Behavioral Ecology and Sociobiology

, Volume 69, Issue 1, pp 61–74 | Cite as

The 2D:4D digit ratio and social behaviour in wild female chacma baboons (Papio ursinus) in relation to dominance, aggression, interest in infants, affiliation and heritability

  • Caroline Howlett
  • Joanna M. Setchell
  • Russell A. Hill
  • Robert A. Barton
Original Paper

Abstract

Prenatal androgens are responsible for sex differences in behaviour and morphology in many species, causing changes in neural structure and function that persist throughout life. Some variation in the expression of behaviour between individuals of the same sex can also be attributed to differences in exposure to prenatal sex hormones. The ratio of the second and fourth digits (2D:4D ratio) is a proposed biomarker for prenatal androgen effects (PAE). Through assessment of 2D:4D ratios, this study aimed to investigate the relationship between inferred PAE and social behaviours in female chacma baboons (Papio ursinus). We validated a new method to measure 2D:4D indirectly using digital photographs and computer-assisted image analysis software. There was a strong correlation between 2D:4D ratio and dominance rank amongst female baboons. Low 2D:4D ratios were associated with high rank, lower submission rates and higher rates of non-contact and contact aggression. This is consistent with the hypothesis that prenatal androgens are linked to the expression of these behaviours in female baboons, although it was not possible to separate the effects of PAE and dominance rank on some rank-related behaviours. The 2D:4D ratio did not correlate with interest in infants or with the rate of affiliative behaviours, possibly because these behaviours are more affected by ovarian hormones in adult life than by PAE. Finally, mean 2D:4D ratios were positively correlated in six mother/infant pairs, consistent with a heritable basis for the 2D:4D ratio in primates. We suggest that PAE contribute significantly to the patterning of social relationships in female primates.

