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Molecular Behavioral Research in Great Apes

  • Miho Inoue-Murayama
  • Alexander Weiss
  • Naruki Morimura
  • Masayuki Tanaka
  • Juichi Yamagiwa
  • Gen’ichi Idani
Part of the Primatology Monographs book series (PrimMono)

Abstract

Since the initial reports linking human “novelty seeking” to the dopamine receptor D4 (DRD4) locus (Benjamin et al. 1996), there have been multiple studies examining associations between human personality traits and specific genotypes of ­neurotransmitter-related proteins (Ebstein 2006) (see Chap. 10). Recently, research on the genetic bases of personality traits has been extended to studies of within- and between-species studies of nonhuman primates. Personality is defined as those characteristics of individuals that describe and account for temporally stable patterns of affect, cognition, and behavior. As is the case in humans, these individual differences have a biological and experiential basis (Gosling 2008).

Keywords

Androgen Receptor Nonhuman Primate Rhesus Macaque Human Personality Japanese Macaque 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We are indebted to the late Professor O. Takenaka, Kyoto University, for providing samples. We are grateful to T. Matsuzawa, T. Udono, T. Ochiai, S. Hirata, and the raters at Ueno Zoo, Higashiyama Zoo, Fukuoka Zoo, Wanpark Kochi Animal Land, Hiroshima City Asa Zoological Park, Kyoto Municipal Zoo, Tama Zoological Park, Itouzu no Mori Zoological Park, Japan Monkey Centre, Ikeda Zoo, Kyoto University Primate Research Institute, Great Ape Research Institute, and Chimpanzee Sanctuary Uto. We also thank S. Kawamura, E. Inoue, Y. Murayama and M.J. Adams for their invaluable comments to the manuscript. This study was supported financially in part by the Ministry of Education, Culture, Sports, Science, and Technology (MEXT) with a Grant-in-aid for Science Research (B: #18310152 and #21310150 to M.I.M.) and the Global Center of Excellence Program “Formation of a Strategic Base for Biodiversity and Evolutionary Research: from Genome to Ecosystem”, and the Cooperation Research Program of the Primate Research Institute, Kyoto University.

