Review Article | Published:

The eloquent ape: genes, brains and the evolution of language

Nature Reviews Geneticsvolume 7pages920 (2006) | Download Citation

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Abstract

The human capacity to acquire complex language seems to be without parallel in the natural world. The origins of this remarkable trait have long resisted adequate explanation, but advances in fields that range from molecular genetics to cognitive neuroscience offer new promise. Here we synthesize recent developments in linguistics, psychology and neuroimaging with progress in comparative genomics, gene-expression profiling and studies of developmental disorders. We argue that language should be viewed not as a wholesale innovation, but as a complex reconfiguration of ancestral systems that have been adapted in evolutionarily novel ways.

Key Points

  • Human language seems to be unique and has often been studied as an isolated phenomenon, but few traits are entirely without precedent. As originally suggested by Darwin, our extraordinary capacity to acquire language should be explicable as the product of descent with modification.

  • Molecular methods offer a new kind of data for shedding light on language evolution, especially in tandem with changing views of neural substrates according to which language depends on a distributed network of cortical and subcortical circuits with substantial overlap with other cognitive domains.

  • Comparisons between the genomes of humans and chimpanzees, our closest extant non-speaking relatives, show over 35 million substitutions and 5 million indels, with most changes resulting from neutral drift. Large-scale between- and within-species sequence comparisons have not yet uncovered specific genes that are related to language.

  • Genes that are expressed in the brain tend to show less human–chimpanzee divergence than other genes, both in terms of protein structure and expression level, probably owing to higher functional constraint in neural tissue. Nonetheless, against this background, there seems to have been accelerated change for brain-related genes on the human lineage when compared with the branch leading to the chimpanzee.

  • Expression-profiling studies have yet to identify any particular human gene (or set of genes) that is uniquely expressed in language-related regions of adult brains. Most observed expression differences between the brains of humans and chimpanzees have been found to be common to all cortical regions, although this might reflect a lack of power when using current approaches.

  • Positional cloning studies of human neurodevelopmental disorders, such as specific language impairment, developmental dyslexia and autism, can provide candidate genes for targeted evolutionary investigation.

  • Direct evidence of a specific gene that influences language acquisition has come from a rare monogenic communication disorder, caused by mutation of a forkhead box transcription factor (FOXP2). Disruption of FOXP2 leads to problems in learning and producing complex sequences of mouth movements, accompanied by wide-ranging linguistic deficits.

  • FOXP2 is highly conserved in distant vertebrates, but underwent a 60-fold increase in amino-acid substitution rate on the human lineage — of three changes that distinguish human and mouse orthologues, two occurred on the human branch after splitting from the chimpanzee. The human within-species variability flanking these substitutions indicates a recent selective sweep.

  • Human FOXP2 gene expression shows intriguing overlaps with sites of pathology identified by structural/functional neuroimaging of patients with FOXP2-associated disorder. These data implicate FOXP2 in the development and/or function of circuitry involving the frontal cortex, striatum and cerebellum — networks that support (among other processes) learning and production of speech sequences.

  • Rodents, birds, reptiles and fish similarly show FoxP2 expression in circuits related to sensory-motor function and control of skilled coordinated movements. Species-specific differences in FoxP2 regulation in the song system of vocal-learning birds seem to relate to changes in vocal plasticity; ancient neural functions of FoxP2 might have been co-opted to subserve vocal communication on more than one occasion.

  • Although FoxP2 is probably just one piece of the evolutionary puzzle, research into the gene highlights how multidisciplinary studies of the functions of language-related genes in humans, animals and birds offer new routes for addressing old questions about the neural systems that subserve language.

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References

  1. 1

    Terrace, H. S., Petitto, L. A., Sanders, R. J. & Bever, T. G. in Children's Language Vol. 2 (ed. Nelson, K. E.) 371–496 (Gardner, New York, 1980).

  2. 2

    Hauser, M. D. The Evolution of Communication (MIT Press, Cambridge, Massachusetts, 1996).

  3. 3

    Chomsky, N. Aspects of the Theory of Syntax (MIT Press, Cambridge, Massachusetts, 1965).

  4. 4

    Pinker, S. The Language Instinct (Allen Lane, London, 1994).

  5. 5

    Petitto, L. A. & Marentette, P. F. Babbling in the manual mode: evidence for the ontogeny of language. Science 251, 1493–1496 (1991).

