Abstract
Behavioral variation within and between populations and species of the genus Papio has been studied extensively, but little is known about the genetic causes of individual- or population-level differences. This study investigates the influence of genetic variation on personality (sometimes referred to as temperament) in baboons and identifies a candidate gene partially responsible for the variation in that phenotype. To accomplish these goals, we examined individual variation in response to both novel objects and an apparent novel social partner (using a mirror test) among pedigreed baboons (n = 578) from the Southwest National Primate Research Center. We investigated the frequency and duration of individual behaviors in response to novel objects and used multivariate factor analysis to identify trait-like dimensions of personality. Exploratory factor analysis identified two distinct dimensions of personality within this population. Factor 1 accounts for 46.8 % of the variance within the behavioral matrix, and consists primarily of behaviors related to the “boldness” of the subject. Factor 2 accounts for 18.8 % of the variation, and contains several “anxiety” like behaviors. Several specific behaviors, and the two personality factors, were significantly heritable, with the factors showing higher heritability than most individual behaviors. Subsequent analyses show that the behavioral reactions observed in the test protocol are associated with animals’ social behavior observed later in their home social groups. Finally we used linkage analysis to map quantitative trait loci for the measured phenotypes. Single nucleotide polymorphisms in a positional candidate gene (SNAP25) are associated with variation in one of the personality factors, and CSF levels of homovanillic acid and 3-methoxy-4-hydroxyphenylglycol. This study documents heritable variation in personality among baboons and suggests that sequence variation in SNAP25 may influence differences in behavior and neurochemistry in these nonhuman primates.
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References
Alberts SC, Altmann J (2001) Immigration and hybridization patterns of yellow and anubis baboons in and around Amboseli. Kenya. Am J Primatol 53(4):139–154
Almasy L, Blangero J (1998) Multipoint quantitative-trait linkage analysis in general pedigrees. Am J Hum Genet 62(5):1198–1211
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(6):336–340
Barr CS, Newman TK, Lindell S, Shannon C, Champoux M, Lesch KP, Suomi SJ, Goldman D, Higley JD (2004) Interaction between serotonin transporter gene variation and rearing condition in alcohol preference and consumption in female primates. Arch Gen Psychiatry 61(11):1146–1152
Bergman TJ, Kitchen DM (2009) Comparing responses to novel objects in wild baboons (Papio ursinus) and geladas (Theropithecus gelada). Anim Cogn 12(1):63–73
Bergman TJ, Phillips-Conroy JE, Jolly CJ (2008) Behavioral variation and reproductive success of male baboons (Papio anubis x Papio hamadryas) in a hybrid social group. Am J Primatol 70(2):136–147
Birn RM, Shackman AJ, Oler JA, Williams LE, McFarlin DR, Rogers GM, Shelton SE, Alexander AL, Pine DS, Slattery MJ, Davidson RJ, Fox AS, Kalin NH (2014) Evolutionarily conserved prefrontal-amygdalar dysfunction in early-life anxiety. Mol Psychiatry 19:915–922
Blangero J, Williams JT, Almasy L (2001) Variance component methods for detecting complex trait loci. Adv Genet 42:151–181