References

  1. Alia-Klein N, Goldstein RZ, Kriplani A, Logan J, Tomasi D, Williams B, Telang F, Shumay E, Biegon A, Craig IW, Henn F, Wang GJ, Volkow ND, Fowler JS (2008) Brain monoamine oxidase A activity predicts trait aggression. J Neurosci 28:5099–5104PubMedCrossRefGoogle Scholar
  2. Anestis SF, Bribiescas RG, Hasselschwert DL (2006) Age, rank, and personality effects on the cortisol sedation stress response in young chimpanzees. Physiol Behav 89:287–294PubMedCrossRefGoogle Scholar
  3. Bailey JN, Breidenthal SE, Jorgensen MJ, McCracken JT, Fairbanks LA (2007) The association of DRD4 and novelty seeking is found in a nonhuman primate model. Psychiatr Genet 17:23–27PubMedCrossRefGoogle Scholar
  4. Barr CS, Newman TK, Becker ML, Parker CC, Champoux M, Lesch KP, Goldman D, Suomi SJ, Higley JD (2003) The utility of the non-human primate; model for studying gene by environment interactions in behavioral research. Genes Brain Behav 2:336–340PubMedCrossRefGoogle Scholar
  5. Barr CS, Schwandt ML, Newman TK, Higley JD (2004) The use of adolescent nonhuman primates to model human alcohol intake: neurobiological, genetic, and psychological variables. Ann N Y Acad Sci 1021:221–233PubMedCrossRefGoogle Scholar
  6. Benjamin J, Li L, Patterson C, Greenberg BD, Murphy DL, Hamer DH (1996) Population and familial association between the D4 dopamine receptor gene and measures of novelty seeking. Nat Genet 12:81–84PubMedCrossRefGoogle Scholar
  7. Cantor N, Sanderson CA (1999) Life task participation and wellbeing: the importance of taking part in daily life. In: Kahneman D, Diener E, Schwarz N (eds) Well-being: the foundations of hedonic psychology. Russell Sage Foundation, New York, pp 425–451Google Scholar
  8. Capitanio JP, Mendoza SP, Baroncelli S (1999) The relationship of personality dimensions in adult male rhesus macaques to progression of simian immunodeficiency virus disease. Brain Behav Immun 13:138–154PubMedCrossRefGoogle Scholar
  9. Capitanio JP, Abel K, Mendoza SP, Blozis SA, McChesney MB, Cole SW, Mason WA (2008) Personality and serotonin transporter genotype interact with social context to affect immunity and viral set-point in simian immunodeficiency virus disease. Brain Behav Immun 22:676–689PubMedCrossRefGoogle Scholar
  10. Caspi A, Sugden K, Moffitt TE, Taylor A, Craig IW, Harrington H, McClay J, Mill J, Martin J, Braithwaite A, Poulton R (2003) Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 301:386–389PubMedCrossRefGoogle Scholar
  11. Catalano M, Nobile M, Novelli E, Nöthen MM, Smeraldi E (1993) Distribution of a novel mutation in the first exon of the human dopamine D4 receptor gene in psychotic patients. Biol Psychiatry 34:459–464PubMedCrossRefGoogle Scholar
  12. Comings DE, Chen C, Wu S, Muhleman D (1999a) Association of the androgen receptor gene (AR) with ADHD and conduct disorder. Neuroreport 10:1589–1592PubMedCrossRefGoogle Scholar
  13. Comings DE, Muhleman D, Johnson P, MacMurray JP (1999b) Potential role of the estrogen receptor gene (ESR1) in anxiety. Mol Psychiatry 4:374–377PubMedCrossRefGoogle Scholar
  14. Danese S, Sans M, Fiocchi C (2004) Inflammatory bowel disease: the role of environmental factors. Autoimmun Rev 3:394–400PubMedCrossRefGoogle Scholar
  15. Deary IJ, Johnson W, Houlihan LM (2009) Genetic foundations of human intelligence. Hum Genet 126:215–232PubMedCrossRefGoogle Scholar
  16. Diener E, Emmons RA (1984) The independence of positive and negative affect. J Pers Soc Psychol 47:1105–1117PubMedCrossRefGoogle Scholar
  17. D’Souza UM, Craig IW (2008) Functional genetic polymorphisms in serotonin and dopamine gene systems and their significance in behavioural disorders. Prog Brain Res 172:73–98PubMedCrossRefGoogle Scholar
  18. Ebstein RP (2006) The molecular genetic architecture of human personality: beyond self-report questionnaires. Mol Psychiatry 11:427–445PubMedCrossRefGoogle Scholar
  19. Forsell C, Enmark E, Axelman K, Blomberg M, Wahlund LO, Gustafsson JA, Lannfelt L (2001) Investigations of a CA repeat in the oestrogen receptor beta gene in patients with Alzheimer’s disease. Eur J Hum Genet 9:802–804PubMedCrossRefGoogle Scholar