  6. 6

    Goldin-Meadow, S. & Mylander, C. Spontaneous sign systems created by deaf children in two cultures. Nature 391, 279–281 (1998).

  7. 7

    Damasio, A. R. Aphasia. N. Engl. J. Med. 326, 531–539 (1992).

  8. 8

    Poeppel, D. & Hickok, G. Towards a new functional anatomy of language. Cognition 92, 1–12 (2004). The introduction to a collection of articles that describe contemporary views of the neurological basis of language, which highlights the limitations of classical models and lays out an agenda for future research in this area.

  9. 9

    Pennisi, E. Bird wings really are like dinosaurs' hands. Science 307, 194 (2005).

  10. 10

    Darwin, C. The Descent of Man and Selection in Relation to Sex (John Murray, London, 1871).

  11. 11

    Christiansen, M. H. & Kirby, S. Language Evolution (Oxford Univ. Press, Oxford; New York, 2003).

  12. 12

    Pinker, S. & Bloom, P. Natural language and natural selection. Behav. Brain Sci. 13, 707–726 (1990).

  13. 13

    Gould, S. J. Evolution: the pleasures of pluralism. NY Rev. Books 44, 47–52 (1997).

  14. 14

    Crow, T. J. Schizophrenia as the price that Homo sapiens pays for language: a resolution of the central paradox in the origin of the species. Brain Res. Brain Res. Rev. 31, 118–129 (2000).

  15. 15

    Klein, R. G. & Edgar, B. The Dawn of Human Culture (Wiley, New York, 2002).

  16. 16

    Dennett, D. C. Darwin's Dangerous Idea: Evolution and the Meanings of Life (Simon & Schuster, New York, 1995).

  17. 17

    Marcus, G. F. Before the word. Nature 431, 745 (2004).

  18. 18

    Miller, G. F. The Mating Mind: How Sexual Choice Shaped the Evolution of Human Nature (Doubleday, New York, 2000).

  19. 19

    Dunbar, R. Evolution of the social brain. Science 302, 1160–1161 (2003).

  20. 20

    Liberman, A. M. & Whalen, D. H. On the relation of speech to language. Trends Cogn. Sci. 4, 187–196 (2000).

  21. 21

    Arensburg, B. et al. A Middle Palaeolithic human hyoid bone. Nature 338, 758–760 (1989).

  22. 22

    Kay, R. F., Cartmill, M. & Balow, M. The hypoglossal canal and the origin of human vocal behavior. Proc. Natl Acad. Sci. USA 95, 5417–5419 (1998).

  23. 23

    MacLarnon, A. M. & Hewitt, G. P. The evolution of human speech: the role of enhanced breathing control. Am. J. Phys. Anthropol. 109, 341–363 (1999).

  24. 24

    Lieberman, P., Laitman, J. T., Reidenberg, J. S., Landahl, K. & Gannon, P. J. Folk psychology and talking hyoids. Nature 342, 486–487 (1989).

  25. 25

    DeGusta, D., Gilbert, W. H. & Turner, S. P. Hypoglossal canal size and hominid speech. Proc. Natl Acad. Sci. USA 96, 1800–1804 (1999).

  26. 26

    Fitch, W. T. The evolution of speech: a comparative review. Trends Cogn. Sci. 4, 258–267 (2000). An accessible overview of the ways in which comparisons between diverse species can help to shed light on the origins of speech.

  27. 27

    Bickerton, D. Language and Species (Univ. Chicago Press, Chicago, 1990).

  28. 28

    Jackendoff, R. Possible stages in the evolution of the language capacity. Trends Cogn. Sci. 3, 272–279 (1999).

  29. 29

    Senghas, A., Kita, S. & Ozyurek, A. Children creating core properties of language: evidence from an emerging sign language in Nicaragua. Science 305, 1779–1782 (2004).

  30. 30

    Nowak, M. A., Komarova, N. L. & Niyogi, P. Evolution of universal grammar. Science 291, 114–118 (2001).

  31. 31

    Kirby, S. Natural language from artificial life. Artif. Life 8, 185–215 (2002).

  32. 32

    Lieberman, P. On the nature and evolution of the neural bases of human language. Am. J. Phys. Anthropol. Suppl. 35, 36–62 (2002).

