Genetic links between brain development and brain evolution

Nature Reviews Genetics

Volumn 6, Issue 7, 2005, Pages 581-590

  Gilbert, Sandra L ^a   Dobyns, William B ^a   Lahn, Bruce T ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DEVELOPMENT; BRAIN SIZE; COGNITION; EVOLUTION; GENE FUNCTION; GENETIC ANALYSIS; GENETIC LINKAGE; HUMAN; MICROCEPHALY; NATURAL SELECTION; PRIORITY JOURNAL; REVIEW;

ANIMALS; BRAIN; EVOLUTION, MOLECULAR; HUMANS; MICROCEPHALY; NERVE TISSUE PROTEINS; PHYLOGENY;

HOMO SAPIENS;

EID: 21344471479     PISSN: 14710056     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrg1634     Document Type: Review

References (118)

1. Jerison, J. H. Evolution of the Brain and Intelligence (Academic Press, New York, 1973).
2. Spuhler, J. N. The Evolution of Man's Capacity for Culture (Wayne State Univ. Press, Detroit, 1959).
3. Olson, M. V. & Varki, A. Sequencing the chimpanzee genome: insights into human evolution and disease. Nature Rev. Genet. 4, 20-28 (2003).
4. Carroll, S. B. Genetics and the making of Homo sapiens. Nature 422, 849-857 (2003).
5. Noback, C. R. & Montagna, W. The Primate Brain (Meredith Corporation, New York, 1970).
6. Armstrong, E. & Falk, D. Primate Brain Evolution: Methods and Concepts (Plenum, New York, 1982).
7. Matsuzawa, T. Primate Origins of Human Cognition and Behavior (Springer, Tokyo, 2001).
8. Jacobs, G. H., Neitz, M., Deegan, J. F. & Neitz, J. Trichromatic colour vision in New World monkeys. Nature 382, 156-158 (1995).
9. Enard, W. et al. Molecular evolution of FOXP2, a gene involved in speech and language. Nature 418, 869-872 (2002).
10. Choi, S. S. & Lahn, B. T. Adaptive evolution of MRG, a neuron-specific gene family implicated in nociception. Genome Res. 13, 2252-2259 (2003).
11. Shi, P., Zhang, J., Yang, H. & Zhang, Y. P. Adaptive diversification of bitter taste receptor genes in mammalian evolution. Mol. Biol. Evol. 20, 805-814 (2003).
12. Mundy, N. I. & Cook, S. Positive selection during the diversification of class I vomeronasal receptor-like (V1RL) genes, putative pheromone receptor genes, in human and primate evolution. Mol. Biol. Evol. 20, 1805-1810 (2003).
13. Zhang, J. Evolution of the human ASPM gene, a major determinant of brain size. Genetics 165, 2063-2070 (2003).
14. Evans, P. D. et al. Adaptive evolution of ASPM, a major determinant of cerebral cortical size in humans. Hum. Mol. Genet. 13, 489-494 (2004).
15. Kouprina, N. et al. Accelerated evolution of the ASPM gene controlling brain size begins prior to human brain expansion. PLoS Biol. 2, e126 (2004).
16. Wang, Y. Q. & Su, B. Molecular evolution of microcephalin, a gene determining human brain size. Hum. Mol. Genet. 13, 1131-1137 (2004).
17. Evans, P. D., Anderson, J. R., Vallender, E. J., Choi, S. S. & Lahn, B. T. Reconstructing the evolutionary history of microcephalin, a gene controlling human brain size. Hum. Mol. Genet. 13, 1139-1145 (2004).
18. Gilad, Y., Wiebe, V., Przeworski, M., Lancet, D. & Paabo, S. Loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates. PLoS Biol. 2, e5 (2004).
19. Ferland R. J. et al. Abnormal cerebellar development and axonal decussation due to mutations in AHI1 in Joubert syndrome. Nature Genet. 36, 1008-1013 (2004).
20. Dorus, S. et al. Accelerated evolution of nervous system genes in the origin of Homo sapiens. Cell 119, 1027-1040 (2004).
21. Stedman, H. H. et al. Myosin gene mutation correlates with anatomical changes in the human lineage. Nature 428, 415-418 (2004).