  20. Furlong RA, Ho L, Rubinsztein JS, Walsh C, Paykel ES, Rubinsztein DC (1999) Analysis of the monoamine oxidase A (MAOA) gene in bipolar affective disorder by association studies, meta-analyses, and sequencing of the promoter. Am J Med Genet 88:398–406PubMedCrossRefGoogle Scholar
  21. Goldberg LR (1990) An alternative “description of personality”: the Big-Five factor structure. J Pers Soc Psychol 59:1216–1229PubMedCrossRefGoogle Scholar
  22. Gosling SD (2008) Personality in non-human animals. Soc Personal Psychol Compass 2(2):985–1001CrossRefGoogle Scholar
  23. Heinz A, Higley JD, Gorey JG, Saunders RC, Jones DW, Hommer D, Zajicek K, Suomi SJ, Lesch KP, Weinberger DR, Linnoila M (1998) In vivo association between alcohol intoxication, aggression, and serotonin transporter availability in nonhuman primates. Am J Psychiatry 155:1023–1028PubMedGoogle Scholar
  24. Hohoff C (2009) Anxiety in mice and men: a comparison. J Neural Transm 116:679–687PubMedCrossRefGoogle Scholar
  25. Hong KW, Hibino E, Takenaka O, Hayasaka I, Murayama Y, Ito S, Inoue-Murayama M (2006) Comparison of androgen receptor CAG and GGN repeat length polymorphism in humans and apes. Primates 47:248–254PubMedCrossRefGoogle Scholar
  26. Hong KW, Iwatsuki H, Takenaka O, Hayasaka I, Murayama Y, Ito S, Inoue-Murayama M (2007a) Comparative analysis of estrogen receptor gene polymorphisms in apes. Primates 48:151–155PubMedCrossRefGoogle Scholar
  27. Hong KW, Sugawara Y, Hasegawa H, Hayasaka I, Hashimoto R, Ito S, Inoue-Murayama M (2007b) A new gain-of-function allele in chimpanzee tryptophan hydroxylase 2 and the comparison of its enzyme activity. Neurosci Lett 412:195–200PubMedCrossRefGoogle Scholar
  28. Hong KW, Hayasaka I, Murayama Y, Ito S, Inoue-Murayama M (2008) Comparative analysis of monoamine oxidase intronic polymorphisms in primates. Gene 418:9–14PubMedCrossRefGoogle Scholar
  29. Hong KW, Matsukawa R, Hirata Y, Hayasaka I, Murayama Y, Ito S, Inoue-Murayama M (2009) Allele distribution and effect on reporter gene expression of vasopressin receptor gene (AVPR1a)-linked VNTR in primates. J Neural Transm 116:535–538PubMedCrossRefGoogle Scholar
  30. Inoue-Murayama M (2009) Genetic polymorphism as a background of animal behavior (review). Anim Sci J 80:113–120PubMedCrossRefGoogle Scholar
  31. Inoue-Murayama M, Takenaka O, Murayama Y (1998) Origin and divergence of tandem repeats of primate D4 dopamine receptor genes. Primates 39:217–224CrossRefGoogle Scholar
  32. Inoue-Murayama M, Niimi Y, Takenaka O, Okada K, Matsuzaki I, Ito S, Murayama Y (2000a) Allelic variation of the serotonin transporter gene polymorphic region in apes. Primates 41:267–273CrossRefGoogle Scholar
  33. Inoue-Murayama M, Niimi Y, Takenaka O, Murayama Y (2000b) Allelic variation of the dopamine receptor D4 gene polymorphic region in gibbons. Primates 41:383–392CrossRefGoogle Scholar
  34. Inoue-Murayama M, Niimi Y, Takenaka O, Murayama Y (2001) Evolution of personality-related genes in primates. In: Miyoshi K et al (eds) Contemporary neuropsychiatry. Springer, Tokyo, pp 425–428CrossRefGoogle Scholar
  35. Inoue-Murayama M, Adachi S, Mishima N, Mitani H, Takenaka O, Terao K, Hayasaka I, Ito S, Murayama Y (2002) Variation of variable number of tandem repeat sequences in the 3′-untranslated region of primate dopamine transporter genes that affects reporter gene expression. Neurosci Lett 334:206–210PubMedCrossRefGoogle Scholar
  36. Inoue-Murayama M, Mishima N, Hayasaka I, Ito S, Murayama Y (2006) Divergence of ape and human monoamine oxidase A gene promoters: comparative analysis of polymorphisms, tandem repeat structures and transcriptional activities on reporter gene expression. Neurosci Lett 405:207–211PubMedCrossRefGoogle Scholar
  37. Inoue-Murayama M, Hibino E, Iwatsuki H, Inoue E, Hong K-W, Nishida T, Hayasaka I, Ito S, Murayama Y (2008) Interspecies and intraspecies variations in the serotonin transporter gene intron 3 VNTR in nonhuman primates. Primates 49:139–142PubMedCrossRefGoogle Scholar
