Visual Phenotype Matching: Cues to Paternity Are Present in Rhesus Macaque Faces

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Kazem, Anahita J N ^a,b   Widdig, Anja ^a,c  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^b NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^c UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ARTICLE; CHILD PARENT RELATION; CONTROLLED STUDY; FACIES; FEMALE; HUMAN; HUMAN EXPERIMENT; MOLECULAR DYNAMICS; MOLECULAR PHYLOGENY; NONHUMAN; PATERNITY TEST; PEDIGREE ANALYSIS; PHENOTYPE; QUANTITATIVE ANALYSIS; RHESUS MONKEY; SPECIES DIFFERENCE; STIMULUS RESPONSE; TASK PERFORMANCE; VISUAL DISCRIMINATION; VISUAL STIMULATION;

ANIMALS; CUES; FACE; FEMALE; HUMANS; MACACA MULATTA; MALE; PATERNITY; PHENOTYPE;

EID: 84874328352     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0055846     Document Type: Article

References (85)

1. Fletcher DJC, Michener CD, editors (1987) Kin recognition. Chichester, UK: Wiley-Blackwell.
2. Hepper PG, editor (1991) Kin recognition. Cambridge, UK: Cambridge University Press.
3. Holmes WG, (2004) The early history of Hamiltonian-based research on kin recognition. Annales Zoologici Fennici 41: 691-711.
4. Hamilton WD, (1964) The genetical evolution of social behaviour I-II. Journal of Theoretical Biology 7: 1-52.
5. Sherman PW, (1980) The meaning of nepotism. The American Naturalist 116: 604-606.
6. Blouin SF, Blouin M, (1988) Inbreeding avoidance behaviors. Trends in Ecology and Evolution 3: 230-233.
7. Pusey A, Wolf M, (1996) Inbreeding avoidance in animals. Trends in Ecology & Evolution 11: 201-206.
8. Bateson P (1983) Optimal outbreeding. In: Bateson P, editor. Mate choice. Cambridge, UK: Cambridge University Press. 257-278.
9. Puurtinen M (2011) Mate choice for optimal (k)inbreeding. Evolution: 1501-1505.
10. Stewart-Williams S, (2007) Altruism among kin vs. nonkin: effects of cost of help and reciprocal exchange. Evolution and Human Behavior 28: 193-198.
11. Lieberman D, Tooby J, Cosmides L, (2007) The architecture of human kin detection. Nature 445: 727-731.
12. Gaulin SJC, McBurney DH, Brakeman-Wartell SL, (1997) Matrilateral biases in the investment of aunts and uncles. Human Nature 8: 139-151.
13. Jeon J, Buss DM, (2007) Altruism towards cousins. Proceedings of the Royal Society B: Biological Sciences 274: 1181-1187.
14. Fox M, Sear R, Beise J, Ragsdale G, Voland E, et al. (2010) Grandma plays favourites: X-chromosome relatedness and sex-specific childhood mortality. Proceedings of the Royal Society B: Biological Sciences 277: 567-573.
15. Rice WR, Gavrilets S, Friberg U, (2010) The evolution of sex-specific grandparental harm. Proceedings of the Royal Society B: Biological Sciences 277: 2727-2735.
16. Chapais B, Berman CM, editors (2004) Kinship and behavior in primates. New York, NY: Oxford University Press.
17. Silk JB, (2009) Nepotistic cooperation in non-human primate groups. Philosophical Transactions of the Royal Society B: Biological Sciences 364: 3243-3254.
18. Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, et al. (2009) The benefits of social capital: close social bonds among female baboons enhance offspring survival. Proceedings of the Royal Society B: Biological Sciences 276: 3099-3104.
19. Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, et al. (2010) Strong and consistent social bonds enhance the longevity of female baboons. Current Biology 20: 1359-1361.
20. Widdig A, Nürnberg P, Krawczak M, Streich WJ, Bercovitch FB, (2001) Paternal relatedness and age proximity regulate social relationships among adult female rhesus macaques. Proceedings of the National Academy of Sciences 98: 13769-13773.