Keywords

Hormone Primate Human Development ImageJ 

References

  1. Adkins-Regan E (2009) Hormonal and sexual differentiation of avian social behaviour. Dev Neurosci-Basel 31:342–350CrossRefGoogle Scholar
  2. Akinyi MY, Tung J, Jeneby M, Patel NB, Altmann J, Alberts SC (2013) Role of grooming in reducing tick load in wild baboons (Papio cynocephalus). Anim Behav 85:559–568PubMedCentralPubMedCrossRefGoogle Scholar
  3. Altmann J (1974) Observational study of behaviour: sampling methods. Behaviour 49:227–267PubMedCrossRefGoogle Scholar
  4. Auger J, Le Denmat D, Berges R, Doridot L, Salmon B, Canivenc-Lavier MC, Eustache F (2013) Environmental levels of oestrogenic and antioestrogenic compounds feminize digit ratios in male rats and their unexposed male progeny. Proc R Soc B 280:20131532PubMedCentralPubMedCrossRefGoogle Scholar
  5. Bailey AA, Hurd PL (2005) Finger length ratio (2D:4D) correlates with physical aggression in men but not in women. Biol Psychol 68:215–222PubMedCrossRefGoogle Scholar
  6. Balthazart J, Ball GF (1995) Sexual-differentiation of brain and behaviour in birds. Trends Endocrin Met 6:21–29CrossRefGoogle Scholar
  7. Barrett L, Henzi SP, Weingrill T, Lycett JE, Hill RA (1999) Market forces predict grooming reciprocity in female baboons. Proc R Soc Lond B 266:665–670CrossRefGoogle Scholar
  8. Barrett L, Gaynor D, Henzi SP (2002) A dynamic interaction between aggression and grooming reciprocity among female Chacma baboons. Anim Behav 63:1047–1053CrossRefGoogle Scholar
  9. Benderlioglu Z, Nelson RJ (2004) Digit lengths predict reactive aggression in women, but not in men. Horm Behav 46:558–564PubMedCrossRefGoogle Scholar
  10. Berger K, Crafford JE, Gaigher I, Gaigher MJ, Hahn N, Macdonals I (2003) A first synthesis of the environment, biological and cultural assets of the Soutpansberg. Leach Printers and Signs, Louis TrichardtGoogle Scholar
  11. Bielsky IF, Young LJ (2004) Oxytocin, vasopressin, and social recognition in mammals. Peptides 25:1565–1574PubMedCrossRefGoogle Scholar
  12. Bodo C, Rissman EF (2008) The androgen receptor is selectively involved in organization of sexually dimorphic social behaviours in mice. Endocrinology 149:4142–4150PubMedCentralPubMedCrossRefGoogle Scholar
  13. Brown WM, Hines M, Fane BA, Breedlove SM (2002) Masculinized finger length patterns in human males and females with congenital adrenal hyperplasia. Horm Behav 42:380–386PubMedCrossRefGoogle Scholar
  14. Buser T (2012) Digit ratios, the menstrual cycle and social preferences. Game Econ Behav 76:457–470CrossRefGoogle Scholar
  15. Christiansen K, Knussmann R (1987) Androgen levels and components of aggressive behavior in men. Horm Behav 21:170–80PubMedCrossRefGoogle Scholar
  16. Clipperton-Allen AE, Almey A, Melichercik A, Allen CP, Choleris E (2011) Effects of and estrogen receptor alpha agonist on agonistic behaviour in intact and gonadectomised male and female mice. Psychoneuroendocrinology 36:981–995PubMedCrossRefGoogle Scholar
  17. Coleman K, Robertson ND, Bethea CL (2011) Long-term ovariectomy alters anxious behaviours in semi-free ranging Japanese macaques. Behav Brain Res 225:317–327PubMedCentralPubMedCrossRefGoogle Scholar
  18. Eaton GG, Johnson DF, Glick BB, Worlein JM (1985) Development in Japanese macaques (Macaca fuscata): sexually dimorphic behaviour during the first year of life. Primates 26:238–248CrossRefGoogle Scholar
  19. Fisher HE, Rich J, Island HD, Marchalik D (2010) The second to fourth digit ratio: a measure of two hormonally-based temperament dimensions. Pers Indiv Differ 49:773–777CrossRefGoogle Scholar
  20. Fitch WT, Braccini SN (2013) Primate laterality and the biology and evolution of human handedness: a review and synthesis. Ann NY Acad Sci 1288:70–85PubMedCrossRefGoogle Scholar
  21. Forstmeier W (2005) Quantitative genetics and behavioural correlates of digit ratio in the zebra finch. Proc R Soc Lond B 272:2641–2649CrossRefGoogle Scholar
  22. Forstmeier W, Rochester J, Millam JR (2008) Digit ratio unaffected by estradiol treatment of zebra finch nestlings. Gen Comp Endocr 156:379–384PubMedCrossRefGoogle Scholar
  23. Herman RA, Measday MA, Wallen K (2003) Sex differences in interest in infants in juvenile rhesus monkeys: relationship to prenatal androgen. Horm Behav 43:573–583PubMedCrossRefGoogle Scholar
