On the evolution of the serotonin transporter linked polymorphic region (5-HTTLPR) in primates

Frontiers in Human Neuroscience

Volumn , Issue NOV, 2013, Pages

  Dobson, Seth D ^a   Brent, Lauren J N ^b  

^a Dartmouth College   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Balancing selection; Group living; Humans; Macaques; Serotonin transporter gene

Indexed keywords

SEROTONIN TRANSPORTER;

ANIMAL BEHAVIOR; ARTICLE; BEHAVIOR GENETICS; COMPETITION; COMPETITIVE BEHAVIOR; GENE FREQUENCY; GENE FUNCTION; GENETIC POLYMORPHISM; GENETIC VARIABILITY; HETEROZYGOTE; HUMAN; MOLECULAR EVOLUTION; NONHUMAN; PARSIMONY ANALYSIS; PHENOTYPE; PHYLOGENY; PRIMATE; PROMOTER REGION; REPRODUCTIVE SUCCESS; SEROTONIN TRANSPORTER GENE; SEROTONINERGIC SYSTEM; TANDEM REPEAT;

EID: 84888091509     PISSN: 16625161     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnhum.2013.00588     Document Type: Article

References (67)

1. Belsky, J., Bakermans-Kranenburg, M. J., and van Ijzendoorn, M. H. (2007). For better and for worse: differential susceptibility to environmental influences. Curr. Dir. Psychol. Sci. 16, 300-304. doi: 10.1111/j.1467-8721.2007.00525.x
2. Belsky, J., Jonassaint, C., Pluess, M., Stanton, M., Brummett, B., and Williams, R. (2009). Vulnerability genes or plasticity genes. Mol. Psychiatry 14, 746-754. doi: 10.1038/mp.2009.44
3. Blomberg, S. P., and Garland, T. (2002). Tempo and mode in evolution: phylogenetic inertia, adaptation and comparative methods. J. Evol. Biol. 15, 899-910. doi: 10.1046/j.1420-9101.2002.00472.x
4. Brent, L. J. N., Heilbronner, S. R., Horvath, J. E., Gonzalez-Martinez, J., Ruiz-Lambides, A., Robinson, A. G., et al. (2013a). Genetic origins of social networks in rhesus macaques. Sci. Rep. 3:1042. doi: 10.1038/srep01042
5. Brent, L. J. N., MacLarnon, A., Platt, M. L., and Semple, S. (2013b). Seasonal changes in the structure of rhesus macaque social networks. Behav. Ecol. Sociobiol. 67, 349-359. doi: 10.1007/s00265-012-1455-8
6. Canli, T., and Lesch, K.-P. (2007). Long story short: the serotonin transporter in emotion regulation and social cognition. Nat. Neurosci. 10, 1103-1109. doi: 10.1038/nn1964
7. Caspi, A., Hariri, A. R., Holmes, A., Uher, R., and Moffitt, T. E. (2010). Genetic sensitivity to the environment: the case of the serotonin transporter gene and its implications for studying complex diseases and traits. Am. J. Psychiatry 167, 509-527. doi: 10.1176/appi.ajp.2010.09101452
8. Caspi, A., Sugden, K., Moffitt, T. E., Taylor, A., Craig, I. W., Harrington, H., et al. (2003). Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 301, 386-389. doi: 10.1126/science.1083968
9. Chakraborty, S., Chakraborty, D., Mukherjee, O., Jain, S., Ramakrishnan, U., and Sinha, A. (2010). Genetic polymorphism in the serotonin transporter promoter region and ecological success in macaques. Behav. Genet. 40, 672-679. doi: 10.1007/s10519-010-9360-2
10. Chang, S. W. C., Brent, L. J. N., Adams, G. K., Klein, J. T., Pearson, J. M., Watson, K. K., et al. (2013). Neuroethology of primate social behavior. Proc. Natl. Acad. Sci. U.S.A. 110, (Suppl. 2) 10387-10394. doi: 10.1073/pnas.1301213110
