The impact of paternity on male-infant association in a primate with low paternity certainty

Molecular Ecology

Volumn 22, Issue 13, 2013, Pages 3638-3651

  Langos, Doreen ^a,b   Kulik, Lars ^a,b   Mundry, Roger ^a   Widdig, Anja ^a,b  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^b UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

kin recognition; male infant association; paternal care; paternity uncertainty; rhesus macaques

Indexed keywords

ANIMAL; ARTICLE; FEMALE; GENETICS; GENOTYPE; MALE; PATERNAL BEHAVIOR; PHYSIOLOGY; PUERTO RICO; REPRODUCTION; RHESUS MONKEY; SEXUAL BEHAVIOR; SEXUAL MATURATION;

ANIMALS; FEMALE; GENOTYPE; MACACA MULATTA; MALE; PATERNAL BEHAVIOR; PUERTO RICO; REPRODUCTION; SEXUAL BEHAVIOR, ANIMAL; SEXUAL MATURATION;

MACACA MULATTA; PRIMATES;

EID: 84879550473     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12328     Document Type: Article

References (88)

1. Albers P, (2001) Elo-rating as a tool in the sequential estimation of dominance strengths. Animal Behaviour, 61, 489-495.
2. Alberts SC, Fitzpatrick CL, (2012) Paternal care and the evolution of exaggerated sexual swellings in primates. Behavioral Ecology, 23, 699-706.
3. Altmann J, (1974) Observational study of behavior sampling methods. Behaviour, 49, 227-267.
4. Baayen H, (2008) Analyzing Linguistic Data: A Practical Introduction to Statistics Using R. Cambridge University Press, Berlin, New York.
5. Bates D, Maechler M, Bolker B, (2011) lme4: Linear mixed-effects models using S4 classes. R package (version 0.999375-34). Institute for Statistics and Mathematics, University of Economics and Business, Vienna. Available at: http://CRAN. R-project. org/package= lme4 (accessed August 2011)
6. Berard JD, (1999) A four-year study of the association between male dominance rank, residency status, and reproductive activity in rhesus macaques (Macaca mulatta). Primates, 40, 159-175.
7. Berard JD, Nürnberg P, Epplen JT, Schmidtke J, (1994) Alternative reproductive tactics and reproductive success in male rhesus macaques. Behaviour, 129, 177-201.
8. Bercovitch FB, (1992) Sperm competition, reproductive tactics, and paternity in savanna baboons and rhesus macaques. In: Paternity in Primates: Genetic Tests and Theories. Implications of Human DNA Fingerprinting (eds, Martin R. D., Dixson A. F., &, Wickings E. J.,), pp. 225-237. Karger, Basel.
9. Bercovitch FB, Widdig A, Trefilov A, et al,. (2003) A longitudinal study of age-specific reproductive output and body condition among male rhesus macaques, Macaca mulatta. Naturwissenschaften, 90, 309-312.
10. Berenstain L, Rodman PS, Smith DG, (1981) Social relations between fathers and offspring in a captive group of rhesus monkeys (Macaca mulatta). Animal Behaviour, 29, 1057-1063.
11. Blomquist GE, (2013) Maternal effects on offspring mortality in rhesus macaques (Macaca mulatta). American Journal of Primatology, 75, 238-251.
12. Boyd R, Silk JB, (2012) How Humans Evolved, vol. 8. Norton & Company, New York.
13. Buchan JC, Alberts SC, Silk JB, Altmann J, (2003) True paternal care in a multi-male primate society. Nature, 425, 179-181.
14. Célérier A, Huchard E, Alvergne A, et al,. (2010) Detective mice assess relatedness in baboons using olfactory cues. Journal of Experimental Biology, 213, 1399-1405.
15. Chapais B, (1983) Reproductive activity in relation to male dominance and likelihood of ovulation in rhesus monkeys. Behavioral Ecology and Sociobiology, 12, 215-228.
16. Charpentier MJE, Van Horn RC, Altmann J, Alberts SC, (2008) Paternal effects on offspring fitness in a multimale primate society. Proceedings of the National Academy of Sciences, USA, 105, 1988-1992.