22. Mochida, G. H. & Walsh, C. A. Molecular genetics of human microcephaly. Curr. Opin. Neurol. 14, 151-156 (2001).
23. Dobyns, W. B. Primary microcephaly: new approaches for an old disorder. Am. J. Hum. Genet. 112, 315-317 (2002).
24. Komai, T., Wshimoto, K. & Ozaki, Y. Genetic study of microcephaly based on Japanese material. Am. J. Hum. Genet. 47, 51-65 (1955).
25. Tramo, M. J. et al. Brain size, head size, and intelligence quotient in monozygotic twins. Neurology 50,1246-1252 (1998).
26. Thompson, P. M. et al. Genetic influences on brain structure. Nature Neurosci. 4, 1253-1258 (2001).
27. Bouchard, T. J. Jr. Genes, environment, arid personality. Science 264, 1700-1701 (1994).
28. Plomin, R., Owen, M. J. & McGuffin, P. The genetic basis of complex human behaviors. Science 264, 1733-1739 (1994).
29. Plomin, R., DeFries, J. C., McClearn, G. E. & Rutter, M. Behavioral Genetics (W. H. Freeman, New York, 1997).
30. Bouchard, T. J. Jr & McGue, M. Genetic and environmental influences on human psychological differences. J. Neurobiol. 54, 4-45 (2003).
31. Rushton, J. P. & Ankney, C. D. Brain size and cognitive ability: correlations with age, sex, social class, and race, Psychon. Bull. Rev. 3, 21-36 (1996).
32. Vernon, P. A., Wickett, J. C., Bazana, P. G. & Stelmack, R. M. in Handbook of Intelligence (ed. Sternberg, R. J.) 245-264 (Cambridge Univ. Press, Cambridge, UK, 2000).
33. Posthuma, D. et al. The association between brain volume and intelligence is of genetic origin. Nature Neurosci. 5, 83-84 (2002).
34. Gray, J. R. & Thompson, P. M. Neurobiology of intelligence: science and ethics. Nature Rev. Neurosci. 5, 471-482 (2004).
35. Schoenemann, P. T., Budinger, T. F., Sarich, V. M. & Wang, W. S. Brain size does not predict general cognitive ability within families. Proc. Natl Acad. Sci. USA 97, 4932-4937 (2000).
36. Williams, M. F. Primate encephalization and intelligence Med. Hypotheses 58, 284-290 (2002).
37. McHenry, H. M. Tempo and mode in human evolution. Proc. Natl Acad. Sci. USA 91, 6780-6786 (1994).
38. Aschoff, J., Gunther, B. & Kramer, K. Energiehaushalt und Temperatursregulation (Urban and Schwarzenberg, Munich, 1971).
39. Armstrong, E. Brains, bodies and metabolism. Brain Behav. Evol. 36, 166-176 (1990).
40. Aiello, L. C. & Wheeler, P. The expensive tissue hypothesis: the brain and the digestive system in human and primate evolution. Curr. Anthropol. 36, 199-221 (1995).
41. Smith, B. H. The cost of a large brain. Behav. Brain Res. 13, 365-366 (1990).
42. Loudon, I. Maternal mortality in the past and its relevance to developing countries today. Am. J. Clin. Nutr. 72, 2413-2463 (2000).
43. Rosenberg, K. R. & Trevathan, W. R. The evolution of human birth. Sci. Am. 285, 72-77 (2001).
44. Lovejoy, C. O. in Primate Functional Morphology and Evolution (ed. Tuttle, R. H.) 291-326 (Mouton, The Hague, 1975).
45. Sacher, G. A. in Primate Brain Evolution: Methods and Concepts (eds Armstrong, E. & Falk, D.) 97-112 (Plenum, New York, 1982).
46. Harvey, P. H. & Clutton-Brock, T. H. Life history variation in primates. Evolution 39, 559-581 (1985).
47. Martin, R. D. Scaling of the mammalian brain: the maternal energy hypothesis. News Physiol. Sci. 11, 149-156 (1996).
48. Ohta, T. Slightly deleterious mutant substitutions in evolution. Nature 246, 96-98 (1973).
49. Enard, W. et al. Intra- and interspecific variation in primate gene expression patterns. Science 296, 340-343 (2002).
