Evo-devo, deep homology and FoxP2: Implications for the evolution of speech and language

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 366, Issue 1574, 2011, Pages 2124-2140

  Scharff, Constance ^a   Petri, Jana ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Avian; Basal ganglia; Bird; Song learning; Vocal learning; Zebra finch

Indexed keywords

FORKHEAD TRANSCRIPTION FACTOR;

ADAPTIVE RADIATION; CONCEPTUAL FRAMEWORK; CONVERGENT EVOLUTION; EMERGENCE; FEATHER; FUNCTIONAL MORPHOLOGY; GENE EXPRESSION; GENETIC ANALYSIS; HOMOLOGY; INSECT; LANGUAGE; MOLECULAR ANALYSIS; NUMERICAL MODEL; PHENOTYPIC PLASTICITY; PROTEIN; SENSORY SYSTEM; SOCIAL BEHAVIOR; TEMPERATURE EFFECT; VERTEBRATE; VOCALIZATION;

ANIMAL; EVOLUTION; GENE EXPRESSION REGULATION; GENETICS; LANGUAGE; METABOLISM; PHYSIOLOGY; REVIEW; SPEECH;

ANIMALS; BIOLOGICAL EVOLUTION; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; LANGUAGE; SPEECH;

ANIMALIA; AVES; HEXAPODA; MAMMALIA; MOLLUSCA; TAENIOPYGIA GUTTATA; TETRAPODA; VERTEBRATA;

EID: 79959436430     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2011.0001     Document Type: Review

References (189)

1. Gilbert, S. F., Opitz, J. M. & Raff, R. A. 1996 Resynthesizing evolutionary and developmental biology. Dev. Biol. 173, 357-372. (doi:10.1006/dbio.1996.0032)
2. Thompson, D. A. W. 1917 On growth and form. Cambridge, UK: Cambridge University Press.
3. Turing, A. M. 1952 The chemical basis of morphogenesis. Phil. Trans. R. Soc. Lond. B 237, 37-72. (doi:10. 1098/rstb.1952.0012)
4. Maynard Smith, J., Burian, R., Kauffman, S., Alberch, P., Campbell, J., Goodwin, B., Lande, R., Raup, D. & Wolpert, L. 1985 Developmental constraints and evolution. Q. Rev. Biol. 60, 265-287. (doi:10.1086/414425)
5. Stern, D. L. & Orgogozo, V. 2009 Is genetic evolution predictable? Science 323, 746-751. (doi:10.1126/ science.1158997)
6. Carroll, S. B. 2008 Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134, 25-36. (doi:10.1016/j.cell.2008.06.030)
7. Hoekstra, H. E. & Coyne, J. A. 2007 The locus of evolution: evo devo and the genetics of adaptation. Evolution 61, 995-1016. (doi:10.1111/j.1558-5646. 2007.00105.x)
8. Brakefield, P. M. 2011 Evo-devo and accounting for Darwin's endless forms. Phil. Trans. R. Soc. B 366, 2069-2075. (doi:10.1098/rstb.2011.0007)
9. Robinson, G. E., Fernald, R. D. & Clayton, D. F. 2008 Genes and social behavior. Science 322, 896-900. (doi:10.1126/science.1159277)
10. Bloch, G. & Grozinger, C. M. 2011 Social molecular pathways and the evolution of bee societies. Phil. Trans. R. Soc. B 366, 2155-2170. (doi:10.1098/rstb. 2010.0346)
11. Reaume, C. J. & Sokolowski, M. B. 2011 Conservation of gene function in behaviour. Phil. Trans. R. Soc. B 366, 2100-2110. (doi:10.1098/rstb.2011.0028)
12. Katz, P. S. 2011 Neural mechanisms underlying the evolvability of behaviour. Phil. Trans. R. Soc. B 366, 2086-2099. (doi:10.1098/rstb.2010.0336)
13. Ghazanfar, A. A. 2008 Language evolution: neural differences that make a difference. Nat. Neurosci. 11, 382-384. (doi:10.1038/nn0408-382)
14. Chomsky, N. 2007 Of minds and language. Biolinguisitcs 1, 9-27.
15. Pinker, S. & Bloom, P. 1990 Natural-language and natural-selection. Behav. Brain Sci. 13, 707-726.
16. Miller, G. F. 2000 The mating mind: how sexual choice shaped the evolution of human nature, 1st edn. New York, NY: Doubleday.
17. Deacon, T. W. 2010 Colloquium paper: a role for relaxed selection in the evolution of the language capacity. Proc. Natl Acad. Sci. USA 107(Suppl. 2), 9000-9006. (doi:10.1073/pnas.0914624107)
18. Dor, D. & Jablonka, E. 2010 Plasticity and canalization in the evolution of linguistic communication: an evolutionary developmental approach. In The evolution of human language: biolinguistic perspectives (eds R. K. Larson & V. De ́prez & H. Yamakido). Cambridge, UK: Cambridge University Press.
19. Zirin, R. A. 1980 Aristotle's biology of language. Trans. Am. Phil. Assoc. 110, 325-347. (doi:10.2307/284226)
20. Herder, J. G. 1772 Abhandlung über den Ursprung der Sprache, welche den von der Kö nigl. Academie der Wissenschaften fü r das Jahr 1779 gesetzten Preise erhalten hat. Berlin, Germany: Christian Friedrich Voß.
21. Lenneberg, E. H. 1967 Biological foundations of language. New York, NY: Wiley.
22. Aitchison, J. 1996 The seeds of speech: language origin and evolution. Cambridge, UK: Cambridge University Press.
23. Dunbar, R. I. M. 1996 Grooming, gossip, and the evolution of language. Cambridge, MA: Harvard University Press.
24. Knight, C., Studdert-Kennedy, M. & Hurford, J. R. 1998 The evolutionary emergence of language. Cambridge, UK: Cambridge University Press.
