, Lent DD, Strausfeld NJ (2004): Spatial learning in the restrained American cockroach Periplaneta americana. J Exp Biol 207: 377-383.
41. Lefebvre L, Reader SM, Boire D (2006): The evolution of encephalization; in Kaas JH (ed): Evolution of Nervous Systems. New York, Academic Press, vol 1, pp 121-141.
42. Lefebvre L, Sol D (2008): Brains, lifestyles and cognition: are there general trends? Brain Behav Evol 72: 135-144.
43. Lent DD, Kwon HW (2004): Antennal movements reveal associative learning in the American cockroach Periplaneta americana. J Exp Biol 207: 369-375.
44. Li YS, Strausfeld NJ (1997): Morphology and sensory modality of mushroom body extrinsic neurons in the brain of the cockroach, Periplaneta americana. J Comp Neurol 387: 631-650.
45. Li YS, Strausfeld NJ (1999): Multimodal efferent and recurrent neurons in the medial lobes of cockroach mushroom bodies. J Comp Neurol 409: 647-663.
46. Lihoreau M, Latty T, Chittka L (2012): An exploration of the social brain hypothesis in insects. Front Physiol 3: 442.
47. Lin HH, Lai JS, Chin AL, Chen YC, Chiang AS (2007): A map of olfactory representation in the Drosophila mushroom body. Cell 128: 1205-1217.
48. Lin C, Strausfeld N (2012): Visual inputs to the mushroom body calyces of the whirligig beetle Dineutus sublineatus: modality switching in an insect. J Comp Neurol 520: 2562-2574.
49. Menzel R (2012): The honeybee as a model for understanding the basis of cognition. Nat Rev Neurosci 13: 758-768.
50. Mizunami M, Okada R, Li YS, Strausfeld NJ (1998a): Mushroom bodies of the cockroach: activity and identities of neurons recorded in freely moving animals. J Comp Neurol 402: 501-519.
51. Mizunami M, Weibrecht JM, Strausfeld NJ (1998b): Mushroom bodies of the cockroach: their participation in place memory. J Comp Neurol 402: 520-537.
52. Mobbs PG (1982): The brain of the honeybee Apis mellifera L: the connections and spatial organization of the mushroom bodies. Philos Trans R Soc Lond B Biol Sci 298: 309-354.
53. Mobbs PG (1984): Neural networks in the mushroom bodies of the honeybee. J Insect Physiol 30: 43-58.
54. Neder R (1959): Allometrisches Wachstum von Hirnteilen bei drei verschieden grossen Schabenarten. Zool Jahrb Anat 77: 411-464.
55. Neuser K, Triphan T, Mronz M, Poeck B, Strauss R (2008): Analysis of a spatial orientation memory in Drosophila. Nature 453: 1244-1247.
56. Newton ET (1879): On the brain of the cockroach, Blatta orientalis. Q J Microsc Sci 19: 340-356.
57. Niven JE, Graham CM, Burrows M (2008): Diversity and evolution of the insect ventral nerve cord. Annu Rev Entomol 53: 253-271.
58. Northcutt RG (2012): Evolution of centralized nervous systems: two schools of evolutionary thought. Proc Nat Acad Sci USA 109: 10626-10633.
59. Ofstad TA, Zuker CS, Reiser MB (2011): Visual place learning in Drosophila melanogaster. Nature 474: 204-207.
60. Okada R, Ikeda J, Mizunami M (1999): Sensory responses and movement-related activities in extrinsic neurons of the cockroach mushroom bodies. J Comp Physiol A 185: 115-129.
61. Panov AA (1957): The structure of the brain in insects in successive stages of postembryonic development. Rev Entomol USSR 36: 269-284.
62. Rakic P (2009): Evolution of the neocortex: a perspective from developmental biology. Nat Rev Neurosci 10: 724-735.
63. Reichert H, Simeone A (2001): Developmental genetic evidence for a monophyletic origin of the bilaterian brain. Philos Trans R Soc Lond B Biol Sci 356: 1533-1544.
64. Rosenheim JA (1987): Host location and exploitation by the cleptoparasitic wasp Argochrysis armilla: the role of learning (Hymenoptera: Chrysididae). Behav Ecol Sociobiol 21: 401-406.
65. Roth TC 2nd, Brodin A, Smulders TV, LaDage LD, Pravosudov VV (2010): Is bigger always better? A critical appraisal of the use of volumetric analysis in the study of the hippocampus. Phil Trans R Soc Lond B Biol Sci 365: 915-931.