  33. 33

    Dronkers, N. F., Wilkins, D. P., Van Valin, R. D. Jr, Redfern, B. B. & Jaeger, J. J. Lesion analysis of the brain areas involved in language comprehension. Cognition 92, 145–177 (2004).

  34. 34

    Nishitani, N. & Hari, R. Temporal dynamics of cortical representation for action. Proc. Natl Acad. Sci. USA 97, 913–918 (2000).

  35. 35

    Maess, B., Koelsch, S., Gunter, T. C. & Friederici, A. D. Musical syntax is processed in Broca's area: an MEG study. Nature Neurosci. 4, 540–545 (2001).

  36. 36

    Gannon, P. J., Holloway, R. L., Broadfield, D. C. & Braun, A. R. Asymmetry of chimpanzee planum temporale: humanlike pattern of Wernicke's brain language area homolog. Science 279, 220–222 (1998).

  37. 37

    Cantalupo, C. & Hopkins, W. D. Asymmetric Broca's area in great apes. Nature 414, 505 (2001).

  38. 38

    Petrides, M., Cadoret, G. & Mackey, S. Orofacial somatomotor responses in the macaque monkey homologue of Broca's area. Nature 435, 1235–1238 (2005).

  39. 39

    Demonet, J. F., Thierry, G. & Cardebat, D. Renewal of the neurophysiology of language: functional neuroimaging. Physiol. Rev. 85, 49–95 (2005).

  40. 40

    Riede, T., Bronson, E., Hatzikirou, H. & Zuberbuhler, K. Vocal production mechanisms in a non-human primate: morphological data and a model. J. Hum. Evol. 48, 85–96 (2005).

  41. 41

    Ramus, F., Hauser, M. D., Miller, C., Morris, D. & Mehler, J. Language discrimination by human newborns and by cotton-top tamarin monkeys. Science 288, 349–351 (2000).

  42. 42

    Hauser, M. D., Chomsky, N. & Fitch, W. T. The faculty of language: what is it, who has it, and how did it evolve? Science 298, 1569–1579 (2002).

  43. 43

    Pinker, S. & Jackendoff, R. The faculty of language: what's special about it? Cognition 95, 201–236 (2005). References 42 and 43 provide in-depth discussions of the relationship between language and other aspects of cognition, and the extent to which the evolution of human communication depended on language- and human-specific adaptations.

  44. 44

    Marcus, G. F. The Birth of the Mind: How a Tiny Number of Genes Creates the Complexities of Human Thought (Basic Books, New York, 2004).

  45. 45

    Olson, M. V. & Varki, A. Sequencing the chimpanzee genome: insights into human evolution and disease. Nature Rev. Genet. 4, 20–28 (2003).

  46. 46

    Preuss, T. M., Caceres, M., Oldham, M. C. & Geschwind, D. H. Human brain evolution: insights from microarrays. Nature Rev. Genet. 5, 850–860 (2004).

  47. 47

    Fisher, S. E., Lai, C. S. & Monaco, A. P. Deciphering the genetic basis of speech and language disorders. Annu. Rev. Neurosci. 26, 57–80 (2003).

  48. 48

    Pääbo, S. et al. Genetic analyses from ancient DNA. Annu. Rev. Genet. 38, 645–679 (2004).

  49. 49

    Noonan, J. P. et al. Genomic sequencing of Pleistocene cave bears. Science 309, 597–599 (2005).

  50. 50

    The Chimpanzee Sequencing and Analysis Consortium. Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437, 69–87 (2005). In this landmark paper, the availability of a complete draft sequence of the Pan troglodytes genome facilitated the first comprehensive comparison with that of Homo sapiens , as well as a large-scale search for signatures of selection. It also showed that most sequence differences between these species are probably due to neutral drift.

  51. 51

    Nielsen, R. et al. A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol. 3, e170 (2005).

  52. 52

    Khaitovich, P. et al. Parallel patterns of evolution in the genomes and transcriptomes of humans and chimpanzees. Science 309, 1850–1854 (2005). This investigation makes use of the draft chimpanzee genome sequence in a thorough exploration of how human–chimpanzee divergence in expression levels and protein structure might differ for genes that are active in different tissues (brain, heart, liver, kidney and testis). Although neural genes diverge the least overall, they have tended to accumulate more changes on the human lineage than on the chimpanzee lineage.

  53. 53

    Dorus, S. et al. Accelerated evolution of nervous system genes in the origin of Homo sapiens. Cell 119, 1027–1040 (2004).