Brandes M, Bienvenu OJ (2006) Personality and anxiety disorders. Curr Psychiatry Rep 8(4):263–269
Briffa M, Weiss A (2010) Animal personality. Curr Biol 20(21):R912–R914
Broman KW, Murray JC, Sheffield VC, White RL, Weber JL (1998) Comprehensive human genetic maps: individual and sex-specific variation in recombination. Am J Hum Genet 63(3):861–869
Brophy K, Hawi Z, Kirley A, Fitzgerald M, Gill M (2002) Synaptosomal-associated protein 25 (SNAP-25) and attention deficit hyperactivity disorder (ADHD): evidence of linkage and association in the Irish population. Mol Psychiatry 7(8):913–917
Capitanio J (2004) Personality factors between and within species. In: Thierry B, Singh M, Kaumanns W (eds) Macaque societies: A Model for the Study of Social Organization. Cambridge University Press, Cambridge, pp 13–33
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(2):138–154
Carter AJ, Marshall HH, Heinsohn R, Cowlishaw G (2012) How not to measure boldness: novel object and antipredator responses are not the same in wild baboons. Anim Behav 84:603–609
Charpentier MJ, Fontaine MC, Cherel E, Renoult JP, Jenkins T, Benoit L, Barthes N, Alberts SC, Tung J (2012) Genetic structure in a dynamic baboon hybrid zone corroborates behavioural observations in a hybrid population. Mol Ecol 21(3):715–731
Chen GL, Novak MA, Meyer JS, Kelly BJ, Vallender EJ, Miller GM (2010) The effect of rearing experience and TPH2 genotype on HPA axis function and aggression in rhesus monkeys: a retrospective analysis. Horm Behav 57(2):184–191
Clark LA, Watson D, Mineka S (1994) Temperament, personality, and the mood and anxiety disorders. J Abnorm Psychol 103(1):103–116
Cloninger CR, Sigvardsson S, Bohman M (1988) Childhood personality predicts alcohol abuse in young adults. Alcohol Clin Exp Res 12(4):494–505
Cole SW, Kemeny ME, Fahey JL, Zack JA, Naliboff BD (2003) Psychological risk factors for HIV pathogenesis: mediation by the autonomic nervous system. Biol Psychiatry 54(12):1444–1456
Costa PT Jr, Terracciano A, McCrae RR (2001) Gender differences in personality traits across cultures: robust and surprising findings. J Pers Soc Psychol 81(2):322–331
Cox LA, Mahaney MC, Vandeberg JL, Rogers J (2006) A second-generation genetic linkage map of the baboon (Papio hamadryas) genome. Genomics 88(3):274–281
Del Giudice M, Booth T, Irwing P (2012) The distance between mars and venus: measuring global sex differences in personality. PloS one 7(1):e29265
Denollet J, Sys SU, Stroobant N, Rombouts H, Gillebert TC, Brutsaert DL (1996) Personality as independent predictor of long-term mortality in patients with coronary heart disease. Lancet 347(8999):417–421
Dyke B (1996) PEDSYS: a pedigree data management system. Tech rep 2, Population Genetics Laboratory, Department of Genetics, Southwest Foundation for Biomedical Research, San Antonio
Etain B, Dumaine A, Mathieu F, Chevalier F, Henry C, Kahn JP, Deshommes J, Bellivier F, Leboyer M, Jamain S (2010) A SNAP25 promoter variant is associated with early-onset bipolar disorder and a high expression level in brain. Mol Psychiatry 15(7):748–755
Fairbanks LA, Fontenot MB, Phillips-Conroy JE, Jolly CJ, Kaplan JR, Mann JJ (1999) CSF monoamines, age and impulsivity in wild grivet monkeys (Cercopithecus aethiops aethiops). Brain Behav Evol 53(5–6):305–312