50. Caceres, M. et al. Elevated gene expression levels distinguish human from non-human primate brains. Proc. Natl Acad. Sci. USA 100, 13030-13035 (2003).
51. Preuss, T. M., Caceres, M., Oldham, M. C. & Geschwind, D. H. Human brain evolution: insights from microarrays. Nature Rev. Genet. 5, 850-860 (2004).
52. Uddin, M. et al. Sister grouping of chimpanzees and humans as revealed by genome-wide phylogenetic analysis of brain gene expression profiles. Proc. Natl Acad. Sci. USA 101, 2957-2962 (2004).
53. Harris, M. A. et al. The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res. 32 (Database issue), D258-D261 (2004).
54. Barkovich, A. J. et al. Microlissencephaly: a heterogeneous malformation of cortical development. Neuropediatrics 29, 113-119 (1998).
55. Tolmie, J. L., McNay, M., Stephenson, J. B. P., Doyle, D. & Connor, J. M, Microcephaly: genetic counseling and antenatal diagnosis after the birth of an affected child. Am. J. Med. Genet. 27, 583-594 (1987).
56. Baraitser, M. The Genetics of Neurological Disorders 456 (Oxford Univ. Press, Oxford. 1997).
57. Peiffer, A., Singh, N., Leppert, M., Dobyns, W. B. & Carey, J. C. Microcephaly with simplified gyral pattern in six related children. Am. J. Med. Genet. 84, 137-144 (1999).
58. Bond, J. et al. ASPM is a major determinant of cerebral cortical size. Nature Genet. 32, 316-320 (2002).
59. Bond, J. et al. Protein-truncating mutations in ASPM cause variable reduction in brain size. Am. J. Hum. Genet. 73, 1170-1177 (2003).
60. Jackson, A. P. et al. Primary autosomal recessive microcephaly (MCPH1) maps to chromosome 8p22-pter. Am. J. Hum. Genet. 63, 541-546 (1998).
61. Jackson, A. P. et al. Identification of microcephalin, a protein implicated in determining the size of the human brain. Am. J. Hum. Genet. 71, 136-142 (2002).
62. Trimborn, M. et al. Mutations in microcephalin cause aberrant regulation of chromosome condensation. Am. J. Hum. Genet. 75, 261-266 (2004).
63. Cohen, M. M. Jr. Perspectives on hotoprosencephaly: Part I. Epidemiology, genetics, and syndromology. Teratology 40, 211-235 (1989).
64. Muenke, M. et al. Linkage of a human brain malformation, familial holoprosencephaly, to chromosome 7 and evidence for genetic heterogeneity. Proc. Natl Acad. Sci. USA 91, 8102-8106 (1994).
65. Roessler, E. et al. Mutations in the human sonic hedgehog gene cause holoprosencephaly. Nature Genet. 14, 357-360 (1996).
66. Roessler, E. et al. Mutations in the C-terminal domain of sonic hedgehog cause holoprosencephaly. Hum. Mol. Genet. 6, 1847-1853 (1997).
67. Dubourg, C. et al. Molecular screening of SHH, ZIC2, SIX3, and TGIF genes in patients with features of holoprosencephaly spectrum: mutation review and genotype-phenotype correlations. Hum. Mutat. 24, 43-51 (2004).
68. Sztriha, L., Al-Gazali, L. I., Varady, E., Goebel, H. H. & Nork, M. Autosomal recessive micrencephaly with simplified gyral pattern, abnormal myelination and arthrogryposis. Neuropediatrics 30, 141-145 (1999).
69. ten Donkelaar, H. J. Major events in the development of the forebrain. Eur. J. Morphol. 38, 301-308 (2000).
70. Sheen, V. L. et al. Mutations in ARFGEF2 implicate vesicle trafficking in neural progenitor proliferation and migration in the human cerebral cortex. Nature Genet. 36, 69-76 (2004).
71. Sheen, V. L. et al. Autosomal recessive form of periventricular heterotopia. Neurology 60, 1108-1112 (2003).
72. Shariske, A., Caride, D. G., Menasse-Palmer, L., Bogdanow, A. & Marion, R. Central nervous system anomalies in Seckel syndrome: report of a new family and review of the literature. Am. J. Med. Genet. 70, 155-158 (1998).