  38. Inoue-Murayama M, Inoue E, Watanabe K, Takenaka A, Murayma Y (2010) Box I: behavior-related candidate genes. In: Nakagawa N, Sugiura H, Nakamichi N (eds) The Japanese macaques. Springer, Tokyo, pp 285–293Google Scholar
  39. Irbis C, Garriga R, Kabasawa A, Ushida K (2008) Phylogenetic analysis of Troglodytella abrassarti isolated from Chimpanzees (Pan troglodytes verus) in the wild and in captivity. J Gen Appl Microbiol 54:409–413PubMedCrossRefGoogle Scholar
  40. Jarrell H, Hoffman JB, Kaplan JR, Berga S, Kinkead B, Wilson ME (2008) Polymorphisms in the serotonin reuptake transporter gene modify the consequences of social status on metabolic health in female rhesus monkeys. Physiol Behav 93:807–819PubMedCrossRefGoogle Scholar
  41. King JE, Figueredo AJ (1997) The five-factor model plus dominance in chimpanzee personality. J Res Pers 31:257–271CrossRefGoogle Scholar
  42. King JE, Weiss A, Sisco MS (2008) Aping humans: age and sex effects in chimpanzee (Pan troglodytes) and human (Homo sapiens) personality. J Comp Psychol 122:418–427PubMedCrossRefGoogle Scholar
  43. Koyama T, Fujii H, Yonekawa F (1981) Comparative studies of gregariousness and social structure among seven feral Macaca fuscata groups. In: Chiarelli AB, Corruccini RS (eds) Primate behavior and sociobiology. Springer, Tokyo, pp 52–63CrossRefGoogle Scholar
  44. Kuhar CW, Stoinski TS, Lukas KE, Maple TL (2006) Gorilla behavior index revisited: age, housing and behavior. Appl Anim Behav Sci 96:315–326CrossRefGoogle Scholar
  45. Lesch KP, Bengel D, Heils A, Sabol SZ, Greenberg BD, Petri S, Benjamin J, Müller CR, Hamer DH, Murphy DL (1996) Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 274:1527–1531PubMedCrossRefGoogle Scholar
  46. Mellick GD, Buchanan DD, Silburn PA, Chan DK, Le Couteur DG, Law LK, Woo J, Pang CP (2000) The monoamine oxidase B gene GT repeat polymorphism and Parkinson’s disease in a Chinese population. J Neurol 247:52–55PubMedCrossRefGoogle Scholar
  47. Miller GM, Bendor J, Tiefenbacher S, Yang H, Novak MA, Madras BK (2004) A mu-opioid receptor single nucleotide polymorphism in rhesus monkey: association with stress response and aggression. Mol Psychiatry 9:99–108PubMedCrossRefGoogle Scholar
  48. Morimura N, Hirata S, Kurashima O, Ochiai-Ohira T (2008) Management of population and welfare of captive chimpanzees in Japan. Primate Res 24:17–24 (English abstract)CrossRefGoogle Scholar
  49. Newman TK, Syagailo YV, Barr CS, Wendland JR, Champoux M, Graessle M, Suomi SJ, Higley JD, Lesch KP (2005) Monoamine oxidase A gene promoter variation and rearing experience influences aggressive behavior in rhesus monkeys. Biol Psychiatry 57:167–172PubMedCrossRefGoogle Scholar
  50. Ochiai-Ohira T, Kurashima O, Akami R, Hasegawa T (2006) History of keeping great apes in Japan. Primate Res 22:123–126 (English abstract)CrossRefGoogle Scholar
  51. Ozer DJ, Benet-Martínez V (2006) Personality and the prediction of consequential outcomes. Annu Rev Psychol 57:401–421PubMedCrossRefGoogle Scholar
  52. Pavot W, Diener E, Colvin CR, Sandvik E (1991) Further validation of the satisfaction with life scale: evidence for the crossmethod convergence of the well-being measures. J Pers Assess 57:149–161PubMedCrossRefGoogle Scholar
  53. Rajender S, Pandu G, Sharma JD, Gandhi KP, Singh L, Thangaraj K (2008) Reduced CAG repeats length in androgen receptor gene is associated with violent criminal behavior. Int J Legal Med 122:367–372PubMedCrossRefGoogle Scholar
  54. Rogers J, Shelton SE, Shelledy W, Garcia R, Kalin NH (2008) Genetic influences on behavioral inhibition and anxiety in juvenile rhesus macaques. Genes Brain Behav 7:463–469PubMedCrossRefGoogle Scholar
  55. Rosso L, Keller L, Kaessmann H, Hammond RL (2008) Mating system and avpr1a promoter variation in primates. Biol Lett 4:375–378PubMedCrossRefGoogle Scholar
  56. Sabol SZ, Nelson ML, Fisher C, Gunzerath L, Brody CL, Hu S, Sirota LA, Marcus SE, Greenberg BD, Lucas FR 4th, Benjamin J, Murphy DL, Hamer DH (1999) A genetic association for cigarette smoking behavior. Health Psychol 18:7–13PubMedCrossRefGoogle Scholar