21. Smith K, Alberts SC, Altmann J, (2003) Wild female baboons bias their social behaviour towards paternal half-sisters. Proceedings of the Royal Society B: Biological Sciences 270: 503-510.
22. Silk JB, Altmann J, Alberts SC, (2006) Social relationships among adult female baboons (Papio cynocephalus) I. Variation in the strength of social bonds. Behavioral Ecology and Sociobiology 61: 183-195.
23. Charpentier MJE, Peignot P, Hossaert-McKey M, Wickings EJ, (2007) Kin discrimination in juvenile mandrills, Mandrillus sphinx. Animal Behaviour 73: 37-45.
24. Buchan JC, Alberts SC, Silk JB, Altmann J, (2003) True paternal care in a multi-male primate society. Nature 425: 179-181.
25. Charpentier M, Van Horn R, Altmann J, Alberts S, (2008) Paternal effects on offspring fitness in a multimale primate society. Proceedings of the National Academy of Sciences 105: 1988-1992.
26. Alberts SC, (1999) Paternal kin discrimination in wild baboons. Proceedings of the Royal Society of London Series B: Biological Sciences 266: 1501-1506.
27. Charpentier M, Peignot P, Hossaert-McKey M, Gimenez O, Setchell JM, et al. (2005) Constraints on control: factors influencing reproductive success in male mandrills (Mandrillus sphinx). Behavioral Ecology 16: 614-623.
28. Muniz L, Perry S, Manson JH, Gilkenson H, Gros-Louis J, et al. (2006) Father-daughter inbreeding avoidance in a wild primate population. Current Biology 16: R156-R157.
29. Kuester J, Paul A, Arnemann J, (1994) Kinship, familiarity and mating avoidance in Barbary macaques, Macaca sylvanus. Animal Behaviour 48: 1183-1194.
30. Widdig A, (2007) Paternal kin discrimination: the evidence and likely mechanisms. Biological Reviews 82: 319-334.
31. Holmes WG, Sherman PW, (1982) The ontogeny of kin recognition in two species of ground squirrels. American Zoologist 22: 491-517.
32. Hauber ME, Sherman PW, (2001) Self-referent phenotype matching: theoretical considerations and empirical evidence. Trends in Neurosciences 24: 609-616.
33. Todrank J, Heth G, (2003) Odor-genes covariance and genetic relatedness assessments: rethinking odor-based "recognition" mechanisms in rodents. Advances in the Study of Behavior 32: 77-130.
34. Célérier A, Huchard E, Alvergne A, Féjan D, Plard F, et al. (2010) Detective mice assess relatedness in baboons using olfactory cues. Journal of Experimental Biology 213: 1399-1405.
35. Charpentier MJE, Crawford JC, Boulet M, Drea CM, (2010) Message "scent": lemurs detect the genetic relatedness and quality of conspecifics via olfactory cues. Animal Behaviour 80: 101-108.
36. Carson E, (2006) Maximum likelihood estimation of human craniometric heritabilities. American Journal of Physical Anthropology 131: 169-180.
37. Jelenkovic A, Poveda A, Susanne C, Rebato E, (2010) Common genetic and environmental factors among craniofacial traits in Belgian nuclear families: comparing skeletal and soft-tissue related phenotypes. HOMO - Journal of Comparative Human Biology 61: 191-203.
38. Sherwood RJ, Duren DL, Mahaney MC, Blangero J, Dyer TD, et al. (2011) A genome-wide linkage scan for quantitative trait loci influencing the craniofacial complex in humans (Homo sapiens sapiens). The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology 294: 664-675.
39. DeBruine LM, Jones BC, Little AC, Perrett DI, (2008) Social perception of facial resemblance in humans. Archives of Sexual Behavior 37: 64-77.
40. Dal Martello MF, Maloney LT, (2006) Where are kin recognition signals in the human face? Journal of Vision 6: 1356-1366.