Fairbanks LA, Newman TK, Bailey JN, Jorgensen MJ, Breidenthal SE, Ophoff RA, Comuzzie AG, Martin LJ, Rogers J (2004) Genetic contributions to social impulsivity and aggressiveness in vervet monkeys. Biol Psychiatry 55(6):642–647
Falconer DS (1981) Introduction to quantitative genetics. Longmans, London
Fawcett GL, Dettmer AM, Kay D, Raveendran M, Higley JD, Ryan ND, Cameron JL, Rogers J (2014) Quantitative genetics of response to novelty and other stimuli by infant rhesus macaques (Macaca mulatta) across three behavioral assessments. Int J Primatol 35(1):325–339
Feingold E, Brown PO, Siegmund D (1993) Gaussian models for genetic linkage analysis using complete high-resolution maps of identity by descent. Am J Hum Genet 53(1):234–251
Feng Y, Crosbie J, Wigg K, Pathare T, Ickowicz A, Schachar R, Tannock R, Roberts W, Malone M, Swanson J, Kennedy JL, Barr CL (2005) The SNAP25 gene as a susceptibility gene contributing to attention-deficit hyperactivity disorder. Mol Psychiatry 10(11):998–1005
Fox AS, Shelton SE, Oakes TR, Davidson RJ, Kalin NH (2008) Trait-like brain activity during adolescence predicts anxious temperament in primates. PLoS One 3(7):e2570
Freeman HD, Brosnan SF, Hopper LM, Lambeth SP, Schapiro SJ, Gosling SD (2013) Developing a comprehensive and comparative questionnaire for measuring personality in chimpanzees using a simultaneous top-down/bottom-up design. Am J Primatol 75(10):1042–1053
Gesquiere LR, Learn NH, Simao MC, Onyango PO, Alberts SC, Altmann J (2011) Life at the top: rank and stress in wild male baboons. Science 333(6040):357–360
Gibbs RA, Rogers J, Katze MG, Bumgarner R, Weinstock GM, Mardis ER, Remington KA, Strausberg RL, Venter JC, Wilson RK, Batzer MA, Bustamante CD, Eichler EE, Hahn MW, Hardison RC, Makova KD, Miller W, Milosavljevic A, Palermo RE, Siepel A, Sikela JM, Attaway T, Bell S, Bernard KE, Buhay CJ, Chandrabose MN, Dao M, Davis C, Delehaunty KD, Ding Y, Dinh HH, Dugan-Rocha S, Fulton LA, Gabisi RA, Garner TT, Godfrey J, Hawes AC, Hernandez J, Hines S, Holder M, Hume J, Jhangiani SN, Joshi V, Khan ZM, Kirkness EF, Cree A, Fowler RG, Lee S, Lewis LR, Li Z, Liu YS, Moore SM, Muzny D, Nazareth LV, Ngo DN, Okwuonu GO, Pai G, Parker D, Paul HA, Pfannkoch C, Pohl CS, Rogers YH, Ruiz SJ, Sabo A, Santibanez J, Schneider BW, Smith SM, Sodergren E, Svatek AF, Utterback TR, Vattathil S, Warren W, White CS, Chinwalla AT, Feng Y, Halpern AL, Hillier LW, Huang X, Minx P, Nelson JO, Pepin KH, Qin X, Sutton GG, Venter E, Walenz BP, Wallis JW, Worley KC, Yang SP, Jones SM, Marra MA, Rocchi M, Schein JE, Baertsch R, Clarke L, Csuros M, Glasscock J, Harris RA, Havlak P, Jackson AR, Jiang H, Liu Y, Messina DN, Shen Y, Song HX, Wylie T, Zhang L, Birney E, Han K, Konkel MK, Lee J, Smit AF, Ullmer B, Wang H, Xing J, Burhans R, Cheng Z, Karro JE, Ma J, Raney B, She X, Cox MJ, Demuth JP, Dumas LJ, Han SG, Hopkins J, Karimpour-Fard A, Kim YH, Pollack JR, Vinar T, Addo-Quaye C, Degenhardt J, Denby A, Hubisz MJ, Indap A, Kosiol C, Lahn BT, Lawson HA, Marklein A, Nielsen R, Vallender EJ, Clark AG, Ferguson B, Hernandez RD, Hirani K, Kehrer-Sawatzki H, Kolb J, Patil S, Pu LL, Ren Y, Smith DG, Wheeler DA, Schenck I, Ball EV, Chen R, Cooper DN, Giardine B, Hsu F, Kent WJ, Lesk A, Nelson DL, O’Brien WE, Prufer K, Stenson PD, Wallace JC, Ke H, Liu XM, Wang P, Xiang AP, Yang F, Barber GP, Haussler D, Karolchik D, Kern AD, Kuhn RM, Smith KE, Zwieg AS (2007) Evolutionary and biomedical insights from the rhesus macaque genome. Science 316(5822):222–234