17. Cheney DL, (1977) The acquisition of rank and the development of reciprocal alliances among free-ranging immature baboons. Behavioral Ecology and Sociobiology, 2, 303-318.
18. Clutton-Brock TH, (1991) The Evolution of Parental Care. Princeton University Press, Princeton.
19. Colvin J, (1983) Familiarity, rank, and the structure of rhesus male peers networks. In: Primate Social Relationship. An Integrated Approach (ed, Hinde R. A.,), pp. 190-200. Blackwell, Oxford.
20. Cooper MA, Berntein IS, Hemelrijk CK, (2005) Reconciliation and relationship quality in Assamese macaques (Macaca assamensis). American Journal of Primatology, 65, 269-282.
21. Datta SB, (1988) The acquisition of dominance among free-ranging rhesus monkey siblings. Animal Behaviour, 36, 754-772.
22. Dobson AJ, (2002) An Introduction to Generalized Linear Models. Chapman & Hall/CRC, Boca Raton.
23. Drickamer LC, (1974) A ten-year summary of reproductive data for free-ranging Macaca mulatta. Folia Primatologica, 21, 61-80.
24. Drickamer LC, Vessey SH, (1973) Group changing in free-ranging rhesus monkeys. Primates, 14, 359-368.
25. Dubuc C, Brent L, Accamando A, et al,. (2009) Sexual skin color contains information about the timing of the fertile phase in free-ranging Macaca mulatta. International Journal of Primatology, 30, 777-789.
26. 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.
27. Dubuc C, Muniz L, Heistermann M, Widdig A, Engelhardt A, (2012) Do males time their mate-guarding effort with the fertile phase in order to secure fertilisation in Cayo Santiago rhesus macaques? Hormones and Behavior, 61, 696-705.
28. Elo AE, (1978) The Rating Of Chess Players, Past & Present. Arco Pub, Batsford, London.
29. Engelhardt A, Pfeifer JB, Heistermann M, Niemitz C, van Hooff JARAM, Hodges JK, (2004) Assessment of female reproductive status by male longtailed macaques, Macaca fascicularis, under natural conditions. Animal Behaviour, 67, 915-924.
30. Engelhardt A, Hodges JK, Niemitz C, Heistermann M, (2005) Female sexual behavior, but not sex skin swelling, reliably indicates the timing of the fertile phase in wild long-tailed macaques (Macaca fascicularis). Hormones and Behavior, 47, 195-204.
31. Engelhardt A, Heistermann M, Hodges JK, Nuernberg P, Niemitz C, (2006) Determinants of male reproductive success in wild long-tailed macaques (Macaca fascicularis) -male monopolization, female mate choice or post-copulatory mechanism? Behavioral Ecology and Sociobiology, 59, 740-752.
32. Fox J, Weisberg S, (2011) An R Companion to Applied Regression. Sage, Thousand Oaks, CA.
33. Fürtbauer I, Schülke O, Heistermann M, Ostner J, (2010) Reproductive and Life History Parameters of Wild Female Macaca assamensis. International Journal of Primatology, 31, 501-517.
34. Fürtbauer I, Heistermann M, Schülke O, Ostner J, (2011) Concealed Fertility and Extended Female Sexuality in a Non-Human Primate (Macaca assamensis). PLoS ONE, 6, e23105.
35. Garcia C, Shimizu K, Huffman M, (2009) Relationship between sexual interactions and the timing of the fertile phase in captive female Japanese macaques (Macaca fuscata). American Journal of Primatology, 71, 868-879.
36. Geary DC, (2000) Evolution and proximate expression of human paternal investment. Psychological Bulletin, 126, 55-77.
37. Gouzoules S, Gouzoules H, (1987) Kinship. In: Primate Societies (eds, Smuts B. B., Cheney D. L., Seyfarth R. M., Wrangham R. W., &, Struhsaker T. T.,), pp. 299-305. University of Chicago Press, Chicago.
38. Greenwood PJ, (1980) Mating systems, philopatry and dispersal in birds and mammals. Animal Behaviour, 28, 1140-1162.
