Grade changes in brain-body allometry. morphological and behavioural correlates of brain size in miniature spiders, insects and other invertebrates

Advances in Insect Physiology

Volumn 40, Issue , 2011, Pages 155-214

  Eberhard, William G ^a,b   Wcislo, William T ^a  

^a SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

^b UNIVERSIDAD DE COSTA RICA   (Costa Rica)

Author keywords

Araneidae; Behavioural imprecision; Brain miniaturization; Brain body allometry; Crustacean, evolution of small body size; Insecta; Kinorhyncha; Nematoda; Orb web construction

Indexed keywords

EID: 80053526142     PISSN: 00652806     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-387668-3.00004-0     Document Type: Chapter

References (211)

1. Altun Z.F., Hall D.H. Handbook of C. elegans anatomy. WormAtlas 2008, http://www.wormatlas.org/hermaphrodite/hermaphroditehomepage.htm.
2. Anderson M.L. Neural reuse: a fundamental organizational principle of the brain. Behav. Brain Sci. 2010, 33:245-313.
3. Anderson A., McShea D.W. Individual versus social complexity, with particular reference to ant colonies. Biol. Rev. 2001, 76:211-237.
4. Avargués-Weber A., Dyer A.G., Giurfa M. Conceptualization of above and below relationships by an insect. Proc. R. Soc. B 2011, 278:898-905.
5. Babu K.S. Post embryonic development of the central nervous system of the spider Argiope aurantia (Lucas). J. Morphol. 1975, 146:325-342.
6. Babu K.S., Barth F. Neuroanatomy of the central nervous system of the wandering spider, Cupiennius salei (Arachnida, Araneida). Zoomorphology 1984, 104:344-359.
7. Banchetti R., Ricci N. The behavior of Heterolepidoderma sp. (Gastrotricha). Zool. Sci. 1998, 15:131-137.
8. Barnes R.S.K., Callow P., Olive P.J.W. The Invertebrates: A New Synthesis 1993, Blackwell Scientific Publications, Boston, MA.
9. Barth F.G. A Spider's World: Senses and Behavior 2002, Springer Verlag, Berlin.
10. Bernays E.A., Wcislo W.T. Sensory capabilities, information processing, and resource specialization. Q. Rev. Biol. 1994, 69:187-204.
11. Beutel R.G., Haas A. Larval head morphology of Hydroscapha natans LeConte 1874 (Coleoptera, Myxophaga, Hydroscaphidae) with special reference to miniaturization. Zoomorphology 1998, 18:103-116.
12. Beutel R.G., Pohl H., Hunefeld F. Strepsipteran brains and effects of miniaturization (Insecta). Arthropod Struct. Dev. 2005, 34:301-313.
13. Bonner J. Why Size Matters 2006, Princeton University Press, Princeton, NJ.
14. Brodin A. Hippocampus volume does not correlate to food hoarding rates in two closely related bird species, the black-capped chickadee Poecile atricapilla and the willow tit Parus montanus. Auk 2005, 122:819-828.
15. Brown F.A. Selected Invertebrate Types 1950, John Wiley and Sons, New York, NY.
16. Brusca R.C., Brusca G.J. Invertebrates 1990, Sinauer, Sunderland, MA.
17. Bullock T.H., Horridge G.A. Structure and Function in the Nervous Systems of Invertebrates 1965, W. H. Freeman and Co, San Francisco, CA, (Vols. I, II).
18. Burger J.M.S., Huang Y., Hemerik L., van Lenteren J.C., Vet L.E.M. Flexible use of patch-leaving decisions in a parasitoid wasp. J. Insect Behav. 2006, 19:155-170.
19. Burns J.G., Arthy Saravanan A., Rodd F.H. Rearing environment affects the brain size of guppies: lab-reared guppies have smaller brains than wild-caught guppies. Ethology 2009, 115:122-133.
20. Burns J.G., Foucaud J., Mery F. Costs of memory: lessons from 'mini' brains. Proc. R. Soc. B. 2011, 278.
21. Byrne R.W. Machiavellian intelligence. Evol. Anthropol. 1997, 5:172-180.
22. Calder W.A.I.I.I. Size, Function, and Life History 1984, Harvard University Press, Cambridge, MA.
23. Calvin W.H., Stephens C.F. Synaptic noise as a source of variability in the interval between action potentials. Science 1967, 155:842-844.
24. Calvin W.H., Stephens C.F. Synaptic noise and other sources of randomness in motoneuron interspike intervals. J. Neurophysiol. 1968, 31:574-587.
25. Campi K.L., Krubitzer L. Comparative studies of diurnal and nocturnal rodents: differences in lifestyle result in alterations in cortical field size and number. J. Comp. Neurol. 2010, 518:4491-4512.