  54. 54

    Tajima, F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595 (1989).

  55. 55

    Fay, J. C. & Wu, C. I. Hitchhiking under positive Darwinian selection. Genetics 155, 1405–1413 (2000).

  56. 56

    King, M. C. & Wilson, A. C. Evolution at two levels in humans and chimpanzees. Science 188, 107–116 (1975).

  57. 57

    Bentwich, I. et al. Identification of hundreds of conserved and nonconserved human microRNAs. Nature Genet. 37, 766–770 (2005).

  58. 58

    Enard, W. et al. Differences in DNA methylation patterns between humans and chimpanzees. Curr. Biol. 14, R148–149 (2004).

  59. 59

    Fortna, A. et al. Lineage-specific gene duplication and loss in human and great ape evolution. PLoS Biol. 2, e207 (2004).

  60. 60

    Cheng, Z. et al. A genome-wide comparison of recent chimpanzee and human segmental duplications. Nature 437, 88–93 (2005).

  61. 61

    Heissig, F. et al. Functional analysis of human and chimpanzee promoters. Genome Biol. 6, R57 (2005).

  62. 62

    Enard, W. et al. Intra- and interspecific variation in primate gene expression patterns. Science 296, 340–343 (2002).

  63. 63

    Càceres, M. et al. Elevated gene expression levels distinguish human from non-human primate brains. Proc. Natl Acad. Sci. USA 100, 13030–13035 (2003).

  64. 64

    Gu, J. & Gu, X. Induced gene expression in human brain after the split from chimpanzee. Trends Genet. 19, 63–65 (2003).

  65. 65

    Hsieh, W. P., Chu, T. M., Wolfinger, R. D. & Gibson, G. Mixed-model reanalysis of primate data suggests tissue and species biases in oligonucleotide-based gene expression profiles. Genetics 165, 747–757 (2003).

  66. 66

    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).

  67. 67

    Khaitovich, P., Pääbo, S. & Weiss, G. Toward a neutral evolutionary model of gene expression. Genetics 170, 929–939 (2005).

  68. 68

    Khaitovich, P. et al. Regional patterns of gene expression in human and chimpanzee brains. Genome Res. 14, 1462–1473 (2004). This study included a systematic comparative analysis of gene expression in Broca's area and other brain areas in human adults, including the corresponding region of the right hemisphere, but did not uncover any clear changes that might relate to language.

  69. 69

    Sun, T. et al. Early asymmetry of gene transcription in embryonic human left and right cerebral cortex. Science 308, 1794–1798 (2005).

  70. 70

    Rossion, B. et al. Hemispheric asymmetries for whole-based and part-based face processing in the human fusiform gyrus. J. Cogn. Neurosci. 12, 793–802 (2000).

  71. 71

    Amunts, K., Schleicher, A., Ditterich, A. & Zilles, K. Broca's region: cytoarchitectonic asymmetry and developmental changes. J. Comp. Neurol. 465, 72–89 (2003).

  72. 72

    Musso, M. et al. Broca's area and the language instinct. Nature Neurosci. 6, 774–781 (2003).

  73. 73

    Clayton, D. F. Songbird genomics: methods, mechanisms, opportunities, and pitfalls. Ann. NY Acad. Sci. 1016, 45–60 (2004).

  74. 74

    Jarvis, E. D. Learned birdsong and the neurobiology of human language. Ann. NY Acad. Sci. 1016, 749–777 (2004).

  75. 75

    Scharff, C. & White, S. A. Genetic components of vocal learning. Ann. NY Acad. Sci. 1016, 325–347 (2004). References 73–75 demonstrate the promise of using contemporary molecular methods to shed light on vocal-learning mechanisms in song-birds, and discuss the relevance of this strategy for understanding human language.

  76. 76

    Gilbert, S. L., Dobyns, W. B. & Lahn, B. T. Genetic links between brain development and brain evolution. Nature Rev. Genet. 6, 581–590 (2005).

  77. 77

    Woods, C. G., Bond, J. & Enard, W. Autosomal recessive primary microcephaly (MCPH): a review of clinical, molecular, and evolutionary findings. Am. J. Hum. Genet. 76, 717–728 (2005).

  78. 78

    Zhang, J. Evolution of the human ASPM gene, a major determinant of brain size. Genetics 165, 2063–2070 (2003).

