Mapping behavioural evolution onto brain evolution: The strategic roles of conserved organization in individuals and species

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 366, Issue 1574, 2011, Pages 2111-2123

  Finlay, Barbara L ^a   Hinz, Flora ^a,b   Darlington, Richard B ^a  

^a Department of Obstetrics Gynecology   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Allometry; Brain evolution; Domestication; Individual variation; Neocortex

Indexed keywords

ALLOMETRY; BEHAVIORAL ECOLOGY; BRAIN; COMPUTER SIMULATION; CONSERVATION GENETICS; HOMEOSTASIS; LIFE HISTORY; MAMMAL; NERVOUS SYSTEM; SENSORY SYSTEM; SPECIES CONSERVATION;

ANIMAL; ANIMAL BEHAVIOR; BRAIN; EVOLUTION; HISTOLOGY; PHYSIOLOGY; REVIEW;

ANIMALS; BEHAVIOR, ANIMAL; BIOLOGICAL EVOLUTION; BRAIN;

MUS; MUSTELA; SUIDAE;

EID: 79959438728     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2010.0344     Document Type: Review

References (103)

1. Dukas, R. 2004 Evolutionary biology of animal cognition. Annu. Rev. Ecol. Evol. Syst. 35, 347-374. doi:10.1146/annurev.ecolsys.35.112202.130152
2. Jerison, H. J. 1973 Evolution of the brain and intelligence. New York, NY: Academic Press.
3. Stephan, H., Baron, G. & Frahm, H. D. 1988 Comparative size of brain and brain components. In Comparative primate biology, pp. 1-38. New York, NY: Alan R. Liss.
4. Dunbar, R. I. M. 1993 Coevolution of neocortical size, group size and language in humans. Behav. Brain Sci. 16, 681-694. doi:10.1017/S0140525X00032325
5. Barton, R. A. & Harvey, P. H. 2000 Mosaic evolution of brain structure in mammals. Nature 405, 1055-1058. doi:10.1038/35016580
6. Striedter, G. 2005 Principles of brain evolution. New York, NY: Sinauer.
7. Jacobs, G. H. 1993 The distribution and nature of colour vision among the mammals. Biol. Rev. 68, 413-471.
8. Jacobs, G. H. 2008 Primate color vision: a comparative perspective. Vis. Neurosci. 25, 619-633. doi:10.1017/ S0952523808080760
9. Hunt, D.M., Carvalho, L. S., Cowing, J. A. & Davies,W. L. 2009 Evolution and spectral tuning of visual pigments in birds and mammals. Phil. Trans. R. Soc. B 364, 2941-2955. (doi:10.1098/rstb.2009.0044)
10. Fernald, R. D. 1997 The evolution of eyes. Brain Behav. Evol. 50, 253-259. doi:10.1159/000113339
11. Changizi, M. A., Zhang, Q. & Shimojo, S. 2006 Bare skin, blood and the evolution of primate colour vision. Biol. Lett. 2, 217-221. doi:10.1098/rsbl.2006.0440
12. Persons, M. H., Fleishman, L. J., Frye, M. A. & Stimphil, M. E. 1999 Sensory response patterns and the evolution of visual signal design in anoline lizards. J. Comp. Physiol. A 184, 585-607. doi:10.1007/s003590050358
13. Osorio, D. & Vorobyev, M. 2008 A review of the evolution of animal colour vision and visual communication signals. Vis. Res. 48, 2042-2051. doi:10.1016/j.visres.2008.06.018
14. Mollon, J. D. 1989 'Tho she kneeled at the place theym grew.' The uses and origins of primate color vision. In Principles of sensory coding and processing (ed. S. B. Laughlin), pp. 21-38. Cambridge, UK: The Company of Biologists, Ltd.
15. Dominy, N. J. & Lucas, P. W. 2001 Ecological importancem of trichromatic vision to primates. Nature 410, 363-366. doi:10.1038/35066567
16. Kingdom, F. A. A. 2003 Color brings relief to human vision. Nat. Neurosci. 6, 641-644. doi:10.1038/nn1060)