  24. Higley JD, Mehlman PT, Poland RE, Taub DM, Vickers J, Suomi SJ, Linnoila M (1996) CSF testosterone and 5-HIAA correlate with different types of aggressive behaviours. Biol Psychiatry 40:1067–82PubMedCrossRefGoogle Scholar
  25. Hines M (2006) Prenatal testosterone and gender-related behaviour. Eur J Endocrinol 155:115–121CrossRefGoogle Scholar
  26. Hines M (2010) Sex-related variation in human behaviour and the brain. Trends Cogn Sci 14:448–456PubMedCentralPubMedCrossRefGoogle Scholar
  27. Hönekopp J, Watson S (2010) Meta-analysis of digit ratio 2D:4D shows greater sex difference in the right hand. Am J Hum Biol 22:619–630PubMedCrossRefGoogle Scholar
  28. Hönekopp J, Bartholdt L, Beier L, Liebert A (2007) Second to fourth digit length ratio (2D:4D) and adult sex hormone levels: new data and a meta-analytic review. Psychoneuroendocrinology 32:313–321PubMedCrossRefGoogle Scholar
  29. Howlett C, Marshall A, Hughes WOH (2012) Digit ratios and dominance in female baboons (Papio hamadryas and Papio ursinus). Int J Primatol 33:1439–1452CrossRefGoogle Scholar
  30. Hurd PL, Vaillancourt KL, Dinsdale NL (2011) Aggression, digit ratio and variation in androgen receptor and monoamine oxidase A genes in men. Behav Genet 41:543–556PubMedCrossRefGoogle Scholar
  31. Johnston AL, File SE (1991) Sex-differences in animal tests of anxiety. Physiol Behav 49:245–250PubMedCrossRefGoogle Scholar
  32. Knickmeyer RC, Woolson S, Hamer RM, Konneker T, Gilmore JH (2011) 2D:4D ratios and the first 2 years of life: stability in relation to testosterone exposure and sensitivity. Horm Behav 60:256–263PubMedCentralPubMedCrossRefGoogle Scholar
  33. Knoll JG, Wolfe CA, Tobet SA (2007) Estrogen modulates neural movements within the developing preoptic area-anterior hypothalamus. Eur J Neurosci 26:1091–1099PubMedCentralPubMedCrossRefGoogle Scholar
  34. Leveroni CL, Berenbaum SA (1998) Early androgen effects on interest in infants: evidence from children with congenital adrenal hyperplasia. Dev Neuropsychol 14:321–340CrossRefGoogle Scholar
  35. Lim MM, Young LJ (2006) Neuropeptide regulation of affiliative behaviour and social bonding in animals. Horm Behav 50:506–517PubMedCrossRefGoogle Scholar
  36. Lombardo MP, Thorpe PA (2008) Digit ratios in Green Anolis Lizards (Anolis carolinensis). Anat Rec 291:433–440CrossRefGoogle Scholar
  37. Lovejoy J, Wallen K (1988) Sexually dimorphic behaviour in grouphoused rhesus monkeys (Macaca mulatta) at 1 year of age. Psychobiol 16:348–356Google Scholar
  38. Manning JT (2002) Digit Ratio: A pointer to fertility, behaviour and health. Rutgers University Press, LondonGoogle Scholar
  39. Manning JT (2011) Resolving the role of prenatal sex steroids in the development of digit ratio. Proc Natl Acad Sci USA 108:16143–16144PubMedCentralPubMedCrossRefGoogle Scholar
  40. Manning JT, Scutt D, Wilson J, Lewis-Jones DI (1998) The ratio of the 2nd to 4th digit length: a predictor of sperm numbers and concentrations of testosterone, luteinizing hormone and oestrogen. Hum Reprod 13:3000–3004PubMedCrossRefGoogle Scholar
  41. Manning JT, Barley L, Walton J, Lewis-Jones DI, Trivers RL et al (2000) The 2nd:4th digit ratio, sexual dimorphism, population differences, and reproductive success: evidence for sexually antagonistic genes? Evol Hum Behav 21:163–183PubMedCrossRefGoogle Scholar
  42. Manning JT, Baron-Cohen S, Wheelwright S, Sanders G (2001) The 2nd to 4th digit ratio and autism. Dev Med Child Neurol 43:160–164PubMedCrossRefGoogle Scholar
  43. Manning JT, Bundred PE, Newton DJ, Flanagan BF (2003) The second to fourth digit ratio and variation in the androgen receptor gene. Evol Hum Behav 24:399–405CrossRefGoogle Scholar
  44. Manning JT, Kilduff LP, Trivers R (2013) Digit ratio (2D:4D) in Klinefelter’s Syndrome. Andrology 1:94–99PubMedCrossRefGoogle Scholar
  45. Martin P, Bateson P (2007) Measuring Behaviour: An introductory guide, 3rd edn. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  46. Mazur A, Booth A (1998) Testosterone and dominance in men. Behav Brain Sci 21:353–397PubMedCrossRefGoogle Scholar
  47. McIntyre MH, Cohn BA, Towne B, Demerath EW, Ellison PT (2005) The pre-pubertal origins of sex differences in digit ratios, and their development from infancy to maturity. Am J Phys Anthropol 40:149Google Scholar
  48. McIntyre MH, Herrman E, Wobber M, Halbwax M, Mohamba C, de Sousa N, Atencia R, Cox D, Hare B (2009) Bonobos have a more human-like second-to-fourth digit ratio (2D:4D) than chimpanzees: a hypothesized indication of lower prenatal androgens. J Hum Evol 56:361–365PubMedCrossRefGoogle Scholar