25. Jackendorff, R. 1999 Possible stages in the evolution of the language capacity. Trends Cogn. Sci. 3, 272-279. (doi:10.1016/S1364-6613(99)01333-9)
26. Corballis, M. C. 2002 From hand to mouth: the origins of language. Princeton, NJ: Princeton University Press.
27. Bickerton, D. 2009 Adam's tongue: how humans made language, how language made humans, 1st edn. New York, NY: Hill and Wang.
28. Fitch, W. T. 2010 The evolution of language. Cambridge, UK: Cambridge University Press.
29. Fitch, W. T. 2000 The evolution of speech: a comparative review. Trends Cogn. Sci. 4, 258-267. (doi:10.1016/ S1364-6613(00)01494-7)
30. Chomsky, N. 1968 Language and mind. New York, NY: Harcourt.
31. Bolhuis, J. J., Okanoya, K. & Scharff, C. 2010 Twitter evolution: converging mechanisms in birdsong and human speech. Nat. Rev. Neurosci. 11, 747-759. (doi:10.1038/nrn2931)
32. Hauser, M. D., Chomsky, N. & Fitch, W. T. 2002 The faculty of language: what is it, who has it, and how did it evolve? Science 298, 1569-1579. (doi:10.1126/science. 298.5598.1569)
33. Fitch, W. T., Hauser, M. D. & Chomsky, N. 2005 The evolution of the language faculty: clarifications and implications. Cognition 97, 179-210 (discussion 1-25). (doi:10.1016/j.cognition.2005.02.005)
34. Pinker, S. & Jackendorff, R. 2009 The components of language: what's specific to language, and what's specific to humans. Lang. Univ. 27, 126-157. (doi:10. 1093/acprof:oso/9780195305432.003.0007)
35. Shubin, N., Tabin, C. & Carroll, S. B. 1997 Fossils, genes and the evolution of animal limbs. Nature 388, 639-648. (doi:10.1038/41710)
36. Shubin, N., Tabin, C. & Carroll, S. B. 2009 Deep homology and the origins of evolutionary novelty. Nature 457, 818-823. (doi:10.1038/nature07891)
37. Kaestner, K.H., Knochel, W. & Martinez, D. E. 2000 Unified nomenclature for the winged helix/forkhead transcription factors. Genes Dev. 14, 142-146. (doi:10. 1101/gad.14.2.142)
38. Bickerton, D. 2000 How protolanguage became language. In The evolutionary emergence of language: social function and the origins of linguistic form (eds M. Studdert-Kennedy, C. Knight & J. R. Hurford). Cambridge, UK: Cambridge University Press.
39. Hauser, M. D. & Konishi, M. 1999 The design of animal communication. Cambridge, MA: MIT Press.
40. Bradbury, J. W. & Vehrencamp, S. L. 1998 Principles of animal communication. Sunderland, MA: Sinauer Associates.
41. Sossinka, R. & Böhner, J. 1980 Song types in the zebrafinch Poephila guttata castanotis. Z. Tierpsychol. 53, 123-132.
42. Hurford, J. R. 2008 The evolution of human communication and language. In Sociobiology of communication: an interdisciplinary perspective (eds P. d'Ettorre & D. P. Hughes), pp. 249-264. New York, NY: Oxford University Press.
43. Patterson, F., Tanner, J. & Mayer, N. 1988 Pragmatic analysis of gorilla utterances: early communicative development in the Gorilla Koko. J. Pragmat. 12, 35-54. (doi:10.1016/0378-2166(88)90018-5)
44. Pepperberg, I. M. 2010 Vocal learning in Grey parrots: a brief review of perception, production, and crossspecies comparisons. Brain Lang. 115, 81-91. (doi:10. 1016/j.bandl.2009.11.002)
45. Marler, P. & Slabbekoorn, H. W. 2004 Nature's music: the science of birdsong. Amsterdam, The Netherlands: Elsevier Academic.
46. Holy, T. E. & Guo, Z. 2005 Ultrasonic songs ofmalemice. PLoS Biol. 3, e386. (doi:10.1371/journal.pbio.0030386)
47. Campbell, P., Pasch, B., Pino, J. L., Crino, O. L., Phillips, M. & Phelps, S. M. 2010 Geographic variation in the songs of neotropical singing mice: testing the relative importance of drift and local adaptation. Evolution 64, 1955-1972.