Gosling SD (2001) From mice to men: what can we learn about personality from animal research? Psychol Bull 127(1):45–86
Henzi SP, Barrett L (2003) Evolutionary ecology, sexual conflict and behavioral differentiation among baboon populations. Evol Anthropol 12:217–230
Hess EJ, Jinnah HA, Kozak CA, Wilson MC (1992) Spontaneous locomotor hyperactivity in a mouse mutant with a deletion including the Snap gene on chromosome 2. J Neurosci 12(7):2865–2874
Hirschfeld RM, Klerman GL, Lavori P, Keller MB, Griffith P, Coryell W (1989) Premorbid personality assessments of first onset of major depression. Arch Gen Psychiatry 46(4):345–350
Hodel A (1998) Snap-25. Int J Biochem Cell Biol 30(10):1069–1073
Hong KW, Weiss A, Morimura N, Udono T, Hayasaka I, Humle T, Murayama Y, Ito S, Inoue-Murayama M (2011) Polymorphism of the tryptophan hydroxylase 2 (TPH2) gene is associated with chimpanzee neuroticism. PLoS ONE 6(7):e22144
Hopkins WD, Donaldson ZR, Young LJ (2012) A polymorphic indel containing the RS3 microsatellite in the 5′ flanking region of the vasopressin V1a receptor gene is associated with chimpanzee (Pan troglodytes) personality. Genes Brain Behav 11(5):552–558
Hopkins WD, Russell JL, Schaeffer J (2014) Chimpanzee intelligence is heritable. Curr Biol 24(14):1649–1652
Hopper LM, Price SA, Freeman HD, Lambeth SP, Schapiro SJ, Kendal RL (2014) Influence of personality, age, sex, and estrous state on chimpanzee problem-solving success. Anim Cogn 17(4):835–847
Jolly CJ (1993) Species, subspecies and baboon systematics. In: Kimbel WH, Martin LB (eds) Species, species concepts and primate evolution. Plenum Press, New York, pp 67–107
Jolly CJ (2001) A proper study for mankind: analogies from the Papionin monkeys and their implications for human evolution. Am J Phys Anthropol 33:177–204
Jolly CJ, Burrell AS, Phillips-Conroy JE, Bergey C, Rogers J (2011) Kinda baboons (Papio kindae) and grayfoot chacma baboons (P. ursinus griseipes) hybridize in the Kafue river valley, Zambia. Am J Primatol 73(3):291–303
Kalin NH, Shelton SE (2003) Nonhuman primate models to study anxiety, emotion regulation, and psychopathology. Ann N Y Acad Sci 1008:189–200
Keller C, Roos C, Groeneveld LF, Fischer J, Zinner D (2010) Introgressive hybridization in southern African baboons shapes patterns of mtDNA variation. Am J Phys Anthropol 142(1):125–136
Kendler KS, Neale MC, Kessler RC, Heath AC, Eaves LJ (1993) A longitudinal twin study of personality and major depression in women. Arch Gen Psychiatry 50(11):853–862
King JE, Weiss A, Susco MM (2008) Aping humans: age and sex effects in chimpanzee (Pan troglodytes) and human (Homo sapiens) personality. J Comp Psychol 122:418–427
Kinnally EL, Whiteman HJ, Mason WA, Mendoza SP, Capitanio JP (2008) Dimensions of response to novelty are associated with social engagement and aggression in adult male rhesus macaques (Macaca mulatta). J Comp Psychol 122(2):195–203
Kong A, Gudbjartsson DF, Sainz J, Jonsdottir GM, Gudjonsson SA, Richardsson B, Sigurdardottir S, Barnard J, Hallbeck B, Masson G, Shlien A, Palsson ST, Frigge ML, Thorgeirsson TE, Gulcher JR, Stefansson K (2002) A high-resolution recombination map of the human genome. Nat Genet 31(3):241–247
Levchenko A, Provost S, Montplaisir JY, Xiong L, St-Onge J, Thibodeau P, Riviere JB, Desautels A, Turecki G, Dube MP, Rouleau GA (2006) A novel autosomal dominant restless legs syndrome locus maps to chromosome 20p13. Neurology 67(5):900–901