  49. Millet K, Dewitte S (2007) Digit ratio (2D:4D) moderates the impact of an aggressive music video on aggression. Pers Indiv Differ 43:289–294CrossRefGoogle Scholar
  50. Millet K, Dewitte S (2009) The presence of aggression cues inverts the relation between digit ratio (2D:4D) and prosocial behaviour in a dictators game. Brit J Psychol 100:151–162PubMedCrossRefGoogle Scholar
  51. Moore FL, Boyd SK, Kelley DB (2005) Historical perspective: hormonal regulation of behaviours in amphibians. Horm Behav 48:373–383PubMedCrossRefGoogle Scholar
  52. Neave N, Laing S, Fink B, Manning JT (2003) Second to fourth digit ratio, testosterone and perceived male dominance. Proc R Soc Lond B 270:2167–2172CrossRefGoogle Scholar
  53. Nelson E, Shultz S (2010) Finger length ratios (2D:4D) in Anthropoids implicate reduced prenatal androgens in social bonding. Am J Phys Anthropol 141:395–405PubMedGoogle Scholar
  54. Nelson E, Voracek M (2010) Heritability of digit ratios (2D:4D) in rhesus macaques (Macaca mulatta). Primates 51:1–5PubMedCrossRefGoogle Scholar
  55. Nelson E, Hoffman CL, Gerald MS, Shultz S (2010) Digit ratio (2D:4D) and dominance rank in female rhesus macaques (Macaca mulatta). Behav Ecol Sociobiol 64:1001–1009CrossRefGoogle Scholar
  56. Paul SN, Kato BS, Cherkas LF, Andrew T, Spector TD (2006) Heritability of the second to fourth digit ratio (2d:4d): a twin study. Twin Res Hum Genet 9:215–219PubMedCrossRefGoogle Scholar
  57. Razzoli M, Cushing BS, Carter SC, Valsecchi P (2003) Hormonal regulation of agonistic and affiliative behaviour in female Mongolian gerbils (Meriones unguiculatus). Horm Behav 43:549–553PubMedCrossRefGoogle Scholar
  58. Roney JR, Whitham JC, Leoni M, Bellem A, Wielebnowski N, Maestripieri D (2004) Relative digit lengths and testosterone levels in Guinea baboons. Horm Behav 45:285–290PubMedCrossRefGoogle Scholar
  59. Ross HE, Young LJ (2009) Oxytocin and the neural mechanisms regulating social cognition and affiliative behaviour. Front Neuroendocrinol 30:534–547PubMedCentralPubMedCrossRefGoogle Scholar
  60. Tanner JM (1990) Foetus into man: physical growth from conception to maturity. Harvard University Press, CambridgeGoogle Scholar
  61. Thornton J, Zehr JL, Loose MD (2009) Effects of prenatal androgens on rhesus monkeys: a model system to explore the organisational hypothesis in primates. Horm Behav 55:633–644PubMedCentralPubMedCrossRefGoogle Scholar
  62. Trivers R, Manning JT, Jacobson A (2006) A longitudinal study of digit ratio (2D:4D) and other finger ratios in Jamaican children. Horm Behav 149:150–156CrossRefGoogle Scholar
  63. von Maltitz G (2003) Classification system for South African indigenous forests. ENV-P-C 2003-017. Environmentek CSIR, Pretoria, South AfricaGoogle Scholar
  64. Wallen K (2005) Hormonal influences on sexually differentiated behaviour in nonhuman primates. Front Neuroendocrinol 26:7–26PubMedCrossRefGoogle Scholar
  65. Willems EP, Hill RA (2009) Predator-specific landscapes of fear and resource distribution: effects on spatial range use. Ecology 90:546–555PubMedCrossRefGoogle Scholar
  66. Willems EP, Barton RA, Hill RA (2009) Remotely sensed productivity, home range selection and local range use by an omnivorous primate. Behav Ecol 20:985–992CrossRefGoogle Scholar
  67. Witt DM, Winslow JT, Insel TR (1992) Enhanced social interactions in rats following chronic, centrally infused oxytocin. Pharmacol Biochem Behav 43:855–861PubMedCrossRefGoogle Scholar
  68. Young LJ, Wang Z, Donaldson R, Rissman EF (1998) Estrogen receptor α is essential for induction of oxytocin receptor by estrogen. Neuroendocrinology 9:933–936Google Scholar
  69. Zeynep B, Nelson RJ (2004) Digit length ratios predict reactive aggression in women, but not in men. Horm Behav 46:558–564CrossRefGoogle Scholar
  70. Zheng Z, Cohn MJ (2011) Developmental basis of sexually dimorphic digit ratios. Proc Natl Acad Sci USA 108:16289–16294PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Caroline Howlett
    • 1
    • 2
  • Joanna M. Setchell
    • 1
  • Russell A. Hill
    • 1
    • 2
  • Robert A. Barton
    • 1
  1. 1.Evolutionary Anthropology Research Group, Department of Anthropology, Dawson BuildingDurham UniversityDurhamUK
  2. 2.Primate and Predator ProjectLajuma Research CentreMakhadoSouth Africa

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