26. Changizi M.A. Relationship between number of muscles, behavioral repertoire size, and encephalization in mammals. J. Theor. Biol. 2003, 220:157-168.
27. Chapman R.F. Chemoreception: the significance of receptor numbers. Adv. Insect Physiol. 1982, 16:247-356.
28. Chen W.Y., Aranda L.C., Luco J.V. Learning and long- and short-term memory in cockroaches. Anim. Behav. 1970, 18:725-732.
29. Cheng K., Srinivasan M.V., Zhang S.W. Error is proportional to distance measured by honeybees: Weber's law in the odometer. Anim. Cogn. 1999, 2:11-16.
30. Cherniak C. Neural component placement. Trends Neurosci. 1995, 18:522-527.
31. Cherniak C., Mokhtarzada Z., Rodriguez-Esteban R., Changzi K. Global optimization of cerebral cortex layout. Proc. Natl. Acad. Sci. USA 2004, 101:1081-1086.
32. Chittka L., Niven J. Are bigger brains better?. Curr. Biol. 2009, 19:995-1008.
33. Clark A. Where brain, body and world collide. Daedalus 1998, 127:257-280.
34. Clark B., Häusser M. Neural coding: hybrid analog and digital signalling in axons. Curr. Biol. 2006, 16:R585-R588.
35. Coddington J.A. The weavers. Discovery 1983, 4:48-53.
36. Coddington J.A. The monophyletic origin of the orb web. Spider Webs Behavior and Evolution 1986, 319-363. Stanford University Press, Palo Alto, CA. W. Shear (Ed.).
37. Coddington J.A. The genera of the spider family Theridiosomatidae. Smiths. Contrib. Zool. 1986, 422:1-96.
38. Coddington J.A. Phylogeny and classification of spiders. Spiders of North America 2005, American Arachnological Society, www.americanarachnology.org. D. Ubick, P. Paquin, P.E. Cushing, V. Roth (Eds.).
39. Coddington J.A., Hormiga G., Scharff N. Giant female or dwarf male spiders?. Nature 1997, 385:687-688.
40. Cole B.J. Size and behavior in ants: constraints on complexity. Proc. Natl. Acad. Sci. USA 1985, 82:8548-8551.
41. Collett T.S., Collett M. Memory use in insect visual navigation. Nat. Rev. Neurosci. 2002, 3:542-552.
42. Comstock J.H. The Spider Book 1967, Cornell Univ. Press/Comstock Publ. Assoc, Ithaca, NY.
43. Coyle F.A. Systematics and natural history of the mygalomorph spider genus Antrodiaetus and related genera (Araneae: Antrodiaetidae). Bull. Mus. Comp. Zool. 1971, 141:269-402.
44. Coyne J.A. Why Evolution is True 2009, Viking Press, New York, NY.
45. Douglass, J. K., Kamhi, J. F. and Wcislo, W. T. (in preparation). Insect brain allometric relationships: A comparative study providing insights into space allocation trade-offs.
46. Dusenbery D.B. Sensory Ecology 1992, W. H. Freeman & Co, New York, NY.
47. Eberhard W.G. The spider Uloborus diversus and its web 1969, (PhD. Thesis, Harvard University).
48. Eberhard W.G. The web of Uloborus diversus (Aranea: Uloboridae). J. Zool. Lond. 1972, 166:417-465.
49. Eberhard W.G. Behavioral characters for the higher classification of orb-weaving spiders. Evolution 1982, 36:1067-1095.
50. Eberhard W.G. Effects of orb-web geometry on prey interception and retention. Spider Webs Behavior and Evolution 1986, 70-100. Stanford University Press, Palo Alto, CA. W. Shear (Ed.).
51. Eberhard W.G. The effect of gravity on temporary spiral construction by the spider Leucauge mariana (Araneae: Tetragnathidae). J. Ethol. 1987, 5:29-36.
52. Eberhard W.G. Orb webs and construction behavior in Anapidae, Symphytognathidae, and Mysmenidae. J. Arachnol. 1987, 14:339-356.
53. Eberhard W.G. Behavioral flexibility in orb web construction: effects of silk supply in different glands. J. Arachnol. 1988, 16:303-320.
54. Eberhard W.G. Memory of distances and directions moved as cues during temporary spiral construction in the spider Leucauge mariana (Araneae: Araneidae). J. Ins. Behav. 1988, 1:51-66.
55. Eberhard W.G. Early stages of orb construction by Philoponella, Leucauge, and Nephila spiders (Araneae: Uloboridae and Araneidae). J. Arachnol. 1990, 18:205-2340.