48. Behr, O. & von Helversen, O. 2004 Bat serenades: complex courtship songs of the sac-winged bat (Saccopteryx bilineata). Behav. Ecol. Sociobiol. 56, 106-115. (doi:10. 1007/s00265-004-0768-7)
49. Bohn, K. M., Schmidt-French, B., Schwartz, C., Smotherman, M. & Pollak, G. D. 2009 Versatility and stereotypy of free-tailed bat songs. PLoS ONE 4, e6746. (doi:10.1371/journal.pone.0006746)
50. Davidson, S. M. & Wilkinson, G. S. 2004 Function of male song in the greater white-lined bat, Saccopteryx bilineata. Anim. Behav. 67, 883-891. (doi:10.1016/j. anbehav.2003.06.016)
51. Payne, R. S. & Mcvay, S. 1971 Songs of humpback whales. Science 173, 585-597. (doi:10.1126/science. 173.3997.585)
52. Clark, C. W. & Clapham, P. J. 2004 Acoustic monitoring on a humpback whale (Megaptera novaeangliae) feeding ground shows continual singing into late Spring. Proc. R. Soc. Lond. B 271, 1051-1057. (doi:10.1098/rspb.2004.2699)
53. Marshall, J. T. J. & Marshall, E. R. 1976 Gibbons and their territorial songs. Science 193, 235-237. (doi:10. 1126/science.193.4249.235)
54. Clarke, E., Reichard, U. H. & Zuberbü hler, K. 2006 The syntax and meaning of wild gibbon songs. PLoS ONE 1, e73. (doi:10.1371/journal.pone.0000073)
55. Mitani, J. C. & Marler, P. 1989 A phonological analysis of male gibbon singing behavior. Behaviour 109, 20-45. (doi:10.1163/156853989X00141)
56. Janik, V. M. & Slater, P. J. B. 2000 The different roles of social learning in vocal communication. Anim. Behav. 60, 1-11. (doi:10.1006/anbe.2000.1410)
57. Thorpe, W. H. 1995 The learning of song patterns by birds, with especial reference to the song of the chaffinch Fringilla coelebs. Ibis 100, 535-570. (doi:10. 1111/j.1474-919X.1958.tb07960.x)
58. Gramza, A. F. 1970 Vocal mimicry in captive budgerigars (Melopsittacus undulatus). Z. Tierpsychol. 27, 971-983. (doi:10.1111/j.1439-0310.1970.tb01913.x)
59. Todt, D. 1975 Social learning of vocal patterns and modes of their applications in Grey Parrots. Z. Tierpsychol. 39, 178-188.
60. Baptista, L. F. & Schuchmann, K. L. 1990 Song learning in the anna hummingbird (Calypte anna). Ethology 84, 15-26. (doi:10.1111/j.1439-0310.1990.tb00781.x)
61. Knö rnschild, M., Behr, O. & von Helversen, O. 2006 Babbling behavior in the sac-winged bat (Saccopteryx bilineata). Naturwissenschaften 93, 451-454. (doi:10. 1007/s00114-006-0127-9)
62. Ralls, K., Fiorelli, P. & Gish, S. 1985 Vocalizations and vocal mimicry in captive harbor seals, Phoca vitulina. Can. J. Zool. 63, 1050-1056. (doi:10.1139/ z85-157)
63. Poole, J. H., Tyack, P. L., Stoeger-Horwath, A. S. & Watwood, S. 2005 Elephants are capable of vocal learning. Nature 434, 455-456. (doi:10.1038/434455a)
64. Hauser, M. D. 1989 Ontogenetic changes in the comprehension and production of vervet monkey (Cercopithecus aethiops) vocalizations. J. Comp. Psychol. 103, 149-158. (doi:10.1037/0735-7036.103.2.149)
65. Seyfarth, R.M. & Cheney, D. L. 1986 Vocal development in vervet monkeys. Anim. Behav. 34, 1640-1658. (doi:10. 1016/S0003-3472(86)80252-4)
66. Doupe, A. J. & Kuhl, P. K. 1999 Birdsong and human speech: common themes and mechanisms. Annu. Rev. Neurosci. 22, 567-631. (doi:10.1146/annurev.neuro. 22.1.567)
67. Hockett, C. F. 1960 The origin of speech. Sci. Am. 203, 89-96. (doi:10.1038/scientificamerican0960-88)
68. Piattelli-Palmarini, M. 1974 A debate on bio-linguistics. Endicott House Dedham, Centre Royaumont pour une science de l'homme report, MA, USA.
69. Boeckx, C. & Grohmann, K. K. 2007 The biolinguistics manifesto. Biolinguistics 1, 1-8.
70. Poeppel, D. & Embick, D. 2005 Defining the relation between linguistics and neuroscience. In Twenty-first century psycholinguistcs: four cornerstones (ed. A. Cutler). Oxford, UK: OxfordUniversity Press/Lawrence Erlbaum Associates.
71. Griffin, D. R. 1992 Animal minds. Chicago, IL: University of Chicago Press.
72. Hurford, J. R. 2007 The origins of meaning. Oxford, NY: Oxford University Press.
73. Emery, N. J., Clayton, N. & Frith, C. 2008 Social intelligence: from brain to culture. Oxford, UK: Oxford University Press.
74. Hultsch, H. & Todt, D. 2001 Developmental trajectories of complex signal systems in animals: the model of bird song. In Approaches to bootstrapping (ed. J. W. B. Hö hle), pp. 309-331. Amsterdam, Philadelphia: John Benjamin Publishing Company.
75. Kipper, S., Mundry, R., Hultsch, H. & Todt, D. 2004 Long-term persistence of song performance rules in nightingales (Luscinia megarhynchos): a longitudinal field study on repertoire size and composition. Behaviour 141, 371-390. (doi:10.1163/1568539043 22981914)
76. Hultsch, H. & Todt, D. 1989 Memorization and reproduction of songs in nightingales (Luscinia megarhynchos): evidence for package formation. J. Comp. Physiol. A 165, 197-203. (doi:10.1007/BF00619194)