17. Hansen, T. & Gegenfurtner, K. R. 2009 Independence of color and luminance edges in natural scenes. Vis. Neurosci. 26, 35-49. doi:10.1017/S0952523808080796
18. Caine, N. G. & Mundy, N. I. 2000 Demonstration of a foraging advantage for trichromatic marmosets (Callithrix geoffroyi) dependent on food colour. Proc. R. Soc. Lond. B 267, 439-444. doi:10.1098/rspb.2000.1019
19. Jacobs, G. H., Williams, G. A., Cahill, H. & Nathans, J. 2007 Emergence of novel color vision in mice engineered to express a human cone photopigment. Science 315, 1723-1725. doi:10.1126/science.1138838
20. Mancuso, K., Hauswirth, W. W., Li, Q., Connor, T. B., Kuchenbecker, J. A., Mauck, M. C., Neitz, J. & Neitz, M. 2009 Gene therapy for red-green colour blindness in adult primates. Nature 461, 784-787. doi:10.1038/nature08401
21. Gerhart, J. & Kirschner, M. 1997 Cells, embryos and evolution. Malden, MA: Blackwell Science.
22. Jablonka, E. & Lamb, M. 2005 Evolution in four dimensions. Cambridge, MA: MIT Press.
23. Kirschner, M. W. & Gerhart, J. C. 2005 The plausibility of life: resolving Darwin's dilemma. New Haven, CT: YaleUniversity Press.
24. Wagner, A. D. 2005 Robustness and evolvability in living systems. Princeton, NJ: Princeton University Press.
25. Westoby, N., Falster, D. S., Moles, A. T., Vesk, P. A. & Wright, I. J. 2002 Plant ecological strategies: some leading dimensions of variation between species. Annu. Rev. Ecol. Evol. Syst. 33, 125-129. doi:10.1146/annurev.ecolsys.33.010802.150452)
26. Shapiro, M. D., Marks, M. E., Peichel, C. L., Blackman, B. K., Nereng, K. S., Junsson, B., Schluter, D. & Kingsley, D. M. 2004 Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 428, 717-723. doi:10.1038/nature02415
27. Schluter, D. 1984 Morphological and phylogenetic relations among the Darwin's finches. Evolution 38, 921-930. doi:10.2307/2408428
28. Schluter, D. 1996 Adaptive radiation along the lines of least resistance. Evolution 50, 1766-1774. doi:10.2307/2410734
29. Mundy, N. I., Badcock, N. S., Hart, T., Scribner, K., Janssen, K. & Nadeau, N. J. 2004 Conserved genetic basis of a quantitative plumage trait involved in mate choice. Science 303, 1870-1873. doi:10.1126/science.1093834)
30. Allender, C. J., Seehausen, O., Knight, M. E. & Turner, G. F. 2003 Divergent selection during speciation of Lake Malawi cichlids inferred from parallel radiations in nuptial coloration. Proc. Natl Acad. Sci. USA 24, 14074-14079.
31. Steiner, C. C., Rompler, H., Boettger, L. M., Schoneberg, T. & Hoekstra, H. E. 2009 The genetic basis of phenotypic convergence in beach mice: similar pigment patterns but different genes. Mol. Biol. Evol. 26, 35-45. doi:10.1093/molbev/msn218)
32. Lefebvre, L., Reader, S. M. & Sol, D. 2004 Brains, innovations and evolution in birds and primates. Brain Behav. Evol. 63, 233-246. doi:10.1159/000076784)
33. tramo, M. J., Loftus, W. C., Stukel, T. A., Green, R. L., Weaver, J. B. & Gazzaniga, M. S. 1998 Brain size, head size, and intelligence quotient in monozygotic twins. Neurology 50, 1246-1252.
34. Shaw, P., Greenstein, D., Lerch, J., Clasen, L., Lenroot, R., Gogtay, N., Evans, A., Rapoport, J. & Giedd, J. 2006 Intellectual ability and cortical development in children and adolescents. Nature 440, 676-679. doi:10.1038/nature04513