  79. 79

    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).

  80. 80

    Kouprina, N. et al. Accelerated evolution of the ASPM gene controlling brain size begins prior to human brain expansion. PLoS Biol. 2, e126 (2004).

  81. 81

    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).

  82. 82

    Wang, Y. Q. & Su, B. Molecular evolution of microcephalin, a gene determining human brain size. Hum. Mol. Genet. 13, 1131–1137 (2004).

  83. 83

    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).

  84. 84

    Piao, X. et al. G protein-coupled receptor-dependent development of human frontal cortex. Science 303, 2033–2036 (2004).

  85. 85

    Bishop, D. V. Genetic and environmental risks for specific language impairment in children. Philos. Trans. R. Soc. Lond. B 356, 369–380 (2001).

  86. 86

    Bishop, D. V., North, T. & Donlan, C. Nonword repetition as a behavioural marker for inherited language impairment: evidence from a twin study. J. Child Psychol. Psychiatry 37, 391–403 (1996).

  87. 87

    Bartlett, C. W. et al. Examination of potential overlap in autism and language loci on chromosomes 2, 7, and 13 in two independent samples ascertained for specific language impairment. Hum. Hered. 57, 10–20 (2004).

  88. 88

    The SLI Consortium. Highly significant linkage to the SLI1 locus in an expanded sample of individuals affected by specific language impairment. Am. J. Hum. Genet. 74, 1225–1238 (2004).

  89. 89

    Stein, C. M. et al. Pleiotropic effects of a chromosome 3 locus on speech-sound disorder and reading. Am. J. Hum. Genet. 74, 283–297 (2004).

  90. 90

    Fisher, S. E. & DeFries, J. C. Developmental dyslexia: genetic dissection of a complex cognitive trait. Nature Rev. Neurosci. 3, 767–780 (2002).

  91. 91

    Wassink, T. H., Brzustowicz, L. M., Bartlett, C. W. & Szatmari, P. The search for autism disease genes. Ment. Retard. Dev. Disabil. Res. Rev. 10, 272–283 (2004).

  92. 92

    Demonet, J. F., Taylor, M. J. & Chaix, Y. Developmental dyslexia. Lancet 363, 1451–1460 (2004).

  93. 93

    Snowling, M. J. From language to reading and dyslexia. Dyslexia 7, 37–46 (2001).

  94. 94

    Taipale, M. et al. A candidate gene for developmental dyslexia encodes a nuclear tetratricopeptide repeat domain protein dynamically regulated in brain. Proc. Natl Acad. Sci. USA 100, 11553–11558 (2003).

  95. 95

    Scerri, T. S. et al. Putative functional alleles of DYX1C1 are not associated with dyslexia susceptibility in a large sample of sibling pairs from the UK. J. Med. Genet. 41, 853–857 (2004).

  96. 96

    Francks, C. et al. A 77-kilobase region of chromosome 6p22.2 is associated with dyslexia in families from the United Kingdom and from the United States. Am. J. Hum. Genet. 75, 1046–1058 (2004).

  97. 97

    Cope, N. et al. Strong evidence that KIAA0319 on chromosome 6p is a susceptibility gene for developmental dyslexia. Am. J. Hum. Genet. 76, 581–591 (2005).

  98. 98

    Tager-Flusberg, H., Joseph, R. & Folstein, S. Current directions in research on autism. Ment. Retard. Dev. Disabil. Res. Rev. 7, 21–29 (2001).

  99. 99

    Bradford, Y. et al. Incorporating language phenotypes strengthens evidence of linkage to autism. Am. J. Med. Genet. 105, 539–547 (2001).

  100. 100

    Alarcón, M., Yonan, A. L., Gilliam, T. C., Cantor, R. M. & Geschwind, D. H. Quantitative genome scan and ordered-subsets analysis of autism endophenotypes support language QTLs. Mol. Psychiatry 10, 747–757 (2005).

  101. 101

    Hurst, J. A., Baraitser, M., Auger, E., Graham, F. & Norell, S. An extended family with a dominantly inherited speech disorder. Dev. Med. Child Neurol. 32, 352–355 (1990).

  102. 102

    Lai, C. S., Fisher, S. E., Hurst, J. A., Vargha-Khadem, F. & Monaco, A. P. A forkhead-domain gene is mutated in a severe speech and language disorder. Nature 413, 519–523 (2001). The first demonstration that specific genetic mutations (a missense mutation and a translocation, both involving FOXP2 ) can lead to a developmental disruption of speech and language acquisition.