77. Kroodsma, D. E. & Parker, L. D. 1977 Vocal virtuosity in brown thrasher. Auk 94, 783-785.
78. Suzuki, R., Buck, J. R. & Tyack, P. L. 2006 Information entropy of humpback whale songs. J. Acoust. Soc. Am. 119, 1849-1866. (doi:10.1121/1.2161827)
79. Zokoll, M. A., Naue, N., Herrmann, C. S. & Langemann, U. 2008 Auditory memory: a comparison between humans and starlings. Brain Res. 1220, 33-46. (doi:10.1016/j.brainres.2008.01.049)
80. Comins, J. A. & Gentner, T. Q. 2010 Working memory for patterned sequences of auditory objects in a songbird. Cognition 117, 38-53. (doi:10.1016/j.cognition. 2010.06.009)
81. Raby, C. R. & Clayton, N. S. 2010 The cognition of caching and recovery in food-storing birds. Adv. Stud. Behav. 41, 1-34. (doi:10.1016/S0065-3454(10) 41001-3)
82. Uy, J. A. C., Patricelli, G. L. & Borgia, G. 2000 Dynamic mate-searching tactic allows female satin bowerbirds Ptilonorhynchus violaceus to reduce searching. Proc. R. Soc. Lond. B 267, 251-256. (doi:10. 1098/rspb.2000.0994)
83. Ouattara, K., Lemasson, A. & Zuberbü hler, K. 2009 Campbell's monkeys use affixation to alter call meaning. PLoS ONE 4, e7808. (doi:10.1371/journal.pone. 0007808)
84. Fitch, W.T. 2009 The biology and evolution of language: 'deep homology' and the evolution of innovation. In The cognitive neurosciences (ed. M. S. Gazzaniga), 4th edn, pp. 873-883. Cambridge, MA: MIT Press.
85. Frisch, K. v. 1967 The dance language and orientation of bees. Cambridge, MA: Belknap Press of Harvard University Press.
86. Rendall, D., Owren, M. J. & Ryan, M. J. 2009 What do animal signals mean? Anim. Behav. 78, 233-240. (doi:10.1016/j.anbehav.2009.06.007)
87. Slobodchikoff, C. N., Paseka, A. & Verdolin, J. L. 2009 Prairie dog alarm calls encode labels about predator colors. Anim. Cogn. 12, 435-439. (doi:10.1007/ s10071-008-0203-y)
88. Sevcik, R. A. & Savagerumbaugh, E. S. 1994 Language comprehension and use by great apes. Lang. Commun. 14, 37-58. (doi:10.1016/0271-5309(94)90019-1)
89. Taglialatela, J. P., Savage-Rumbaugh, S. & Baker, L. A. 2003 Vocal production by a language-competent Pan paniscus. Int. J. Primatol. 24, 1-17. (doi:10.1023/ A:1021487710547)
90. Bickerton, D. 2010 On two incompatible theories of language evolution. In The evolution of human language: biolinguistic perspectives (eds R. Larson, V. De ́prez & H. Yamakido), pp. 199-269. Cambridge, UK: Cambridge University Press.
91. Osvath, M., Raby, C. R. & Clayton, N. S. 2010 What should be compared in comparative mental time travel? Trends Cogn. Sci. 14, 51-52. (doi:10.1016/j. tics.2009.11.007)
92. Raby, C. R. & Clayton, N. S. 2009 Prospective cognition in animals. Behav. Process. 80, 314-324. (doi:10. 1016/j.beproc.2008.12.005)
93. Roberts, W. A. & Feeney, M. C. 2009 The comparative study of mental time travel. Trends Cogn. Sci. 13, 271-277. (doi:10.1016/j.tics.2009.03.003)
94. Yip, M. J. 2006 The search for phonology in other species. Trends Cogn. Sci. 10, 442-446. (doi:10.1016/j. tics.2006.08.001)
95. van Heijningen, C. A. A., de Visser, J., Zuidema, W. & Ten Cate, C. 2009 Simple rules can explain discrimination of putative recursive syntactic structures by a songbird species. Proc. Natl Acad. Sci. USA 106, 20 538-20 543. (doi:10.1073/pnas.0908113106)
96. Ohms, V. R., Gill, A., Van Heijningen, C. A. A., Beckers, G. J. L. & Ten Cate, C. 2010 Zebra finches exhibit speaker-independent phonetic perception of human speech. Proc. R. Soc. B 277, 1003-1009. (doi:10. 1098/rspb.2009.1788)
97. Fernald, R. D. 2006 Casting a genetic light on the evolution of eyes. Science 313, 1914-1918. (doi:10.1126/ science.1127889)
98. Mü ller, U. 2006 Memory: cellular and molecular networks. Cell. Mol. Life Sci. 63, 961-962. (doi:10.1007/ s00018-006-6021-y)
99. Knö rnschild, M., Glöckner, V. & Helversen, O. v. 2010 The vocal repertoire of two sympatric species of nectarfeeding bats (Glossophaga soricina and G. commissarisi). Acta Chiropterol. 12, 205-215. (doi:10.3161/15081101 0X504707)
100. Toth, A. L. & Robinson, G. E. 2007 Evo-devo and the evolution of social behavior. Trends Genet. 23, 334-341. (doi:10.1016/j.tig.2007.05.001)
101. Goodson, J. L. & Kabelik, D. 2009 Dynamic limbic networks and social diversity in vertebrates: from neural context to neuromodulatory patterning. Front. Neuroendocrinol. 30, 429-441. (doi:10.1016/j.yfrne. 2009.05.007)
102. Lai, C. S., Fisher, S. E., Hurst, J. A., Vargha-Khadem, F. & Monaco, A. P. 2001 A forkhead-domain gene is mutated in a severe speech and language disorder. Nature 413, 519-523. (doi:10.1038/35097076)
103. Hurst, J. A., Baraitser, M., Auger, E., Graham, F. & Norell, S. 1990 An extended family with a dominantly inherited speech disorder. Dev. Med. Child. Neurol. 32, 352-355. (doi:10.1111/j.1469-8749.1990. tb16948.x)