41. DeBruine LM, Smith FG, Jones BC, Craig Roberts S, Petrie M, et al. (2009) Kin recognition signals in adult faces. Vision Research 49: 38-43.
42. Kaminski G, Dridi S, Graff C, Gentaz E, (2009) Human ability to detect kinship in strangers' faces: effects of the degree of relatedness. Proceedings of the Royal Society B: Biological Sciences 276: 3193-3200.
43. Alvergne A, Faurie C, Raymond M, (2009) Father-offspring resemblance predicts paternal investment in humans. Animal Behaviour 78: 61-69.
44. Burch RL, Gallup GG, (2000) Perceptions of paternal resemblance predict family violence. Evolution and Human Behavior 21: 429-435.
45. Leopold DA, Rhodes G, (2010) A comparative view of face perception. Journal of Comparative Psychology 124: 233-251.
46. Pascalis O, Bachevalier J, (1998) Face recognition in primates: a cross-species study. Behavioural Processes 43: 87-96.
47. Parr LA, (2011) The evolution of face processing in primates. Philosophical Transactions of the Royal Society B: Biological Sciences 366: 1764-1777.
48. Cheverud JM, Buikstra JE, (1982) Quantitative genetics of skeletal nonmetric traits in the rhesus macaques of Cayo Santiago. III. Relative heritability of skeletal nonmetric and metric traits. American Journal of Physical Anthropology 59: 151-155.
49. Dasser V, (1988) A social concept in Java monkeys. Animal Behaviour 36: 225-230.
50. Cheney DL, Seyfarth RM, (1999) Recognition of other individuals' social relationships by female baboons. Animal Behaviour 58: 67-75.
51. Schino G, Tiddi B, Di Sorrentino EP, (2006) Simultaneous classification by rank and kinship in Japanese macaques. Animal Behaviour 71: 1069-1074.
52. Wittig RM, Crockford C, Wikberg E, Seyfarth RM, Cheney DL, (2007) Kin-mediated reconciliation substitutes for direct reconciliation in female baboons. Proceedings of the Royal Society B: Biological Sciences 274: 1109-1115.
53. Vokey JR, Rendall D, Tangen JM, Parr LA, de Waal F, (2004) Visual kin recognition and family resemblance in chimpanzees (Pan troglodytes). Journal of Comparative Psychology 118: 194-199.
54. Alvergne A, Huchard E, Caillaud D, Charpentier MJE, Setchell JM, et al. (2009) Human ability to recognize kin visually within primates. International Journal of Primatology 30: 199-210.
55. Parr LA, Heintz M, Lonsdorf E, Wroblewski E, (2010) Visual kin recognition in nonhuman primates: Pan troglodytes and Macaca mulatta: inbreeding avoidance or male distinctiveness? Journal of Comparative Psychology 124: 343-350.
56. Zajonc RB, Adelmann PK, Murphy ST, Niedenthal PM, (1987) Convergence in the physical appearance of spouses. Motivation & Emotion 11: 335-346.
57. Rawlins RG, Kessler MJ, editors (1986) Cayo Santiago macaques: history, behaviour and biology. New York, NY: State University of New York Press.
58. Bressan P, Grassi M, (2004) Parental resemblance in 1-year-olds and the Gaussian curve. Evolution and Human Behavior 25: 133-141.
59. Nürnberg P, Sauermann U, Kayser M, Lanfer C, Manz E, et al. (1998) Paternity assessment in rhesus macaques (Macaca mulatta): multilocus DNA fingerprinting and PCR marker typing. American Journal of Primatology 44: 1-18.
60. Dubuc C, Muniz L, Heistermann M, Engelhardt A, Widdig A, (2011) Testing the priority-of-access model in a seasonally breeding primate species. Behavioral Ecology and Sociobiology 65: 1615-1627.
61. Kulik L, Muniz L, Mundry R, Widdig A, (2012) Patterns of interventions and the effect of coalitions and sociality on male fitness. Molecular Ecology 21: 699-714.