  103. 103

    Vargha-Khadem, F. et al. Neural basis of an inherited speech and language disorder. Proc. Natl Acad. Sci. USA 95, 12695–12700 (1998).

  104. 104

    Gopnik, M. & Crago, M. B. Familial aggregation of a developmental language disorder. Cognition 39, 1–50 (1991).

  105. 105

    Watkins, K. E., Dronkers, N. F. & Vargha-Khadem, F. Behavioural analysis of an inherited speech and language disorder: comparison with acquired aphasia. Brain 125, 452–464 (2002).

  106. 106

    Marcus, G. F. & Fisher, S. E. FOXP2 in focus: what can genes tell us about speech and language? Trends Cogn. Sci. 7, 257–262 (2003).

  107. 107

    Vargha-Khadem, F., Gadian, D. G., Copp, A. & Mishkin, M. FOXP2 and the neuroanatomy of speech and language. Nature Rev. Neurosci. 6, 131–138 (2005).

  108. 108

    Fisher, S. E., Vargha-Khadem, F., Watkins, K. E., Monaco, A. P. & Pembrey, M. E. Localisation of a gene implicated in a severe speech and language disorder. Nature Genet. 18, 168–170 (1998).

  109. 109

    Lai, C. S. et al. The SPCH1 region on human 7q31: genomic characterization of the critical interval and localization of translocations associated with speech and language disorder. Am. J. Hum. Genet. 67, 357–368 (2000).

  110. 110

    Newbury, D. F. et al. FOXP2 is not a major susceptibility gene for autism or specific language impairment. Am. J. Hum. Genet. 70, 1318–1327 (2002).

  111. 111

    MacDermot, K. D. et al. Identification of FOXP2 truncation as a novel cause of developmental speech and language deficits. Am. J. Hum. Genet. 76, 1074–1080 (2005).

  112. 112

    Sarda, P. et al. [Interstitial deletion in the long arm of chromosome 7]. Ann. Genet. 31, 258–261 (1988) (in French).

  113. 113

    Enard, W. et al. Molecular evolution of FOXP2, a gene involved in speech and language. Nature 418, 869–872 (2002).

  114. 114

    Zhang, J., Webb, D. M. & Podlaha, O. Accelerated protein evolution and origins of human-specific features: FOXP2 as an example. Genetics 162, 1825–1835 (2002). Driven by the finding that FOXP2 disruption is implicated in a human speech and language disorder, references 113 and 114 describe two independent targeted examinations of the primate evolution of this gene, each reaching the conclusion that FOXP2 was subject to positive selection in recent human history.

  115. 115

    Webb, D. M. & Zhang, J. FoxP2 in song-learning birds and vocal-learning mammals. J. Hered. 96, 212–216 (2005).

  116. 116

    Belton, E., Salmond, C. H., Watkins, K. E., Vargha-Khadem, F. & Gadian, D. G. Bilateral brain abnormalities associated with dominantly inherited verbal and orofacial dyspraxia. Hum. Brain Mapp. 18, 194–200 (2003).

  117. 117

    Liégeois, F. et al. Language fMRI abnormalities associated with FOXP2 gene mutation. Nature Neurosci. 6, 1230–1237 (2003). References 116 and 117 provide essential insights into the consequences of FOXP2 disruption for the structure and function of the adult human brain, uncovering a distributed pathology that involves cortical and subcortical structures.

  118. 118

    Lai, C. S., Gerrelli, D., Monaco, A. P., Fisher, S. E. & Copp, A. J. FOXP2 expression during brain development coincides with adult sites of pathology in a severe speech and language disorder. Brain 126, 2455–2462 (2003). This study revealed striking overlaps between the sites of FOXP2 expression in the human fetal brain and known sites of anomaly in a FOXP2 -related disorder, previously highlighted by structural or functional neuroimaging. There was also remarkable concordance between the human neural expression pattern and that observed for rodent Foxp2 , described here and in references 119 and 120.

  119. 119

    Ferland, R. J., Cherry, T. J., Preware, P. O., Morrisey, E. E. & Walsh, C. A. Characterization of Foxp2 and Foxp1 mRNA and protein in the developing and mature brain. J. Comp. Neurol. 460, 266–279 (2003).