73. Goodship, J. et al. Autozygosity mapping of a Seckel syndrome locus to chromosome 3q22.1-q24. Am. J. Hum. Genet. 67, 498-503 (2000)
74. Capovilla, G. et al. Seckel's syndrome and malformations of cortical development: report of three new cases and review of the literature. J. Child. Neurol. 16, 382-386 (2001).
75. O'Driscoll, M., Ruiz-Perez, V. L., Woods, C. G., Jeggo, P. A. & Goodship, J. A. A splicing mutation affecting expression of ataxia- telangiectasia and Rad3-related protein (ATR) results in Seckel syndrome. Nature Genet 33, 497-501 (2003).
76. Alderton, G. K. et al. Seckel syndrome exhibits cellular features demonstrating defects in the ATR-signalling pathway. Hum. Mol. Genet. 13, 3127-3138 (2004).
77. Kelley, R. I., Robinson, D., Puffenberger, E. G., Strauss, K. A. & Morton, D. H. Amish lethal microcephaly: a new metabolic disorder with severe congenital microcephaly and 2-ketoglutaric aciduria. Am. J. Med. Genet 112, 318-326 (2002).
78. Rosenberg, M. J. et al. Mutant deoxynucleotide carrier is associated witn congenital microcephaly. Nature Genet. 32, 175-179 (2002).
79. Strauss, K. A., Pfanni, R. & Morton, D. H. The neuropathology of Amish lethal microcephaly. Am. J. Hum. Genet. 71, A517 (2002).
80. Roberts, E. et al. The second locus for autosomal recessive primary microcephaly (MCPH2) maps to chromosome 19q13.1-13.2. Eur J. Hum. Genet. 7, 815-820 (1999).
81. Moynihan, L. et al. A third novel locus for primary autosomal recessive microcephaly maps to chromosome 9q34. Am. J. Hum. Genet. 66, 724-727 (2000).
82. Jamieson, C. R., Govaerts, C. & Abramowicz, M. J. Primary autosomal recessive microcephaly: homozygosity mapping of MCPH4 to chromosome 15. Am. J. Hum. Genet. 65, 1465-1469 (1999).
83. Jamieson, C. R., Fryns, J. P., Jacobs, J., Matthijs, G. & Abramowicz, M. J. Primary autosomal recessive microcephaly: MCPH5 maps to 1q25-q32. Am. J. Hum. Genet 67, 1575-1577 (2000).
84. Pattison, L. et al. A fifth locus for primary autosomal recessive microcephaly maps to chromosome 1q31. Am. J. Hum. Genet. 67, 1578-1580 (2000).
85. Leal, G. F. et al. A novel locus for autosomal recessive primary microcephaly (MCPH6) maps to 13q12.2. J. Med. Genet. 40, 540-542 (2003).
86. Li, W. H. Molecular Evolution (Sinauer, Sunderland, Massachusetts, 1997).
87. McDonald, J. H, & Kreitman, M. Adaptive protein evolution at the Adh locus in Drosophila. Nature 351, 652-654 (1991).
88. Kreitman, M. Methods to detect selection in populations with applications to the human. Annu. Rev. Genomics Hum. Genet. 1, 539-559 (2000).
89. Duret, L. & Mouchiroud, D. Determinants of substitution rates in mammalian genes: expression pattern affects selection intensity but not mutation rate. Mol. Biol. Evol. 17, 68-74 (2000).
90. Ripoll, P., Pimpinelli, S., Valdivia, M. M. & Avila, J. A cell division mutant of Drosophila with a functionally abnormal spindle. Cell 41, 907-912 (1985).
91. Saunders, R. D., Avides, M. C., Howard, T., Gonzalez, C. & Glover, D. M. The Drosophila gene abnormal spindle encodes a novel microtubule-associated protein that associates with the polar regions of the mitotic spindle. J. Cell. Biol. 137, 881-890 (1997).
92. do Carmo Avides, M., Tavares, A. & Glover, D. M. Polo kinase and Asp are needed to promote the mitotic organizing activity of centrosomes. Nature Cell Biol. 3, 421-424 (2001).
93. Huyton, T., Bates, P. A., Zhang, X., Sternberg, M. J. & Freemont, P. S. The BRCA1 C-terminal domain: structure and function. Mutat Res 460, 319-332 (2000).