104. Stackhouse, J. 1992 Developmental verbal dyspraxia. I: a review and critique. Eur. J. Disord. Commun. 27, 19-34. (doi:10.3109/13682829209012027)
105. Sanger, T. D., Chen, D., Delgado, M. R., Gaebler- Spira, D., Hallett, M. & Mink, J. W. 2006 Definitionand classification of negative motor signs in childhood. Pediatrics 118, 2159-2167. (doi:10.1542/peds. 2005-3016)
106. Enard, W., Przeworski, M., Fisher, S. E., Lai, C. S., Wiebe, V., Kitano, T., Monaco, A. P. & Pääbo, S. 2002 Molecular evolution of FOXP2, a gene involved in speech and language. Nature 418, 869-872. (doi:10.1038/nature01025)
107. Yu, F., Keinan, A., Chen, H., Ferland, R. J., Hill, R. S., Mignault, A. A., Walsh, C. A. & Reich, D. 2009 Detecting natural selection by empirical comparison to random regions of the genome. Hum. Mol. Genet. 18, 4853-4867. (doi:10.1093/hmg/ddp457)
108. MacDermot, K. D. et al. 2005 Identification of FOXP2 truncation as a novel cause of developmental speech and language deficits. Am. J. Hum. Genet. 76, 1074-1080. (doi:10.1086/430841)
109. Fisher, S. E. & Scharff, C. 2009 FOXP2 as a molecular window into speech and language. Trends Genet. 25, 166-177. (doi:10.1016/j.tig.2009.03.002)
110. White, S. A. 2009 Genes and vocal learning. Brain Lang. 115, 21-28. (doi:10.1016/j.bandl.2009. 10.002)
111. Carroll, S. B. 2005 Evolution at two levels: on genes and form. PLoS Biol. 3, 1159-1166. (doi:10.1371/ journal.pbio.0030245)
112. Shu, W., Yang, H., Zhang, L., Lu, M. M. & Morrisey, E. E. 2001 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, 27 488-27 497. (doi:10.1074/jbc. M100636200)
113. Vernes, S. C., Spiteri, E., Nicod, J., Groszer, M., Taylor, J. M., Davies, K. E., Geschwind, D. & Fisher, S. 2007 High-throughput analysis of promoter occupancy reveals direct neural targets of FOXP2, a gene mutated in speech and language disorders. Am. J. Hum. Genet. 81, 1232-1250. (doi:10.1086/522238)
114. Wang, B., Lin, D., Li, C. & Tucker, P. 2003 Multiple domains define the expression and regulatory properties of Foxp1 forkhead transcriptional repressors. J. Biol. Chem. 278, 24 259-24 268. (doi:10.1074/jbc. M207174200)
115. Li, S., Weidenfeld, J. & Morrisey, E. E. 2004 Transcriptional and DNA binding activity of the Foxp1/2/4 family is modulated by heterotypic and homotypic protein interactions. Mol. Cell. Biol. 24, 809-822. (doi:10.1128/MCB.24.2.809-822.2004)
116. Shao, J. & Diamond, M. I. 2007 Polyglutamine diseases: emerging concepts in pathogenesis and therapy. Hum. Mol. Genet. 16, R115-R123. (doi:10.1093/hmg/ ddm213)
117. Spiteri, E. et al. 2007 Identification of the transcriptional targets of FOXP2, a gene linked to speech and language, in developing human brain. Am. J. Hum. Genet. 81, 1144-1157. (doi:10.1086/522237)
118. Caceres, M., Lachuer, J., Zapala, M. A., Redmond, J. C., Kudo, L., Geschwind, D. H., Lockhart, D. J., Preuss, T. M. & Barlow, C. 2003 Elevated gene expression levels distinguish human from non-human primate brains. Proc. Natl Acad. Sci. USA 100, 13 030-13 035. (doi:10.1073/pnas.2135499100)
119. Konopka, G. et al. 2009 Human-specific transcriptional regulation of CNS development genes by FOXP2. Nature 462, 213-217. (doi:10.1038/nature08549)
120. Vernes, S. C. et al. 2008 A functional genetic link between distinct developmental language disorders. N. Engl. J. Med. 359, 2337-2345. (doi:10.1056/ NEJMoa0802828)
121. Panaitof, S. C., Abrahams, B. S., Dong, H., Geschwind, D. H. & White, S. A. 2010 Languagerelated Cntnap2 gene is differentially expressed in sexually dimorphic song nuclei essential for vocal learning in songbirds. J. Comp. Neurol. 518, 1995-2018. (doi:10.1002/cne.22318)
122. Carroll, S. B. 2003 Genetics and the making of Homo sapiens. Nature 422, 849-857. (doi:10.1038/ nature01495)
123. Bonkowsky, J. L., Wang, X., Fujimoto, E., Lee, J. E., Chien, C. B. & Dorsky, R. I. 2008 Domain-specific regulation of foxP2 CNS expression by lef1. BMC Dev. Biol. 8, 103. (doi:10.1186/1471-213X-8-103)
124. Soderstrom, K. & Luo, B. 2009 Late-postnatal cannabinoid exposure persistently increases FoxP2 expression within zebra finch striatum. Dev. Neurobiol. 70, 195-203. (doi:10.1002/dneu.20772)
125. Lai, C. S., Gerrelli, D., Monaco, A. P., Fisher, S. E. & Copp, A. J. 2003 FOXP2 expression during brain development coincides with adult sites of pathology in a severe speech and language disorder. Brain 126, 2455-2462. (doi:10.1093/brain/awg247)
126. Takahashi, K., Liu, F. C., Hirokawa, K. & Takahashi, H. 2003 Expression of Foxp2, a gene involved in speech and language, in the developing and adult striatum. J. Neurosci. Res. 73, 61-72. (doi:10.1002/jnr. 10638)