35. Reep, R., Darlington, R. B. & Finlay, B. L. 2007 The limbic system in mammalian brain evolution. Brain Behav. Evol. 70, 57-70. doi:10.1159/000101491
36. Finlay, B. L. & Darlington, R. B. 1995 Linked regularities in the development and evolution of mammalian brains. Science 268, 1578-1584. doi:10.1126/science.7777856
37. Finlay, B. L., Darlington, R. B. & Nicastro, N. 2001 Developmental structure in brain evolution. Behav. Brain Sci. 24, 263-307.
38. Finlay, B. L., Hersman, M. N. & Darlington, R. B. 1998 Patterns of vertebrate neurogenesis and the paths of vertebrate evolution. Brain Behav. Evol. 52, 232-242. doi:10.1159/000006566
39. Finlay, B. L., Silveira, L. C. L. & Reichenbach, A. 2005 Comparative aspects of visual system development. In The structure, function and evolution of the primate visual system (ed. J. Kremers), pp. 37-72. New York, NY: John Wiley and Sons.
40. Dyer, M. A., Martins, R., da Silva Filho, M., Muniz, J. A., Silveira, L. C. L., Cepko, C. & Finlay, B. L. 2009 Developmental sources of conservation and variation in the evolution of the primate eye. Proc. Natl Acad. Sci. USA 106, 8963-8968. doi:10.1073/pnas.0901484106
41. Williams, R. W., Strom, R. C. & Goldowitz, D. 1998 Natural variation in neuron number in mice is linked to a major quantitative trait locus on Chr 11.J. Neurosci. 18, 138-146.
42. Airey, D. C., Lu, L. & Williams, R. W. 2001 Geneticcontrol of the mouse cerebellum: identification of quantitative trait loci modulating size and architecture. J. Neurosci. 21, 5099-5109.
43. Lu, L., Airey, D. C. & Williams, R. W. 2001 Complex trait analysis of the hippocampus: mapping and biometric analysis of two novel gene loci with specific effects on hippocampal structure in mice. J. Neurosci. 21, 3503-3514.
44. Badea, A., Johnson, G. A. & Williams, R. W. 2009 Genetic dissection of the mouse brain using highfieldmagnetic resonance microscopy. NeuroImage 45,1067-1079. doi:10.1016/j.neuroimage.2009.01.021
45. Gleeson, J. G. et al. 1998 Doublecortin, a brain-specificgene mutated in human X-linked lissencephaly and double cortex syndrome, encodes a putative signaling protein. Cell 92, 63-72. doi:10.1016/S0092-8674(00)80899-5
46. Kingsbury, M. A., Rehen, S. K., Contos, J. J. A., Higgins, C. M. & Chun, J. 2003 Non-proliferative effects of lysophosphatidic acid enhance cortical growth and folding. Nat. Neurosci. 6, 1292-1299. doi:10.1038/nn1157
47. Evans, P. D., Gilbert, S. L., Mekel-Bobrov, N., Vallender, E. J., Anderson, J. R., Vaez-Azizi, L. M., Tishkoff, S. A., Hudson, R. R. & Lahn, B. T. 2005 Microcephalin, gene regulating brain size, continues to evolve adaptively in humans. Science 309, 1717-1720. doi:10.1126/science.1113722
48. Hill, R. S. & Walsh, C. A. 2005 Molecular insights into human brain evolution. Nature 437, 64-67. doi:10.1038/nature04103
49. Vallender, E. J. 2008 Exploring the origins of the human brain through molecular evolution. Brain Behav. Evol. 72, 168-177. doi:10.1159/000151476
50. Gould, S. J. 1975 Allometry in primates, with emphasis on scaling and the evolution of the brain. In Approaches to primate paleobiology (ed. F. S. Szalay), pp. 244-292. Basel, Switzerland: Karger.