39. Gubernick DJ, Teferi T, (2000) Adaptive significance of male parental care in a monogamous mammal. Proceedings of the Royal Society B: Biological Sciences, 267, 147-150.
40. Heistermann M, Ziegler T, van Schaik CP, Launhardt K, Winkler P, Hodges JK, (2001) Loss of oestrus, concealed ovulation and paternity confusion in free-ranging Hanuman langurs. Proceedings of the Royal Society B: Biological Sciences, 268, 2445-2451.
41. Higham JP, Brent LJN, Dubuc C, et al,. (2010) Color signal information content and the eye of the beholder: a case study in the rhesus macaque. Behavioral Ecology, 21, 739-746.
42. Higham JP, Hughes KD, Brent LJN, et al. (2011) Familiarity affects the assessment of female facial signals of fertility by free-ranging male rhesus macaques. Proceedings of the Royal Society B: Biological Sciences, 278, 3452-3458.
43. Hill D, (1986) Social relationships between adult male and immature rhesus macaques. Primates, 27, 425-440.
44. van Horn RC, Wahaj SA, Holekamp KE, (2004) Role-reversed nepotism among cubs and sires in the spotted hyena. Ethology, 110, 413-426.
45. Hrdy SB, (1979) Infanticide among animals: a review, classification, and examination of implications for the reproductive strategies of females. Ethology and Sociobiology, 1, 13-40.
46. Huchard E, Alvergne A, Féjan D, Knapp L, Cowlishaw G, Raymond M, (2010) More than friends? Behavioural and genetic aspects of heterosexual associations in wild chacma baboons. Behavioral Ecology and Sociobiology, 64, 769-781.
47. Huchard E, Charpentier MJ, Marshall H, King AJ, Knapp LA, Cowlishaw G, (2013) Paternal effects on access to resources in a promiscuous primate society. Behavioral Ecology, 24, 229-236.
48. Jones JS, Wynne-Edwards KE, (2001) Paternal behaviour in biparental hamsters, Phodopus campbelli, does not require contact with the pregnant female. Animal Behaviour, 62, 453-464.
49. 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.
50. Kaufman AB, Rosenthal R, (2009) Can you believe my eyes? The importance of interobserver reliability statistics in observations of animal behaviour. Animal Behaviour, 78, 1487-1491.
51. Kazem AJN, Widdig A, (2013) Visual phenotype matching: cues to paternity are present in rhesus macaque faces. PLoS ONE, 8, e55846.
52. Keddy Hector AC, Seyfarth RM, Raleigh MJ, (1989) Male paternal care, female choice and the effect of an audience in vervet monkeys. Animal Behaviour, 38, 262-271.
53. 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.
54. Lehmann J, Boesch C, (2008) Sexual differences in chimpanzee sociality. International Journal of Primatology, 29, 65-81.
55. Li JH, Yin HB, Wang QS, (2005) Seasonality of reproduction and sexual activity in female Tibetan macaques (Macaca thibetana) at Huangshan, China. Acta Zoologica Sinica, 51, 365-375.
56. Lindburg DG, (1969) Rhesus monkeys: mating season mobility of adult males. Science, 166, 1176-1178.
57. Lindburg DG, (1971) The rhesus monkeys in North India: an ecological and behavioral study. In: Primate Behavior (ed, Rosenblum L. A.,), pp. 1-106. Academic Press, New York.
58. Maestripieri D, (1994) Costs and benefits of maternal aggression in lactating female rhesus macaques. Primates, 35, 443-453.
59. Makin JW, Porter RH, (1984) Paternal behavior in the spiny mouse (Acomys cahirinus). Behavioral and Neural Biology, 41, 135-151.
60. Manson JH, (1992) Measuring female mate choice in Cayo Santiago rhesus macaques. Animal Behaviour, 44, 405-416.
61. Ménard N, Segesser F, Scheffrahn W, et al,. (2001) Is male-infant caretaking related to paternity and/or mating activities in wild Barbary macaques (Macaca sylvanus)? Comptes rendus de l'Académie des Sciences III Vie, 324, 601-610.