  120. 120

    Takahashi, K., Liu, F. C., Hirokawa, K. & Takahashi, H. Expression of Foxp2, a gene involved in speech and language, in the developing and adult striatum. J. Neurosci. Res. 73, 61–72 (2003).

  121. 121

    Haesler, S. et al. FoxP2 expression in avian vocal learners and non-learners. J. Neurosci. 24, 3164–3175 (2004).

  122. 122

    Teramitsu, I., Kudo, L. C., London, S. E., Geschwind, D. H. & White, S. A. Parallel FoxP1 and FoxP2 expression in songbird and human brain predicts functional interaction. J. Neurosci. 24, 3152–3163 (2004). The molecular studies of song-bird brains in references 121 and 122 support the intriguing hypothesis that regulation of FoxP1 and FoxP2 in the song nuclei of vocal-learning species might be related to vocal plasticity.

  123. 123

    Bonkowsky, J. L. & Chien, C. B. Molecular cloning and developmental expression of foxP2 in zebrafish. Dev. Dyn. 234, 740–746 (2005).

  124. 124

    Wang, B., Lin, D., Li, C. & Tucker, P. Multiple domains define the expression and regulatory properties of Foxp1 forkhead transcriptional repressors. J. Biol. Chem. 278, 24259–24268 (2003).

  125. 125

    Shu, W., Yang, H., Zhang, L., Lu, M. M. & Morrisey, E. E. Characterization of a new subfamily of winged-helix/forkhead (Fox) genes that are expressed in the lung and act as transcriptional repressors. J. Biol. Chem. 276, 27488–27497 (2001).

  126. 126

    Ehret, G. Infant rodent ultrasounds — a gate to the understanding of sound communication. Behav. Genet. 35, 19–29 (2005).

  127. 127

    Holy, T. E & Guo Z. Ultrasonic songs of male mice. PLoS Biol. 3, e386 (2005). This is the first description of the properties of mouse song, which demonstrates unexpected similarities with bird song. These findings indicate that the neural underpinnings of song production and perception might be studied using the well-established techniques of genetic manipulation that are available for the mouse.

  128. 128

    Shu, W. et al. Altered ultrasonic vocalization in mice with a disruption in the Foxp2 gene. Proc. Natl Acad. Sci. USA 102, 9643–9648 (2005).

  129. 129

    Kuhl, P. K. Early language acquisition: cracking the speech code. Nature Rev. Neurosci. 5, 831–843 (2004).

  130. 130

    Crosson, B. Subcortical Functions in Language and Memory (Guilford, New York, 1992).

  131. 131

    Jarvis, E. D. et al. Avian brains and a new understanding of vertebrate brain evolution. Nature Rev. Neurosci. 6, 151–159 (2005).

  132. 132

    Clark, A. G. et al. Inferring nonneutral evolution from human–chimp–mouse orthologous gene trios. Science 302, 1960–1963 (2003).

  133. 133

    McDonald, J. H. & Kreitman, M. Adaptive protein evolution at the Adh locus in Drosophila. Nature 351, 652–654 (1991).

  134. 134

    Groszer, M. et al. Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor suppressor gene in vivo. Science 294, 2186–2189 (2001).

  135. 135

    Chenn, A. & Walsh, C. A. Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297, 365–369 (2002).

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Acknowledgements

We thank W. Enard for his helpful comments on this manuscript, and C. S. Lai and F. J. Liégeois for assistance with the figures. S.E.F. is a Royal Society Research Fellow, and his research is also supported by the Wellcome Trust, the 6th European Community Framework Programme and the Brain Sciences Initiative of the UK Medical Research Council. G.F.M. thanks the US National Institutes of Health and the Human Frontier Science Program for financial support.

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  1. Wellcome Trust Centre for Human Genetics, University of Oxford, Roosevelt Drive, Oxford, OX3 7BN, UK

    • Simon E Fisher
  2. Department of Psychology, New York University, 6 Washington Place, New York, 10003, USA

    • Gary F. Marcus

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The authors declare no competing financial interests.

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Correspondence to Simon E Fisher.

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Glossary

Linguistics

The scientific study of language.

Phonetics

The study of the production, perception and physical properties of speech sounds.

Phonology

The study of the sound systems of languages and the ways in which speech sounds can be combined.

Cerebral cortex

The outer layer of the mammalian cerebrum, which is involved in processes such as sensation, perception, cognition and (in humans) language.