11. Chiao, J. Y., and Blizinsky, K. D. (2010). Culture-gene coevolution of individualism-collectivism and the serotonin transporter gene. Proc. R. Soc. B Biol. Sci. 277, 529-537. doi: 10.1098/rspb.2009.1650
12. Crişan, L. G., Panã, S., Vulturar, R., Heilman, R. M., Szekely, R., Drugã, B., et al. (2009). Genetic contributions of the serotonin transporter to social learning of fear and economic decision making. Soc. Cogn. Affect. Neurosci. 4, 399-408. doi: 10.1093/scan/nsp019
13. Di Fiore, A., and Rendall, D. (1994). Evolution of social-organization-a reappraisal for primates by using phylogenetic methods. Proc. Natl. Acad. Sci. U.S.A. 91, 9941-9945. doi: 10.1073/pnas.91.21.9941
14. Duncan, L. E., and Keller, M. C. (2011). A critical review of the first 10 years of candidate gene-by-environment interaction research in psychiatry. Am. J. Psychiatry 168, 1041-1049. doi: 10.1176/appi.ajp.2011.11020191
15. Flack, J. C., and de Waal, F. (2007). Context modulates signal meaning in primate communication. Proc. Natl. Acad. Sci. U.S.A. 104, 1581-1586. doi: 10.1073/pnas.0603565104
16. Flint, J., and Munafo, M. R. (2007). The endophenotype concept in psychiatric genetics. Psychol. Med. 37, 163-180. doi: 10.1017/S0033291706008750
17. Flint, J., and Munafo, M. R. (2013). Candidate and non-candidate genes in behavior genetics. Curr. Opin. Neurobiol. 23, 57-61. doi: 10.1016/j.conb.2012.07.005
18. Fredericks, C. A., Drabant, E. M., Edge, M. D., Tillie, J. M., Hallmayer, J., Ramel, W., et al. (2010). Healthy young women with serotonin transporter SS polymorphism show a pro-inflammatory bias under resting and stress conditions. Brain Behav. Immun. 24, 350-357. doi: 10.1016/j.bbi.2009.10.014
19. Gotlib, I. H., Joormann, J., Minor, K. L., and Hallmayer, J. (2008). HPA axis reactivity: a mechanism underlying the associations among 5-HTTLPR, stress, and depression. Biol. Psychiatry 63, 847-851. doi: 10.1016/j.biopsych.2007.10.008
20. Greenberg, B. D., Tolliver, T. J., Huang, S. J., Li, Q., Bengel, D., and Murphy, D. L. (1999). Genetic variation in the serotonin transporter promoter region affects serotonin uptake in human blood platelets. Am. J. Med. Genet. 88, 83-87. doi: 10.1002/(SICI)1096-8628(19990205)88:1<83::AID-AJMG15>3.0.CO;2-0
21. Hariri, A. R., Drabant, E. M., Munoz, K. E., Kolachana, L. S., Mattay, V. S., Egan, M. F., et al. (2005). A susceptibility gene for affective disorders and the response of the human amygdala. Arch. Gen. Psychiatry 62, 146-152. doi: 10.1001/archpsyc.62.2.146
22. Hariri, A. R., Drabant, E. M., and Weinberger, D. R. (2006). Imaging genetics: perspectives from studies of genetically driven variation in serotonin function and corticolimbic affective processing. Biol. Psychiatry 59, 888-897. doi: 10.1016/j.biopsych.2005.11.005
23. Hariri, A. R., Mattay, V. S., Tessitore, A., Kolachana, B., Fera, F., Goldman, D., et al. (2002). Serotonin transporter genetic variation and the response of the human amygdala. Science297, 400-403. doi: 10.1126/science.1071829
24. Hedrick, P. W. (2009). Genetics of Populations 4th Edn., Sudbury, MA: Jones and Bartlett Publishers.