  57. Seaman MI, Chang FM, Quiñones AT, Kidd KK (2000) Evolution of exon 1 of the dopamine D4 receptor (DRD4) gene in primates. J Exp Zool 288:32–38PubMedCrossRefGoogle Scholar
  58. Shimada MK, Inoue-Murayama M, Ueda Y, Maejima M, Murayama Y, Takenaka O, Hayasaka I, Ito S (2004) Polymorphism in the second intron of dopamine receptor D4 gene in humans and apes. Biochem Biophys Res Commun 316:1186–1190PubMedCrossRefGoogle Scholar
  59. Spinelli S, Schwandt ML, Lindell SG, Newman TK, Heilig M, Suomi SJ, Higley JD, Goldman D, Barr CS (2007) Association between the recombinant human serotonin transporter linked promoter region polymorphism and behavior in rhesus macaques during a separation paradigm. Dev Psychopathol 19:977–987PubMedCrossRefGoogle Scholar
  60. Terracciano A, Sanna S, Uda M, Deiana B, Usala G, Busonero F, Maschio A, Scally M, Patriciu N, Chen W-M, Distel MA, Slagboom EP, Boomsma DI, Villafuerte S, Śliwerska E, Burmeister M, Amin N, Janssens ACJW, van Duijn CM, Schlessinger D, Abecasis GR, Costa PT Jr (2008) Genome-wide association scan for five major dimensions of personality. Mol Psychiatry. doi:10.1038/mp.2008.113Google Scholar
  61. Uher J, Asendorpf JB, Call J (2008) Personality in the behaviour of Great Apes: temporal stability, cross-situational consistency and coherence in response. Anim Behav 75:99–112CrossRefGoogle Scholar
  62. Vormfelde SV, Hoell I, Tzvetkov M, Jamrozinski K, Sehrt D, Brockmöller J, Leibing E (2006) Anxiety- and novelty seeking-related personality traits and serotonin transporter gene polymorphisms. J Psychiatr Res 40:568–576PubMedCrossRefGoogle Scholar
  63. Walum H, Westberg L, Henningsson S, Neiderhiser JM, Reiss D, Igl W, Ganiban JM, Spotts EL, Pedersen NL, Eriksson E, Lichtenstein P (2008) Genetic variation in the vasopressin receptor 1a gene (AVPR1A) associates with pair-bonding behavior in humans. Proc Natl Acad Sci USA 105:14153–14156PubMedCrossRefGoogle Scholar
  64. Watson KK, Ghodasra JH, Platt ML (2009) Serotonin transporter genotype modulates social reward and punishment in rhesus macaques. PLoS One 4:e4156PubMedCrossRefGoogle Scholar
  65. Weiss A, King JE, Perkins L (2006) Personality and subjective well-being in orangutans (Pongo pygmaeus and Pongo abelli). J Pers Soc Psychol 90:501–511PubMedCrossRefGoogle Scholar
  66. Weiss A, Inoue-Murayama M, Hong K-W, Inoue E, Udono T, Ochiai T, Matsuzawa T, Hirata S, King JE (2009) Assessing chimpanzee personality and subjective well-being in Japan. Am J Primatol 71:283–292PubMedCrossRefGoogle Scholar
  67. Wendland JR, Lesch KP, Newman TK, Timme A, Gachot-Neveu H, Thierry B, Suomi SJ (2006) Differential functional variability of serotonin transporter and monoamine oxidase a genes in macaque species displaying contrasting levels of aggression-related behavior. Behav Genet 36:163–172PubMedCrossRefGoogle Scholar
  68. Westberg L, Henningsson S, Landén M, Annerbrink K, Melke J, Nilsson S, Rosmond R, Holm G, Anckarsäter H, Eriksson E (2009) Influence of androgen receptor repeat polymorphisms on personality traits in men. J Psychiatry Neurosci 34:205–213PubMedGoogle Scholar
  69. Zhang X, Gainetdinov RR, Beaulieu JM, Sotnikova TD, Burch LH, Williams RB, Schwartz DA, Krishnan KR, Caron MG (2005) Loss-of-function mutation in tryptophan hydroxylase-2 identified in unipolar major depression. Neuron 45:11–16PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2011

Authors and Affiliations

  • Miho Inoue-Murayama
    • 1
  • Alexander Weiss
    • 2
  • Naruki Morimura
    • 1
  • Masayuki Tanaka
    • 1
  • Juichi Yamagiwa
    • 3
  • Gen’ichi Idani
    • 1
  1. 1.Wildlife Research Center of Kyoto UniversitySakyo-kuJapan
  2. 2.Psychology, School of Philosophy, Psychology and Language SciencesThe University of EdinburghEdinburghUK
  3. 3.Human Evolution Studies, Department of Zoology, Graduate School of ScienceKyoto UniversitySakyo-kuJapan

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