56. Eberhard W.G. Imprecision in the behavior of larval fungus gnats and the origin of new behavior patterns in animals. J. Ins. Behav. 1990, 3:327-357.
57. Eberhard W.G. Niche expansion in the spider Wendilgarda galapagensis (Araneae, Theridiosomatidae) on Cocos Island. Rev. Biol. Trop. 1990, 37:163-168.
58. Eberhard W.G. Breaking the mold: behavioral imprecision and evolutionary innovation in Wendilgarda spiders (Araneae, Theridiosomatidae). Ethol. Ecol. Evol. 2000, 12:223-235.
59. Eberhard W.G. Miniaturized orb weaving spiders: behavioral precision is not limited by small size. Proc. Roy. Soc. Lond B 2007, 274:2203-2209.
60. Eberhard W.G. Recovery of spiders from the effects of parasitic wasps: implications for fine-tuned mechanisms of manipulation. Anim. Behav. 2007, 79:375-383.
61. Eberhard W.G. Are smaller animals behaviorally limited? Lack of clear constraints in miniature spiders. Anim. Behav. 2011, 81:813-823.
62. Eberhard, W. G. and Barrantes, G. (in preparation). A new behavioral test with Zosis geniculatus (Araneae, Uloboridae) supports orb web monophyly.
63. Eberhard, W. G. and Hesselberg, T. (submitted). Errors by spiders (Araneae: Araneidae, Tetragnathidae) building orbs: lapses in attention due to recent memories? Ethology.
64. Edelman G. Building a picture of the brain. Daedalus 1998, 127(2):37-70.
65. Edmunds J. The web of Paraneus cyrtoscapus (Pocock, 1899) (Araneae: Araneidae) in Ghana. Symposia of the Zoological Society of London 1978, vol 42:485. Academic Press, New York, NY. P. Merrett (Ed.).
66. Eisenberg J.G. The mammalian radiations. An analysis of Trends in Evolution, Adaptation and Behavior 1981, University of Chicago Press, Chicago, IL.
67. Eisenberg J.F., Wilson D.E. Relative brain size and feeding strategies in the Chiroptera. Evolution 1978, 32:740-751.
68. Faisal A.A., White J.A., Laughlin S.B. Ion-channel noise places limits on the miniaturization of the brain's wiring. Curr. Biol. 2005, 15:1143-1149.
69. Fankhauser G., Vernon J.A., Frank W.H., Slack W.V. Effect of size and number of brain cells on learning in larvae of the salamander, Triturus viridescens. Science 1955, 122:692-693.
70. Felsenstein J. Phylogenies and the comparative method. Am. Nat. 1985, 125:1-15.
71. Foelix R.F. Biology of Spiders 1996, Harvard University Press, Cambridge, MA. 2nd ed.
72. Franzl P., Barth F.G. Biomaterial systems for mechanosensing and actuation. Nature 2009, 462:442-448.
73. García-Arrarás J.E., Rojas-Soto M., Jiménez L.B., Díaz-Miranda L. The enteric nervous system of echinoderms: unexpected complexity revealed by neurochemical analyses. J. Exp. Biol. 2001, 204Ñ:865-873.
74. Gaston K.J., Chown S.L., Mercer R.D. The animal species-body size distribution of Marion Island. Proc. Natl. Acad. Sci. USA 2001, 98:14493-14496.
75. Goldschmidt R. Das Nervensystem von Ascaris lumbricoides und megalocephala II. Z. wiss. Zool. 1909, 92:306-357.
76. Gonzalez-Voyer A., Winberg S., Kolm N. Distinct evolutionary patterns of brain and body size during adaptive radiation. Evolution 2009, 63:2266-2274.
77. Grebennikov V.V. How small you can go: factors limiting body miniaturization in winged insects with a review of the pantropical genus Discheramocephalus and description of six new species of the smallest beetles (Pterygota: Coleoptera: Ptiliidae). Eur. J. Ent. 2008, 105:313-328.
78. Grebennikov V.V., Beutel R.G. Morphology of the minute larva of Ptinella tenella, with specific reference to effects of miniaturization and the systematic position of Ptiliidae (Coleoptera: Staphylinoidea). Arthrop. Struct. Dev. 2002, 31:157-172.
79. Gregory T.R. A bird's-eye view of the C-value enigma: genome size, cell size, and metabolic rate in the class Aves. Evolution 2002, 56:121-130.
80. Griswold C.E., Coddington J.A., Hormiga G., Scharff N. Phylogeny of the orb-building spiders (Araneae, Orbiculariae: Deinopidae, Araneoidea). Zool. J. Linn. Soc. 1998, 123:1-99.