25. Heiming, R. S., Bodden, C., Jansen, F., Lewejohann, L., Kaiser, S., Lesch, K. P., et al. (2011). Living in a dangerous world decreases maternal care: a study in serotonin transporter knockout mice. Horm. Behav. 60, 397-407. doi: 10.1016/j.yhbeh.2011.07.006
26. Homberg, J. R., and Lesch, K.-P. (2011). Looking on the bright side of serotonin transporter gene variation. Biol. Psychiatry 69, 513-519. doi: 10.1016/j.biopsych.2010.09.024
27. Homberg, J. R., and van den Hove, D. L. A. (2012). The serotonin transporter gene and functional and pathological adaptation to environmental variation across the life span. Prog. Neurobiol. 99, 117-127. doi: 10.1016/j.pneurobio.2012.08.003
28. Hu, X. Z., Lipsky, R. H., Zhu, G., Akhtar, L. A., Taubman, J., Greenberg, B. D., et al. (2006). Serotonin transporter promoter gain-of-function genotypes are linked to obsessive-compulsive disorder. Am. J. Hum. Genet. 78, 815-826. doi: 10.1086/503850
29. Inoue-Murayama, M., Hibino, E., Iwatsuki, H., Inoue, E., Hong, K.-W., Nishida, T., et al. (2008). Interspecies and intraspecies variations in the serotonin transporter gene intron 3 VNTR in nonhuman primates. Primates 49, 139-142. doi: 10.1007/s10329-007-0077-7
30. Inoue-Murayama, M., Niimi, Y., Takenaka, O., Okada, K., Matsuzaki, I., Ito, S., et al. (2000). Allelic variation of the serotonin transporter gene polymorphic region in apes. Primates 41, 267-273. doi: 10.1007/BF02557596
31. Jansen, F., Heiming, R. S., Lewejohann, L., Touma, C., Palme, R., Schmitt, A., et al. (2010). Modulation of behavioural profile and stress response by 5-HTT genotype and social experience in adulthood. Behav. Brain Res. 207, 21-29. doi: 10.1016/j.bbr.2009.09.033
32. Jedema, H. P., Gianaros, P. J., Greer, P. J., Kerr, D. D., Liu, S., Higley, J. D., et al. (2010). Cognitive impact of genetic variation of the serotonin transporter in primates is associated with differences in brain morphology rather than serotonin neurotransmission. Mol. Psychiatry 15, 512-522. doi: 10.1038/mp.2009.90
33. Krawczak, M., Trefilov, A., Berard, J., Bercovitch, F., Kessler, M., Sauermann, U., et al. (2005). Male reproductive timing in rhesus macaques is influenced by the 5HTTLPR promoter polymorphism of the serotonin transporter gene. Biol. Reprod. 72, 1109-1113. doi: 10.1095/biolreprod.104.038059
34. Kudo, H., and Dunbar, R. I. M. (2001). Neocortex size and social network size in primates. Anim. Behav. 62, 711-722. doi: 10.1006/anbe.2001.1808
35. Kuhnen, C. M., and Chiao, J. Y. (2009). Genetic determinants of financial risk taking. PLoS ONE 4:e4362. doi: 10.1371/journal.pone.0004362
36. Lesch, K. P., Bengel, D., Heils, A., Sabol, S. Z., Greenberg, B. D., Petri, S., et al. (1996). Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 274, 1527-1531. doi: 10.1126/science.274.5292.1527
37. Lesch, K. P., Meyer, J., Glatz, K., Flugge, G., Hinney, A., Hebebrand, J., et al. (1997). The 5-HT transporter gene-linked polymorphic region (5-HTTLPR) in evolutionary perspective: alternative biallelic variation in rhesus monkeys. J. Neural Transm. 104, 1259-1266. doi: 10.1007/BF01294726