127. Teramitsu, I., Kudo, L. C., London, S. E., Geschwind, D. H. & White, S. A. 2004 Parallel FoxP1 and FoxP2 expression in songbird and human brain predicts functional interaction. J. Neurosci. 24, 3152-3163. (doi:10. 1523/JNEUROSCI.5589-03.2004)
128. Ferland, R. J., Cherry, T. J., Preware, P. O., Morrisey, E. E. & Walsh, C. A. 2003 Characterization of Foxp2 and Foxp1 mRNA and protein in the developing and mature brain. J. Comp. Neurol. 460, 266-279. (doi:10. 1002/cne.10654)
129. Hisaoka, T., Nakamura, Y., Senba, E. & Morikawa, Y. 2010 The forkhead transcription factors, Foxp1 and Foxp2, identify different subpopulations of projection neurons in the mouse cerebral cortex. Neuroscience 166, 551-563. (doi:10.1016/j.neuroscience.2009.12.055)
130. Shu, W. et al. 2005 Altered ultrasonic vocalization in mice with a disruption in the Foxp2 gene. Proc. Natl Acad. Sci. USA 102, 9643-9648. (doi:10.1073/pnas. 0503739102)
131. French, C. A., Groszer, M., Preece, C., Coupe, A. M., Rajewsky, K. & Fisher, S. E. 2007 Generation of mice with a conditional Foxp2 null allele. Genesis 45, 440-446. (doi:10.1002/dvg.20305)
132. Groszer, M. et al. 2008 Impaired synaptic plasticity and motor learning in mice with a point mutation implicated in human speech deficits. Curr. Biol. 18, 354-362. (doi:10.1016/j.cub.2008.01.060)
133. Fujita, E., Tanabe, Y., Shiota, A., Ueda, M., Suwa, K., Momoi, M. Y. & Momoi, T. 2008 Ultrasonic vocalization impairment of Foxp2 (R552H) knockin mice related to speech-language disorder and abnormality of Purkinje cells. Proc. Natl Acad. Sci. USA 105, 3117-3122. (doi:10.1073/pnas.0712298105)
134. Enard, W. et al. 2009 A humanized version of Foxp2 affects cortico-basal ganglia circuits in mice. Cell 137,961-971. (doi:10.1016/j.cell.2009.03.041)
135. Horng, S., Kreiman, G., Ellsworth, C., Page, D., Blank, M., Millen, K. & Sur, M. 2009 Differential gene expression in the developing lateral geniculate nucleus and medial geniculate nucleus reveals novel roles for Zic4 and Foxp2 in visual and auditory pathwaydevelopment. J. Neurosci. 29, 13 672-13 683. (doi:10.1523/JNEUROSCI.2127-09.2009)
136. Haesler, S., Wada, K., Nshdejan, A., Morrisey, E. E., Lints, T., Jarvis, E. D. & Scharff, C. 2004 FoxP2 expression in avian vocal learners and non-learners. J. Neurosci. 24, 3164-3175. (doi:10.1523/JNEUR OSCI.4369-03.2004)
137. Rochefort, C., He, X., Scotto-Lomassese, S. & Scharff, C. 2007 Recruitment of FoxP2-expressing neurons to Area X varies during song development. Dev. Neurobiol. 67, 809-817. (doi:10.1002/dneu.20393)
138. Teramitsu, I., Poopatanapong, A., Torrisi, S. & White, S. A. 2010 Striatal FoxP2 is actively regulated during songbird sensorimotor learning. PLoS ONE 5, e8548. (doi:10.1371/journal.pone.0008548)
139. Haesler, S., Rochefort, C., Georgi, B., Licznerski, P., Osten, P. & Scharff, C. 2007 Incomplete and inaccurate vocal imitation after knockdown of FoxP2 in songbird basal ganglia nucleus Area X. PLoS Biol. 5, e321. (doi:10.1371/journal.pbio.0050321)
140. Shah, R., Medina-Martinez, O., Chu, L.F., Samaco, R.C. & Jamrich, M. 2006 Expression of FoxP2 during zebrafish development and in the adult brain. Int. J. Dev. Biol. 50, 435-438. (doi:10.1387/ijdb.052065rs)
141. Takahashi, K., Liu, F. C., Oishi, T., Mori, T., Higo, N., Hayashi, M., Hirokawa, K. & Takahashi, H. 2008 Expression of FOXP2 in the developing monkey forebrain: comparison with the expression of the genes FOXP1, PBX3, and MEIS2. J. Comp. Neurol. 509, 180-189. (doi:10.1002/cne.21740)
142. Itakura, T. et al. 2008 The medaka FoxP2, a homologue of human language gene FOXP2, has a diverged structure and function. J. Biochem. 143, 407-416. (doi:10. 1093/jb/mvm235)
143. Bonkowsky, J. L. & Chien, C. B. 2005 Molecular cloning and developmental expression of foxP2 in zebrafish. Dev. Dyn. 234, 740-746. (doi:10.1002/dvdy. 20504)
144. Schön, C., Wochnik, A., Rossner, A., Donow, C. & Knochel, W. 2006 The FoxP subclass in Xenopus laevis development. Dev. Genes Evol. 216, 641-646. (doi:10.1007/s00427-006-0073-8)
145. Watkins, K. E., Dronkers, N. F. & Vargha-Khadem, F. 2002 Behavioural analysis of an inherited speech and language disorder: comparison with acquired aphasia. Brain 125, 452-464. (doi:10.1093/brain/awf058)
146. Alcock, K. J., Passingham, R. E., Watkins, K. & Vargha- Khadem, F. 2000 Pitch and timing abilities in inherited speech and language impairment. Brain Lang. 75, 34-46. (doi:10.1006/brln.2000.2323)
147. Heiman, M. et al. 2008 A translational profiling approach for the molecular characterization of CNS cell types. Cell 135, 738-748. (doi:10.1016/j.cell. 2008.10.028)