81. Gronenberg W., Riveros A.J. Social brains and behavior-past and present. Organization of Insect Societies 2009, 377-401. Harvard University Press, Cambridge. J. Gadau, J. Fewell (Eds.).
82. Hanken J. Miniaturization and its effects on cranial morphology in plethodontid salamanders, genus Thorius (Amphibia: Plethodontidae) II. The fate of the brain and sense organs and their role in skull morpholgenesis and evolution. J. Morphol. 1983, 177:255-268.
83. Hanken J., Wake D.B. Miniaturization of body size: organismal consequences and evolutionary significance. Ann. Rev. Ecol. Syst. 1993, 24:501-519.
84. Hanson P.E., Gauld I.D. 2.5 Los parasitoides: la hembra adulta. Memoirs of the American Entomological Society 2006, 77:49-62. (1-994). P.E. Hanson, I.D. Gauld (Eds.).
85. Harvey P.H., Pagel M.D. The Comparative Method in Evolutionary Biology 1991, Oxford University Press, New York, NY.
86. Harvey P.H., Clutton-Brock T.H., Mace G.M. Brain size and ecology in small mammals and primates. Proc. Natl. Acad. Sci. USA 1980, 77:4387-4389.
87. Hasenstaub A., Otte S., Callaway E., Sejnowski T.J. Metabolic cost as a unifying principle governing neuronal biophysics. Proc. Natl. Acad. Sci. USA 2010, 107:12329-12334.
88. Head G. Selection on fecundity and variation in the degree of sexual size dimorphism among spider species (Class Araneae). Evolution 1995, 49:776-781.
89. Healy S.D., Rowe C. A critique of comparative studies of brain size. Proc. R. Soc. B 2007, 274:453-464.
90. Heisenberg M., Heusipp M., Wanke C. Structural plasticity in the Drosophila brain. J. Neurosci. 1995, 15:1951-1960.
91. Herculano-Houzel S. Coordinated scaling of cortical and cerebellar numbers of neurons. Front. Neuroanat. 2010, 4:1-8.
92. Herculano-Houzel S., Mota B., Lent R. Cellular scaling rules for rodent brains. Proc. Natl. Acad. Sci. USA 2006, 103:12138-12143.
93. Hesselberg T. Ontogenetic changes in web design in two orb-web spiders. Ethology 2010, 116:535-545.
94. Higgins R.P. The Atlantic barrier reef ecosystem at Carrie Bow Cay, Belize. II. Kinorhyncha. Smiths. Contrib. Mar. Sci. 1983, 18:1-131.
95. Hill D.E. The structure of the central nervous system of jumping spiders of the genus Phidippus (Araneae: Salticidae). M.S. thesis. Oregon State University 1975, 1-94.
96. Hingston R.W.G. A Naturalist in the Himalaya 1920, Small, Maynard and Co, Boston, MA.
97. Hochberg R. Three-dimensional reconstruction and neural map of the serotonergic brain of Asplanchna brightwellii (Rotifera, Monogononta). J. Morphol. 2009, 270:430-441.
98. Hoedjes K.M., Kruidhof H.M., Huigens M.E., Dicke M., Vet L.E.M., Smid H.M. Natural variation in learning rate and memory dynamics in parasitoid wasps: opportunities for converging ecology and neuroscience. Proc. R. Soc. B 2011, 278:889-897.
99. Homberg U. Evolution of the central complex in the arthropod brain with respect to the visual system. Arthropod Struct. Dev. 2008, 37:347-362.
100. Homberg U., Heinze S., Pfeiffer K., Kinoshita M., el Jundi B. Central neural coding of sky polarization in insects. Phil. Trans. R. Soc. Lond. B Biol. Sci. 2011, 366:680-687.
101. Hormiga G., Scharff N., Coddington J.A. The phylogenetic basis of sexual size dimorphism in orb-weaving spiders (Araneae, Orbiculariae). Syst. Biol. 2000, 49:435-462.
102. Horridge G.A. Learning of leg position by the ventral nerve cord in headless insects. Proc. R. Soc. Lond. B 1962, 157:33-52.
103. Howard C.V., Reed M.G. Unbiased Stereology: Three-dimensional Measurement in Microscopy 1998, Bios Scientific Publishers, Oxford.
104. Howse P.E. Design and function in the insect brain. Experimental Analysis of Insect Behaviour 1974, Springer, New York. L. Barton-Browne (Ed.).
105. Iwaniuk A.N., Wylie D.R.W. Neural specialization for hovering in hummingbirds: hypertrophy of the pretectal nucleus lentiformis mesencephali. J. Comp. Neurol. 2007, 500:211-221.
106. Iwaniuk A.N., Nelson J.E., Whishaw I.Q. The relationships between brain regions and forelimb dexterity in marsupials (Marsupialia): a comparative test of the principle of proper mass. Aust. J. Zoo. 2000, 48:99-110.