Matise TC, Perlin M, Chakravarti A (1994) Automated construction of genetic linkage maps using an expert system (MultiMap): a human genome linkage map. Nat Genet 6(4):384–390
Morton FB, Lee PC, Buchanan-Smith HM, Brosnan SF, Thierry B, Paukner A, de Waal FB, Widness J, Essler JL, Weiss A (2013) Personality structure in brown capuchin monkeys (Sapajus apella): comparisons with chimpanzees (Pan troglodytes), orangutans (Pongo spp.), and rhesus macaques (Macaca mulatta). J Comp Psychol 127(3):282–298
Moscovice LR, Heesen M, Di Fiore A, Seyfarth RM, Cheney DL (2009) Paternity alone does not predict long-term investment in juveniles by male baboons. Behav Ecol Sociobiol 63(10):1471–1482
Nettle D, Penke L (2010) Personality: bridging the literatures from human psychology and behavioural ecology. Philos Trans R Soc Lond B Biol Sci 365(1560):4043–4050
Oedegaard KJ, Greenwood TA, Lunde A, Fasmer OB, Akiskal HS, Kelsoe JR (2010) A genome-wide linkage study of bipolar disorder and co-morbid migraine: replication of migraine linkage on chromosome 4q24, and suggestion of an overlapping susceptibility region for both disorders on chromosome 20p11. J Affect Disord 122(1–2):14–26
Oler JA, Fox AS, Shelton SE, Rogers J, Dyer TD, Davidson RJ, Shelledy W, Oakes TR, Blangero J, Kalin NH (2010) Amygdalar and hippocampal substrates of anxious temperament differ in their heritability. Nature 466(7308):864–868
Raveendran M, Harris RA, Milosavljevic A, Johnson Z, Shelledy W, Cameron J, Rogers J (2006) Designing new microsatellite markers for linkage and population genetic analyses in rhesus macaques and other nonhuman primates. Genomics 88(6):706–710
Reale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev Camb Philos Soc 82(2):291–318
Reale D, Dingemanse NJ, Kazem AJ, Wright J (2010) Evolutionary and ecological approaches to the study of personality. Philos Trans R Soc Lond B Biol Sci 365(1560):3937–3946
Rizo J, Sudhof TC (2002) Snares and Munc18 in synaptic vesicle fusion. Nat Rev Neurosci 3(8):641–653
Rogers J, Mahaney MC, Almasy L, Comuzzie AG, Blangero J (1999) Quantitative trait linkage mapping in anthropology. Am J Phys Anthropol 29:127–151
Rogers J, Mahaney MC, Witte SM, Nair S, Newman D, Wedel S, Rodriguez LA, Rice KS, Slifer SH, Perelygin A, Slifer M, Palladino-Negro P, Newman T, Chambers K, Joslyn G, Parry P, Morin PA (2000) A genetic linkage map of the baboon (Papio hamadryas) genome based on human microsatellite polymorphisms. Genomics 67(3):237–247
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(4):463–469
Rogers J, Raveendran M, Fawcett GL, Fox AS, Shelton SE, Oler JA, Cheverud J, Muzny DM, Gibbs RA, Davidson RJ, Kalin NH (2013) CRHR1 genotypes, neural circuits and the diathesis for anxiety and depression. Mol Psychiatry 18(6):700–707
Roseboom PH, Nanda SA, Fox AS, Oler JA, Shackman AJ, Shelton SE, Davidson RJ, Kalin NH (2013) Neuropeptide Y receptor gene expression in the primate amygdala predicts anxious temperament and brain metabolism. Biol Psychiatry 76:850–857
Seyfarth RM, Silk JB, Cheney DL (2012) Variation in personality and fitness in wild female baboons. Proc Natl Acad Sci USA 109(42):16980–16985
Silk JB, Alberts SC, Altmann J (2003) Social bonds of female baboons enhance infant survival. Science 302(5648):1231–1234
Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, Wittig RM, Seyfarth RM, Cheney DL (2009) The benefits of social capital: close social bonds among female baboons enhance offspring survival. Proc Biol Sci 276(1670):3099–3104
Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, Wittig RM, Seyfarth RM, Cheney DL (2010) Strong and consistent social bonds enhance the longevity of female baboons. Curr Biol 20(15):1359–1361
Smith BR, Blumstein DT (2008) Fitness consequences of personality: a meta-analysis. Behav Ecol 19:448–455
Smuts BB (1985) Sex and friendship in baboons. Aldine Publishing Co., New York
Stevenson-Hinde J, Zunz MM (1978) Subjective assessment of individual rhesus monkeys. Primates 19:473–482
Terracciano A, Sanna S, Uda M, Deiana B, Usala G, Busonero F, Maschio A, Scally M, Patriciu N, Chen WM, Distel MA, Slagboom EP, Boomsma DI, Villafuerte S, Sliwerska E, Burmeister M, Amin N, Janssens AC, van Duijn CM, Schlessinger D, Abecasis GR, Costa PT Jr (2010) Genome-wide association scan for five major dimensions of personality. Mol Psychiatry 15(6):647–656
Trefilov A, Berard J, Krawczak M, Schmidtke J (2000) Natal dispersal in rhesus macaques is related to serotonin transporter gene promoter variation. Behav Genet 30(4):295–301
Tung J, Charpentier MJ, Mukherjee S, Altmann J, Alberts SC (2012) Genetic effects on mating success and partner choice in a social mammal. Am Nat 180(1):113–129
Vilinsky I, Stewart BA, Drummond J, Robinson I, Deitcher DL (2002) A Drosophila SNAP-25 null mutant reveals context-dependent redundancy with SNAP-24 in neurotransmission. Genetics 162(1):259–271
Weiss A, King JE, Perkins L (2006) Personality and subjective well-being in orangutans (Pongo pygmaeus and Pongo abelii). J Pers Soc Psychol 90(3):501–511
Weiss A, Inoue-Murayama M, Hong KW, 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(4):283–292
Weiss A, Adams MJ, Widdig A, Gerald MS (2011) Rhesus macaques (Macaca mulatta) as living fossils of hominoid personality and subjective well-being. J Comp Psychol 125(1):72–83
Weiss A, Gartner MC, Gold KC, Stoinski TS (2013) Extraversion predicts longer survival in gorillas: an 18-year longitudinal study. Proc Biol Sci 280(1752):20122231
Wills TA, Vaccaro D, McNamara G (1994) Novelty seeking, risk taking, and related constructs as predictors of adolescent substance use: an application of Cloninger’s theory. J Subst Abuse 6(1):1–20
Wolf M, Weissing FJ (2012) Animal personalities: consequences for ecology and evolution. Trends Ecol Evol 27(8):452–461
Zinner D, Wertheimer J, Liedigk R, Groeneveld LF, Roos C (2013) Baboon phylogeny as inferred from complete mitochondrial genomes. Am J Phys Anthropol 150(1):133–140
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Zachary Johnson, Linda Brent, Juan Carlos Alvarenga, Anthony G. Comuzzie, Wendy Shelledy, Stephanie Ramirez, Laura Cox, Michael C. Mahaney, Yung-Yu Huang, J. John Mann, Jay R. Kaplan, and Jeffrey Rogers declare that they have no conflict of interest. This research was funded by National Institutes of Health grant R01-MH65462 to Jeffrey Rogers.
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Johnson, Z., Brent, L., Alvarenga, J.C. et al. Genetic Influences on Response to Novel Objects and Dimensions of Personality in Papio Baboons. Behav Genet 45, 215–227 (2015). https://doi.org/10.1007/s10519-014-9702-6
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DOI: https://doi.org/10.1007/s10519-014-9702-6