148. Kurt, S., Groszer, M., Fisher, S. E. & Ehret, G. 2009 Modified sound-evoked brainstem potentials in Foxp2 mutant mice. Brain Res. 1289, 30-36. (doi:10.1016/j. brainres.2009.06.092)
149. Teramitsu, I. & White, S. A. 2006 FoxP2 regulation during undirected singing in adult songbirds. J. Neurosci. 26, 7390-7394. (doi:10.1523/JNEUR OSCI.1662- 06.2006)
150. Miller, J.E., Spiteri, E., Condro, M.C., Dosumu-Johnson, R. T., Geschwind, D. H. & White, S. A. 2008 Birdsong decreases protein levels of FoxP2, a molecule required for human speech. J. Neurophysiol. 100, 2015-2025. (doi:10.1152/jn.90415.2008)
151. Gerfen, C. R. 1992 The neostriatal mosaic: multiple levels of compartmental organization. Trends Neurosci. 15, 133-139. (doi:10.1016/0166-2236(92)90355-C)
152. Jacobson, G. A., Rokni, D. & Yarom, Y. 2008 A model of the olivo-cerebellar system as a temporal pattern generator. Trends Neurosci. 31, 617-625. (doi:10.1016/ j.tins.2008.09.005)
153. Meck, W. H., Penney, T. B. & Pouthas, V. 2008 Cortico-striatal representation of time in animals and humans. Curr. Opin. Neurobiol. 18, 145-152. (doi:10. 1016/j.conb.2008.08.002)
154. Scharff, C. & Nottebohm, F. 1991 A comparative study of the behavioral deficits following lesions of various parts of the zebra finch song system: implications for vocal learning. J. Neurosci. 11, 2896-2913.
155. Sohrabji, F., Nordeen, E. J. & Nordeen, K. W. 1990 Selective impairment of song learning following lesions of a forebrain nucleus in the juvenile zebra finch. Behav. Neural. Biol. 53, 51-63. (doi:10.1016/0163-1047(90) 90797-A)
156. Kao, M. H., Doupe, A. J. & Brainard, M. S. 2005 Contributions of an avian basal ganglia-forebrain circuit to real-time modulation of song. Nature 433, 638-643. (doi:10.1038/nature03127)
157. Kobayashi, K., Uno, H. & Okanoya, K. 2001 Partial lesions in the anterior forebrain pathway affect song production in adult Bengalese finches. Neuroreport 12, 353-358. (doi:10.1097/00001756-200102120-00034)
158. Lombardino, A. J., Hertel, M., Li, X. C., Haripal, B., Martin-Harris, L., Pariser, E. & Nottebohm, F. 2006 Expression profiling of intermingled long-range projection neurons harvested by laser capture microdissection. J. Neurosci. Methods 157, 195-207. (doi:10. 1016/j.jneumeth.2006.04.026)
159. Miller, J. E., Hilliard, A. T. & White, S. A. 2010 Song practice promotes acute vocal variability at a key stage of sensorimotor learning. PLoS ONE 5, e8592. (doi:10.1371/journal.pone.0008592)
160. Deregnaucourt, S., Mitra, P. P., Feher, O., Pytte, C. & Tchernichovski, O. 2005 How sleep affects the developmental learning of bird song. Nature 433, 710-716. (doi:10.1038/nature03275)
161. Wada, K. et al. 2006 A molecular neuroethological approach for identifying and characterizing a cascade of behaviorally regulated genes. Proc. Natl Acad. Sci. USA 103, 15 212-15 217. (doi:10.1073/ pnas.0607098103)
162. Marco, E. J., Abidi, F. E., Bristow, J., Dean, W. B., Cotter, P., Jeremy, R. J., Schwartz, C. E. & Sherr, E. H. 2008 ARHGEF9 disruption in a female patient is associated with X linked mental retardation and sensory hyperarousal. J. Med. Genet. 45, 100-105. (doi:10. 1136/jmg.2007.052324)
163. Kalscheuer, V. M. et al. 2009 A balanced chromosomal translocation disrupting ARHGEF9 is associated with epilepsy, anxiety, aggression, and mental retardation. Hum. Mutat. 30, 61-68. (doi:10.1002/ humu.20814)
164. Hackett, S. J. et al. 2008 A phylogenomic study of birds reveals their evolutionary history. Science 320, 1763-1768. (doi:10.1126/science.1157704)
165. Jarvis, E. D. 2004 Learned birdsong and the neurobiology of human language. Ann. NY Acad. Sci. 1016, 749-777. (doi:10.1196/annals.1298.038)
166. Kroodsma, D. E. & Konishi, M. 1991 A suboscine bird (Eastern Phoebe, Sayornis phoebe) develops normal song without auditory-feedback. Anim. Behav. 42, 477-487. (doi:10.1016/S0003-3472(05)80047-8)
167. Santos, M. E., Athanasiadis, A., Leitao, A. B., Dupasquier, L. & Sucena, E. 2011 Alternative splicing and gene duplication in the evolution of the FoxP gene subfamily. Mol. Biol. Evol. 28, 237-247. (doi:10.1093/ molbev/msq182)
168. Kiya, T., Itoh, Y. & Kubo, T. 2008 Expression analysis of the FoxP homologue in the brain of the honeybee, Apis mellifera. Insect Mol. Biol. 17, 53-60. (doi:10.1111/ j.1365-2583.2008.00775.x)
169. Brembs, B. P., Pauly, D., Schade, R., Mendoza, E., Pflü ger, H.J., Scharff, C. & Tzars, T. 2010 The Drosophila Fox P gene is necessary for operant self-learning: implications for the evolutionary origin of language. In Society for neuroscience. San Diego, CA: Society for Neuroscience.