107. Iwata K., Sakagami S.F. Gigantism and dwarfism in bee eggs in relation to the modes of life, with notes on the number of ovarioles. Jpn. J. Ethol. 1966, 16:4-16.
108. Jander U., Jander R. Allometry and resolution of bee eyes (Apoidea). Arthropod Struct. Dev. 2002, 30:179-193.
109. Jerison H.J. Evolution of the Brain and Intelligence 1973, Academic Press, New York.
110. Jerison H.J. The evolution of the mammalian brain as an information-processing system. Advances in the Study of Mammalian Behavior 1983, The American Society of Mammalogist, New York. J.F. Eisenberg, D.G. Kleinman (Eds.).
111. Jindrich D.L., Joseph M.S., Otoshi C.K., Wei R.Y., Zhong H., Roy R.R., Tillakaratne N.J.K., Edgerton V.R. Spinal learning in the adult mouse using the Horridge paradigm. J. Neurosci. Methods 2009, 182:250-254.
112. Kaestner A. Invertebrate Zoology 1968, Interscience Publishers, New York, NY, Vol. II. (Translated and adapted by H. W. Levi and L. Levi).
113. Katz P. Beyond Neurotransmission: Neuromodulation and Its Importance for Information Processing 1999, Oxford University Press, Oxford.
114. Kaushal D., Contos J.J.A., Treunere K., Yang A.H., Kingsbury M.A., Rehen S.K., McConnell M.J., Okabe M., Barlow C., Chun J. Alteration of gene expression by chromosome loss in the postnatal mouse brain. J. Neurosci. 2003, 23:5599-5606.
115. Kelber A., Warrant E., Pfaff M., Wallén R., Theobald J.C., Wcislo W.T., Raguso R.A. Light intensity limits foraging activity in nocturnal and crepuscular bees. Behav. Ecol. 2006, 17:63-72.
116. Keshmirian J., Nogrady T. Histofluorescent labeling of catecholaminergic structures in rotifers (Aschelminthes) in whole animals. Histochemistry 1987, 87:351-357.
117. Kiltie R.A. Scaling of visual acuity with body size in mammals and birds. Funct. Ecol. 2000, 14:226-234.
118. Kingsbury M.A., Friedman B., McConnell J.J., Rehen S.K., Yang A.H., Kaushal D., Chun J. Aneuploid neurons are functionally active and integrated into brain circuitry. Proc. Natl. Acad. Sci. USA 2005, 102:6143-6147.
119. Kingsford M.J., Leis J.M., Shanks A., Lindeman K.C., Morgan S.G., Pineda J. Sensory environmental, larval abilities and local self-recruitment. Bull. Mar. Sci. 2002, 70:309-340.
120. Kollmann M., Bonhomme J., Homberg U., Schachter J., Tagu D., Anton S. Revisiting the anatomy of the central nervous system of a hemimetabolous model insect species: the pea aphid Acyrthosiphon pisum. Cell Tissue Res. 2011, 343:343-355.
121. Krink T., Vollrath F. A virtual robot to model the use of regenerated legs in a web-building spider. Anim. Behav. 1999, 57:223-232.
122. Kristensen R.M., Higgins R.P. Revision of Styraconyx (Tardigrada: Halechinischidae), with description of two species from Disko Bay, West Greenland. Smithson. Contrib. Zool. 1984, 391. (iii-40).
123. Kuntner M., Coddington J.A., Hormiga G. Phylogeny of extant nephilid orb-weaving spiders (Araneae, Nephilidae): testing morphological and ethological homologies. Cladistics 2008, 24:147-217.
124. Lacalli T.C. Serial EM analysis of a copepod larval nervous system: naupliar eye, optic circuitry, and prospects for full CNS reconstruction. Arthrop. Struct. Dev. 2009, 38:361-375.
125. Land M.F., Nilsson D.E. Animal Eyes 2002, Oxford Animal Biology Series, Oxford.
126. Lande R. Quantitative genetic analysis of multivariate evolution, applied to brain-body size allometry. Evolution 1979, 33:402-416.
127. LeGuelte L. Structure de la toile de Zygiella x-notata Cl. et facterus que regissent le comportement de l'araignee pendant la construction de la toile 1967, (PhD. Thesis, Univ. Nancy, France).
128. Lopardo L., Giribet G., Hormiga G. Morphology to the rescue: molecular data and the signal of morphological characters in combined phylogenetic analyses-a case study from mysmenid spiders (Araneae, Mysmenidae), with comments on the evolution of web architecture. Cladistics 2010, 27:278-330.