38. Majolo, B., Lehmann, J., Vizioli, A. D., and Schino, G. (2012). Fitness-related benefits of dominance in primates. Am. J. Phys. Anthropol. 147, 652-660. doi: 10.1002/ajpa.22031
39. McEwen, B. S. (1998). Protective and damaging effects of stress mediators. N. Engl. J. Med. 338, 171-179. doi: 10.1056/NEJM199801153380307
40. McEwen, B. S., and Seeman, T. (1999). Protective and damaging effects of mediators of stress-elaborating and testing the concepts of allostasis and allostatic load. Ann. N. Y. Acad. Sci. 896, 30-47. doi: 10.1111/j.1749-6632.1999.tb08103.x
41. McEwen, B. S., and Wingfield, J. C. (2003). The concept of allostasis in biology and biomedicine. Horm. Behav. 43, 2-15. doi: 10.1016/S0018-506X(02)00024-7
42. Molur, S., Brandon-Jones, D., Dittus, W., Eudey, A., Kumar, A., Singh, M., et al. (Eds.). (2003). Status of South Asian Primates: Conservation Assessment and Management Plan (CAMP) Workshop Report, 2003. Zoo Outreach Organisation, IUCN/SCC Conservation Breeding Specialist Group-South Asia, Coimbatore, India. viii+432pp.
43. Mueller, A., Brocke, B., Fries, E., Lesch, K. P., and Kirschbaum, C. (2010). The role of the serotonin transporter polymorphism for the endocrine stress response in newborns. Psychoneuroendocrinology 35, 289-296. doi: 10.1016/j.psyneuen.2009.07.002
44. Munafo, M. R., Brown, S. M., and Hariri, A. R. (2008). Serotonin transporter (5-HTTLPR) genotype and amygdala activation: a meta-analysis. Biol. Psychiatry 63, 852-857. doi: 10.1016/j.biopsych.2007.08.016
45. Munafo, M. R., Freimer, N. B., Ng, W., Ophoff, R., Veijola, J., Miettunen, J., et al. (2009). 5-HTTLPR genotype and anxiety-related personality traits: a meta-analysis and new data. Am. J. Med. Genet. B Neuropsychiatr. Genet. 150B, 271-281. doi: 10.1002/ajmg.b.30808
46. Murphy, S. E., Norbury, R., Godlewska, B. R., Cowen, P. J., Mannie, Z. M., Harmer, C. J., et al. (2013). The effect of the serotonin transporter polymorphism (5-HTTLPR) on amygdala function: a meta-analysis. Mol. Psychiatry 18, 512-520. doi: 10.1038/mp.2012.19
47. Nakamura, M., Ueno, S., Sano, A., and Tanabe, H. (2000). The human serotonin transporter gene linked polymorphism (5-HTTLPR) shows ten novel allelic variants. Mol. Psychiatry 5, 32-38. doi: 10.1038/sj.mp.4000698
48. Nunn, C. L., and Barton, R. A. (2001). Comparative methods for studying primate adaptation and allometry. Evol. Anthropol. 10, 81-98. doi: 10.1002/evan.1019
49. Ohira, H., Matsunaga, M., Isowa, T., Nomura, M., Ichikawa, N., Kimura, K., et al. (2009). Polymorphism of the serotonin transporter gene modulates brain and physiological responses to acute stress in Japanese men. Stress Int. J. Biol. Stress 12, 533-543. doi: 10.3109/10253890902787826
50. Pascale, E., Lucarelli, M., Passarelli, F., Butler, R. H., Tamellini, A., Addessi, E., et al. (2012). Monomorphic region of the serotonin transporter promoter gene in new world monkeys. Am. J. Primatol. 74, 1028-1034. doi: 10.1002/ajp.22056
51. Sapolsky, R. M. (2000). Stress hormones: good and bad. Neurobiol. Dis. 7, 540-542. doi: 10.1006/nbdi.2000.0350