62. Kalinowski ST, Taper ML, Marshall TC, (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molecular Ecology 16: 1099-1106.
63. Bercovitch FB, Widdig A, Trefilov A, Kessler MJ, Berard JD, et al. (2003) A longitudinal study of age-specific reproductive output and body condition among male rhesus macaques, Macaca mulatta. Naturwissenschaften 90: 309-312.
64. Silk J, Short J, Roberts J, Kusnitz J, (1993) Gestation length in rhesus macaques (Macaca mulatta). International Journal of Primatology 14: 95-104.
65. Widdig A, Bercovitch FB, Streich WJ, Sauermann U, Nürnberg P, et al. (2004) A longitudinal analysis of reproductive skew in male rhesus macaques. Proceedings of the Royal Society B: Biological Sciences 271: 819-826.
66. Baayen RH (2008) Analyzing linguistic data: a practical introduction to statistics using R. Cambridge, UK: Cambridge University Press.
67. Schielzeth H, Forstmeier W, (2009) Conclusions beyond support: overconfident estimates in mixed models. Behavioral Ecology 20: 416-420.
68. Forstmeier W, Schielzeth H, (2011) Cryptic multiple hypotheses testing in linear models: overestimated effect sizes and the winner's curse. Behavioral Ecology and Sociobiology 65: 47-55.
69. R Development Core Team (2009) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available: http://www.R-project.org/.
70. Bates D, Maechler M (2009) lme4: Linear mixed-effects models using S4 classes. R package version 0.999375. Available: http://CRAN.R-project.org/package=lme4.
71. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, et al. (2008) Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology & Evolution 24: 127-135.
72. Baayen RH (2009) languageR: Data sets and functions with "Analyzing linguistic data: a practical introduction to statistics". R package version 0.955. Available: http://CRAN.R-project.org/package=languageR.
73. Haig D, (2011) Genomic imprinting and the evolutionary psychology of human kinship. Proceedings of the National Academy of Sciences 108: 10878-10885.
74. Brandvain Y, Van Cleve J, Úbeda F, Wilkins JF, (2011) Demography, kinship, and the evolving theory of genomic imprinting. Trends in Genetics 27: 251-257.
75. Pagel M, (1997) Desperately concealing father: a theory of parent-infant resemblance. Animal Behaviour 53: 973-981.
76. Johnstone RA, (1997) Recognition and the evolution of distinctive signatures: when does it pay to reveal identity? Proceedings of the Royal Society of London Series B: Biological Sciences 264: 1547-1553.
77. de RuiterJR, Geffen E, (1998) Relatedness of matrilines, dispersing males and social groups in long-tailed macaques, Macaca fascicularis. Proceedings of the Royal Society of London Series B: Biological Sciences 265: 79-87.
78. Lukas D, Reynolds V, Boesch C, Vigilant L, (2005) To what extent does living in a group mean living with kin? Molecular Ecology 14: 2181-2196.
79. Waser PM, Austad SN, Keane B, (1986) When should animals tolerate inbreeding? The American Naturalist 128: 529-537.
80. Lehmann L, Perrin N, (2003) Inbreeding avoidance through kin recognition: choosy females boost male dispersal. The American Naturalist 162: 638-652.
81. Bower S, Suomi SJ, Paukner A, (2012) Evidence for kinship information contained in the rhesus macaque (Macaca mulatta) face. Journal of Comparative Psychology 126: 318-323.
82. Pascalis O, Scott L, Kelly D, Shannon R, Nicholson E, et al. (2005) Plasticity of face processing in infancy. Proceedings of the National Academy of Sciences of the United States of America 102: 5297-5300.
83. Dufour V, Petit O, (2010) Recognition of monkey faces by monkey experts. Journal of Ethology 28: 231-238.
84. Scott LS, Monesson A, (2009) The origin of biases in face perception. Psychological Science 20: 676-680.
85. Mateo JM, (2002) Kin-recognition abilities and nepotism as a function of sociality. Proceedings of the Royal Society B: Biological Sciences 269: 721-727.