129. MacLarnon A. The scaling of gross dimensions of the spinal cord in primates and other species. J. Human Evol. 1996, 30:71-87.
130. Madrigal-Brenes, R. (in preparation). Sternal bulges in spiders of different sizes.
131. Main B.Y. Spiders 1976, Collins, London.
132. Manger P.R., Cort J., Ebrahim N., Goodman A., Henning J., Karolia M., Rodrigues S.-L., Štrkalj G. Is 21st century neuroscience too focussed on the rat/mouse model of brain function and dysfunction?. Front. Neuroanat. 2008, 2:1-7.
133. Mares S., Ash L., Gronenberg W. Brain allometry in bumblebee and honey bee workers. Brain Behav. Evol. 2005, 66:50-61.
134. Martin R.D. Relative brain size and basal metabolic-rate in terrestrial vertebrates. Nature 1981, 293:57-60.
135. Martini E. Die Anatomie der Oxyuris curvula. Z. wiss. Zool. 1916, 116:137-534.
136. Mayer G. Untersuchengen ueber Herstellung und Struktur des Radnetz von Aranea diadema und Zilla x-notata mit besonderer Beruecksichtigung des Unterschiedes von Jungend- und Altersnetzen. Z. Tierpsychol. 1952, 9:337-362.
137. Mercer A. Changing the way we perceive things: sensory systems modulation. Beyond Neurotransmission: Neuromodulation And Its Importance for Information Processing 1999, 198-240. Oxford University Press, Oxford. P. Katz (Ed.).
138. Michener C.D. Comments on minute Meliponini and the male of the genus Paratrigona (Hymenoptera: Apidae). J. Kansas Entomol. Soc. 2001, 74:231-236.
139. Miklos G.L.G. The evolution and modification of brains and sensory systems. Daedalus 1998, 127:197-216.
140. Miller G.A., Galanter E., Pribram K.H. Plans and the Structure of Behavior 1960, Henry Holt & Co., NY.
141. Misunami M., Yokohari F., Takahata M. Further exploration into the adaptive design of the arthropod "microbrain": I. Sensory and mamory-processing systems. Zool. Sci. 2004, 21:1141-1151.
142. Niven J.E. Nervous system evolution in relation to behavior. Encyclopedia of Animal Behavior, Vol. 2 2010, 527-533. Oxford Academic Press, New York, NY. M.D. Breed, J. Moore (Eds.).
143. Niven J.E., Laughlin S.B. Energy limitation as a selective pressure on the evolution of sensory systems. J. Exp. Biol. 2008, 211:1792-1804.
144. Niven J.E., Anderson J.C., Laughlin S.B. Energy-information trade-offs during signal transmission by single sensory receptors. PLoS Biol. 2007, 5:e116.
145. Niven J.E., Graham C.M., Burrows M. Diversity and evolution of the insect ventral nerve cord. Annu. Rev. Entomol. 2008, 53:253-271.
146. Nuss A.B., Forschler B.T., Crim J.W., Brown M.R. Distribution of neuropeptide F-like immunoreactivity in the eastern subterranean termite, Reticulitermes flavipes. J. Insect Sci. 2008, 8:1536-2442.
147. Osborne K.A., de Belle J.S., Sokolowski M.B. Foraging behaviour in Drosophila larvae: mushroom body ablation. Chem. Senses 2001, 26:223-230.
148. Insect Learning 1993, Chapman & Hall, NY. D.R. Papaj, A.C. Lewis (Eds.).
149. Platnick N., Shadab M. A review of the spider genus Anapis (Araneae: Anapidae) with a dual cladistic analysis. Am. Mus. Novit. 1978, 2663:1-23.
150. Platnick N.I., Shadab M. A review of the spider genera Anapisona and Pseudanapis (Araneae, Anapidae). Am. Mus. Novit. 1979, 2672:1-20.
151. Polilov A.A. Anatomy of the feather-winged beetles Acrotrichis montandoni and Ptilium myrmecophilum (Coleoptera, Ptiliidae). Zool. Zh. 2005, 84:181-189. (in Russian).
152. Polilov A.A. Anatomy of the smallest Coleoptera, featherwing beetles of the tribe Nanosellini (Coleoptera, Ptiliidae), and limits of insect miniaturization. Entomol. Rev. 2008, 88:26-33.
153. Polilov A.A., Beutel R.G. Developmental stages of the hooded beetle Sericoderus lateralis (Coleoptera: Corylophidae) with comments on the phylogenetic position and effects of miniaturization. Arth. Struct. Dev. 2010, 39:52-69.
154. Polivov A.A., Beutel R.G. Miniaturization effects in larvae and adults of Mikado sp. (Coleoptera: Ptiliidae), one of the smallest free-living insects. Arthrop. Struct. Dev. 2009, 38:247-270.