51. Yopak, K. E., Lisney, T. J., Darlington, R. B., Collin, S. P., Montgomery, J. C. & Finlay, B. L. 2010 A conserved pattern of brain scaling from sharks to primates. Proc.Natl Acad. Sci. USA 107, 12 946-12 951. doi:10.1073/pnas.1002195107
52. Duchaine, B., Cosmides, L. & Tooby, J. 2001 Evolutionarypsychology and the brain. Curr. Opin. Neurobiol. 11, 225-230. doi:10.1016/S0959-4388(00)00201-4
53. Op de Beeck, H. P. & Baker, C. I. 2010 The neural basis of visual object learning. Trends Cogn. Sci. 14, 22-30. doi:10.1016/j.tics.2009.11.002
54. Kaskan, P., Franco, C., Yamada, E., Silveira, L. C. L., Darlington, R. & Finlay, B. L. 2005 Peripheral variability and central constancy in mammalian visual system evolution. Proc. R. Soc B 272, 91-100. doi:10.1098/rspb.2004.2925
55. Perez-Barberia, F. J., Shultz, S., Dunbar, R. I. M. & Janis, C. 2009 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
56. Jacobs, L. F. & Spencer, W. D. 1994 Natural space-usepatterns and hippocampal size in kangaroo rats. Brain Behav. Evol. 44, 125-132. (doi:10.1159/000113584)
57. Clayton, N. S. 1995 Development of memory and thehippocampus: comparison of food-storing and nonstoring birds on a one-trial associative memory task. J. Neurosci. 15, 2796-2807.
58. Sherry, D. F. & Hoshooley, J. S. 2010 Seasonal hippocampal plasticity in food-storing birds. Phil. Trans. R. Soc. B 365, 933-943. doi:10.1098/rstb.2009.0220
59. Stephan, H. & Manolescu, J. 1980 Comparative investigations on hippocampus in insectivores and primate. Z mikrosk-anat Forsch. 94, 1025-1050.
60. Fox, J. H. & Wilczynski, W. 1986 Allometry of major CNS divisions: towards a reevaluation of somatic brain-body scaling. Brain Behav. Evol. 28, 157-169. doi:10.1159/000118700
61. Kruska, D. 1970 Vergleichend cytoarchitektonische Untersuchungen an Gehirnen von Wild- und Hausschweinen. Z. Anat. Entwickl. Gesch. 131, 291-324. doi:10.1007/BF00519973
62. Kruska, D. 1996 The effect of domestication on brain size and composition in the mink (Mustela vison).J. Zool. 239, 645-661. doi:10.1111/j.1469-7998.1996.tb05468.x
63. Kruska, D. 1980 Domestikations bedingte Hirngrosse nanderungen bei Saugetieren. J. Zool. Syst. Evol. Res. 18, 161-195. doi:10.1111/j.1439-0469.1980.tb00738.x
64. Kruska, D. 1988 Mammalian domestication and its effect on brain structure and behavior. In Intelligence and evolutionary biology (eds H. J. Jerison & I. Jerison). Berlin, Germany: Springer.
65. Kruska, D. C. 2005 On the evolutionary significance of encephalization in some eutherian mammals: effects of adaptive radiation, domestication, and feralization. Brain Behav. Evol. 65, 73-108. doi:10.1159/000082979)
66. Williams, R. W. 2007 Mouse brain library. See http://www.mbl.org/.
67. Koide, T., Moriwaki, K., Ikeda, K., Niki, H. & Shiroishi, T. 2000 Multi-phenotype behavioural characterization of inbred strains derived from wild stocks of Mus musculus. Mamm. Genome 11, 664-670. doi:10.1007/s003350010129
68. Santos, J., Cole, Y. & Pellicer, A. 1993 Phylogenetic relationships among lab and wild-origin Mus musculus strains on the basis of genomic DNA RFLPs. Mamm. Genome 4, 485-492. doi:10.1007/BF00364782
69. Sebastiani, G., Olien, L., Gauthier, S., Skamene, E., Morgan, K., Gros, P. & Malo, D. 1998 Mapping of genetic modulators of natural resistance to infection with Salmonella typhimurium in wild-derived mice. Genomics 47, 180-186. doi:10.1006/geno.1997.5116