94. Haldane, J. B. S. The rate of mutation of human genes. Hereditas 35 (Suppl. 1), 267-272 (1949).
95. Mears, J. G. et al. Sickle gene. Its origin and diffusion from West Africa, J. Clin. Invest. 68, 606-610 (1981).
96. Flint, J. et al. High frequencies of α-thalassaemia are the result of natural selection by malaria. Nature 321, 744-750 (1986).
97. Lell, B. et al. The role of red blood cell polymorphisms in resistance and susceptibility to malaria. Clin. Infect. Dis. 28, 794-799 (1999).
98. Tishkoff, S. A. et al. Haplotype diversity and linkage disequilibrium at human G6PD: recent origin of alleles that confer malarial resistance. Science 293, 455-462 (2001).
99. Sabeti, P. C. et al. Detecting recent positive selection in the human genome from haplotype structure. Nature 419, 832-837 (2002).
100. Aidoo, M. et al. Protective effects of the sickle cell gene against malaria morbidity and mortality. Lancet 359, 1311-1312 (2002).
101. Ayi, K., Turrini, F., Piga, A. & Arese, P. Enhanced phagocytosis of ring-parasitized mutant erythrocytes: a common mechanism that may explain protection against falciparum malaria in sickle trait and β-thalassemia trait. Blood 104, 3364-3371 (2004).
102. Bauchot, R. Encephalization in vertebrates. A new mode of calculation for allometry coefficients and isoponderal indices. Brain Behav. Evol. 15, 1-18 (1978).
103. Martin, R. D. Relative brain size and basal metabolic rate in terrestrial vertebrates. Nature 293, 57-60 (1981).
104. Lapicque, L. Sur la relation du poids de l'encéphale au poids du corps. C. R. Seances Soc. Biol. Fil. 50, 62-63 (1898).
105. Martin, R. D. & Harvey, P. H. in See and Scaling in Primate Biology (ed. Jungers, W. L.) (Plenum, New York, 1985).
106. Pilbeam, D. & Gould, S. J. Size and scaling in human evolution. Science 186, 892-901 (1974).
107. Martin, R. D. Primate Origins and Evolution: a Phylogenetic Reconstruction (Princeton Univ. Press, Princeton, 1990).
108. Kruska, D. C. On the evolutionary significance of encephalization in some eutherian mammals: effects of adaptive radiation, domestication, and feralization. Brain Behav. Evol. 65, 73-108 (2005).
109. Finlay, B. L., Darlington, R. B. & Nicastro, N. Developmental structure in brain evolution. Behav. Brain Sci. 24, 263-278; discussion 278-308 (2001).
110. Radinsky, L. Early primate brains: facts and fiction. J. Hum. Evol. 6, 79-86 (1977).
111. Radinsky, L. Aegyptopithecus endocasts: oldest record of a pongid brain. Am. J. Phys. Anthropol. 39, 239-247 (1973).
112. Gingerich, P. D. Correlation of tooth size and body size in living hominoid primates, with a note on relative brain size in Aegyptopithecus and Proconsul. Am. J. Phys. Anthropol. 47, 395-398 (1977).
113. Walker, A., Falk, D., Smith, R. & Pickford, M. The skull of Proconsul africanus: reconstruction and cranial capacity. Nature 305, 525-527 (1983).
114. Kumar, S. & Hedges, S. B. A molecular timescale for vertebrate evolution. Nature 392, 917-920 (1998).
115. Murphy, W. J. et al. Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294, 2348-2351 (2001).
116. Page, S. L. & Goodman, M. Catarrhine phytogeny: noncoding DNA evidence for a diphyletic origin of the mangabeys and for a human-chimpanzee clade. Mol. Phylogenet. Evol. 18, 14-25 (2001).
117. Poux, C. & Douzery, E. J. Primate phytogeny, evolutionary rate variations, and divergence times: a contribution from the nuclear gene IRBP. Am. J. Phys. Anthropol. 124, 1-16 (2004).
118. Springer, M. S., Murphy, W. J., Eizirik, E. & O'Brien, S. J. Placental mammal diversification and the Cretaceous-Tertiary boundary. Proc. Natl Acad. Sci. USA. 100, 1056-1061 (2003).