155. Quesada, R., Triana, E., Vargas, G., Seid, M., Douglass, J., Eberhard, W. G. and Wcislo, W. (in press). Large brains in small spiders: the central nervous system extends into the legs of miniature spiders. Arthr. Struct. Develop. doi:10.1016/j.asd.2011.07.002.
156. Reed C.F., Witt P.N., Jones R.L. The measuring function of the first legs of Araneus diadematus Cl. Behaviour 1965, 25:98-118.
157. Reed C.F., Witt P.N., Scarboro M.B. The orb web during the life of Argiope aurantia (Lucas). Dev. Psychobiol. 1969, 2:120-129.
158. Reed C.F., Witt P.N., Scarboro M.B., Peakall D.B. Experience and the orb web. Dev. Psychobiol. 1970, 3:251-265.
159. Rehen S.K., McConnell J.J., Kaushal D., Kingsbury M.A., Yang A.H., Chun J. Chromosomal variation in neurons of the developing and adult mammalian nervous system. Proc. Natl. Acad. Sci. USA 2001, 98:13361-13366.
160. Rensch B. Histological change with evolutionary changes of body size. Evolution 1948, 2:218-230.
161. Rensch B. Evolution above the Species Level 1960, Columbia University Press, New York, NY.
162. Riska B., Atchley W. Genetics of growth predict patterns of brain-size evolution. Science 1985, 229:668-671.
163. Riveros, A. J., Seid, M. and Wcislo, W. T. (submitted). Evolution of brain size in class-based societies of fungus-growing ants. Animal Behaviour.
164. Roth L.M., Willis E.R. The reproduction of cockroaches. Smithsonian Misc. Coll. 1958, 122:1-49.
165. Roth G., Rottluff B., Linke R. Miniaturization, genome size and the origin of functional constraints in the visual system of salamanders. Naturwissenschaften 1988, 75:297-304.
166. Roth G., Rottluff B., Grunwald W., Hanken J., Linke R. Miniaturization in plethodontid salamanders (Caudata: Plethodontidae) and its consequences for the brain and visual system. Biol. J. Linn. Soc. 1990, 40:165-190.
167. Roth G., Blanke J., Wake D.B. Cell size predicts morphological complexity in the brains of frogs and salamanders. Proc. Natl. Acad. Sci. USA 1994, 91:4796-4800.
168. Rutowski R.L. Variation of eye size in butterflies: inter- and intraspecific patterns. J. Zool. Lond 2000, 252:187-195.
169. Sandoval C.P. Plasticity in web design in the spider Parawixia bistriata: a response to variable prey type. Funct. Ecol. 1994, 8:701-707.
170. Sarko D.K., Catania K.C., Leitch D.B., Kaas J.H., Herculano-Houzel S. Cellular scaling rules of insectivore brains. Frontiers in Neuroanatomy 2009, 3:1-12.
171. Sarpeshkar R. Analog versus digital: Extrapolating from electronics to neurobiology. Neural Computation 1998, 10:1601e1638.
172. Scharff N., Coddington J.A. A phylogenetic analysis of the orb-weaving spider family Araneidae (Arachnida, Araneae). Zool. J. Linn. Soc. 1997, 120:355-434.
173. Schoenemann P.T. Brain size, scaling and body composition in mammals. Brain Behav. Evol. 2004, 63:47-60.
174. Seeley T.D. Honey Bee Ecology 1985, Princeton University Press, Princeton.
175. Seeley T.D. Honey Bee Democracy 2010, Princeton University Press, Princeton.
176. Seid M.A., Castillo A., Wcislo W.T. The allometry of brain miniaturization in ants. Brain Behav. Evol. 2011, 77:5-13.
177. Sherry D.F., Forbes M.R.L., Khurgel M., Ivy G.O. Females have a larger hippocampus than males in the brood-parasitic brown-headed cowbird. Proc. Natl. Acad. Sci. USA 1993, 90:7839-7843.
178. Shettleworth S. Cognition, Evolution, and Behavior 2010, Oxford University Press, New York, NY. 2nd ed.
179. Smith D., Wessnitzer J., Webb B. A model of association learning in the mushroom body. Biol. Cybern. 2008, 99:89-103.
180. Spaethe J., Chittka L. Interindividual variation of eye optics and single object resolution in bumblebees. J. Expt. Biol. 2003, 206:3447-3453.