70. Maeda, Y. Y., Takahama, S., Kohara, Y. & Yonekawa, H. 1996 Two genes controlling acute phase responses by the antitumor polysaccharide, lentinan. Immunogenetics 43, 215-219. doi:10.1007/s002510050048
71. Rosenberg, D. W. 1995 Non/homogeneous marking of distal colonic mucosa using Dolichos biflorus lectin. Cancer Lett. 98, 33-37. doi:10.1016/S0304-3835(06)80007-8
72. Downes, J. E., Schwann, P. G. & Holmes, R. S. 1994 Differential corneal sensitivity to ultraviolet light among inbred strains of mice: correlation of ultraviolet B sensitivity with aldehyde dehydrogenase deficiency. Cornea 13, 67-72.
73. Kobayashi, M., Lo, F., Kawai, T., Kumazawa, M., Ikegami, H., Nishimura, M., Ohno, T. & Horio, F. 2006 Major quantitative trait locus on chromosome 2 for glucose tolerance in diabetic SMXA-5 mouse established from non-diabetic SM/J and A/J strains. Diabetologia 49, 431-433. doi:10.1007/s00125-005-0121-3
74. Rottier, R. J., Bonten, E. & d'Azzo, A. 1998 A point mutation in the neu-1 locus causes the neuraminidase defect in the SM/J mouse. Hum. Mol. Genet. 7, 313-321. doi:10.1093/hmg/7.2.313
75. Clark, E. A., Engel, D. & Windsor, N. T. 1981 Immune responsiveness of SM/J mice: hyper NK cell activity mediated by NK 1{thorn} Qa 52 cells. J. Immunol. 127, 2391-2395.
76. Nandakumar, K. S. & Holmdahl, R. 2005 A geneticcontamination in the MHC-congenic mouse strains reveals a locus on the chromosome 10 that determines autoimmunity and arthritis susceptibility. Eur. J. Immunol. 35, 1275-1282. doi:10.1002/eji.200425925
77. Hiernaux, J. R., Goidl, E. A., McEvoy, S. J., Stashak, P. W., Baker, P. J. & Holmes, K. L.1989 Characterization of the immunodeficiency of RIIIS/J mice.I.Association with the CD5 (LY-1) B cell lineage. J. Immunol. 142, 1813-1817.
78. Kess, D. et al. 2006 Identification of susceptibility loci for skin disease in a murine psoriasis model. J. Immunol. 177, 4612-4619.
79. Williams, R., Airey, D., Kulkarni, A., Zhou, G. & Lu, L. 2001 Genetic dissection of the olfactory bulbs of mice: QTLs on four chromosomes modulate bulb size. Behav. Genet. 31, 61-77. doi:10.1023/A:1010209925783
80. Barton, R. A. 1998 Visual specialization and brain evolution in primates. Proc. R. Soc. Lond. B 265, 1933-1937. doi:10.1098/rspb.1998.0523
81. Barton, R. A., Aggleton, J. P. & Grenyer, R. 2003 Evolutionary oherence of the mammalian amygdala. Proc. R. Soc. Lond. B 270, 539-543. doi:10.1098/rspb.2002.2276
82. Brodin, A. 2010 The history of scatter hoarding studies. Phil. Trans. R. Soc. B 365, 869-881. doi:10.1098/rstb.2009.0217
83. Roth, T. C., Brodin, A., Smulders, T. V., LaDage, L.D. & Pravosudov, V. V. 2010 Is bigger always better?A critical appraisal of the use of volumetric analysis in the study of the hippocampus. Phil. Trans. R. Soc. B 365, 915-931. doi:10.1098/rstb.2009.0208
84. Brooks, R. 1986 A robust layered control system for a mobile robot. IEEE J. Robot. Autom. 2, 14-23. doi:10.1109/JRA.1986.1087032
85. Hawes, N., Sloman, A., Wyatt, J., Zillich, M., Jacobsson, A., Kruijff, G., Brenner, M., Berginc, G. & Skočaj, D. 2007 Towards an integrated robot with multiple cognitive functions. Proc. Assoc. Adv. Artifical Intell. 7, 1-6.