170. Vernes, S. C., Nicod, J., Elahi, F. M., Coventry, J. A., Kenny, N., Coupe, A. M., Bird, L. E., Davies, K. E. & Fisher, S. E. 2006 Functional genetic analysis of mutations implicated in a human speech and language disorder. Hum. Mol. Genet. 15, 3154-3167. (doi:10. 1093/hmg/ddl392)
171. Gaub, S., Groszer, M., Fisher, S. E. & Ehret, G. 2010 The structure of innate vocalizations in Foxp2-deficient mouse pups. Genes Brain Behav. 9, 390-401. (doi:10.1111/j.1601-183X.2010.00570.x)
172. Campbell, P., Reep, R. L., Stoll, M. L., Ophir, A. G. & Phelps, S. M. 2009 Conservation and diversity of Foxp2 expression in muroid rodents: functional implications. J. Comp. Neurol. 512, 84-100. (doi:10.1002/ cne.21881)
173. Welsh, J. P., Lang, E. J., Suglhara, I. & Llinas, R. 1995 Dynamic organization of motor control within the olivocerebellar system. Nature 374, 453-457. (doi:10. 1038/374453a0)
174. Yarom, Y. & Cohen, D. 2002 The olivocerebellar system as a generator of temporal patterns. Ann. NY Acad. Sci. 978, 122-134. (doi:10.1111/j.1749-6632. 2002.tb07561.x)
175. Farries, M. A., Meitzen, J. & Perkel, D. J. 2005 Electrophysiological properties of neurons in the basal ganglia of the domestic chick: conservation and divergence in the evolution of the avian basal ganglia. J. Neurophysiol. 94, 454-467. (doi:10.1152/jn.00539.2004)
176. Goldberg, J. H., Adler, A., Bergman, H. & Fee, M. S. 2010 Singing-related neural activity distinguishes two putative pallidal cell types in the songbird basal ganglia: comparison to the primate internal and external pallidal segments. J. Neurosci. 30, 7088-7098. (doi:10.1523/ JNEUROSCI.0168-10.2010)
177. Person, A. L., Gale, S. D., Farries, M. A. & Perkel, D. J. 2008 Organization of the songbird basal ganglia, including area X. J. Comp. Neurol. 508, 840-866. (doi:10.1002/cne.21699)
178. Schulz, S. B., Haesler, S., Scharff, C. & Rochefort, C. 2010 Knockdown of FoxP2 alters spine density in Area X of the zebra finch. Genes Brain Behav. 9, 732-740. (doi:10.1111/j.1601-183X.2010.00607.x)
179. Reimers-Kipping, S., Hevers, W., Pääbo, S. & Enard, W. 2011 Humanized Foxp2 specifically affects cortico-basal ganglia circuits. Neuroscience 175, 7584. (doi:10.1016/j.neuroscience.2010.11.042)
180. Zhang, J., Webb, D. M. & Podlaha, O. 2002 Accelerated protein evolution and origins of human-specific features: Foxp2 as an example. Genetics 162, 1825-1835.
181. Ptak, S. E., Enard, W., Wiebe, V., Hellmann, I., Krause, J., Lachmann, M. & Pääbo, S. 2009 Mol. Biol. Evol. 26, 2181-2184. (doi:10.1093/molbev/msp143)
182. Krause, J. et al. 2007 The derived FOXP2 variant of modern humans was shared with Neanderthals. Curr. Biol. 17, 1908-1912. (doi:10.1016/j.cub.2007.10.008)
183. Coop, G., Bullaughey, K., Luca, F. & Przeworski, M. 2008 The timing of selection at the human FOXP2 gene. Mol. Biol. Evol. 25, 1257-1259. (doi:10.1093/ molbev/msn091)
184. Li, G., Wang, J., Rossiter, S. J., Jones, G. & Zhang, S. 2007 Accelerated FoxP2 evolution in echolocating bats. PLoS ONE 2, e900. (doi:10.1371/journal.pone. 0000900)
185. Esser, K. H. 1994 Audio-vocal learning in a nonhuman mammal: the lesser spear-nosed bat Phyllostomus discolor. Neuroreport 5, 1718-1720. (doi:10.1097/ 00001756-199409080-00007)
186. Knö rnschild, M., Nagy, M., Metz, M., Mayer, F. & von Helversen, O. 2010 Complex vocal imitation during ontogeny in a bat. Biol. Lett. 6, 156-159. (doi:10. 1098/rsbl.2009.0685)
187. Scharff, C. & Haesler, S. 2005 An evolutionary perspective on FoxP2: strictly for the birds? Curr. Opin. Neurobiol. 15, 694-703. (doi:10.1016/j.conb. 2005.10.004)
188. Webb, D. M. & Zhang, J. 2005 FoxP2 in song-learning birds and vocal-learning mammals. J. Hered. 96, 212-216. (doi:10.1093/jhered/esi025)
189. Feenders, G., Liedvogel, M., Rivas, M., Zapka, M., Horita, H., Hara, E., Wada, K., Mouritsen, H. & Jarvis, E. D. 2008 Molecular mapping of movementassociated areas in the avian brain: a motor theory for vocal learning origin. PLoS ONE 3, e1768. (doi:10. 1371/journal.pone.0001768)