181. Stachowitsch M. The Invertebrates 1992, Wiley-Liss, New York, NY.
182. Stevens S.S. Psychophysics 1975, John Wiley & Sons, New York, NY.
183. Stewart P. Jacobellis v. Ohio 1964, (U.S. Supreme Court 378 U.S. 184).
184. Strathmann R.R. Larval feeding in echinoderms. Am. Zool. 1975, 15:717-730.
185. Strausfeld N. Atlas of an Insect Brain 1976, Springer, Berlin.
186. Striedter G.F. The Principles of Brain Evolution 2005, Sinaur Assoc. Inc., Sunderland, MA.
187. Tinbergen N. The Study of Instinct 1951, Oxford University Press, Oxford.
188. Tononi G., Sporns O., Edelman G.M. A measure for brain complexity: relating functional segregation and integration in the nervous system. Proc. Natl. Acad. Sci. USA 1994, 91:5033-5037.
189. Van Essen D.C., Gallant J. Neural mechanisms of form and motion processing in the primate visual system. Neuron 1994, 13:1-10.
190. van Wijk M., Wadman W.J., Sabelis M.W. Gross morphology of the central nervous system of a phytoseiid mite. Expt. Appl. Acarol. 2006, 40:205-216.
191. Vollrath F. Spiders with regenerated legs can build normal webs. Nature (London) 1987, 328:247-248.
192. Vollrath F. Analysis and interpretation of orb spider exploration and web-building behavior. Adv. Stud. Behav. 1992, 21:147-199.
193. von Frisch K. The Dance Language and Orientation of Bees 1967, Harvard University Press, Cambridge.
194. Vos M., Hemerik L., Vet L.E.M. Patch exploitation by the parasitoids Cotesia rubecula and Cotesia glomerulata in multi-patch environments with different host distributions. J. Anim. Ecol. 1998, 67:774-783.
195. Walter D.E., Proctor H.C. Mites, Ecology, Evolution and Behavior 1999, CABI Publishing, New York, NY.
196. Warrant E.J. Seeing in the dark: vision and visual behaviour in nocturnal bees and wasps. J. Exp. Biol. 2008, 211:1737-1746.
197. Warrant E.J., Kelber A., Gislén A., Greiner B., Ribi W., Wcislo W.T. Nocturnal vision and landmark orientation in a tropical halictid bee. Curr. Biol. 2004, 14:1309-1318.
198. Watts D.J., Strogatz S.H. Collective dynamics of 'small world' networks. Nature 1998, 393:440-442.
199. Wcislo W.T. Sensilla numbers and antennal morphology of bees (Hymenoptera: Apoidea), in relation to behavior and taxonomy. Int. J. Insect. Morphol. Embryol. 1995, 24:63-81.
200. Wcislo W.T., Tierney S. Behavioral environments and niche construction: the evolution of dim-light foraging in bees. Biol. Rev. Cambr. Phil. Soc. 2009, 84:19-37.
201. Wehner R. 'Matched filters' - neural models of the external world. J. Comp. Physiol. A 1987, 161:511-531.
202. Wehner R., Fukushi T., Isler K. On being small: brain allometry in ants. Brain Behav. Evol. 2007, 69:220-228.
203. Wheeler W.C., Hayashi C.Y. The phylogeny of the extant chelicerate orders. Cladistics 1998, 14:173-192.
204. White J.G., Southgate E., Thomson J.N., Brenner S. The structure of the ventral nerve cord of Caenorhabditis elegans. Philos. Trans. R. Soc. Lond. B 1975, 275:327-348.
205. Wille A. Evolutionary trends in the ventral nerve cord of the stingless bees (Meliponini). Rev. Biol. Trop. 1961, 9:117-129.
206. Wilson E.O. The relation between caste ratios and division of labor in the ant genus Pheidole (Hymenoptera: Formicidae). Behav. Ecol. Sociobiol. 1984, 16:89-98.
207. Windhoffer R., Westheide W. The nervous system of the male Dinophilus gyrociliatus (Annelida: Polychaeta). I. Number, types and distribution pattern of sensory cells. Acta Zool. (Stockholm) 1988, 69:55-64.
208. Witt P.N. Do we live in the best of all possible worlds? Spider webs suggest an answer. Perspect. Biol. Med. 1965, 8:475-487.
209. Witt P.N., Reed C.F., Peakall D.B. A Spider's Web 1968, Problems in Regulatory Biology, Springer-Verlag, New York.
210. Wittenberg G.M., Wang S.S.H. Evolution and scaling of dendrites. Dendrites 2007, 43-67. Oxford University Press, New York, NY. 2nd ed. M. Häusser, N. Spruston, G. Stuart (Eds.).
211. Yurov Y.B., Iourov I.Y., Monakhov V.V., Soloviev I.V., Vostrikov V.M., Vorsanova S.G. The variation of aneuploidy frequency in the developing and adult human brain revealed by an interphase FISH study. J. Histochem. Cytochem. 2005, 53:385-390.