Macromutation

A single evolutionary event that has large-scale effects on a phenotype, which involves concurrent alteration of numerous characteristics.

Sexual selection

The evolution of a trait as a consequence of competition among members of one sex (usually males) for fertilization opportunities with the other sex.

Hominin

Modern humans and all extinct human-like ancestors and their relatives that existed following divergence from other ape lineages. Includes all species of the genera Homo and Australopithecus, and other ancient forms such as Paranthropus and Ardipithecus.

Larynx

The specialized upper portion of the respiratory tract that houses the vocal cords — folds of mucous membrane that provide the source for vocal sounds. The low position of the larynx in adult humans allows a rich phonetic repertoire, but its significance for language evolution remains a matter of debate.

Lexicon

The vocabulary and word forms of a language.

Aphasia

An inability to produce and/or comprehend language that is due to brain injury or disease.

Subcortical

Describes the brain structures that are below the cerebral cortex.

Striatum

Part of the group of interconnected subcortical nuclei that are known as the basal ganglia. The striatum comprises two nuclei the — caudate and putamen — and is involved in the planning and modulation of movement pathways, as well as a range of other cognitive processes.

Thalamus

A forebrain structure that is located beneath the cerebral hemispheres and that modulates and relays sensory signals to and from the cerebral cortex.

Cerebellum

A multilayered structure in the vertebrate hindbrain that comprises a complex mixture of different cell types. The cerebellum modulates the force and range of movements, maintains balance and is involved in motor learning.

Hemispheric asymmetries

These are differences in the structure or function of the left and right hemisphere counterparts of a particular brain region.

Motor control

The ability to direct and coordinate muscle movements.

Formants

Peaks in the acoustic energy spectrum that result from the resonant frequencies of vocal tracts.

Recursion

A process by which ever more complex elements are generated through the repeated recombination of simpler elements.

Positive selection

When a novel allele that increases the fitness of an organism becomes more prevalent in the population.

Purifying selection

Selection against alleles that have harmful phenotypic effects, which leads to their loss from the population.

Outgroups

When two closely related species are compared, the status of the common ancestor (for example, at a site of substitution) could be deduced by including a more distant third species that branched from the parent group before the other two groups diverged.

Functional constraint

The degree to which changes in gene sequence are tolerated. For genes that have higher functional constraints a larger proportion of potential mutations are deleterious, reducing the substitution rate.

Maximum likelihood

A statistical method that is commonly used to make inferences about the most likely value of one of more parameters that underlie a given data set.

Selective sweep

Occurs when an allele increases in frequency as a consequence of positive selection and concurrently eliminates neutral variation at linked chromosomal sites.

Indel

A difference between sequences of related genomes that results from an insertion or deletion event; a term that is especially used when the evolutionary direction of the change is unknown.

Encephalization quotient

A measure of the relative brain size, in which the brain weight is compared with that of the average living mammal of equal body weight.

Cytoarchitecture

The cellular composition of a bodily structure. In neuroscience the term is used to refer to local differences in the arrangement of nerve cells in particular regions of the brain.

Speech-sound disorder

An inability to produce speech sounds that would be expected on the basis of age and dialect, but in the absence of an obvious cause (such as cerebral palsy or hearing impairment). This disorder might occur in isolation or together with other linguistic deficits.

Pragmatics

Social aspects of communication — in particular the influence of context on the interpretation of meaning.

Endophenotype

A measurable intermediate trait that is assumed to provide a closer link to the neurobiological substrate of a disorder.

Forkhead box

An 80–100 amino-acid motif that is found in a similar form in every member of the forkhead box family of transcription factors. It forms a winged-helix structure that allows the protein to bind to DNA.

Nuclear localization signals

Short stretches of amino acids that help to mediate the transport of proteins to the nucleus of the cell.

Atavism

The reappearance in an organism of characteristics that were typical of the organism's remote ancestors.

Purkinje cells

The output neurons of the cerebellum, which integrate complex inputs and project to the deep motor nuclei of the brain.

Inferior olivary nucleus

A precerebellar nucleus that provides direct input to the Purkinje cells through a network of climbing fibres. Olivocerebellar circuits have a crucial role in controlling movement.

Area X

A striatal nucleus that is present in the song system in the brains of vocal-learning birds.

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https://doi.org/10.1038/nrg1747

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