66. Schildberger K (1984): Multimodal interneurons in the cricket brain: properties of identified extrinsic mushroom body cells. J Comp Physiol 154: 71-79.
67. Schröter U, Menzel R (2003): A new ascending sensory tract to the calyces of the honeybee mushroom body, the subesophageal-calycal tract. J Comp Neurol 465: 168-178.
68. Shellman-Reeve JS (1997): The spectrum of eusociality in termites; in Choe JC, Crespi BJ (eds): The Evolution of Social Behavior in Insects and Arachnids. Cambridge, Cambridge University Press, pp 52-93.
69. Sinakevitch I, Sjölholm M, Hansson BS, Strausfeld NJ (2008): Global and local modulatory supply to the mushroom bodies of the moth Spodoptera littoralis. Arthropod Struct Dev 37: 260-272.
70. Sivinski J (1989): Mushroom body development in nymphalid butterflies: a correlate of learning? J Insect Behav 2: 277-283.
71. Snell-Rood EC, Papaj DR, Gronenberg W (2009): Brain size: a global or induced cost of learning? Brain Behav Evol 73: 111-128.
72. Sprecher SG, Reichert H (2003): The urbilaterian brain: developmental insights into the evolutionary origin of the brain in insects and vertebrates. Arthropod Struct Dev 32: 141-156.
73. Strausfeld NJ (1976): Atlas of an Insect Brain. Berlin, Springer.
74. 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.
75. Strausfeld NJ (2012): Arthropod Brains: Evolution, Functional Elegance, and Historical Significance. Cambridge, Harvard University Press.
76. Strausfeld NJ, Homberg U, Kloppenburg P (2000): Parallel organization in honey bee mushroom bodies by peptidergic Kenyon cells. J Comp Neurol 424: 179-195.
77. Strausfeld NJ, Li YS (1999): Organization of olfactory and multimodal afferent neurons supplying the calyx and pedunculus of the cockroach mushroom bodies. J Comp Neurol 409: 603-625.
78. Strausfeld NJ, Sinakevitch I, Brown SM, Farris SM (2009): Ground plan of the insect mushroom body: functional and evolutionary implications. J Comp Neurol 513: 265-291.
79. Svidersky VL, Plotnikova SI (2004): On structural-functional organization of dragonfly mushroom bodies and some general considerations about purpose of these formations. J Evol Biochem Physiol 40: 608-624.
80. Tanaka NK, Awasaki T, Shimada T, Ito K (2004): Integration of chemosensory pathways in the Drosophila second-order olfactory centers. Curr Biol 14: 449-457.
81. Tanaka NK, Tanimoto H, Ito K (2008): Neuronal assemblies of the Drosophila mushroom body. J Comp Neurol 508: 711-755.
82. Truman JW, Bate M (1988): Spatial and temporal patterns of neurogenesis in the CNS of Drosophila melanogaster. Dev Biol 125: 146-157.
83. Urbach R, Technau GM (2003): Early steps in building the insect brain: neuroblast formation and segmental patterning in the developing brain of different insect species. Arthropod Struct Dev 32: 103-123.
84. van Nouhuys S, Ehrnsten J (2004): Wasp behavior leads to uniform parasitism of a host available for only a few hours per year. Behav Ecol 15: 661-665.
85. van Nouhuys S, Kaartinen R (2008): A parasitoid wasp uses landmarks while monitoring potential resources. Proc Biol Sci 275: 377-385.
86. van Schaik CP, Isler K, Burkhart JM (2012): Explaining brain size variation: from social to cultural brain. Trends Cogn Sci 16: 277-284.
87. Vandersal ND (2008): Rapid spatial learning in a velvet ant (Dasymutilla coccineohirta). Anim Cogn 11: 563-567.
88. Winston ML (1987): The Biology of the Honey Bee. Cambridge, Harvard University Press.
89. 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.
90. Witthöft W (1967): Absolute Anzahl und Verteilung der Zellen im Hirn der Honigbiene. Z Morphol Okol Tiere 61: 160-164.
91. Wolf R, Wittig T, Liu L, Wustmann G, Eyding D, Heisenberg M (1998): Drosophila mushroom bodies are dispensable for visual, tactile, and motor learning. Learn Mem 5: 166-178.
92. Zars T (2009): Spatial orientation in Drosophila. J Neurogenet 23: 104-110.