86. Finlay, B. L. & Brodsky, P. B. 2006 Cortical evolution as the expression of a program for disproportionate growth and the proliferation of areas. In Evolution of nervous systems (eds J. H. Kaas & L. A. Krubitzer), pp. 73-96. Oxford, UK: Academic Press.
87. Suga, N., Kuzirai, K. & O'Neill, W. E. 1981 How biosonar information is represented in the bat cerebral cortex. In Neuronal mechanisms of hearing (eds J. Syka & L. Aitken). New York, NY: Plenum Press.
88. Van der Loos, H. & Welker, E. 1985 Development and plasticity of somatosensory brain maps. In Development, organization, and processing in somatosensory pathways; neurology and neurobiology (eds M. Rowe Jr, & W. D. Willis Jr), pp. 53-67. New York, NY: Alan R. Liss.
89. Silveira, L. C. L., Pincanco-Diniz, C. W., Sampaio, L. F. S. & Oswaldo-Cruz, E. 1989 Retinal ganglion cell distribution in the Cebus monkey: a comparison with the cortical magnification factors. Vis. Res. 29, 1471-1483. doi:10.1016/0042-6989(89)90131-4
90. Catania, K. C. 2002 Barrels, stripes and fingerprints in the brain: implications for theories of cortical organization. J. Neurocytol. 31, 347-358. doi:10.1023/A:1024186329012
91. Burton, H. 2003 Visual cortex activity in early and late blind people. J. Neurosci. 23, 4005-4011.
92. Insel, T. R. & Young, L. J. 2000 Neuropeptides and the evolution of social behavior. Curr. Opin. Neurobiol. 10, 784-789. doi:10.1016/S0959-4388(00)00146-X
93. 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
94. Kingsbury, M. A. & Finlay, B. L. 2001 The cortex in multidimensional space: where do cortical areas come from? Dev. Sci. 4, 125-156. doi:10.1111/1467-7687.00158
95. Sadato, N., Pascualleone, A., Grafman, J., Ibanez, V., Deiber, M. P., Dold, G. & Hallett, M. 1996 Activation of the primary visual cortex by Braille reading in blind subjects. Nature 380, 526-528. doi:10.1038/380526a0
96. Bavalier, D., Tomann, A., Hutton, C., Mitchel, T., Corina, D., Liu, G. & Neville, H. 2000 Visual attention in the periphery is enhanced in congenitally deaf individuals. J. Neurosci. 20, 85-93.
97. Pallas, S. L. 2001 Cross-modal plasticity as a tool for understanding the ontogeny and phylogeny of cerebral cortex. Trends Neurosci. 24, 417-423. doi:10.1016/S0166-2236(00)01853-1
98. Gilbert, C. D., Das, A., Ito, M., Kapadia, M. & Westheimer, G. 1996 Spatial integration and cortical dynamics. Proc. Natl Acad. Sci. USA 93, 615-622. doi:10.1073/pnas.93.2.615
99. Duncan, J. & Owen, A. M. 2000 Common regions of the human frontal lobe recruited by diverse cognitive demands. Trends Neurosci. 23, 475-481. doi:10.1016/S0166-2236(00)01633-7
100. Anderson, M. L. 2010 Neural reuse as a fundamental organizational principal of the brain. Behav. Brain Sci. 33, 245-266. doi:10.1017/S0140525X10000853
101. Passingham, R. E. 1985 Rates of brain development in mammals including man. Brain Behav. Evol. 26, 167-175. doi:10.1159/000118773
102. Finlay, B. L., Franco, E. C., Yamada, E. S., Crowley, J. C., Parsons, M., Muniz, J. A. & Silveira, L. C. 2008 Number and topography of cones, rods and optic nerve axons in New and Old World primates. Vis. Neurosci. 25, 289-299. doi:10.1017/S0952523808080371
103. Finlay, B. L. 2008 The developing and evolving retina: using time to organize form. Brain Res. 1192, 5-16. doi:10.1016/j.brainres.2007.07.005