52. Schinka, J. A., Busch, R. M., and Robichaux-Keene, N. (2004). A meta-analysis of the association between the serotonin transporter gene polymorphism (5-HTTLPR) and trait anxiety. Mol. Psychiatry 9, 197-202. doi: 10.1038/sj.mp.4001405
53. Sen, S., Burmeister, M., and Ghosh, D. (2004). Meta-analysis of the association between a serotonin transporter promoter polymorphism (5-HTTLPR) and anxiety-related personality traits. Am. J. Med. Genet. B Neuropsychiatr. Genet. 127B, 85-89. doi: 10.1002/ajmg.b.20158
54. Shattuck, M. (2011). The Molecular Evolution of the Serotonin System in Macaques (Macaca): A Detailed Survey of Four Serotonin-Related Genes. PhD thesis, Urbana-Champaign: University of Illinois.
55. Silk, J. B., Alberts, S. C., and Altmann, J. (2003). Social bonds of female baboons enhance infant survival. Science 302, 1231-1234. doi: 10.1126/science.1088580
56. Silk, J. B., Beehner, J. C., Bergman, T. J., Crockford, C., Engh, A. L., Moscovice, L. R., et al. (2010). Strong and consistent social bonds enhance the longevity of female baboons. Curr. Biol. 20, 1359-1361. doi: 10.1016/j.cub.2010.05.067
57. Silk, J. B., Kaldor, E., and Boyd, R. (2000). Cheap talk when interests conflict. Anim. Behav. 59, 423-432. doi: 10.1006/anbe.1999.1312
58. Simons, N. D., Winters, S., and Lorenz, J. G. (2011). "Comparative analysis of length polymorphisms in the promoter region of the serotonin transporter gene (SCL6A4) in Cercopithecidae, " in 34th Meeting of the American Society of Primatologists (Austin, TX).
59. Sterck, E. H. M., Watts, D. P., and vanSchaik, C. P. (1997). The evolution of female social relationships in nonhuman primates. Behav. Ecol. Sociobiol. 41, 291-309. doi: 10.1007/s002650050390
60. Suomi, S. J. (2006). Risk, resilience, and gene x environment interactions in rhesus monkeys. Resilience Child. 1094, 52-62. doi: 10.1196/annals.1376.006
61. Thierry, B. (2007). Unity in diversity: lessons from macaque societies. Evol. Anthropol. 16, 224-238. doi: 10.1002/evan.20147
62. Thierry, B., Iwaniuk, A. N., and Pellis, S. M. (2000). The influence of phylogeny on the social behaviour of macaques (Primates: cercopithecidae, genus Macaca). Ethology 106, 713-728. doi: 10.1046/j.1439-0310.2000.00583.x
63. Vallender, E. J., Lynch, L., Novak, M. A., and Miller, G. M. (2009). Polymorphisms in the 3' UTR of the serotonin transporter are associated with cognitive flexibility in rhesus macaques. Am. J. Med. Genet. B Neuropsychiatr. Genet. 150B, 467-475. doi: 10.1002/ajmg.b.30835
64. Van Schaik, C. P. (1983). Why are diurnal primates living in groups. Behaviour 87, 120-144. doi: 10.1163/156853983X00147
65. Watson, K. K., Ghodasra, J. H., and Platt, M. L. (2009). Serotonin transporter genotype modulates social reward and punishment in rhesus macaques. PLoS ONE 4:e4156. doi: 10.1371/journal.pone.0004156
66. Way, B. M., and Taylor, S. E. (2010). The serotonin transporter promoter polymorphism is associated with cortisol response to psychosocial stress. Biol. Psychiatry 67, 487-492. doi: 10.1016/j.biopsych.2009.10.021
67. Wendland, J. R., Lesch, K. P., Newman, T. K., Timme, A., Gachot-Neveu, H., Thierry, B., et al. (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, 163-172. doi: 10.1007/s10519-005-9017-8