62. Moscovice LR, Heesen M, Di Fiore A, Seyfarth R, Cheney D, (2009) Paternity alone does not predict long-term investment in juveniles by male baboons. Behavioral Ecology and Sociobiology, 63, 1471-1482.
63. Moscovice LR, Di Fiore A, Crockford C, et al,. (2010) Hedging their bets? Male and female chacma baboons form friendships based on likelihood of paternity. Animal Behaviour, 79, 1007-1015.
64. Nagy M, Otremba P, Krüger C, et al. (2005) Optimization and validation of a fully automated silica-coated magnetic beads purification technology in forensics. Forensic Science International, 152, 13-22.
65. Neumann C, Duboscq J, Dubuc C, et al,. (2011) Assessing dominance hierarchies: validation and advantages of progressive evaluation with Elo-rating. Animal Behaviour, 82, 911-921.
66. Onyango PO, Gesquiere LR, Altmann J, Alberts SC, (2012) Testosterone positively associated with both male mating effort and paternal behavior in savanna baboons (Papio cynocephalus). Hormones and Behavior 63, 430-436.
67. Ostner J, Chalise MK, Koenig A, et al,. (2006) What hanuman langur males know about female reproductive status. American Journal of Primatology, 68, 701-712.
68. Paul A, Kuester J, Arnemann J, (1996) The sociobiology of male-infant interactions in Barbary macaques, Macaca sylvanus. Animal Behaviour, 51, 155-170.
69. Quinn GP, Keough MJ, (2002) Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge, UK.
70. R Development Core Team (2012) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
71. Rawlins RG, Kessler MJ, (eds.) (1986) The Cayo Santiago Macaques. History, Behavior and Biology. State University of New York Press, Albany.
72. Ribble D, Perrin M, (2005) Social organization of the Eastern Rock Elephant-shrew (Elephantulus myurus): the evidence for mate guarding. Belgian Journal of Zoology, 135, 167-173.
73. Santos CV, Martins MM, (2000) Parental care in the buffy-tufted-ear marmoset (Callithrix aurita) in wild and captive groups. Revista Brasileira de Biologia, 60, 667-672.
74. van Schaik CP, Janson CH, (eds.) (2000) Infanticide by Males and its Implications. Cambridge University Press, Cambridge.
75. van Schaik CP, Paul A, (1996) Male care in primates: does it ever reflect paternity? Evolutionary Anthropology, 5, 152-156.
76. Sherman PW, (1989) Mate guarding as paternity insurance in Idaho ground squirrels. Nature, 338, 418-420.
77. Silk JB, Short J, Roberts J, Kusnitz J, (1993) Gestation length in rhesus macaques (Macaca mulatta). International Journal of Primatology, 14, 95-104.
78. Smuts BB, (1985) Sex and Friendship in Baboons. Aldine, New York, NY.
79. Stoehr AM, (1999) Are significance thresholds appropriate for the study of animal behaviour? Animal Behaviour, 57, F22-F25.
80. Trainor BC, Marler CA, (2001) Testosterone, paternal behavior, and aggression in the monogamous California mouse (Peromyscus californicus). Hormones and Behavior, 40, 32-42.
81. Trivers RL, (1972) Parental investment and sexual selection. In: Sexual Selection and the Descent of man (ed, Campbell B.,), pp. 139-179. Aldine, Chicago.
82. de Vries H, (1998) Finding a dominance order most consistent with a linear hierarchy: a new procedure and review. Animal Behaviour, 55, 827-843.
83. 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, USA, 98, 13769-13773.
84. Widdig A, Bercovitch FB, Streich WJ, Sauermann U, Nürnberg P, Krawczak M, (2004) A longitudinal analysis of reproductive skew in male rhesus macaques. Proceedings. Biological Sciences/The Royal Society, 271, 819-826.
85. Widdig A, Nürnberg P, Bercovitch FB, et al,. (2006a) Consequences of group fission for the patterns of relatedness among rhesus macaques. Molecular Ecology, 15, 3825-3832.
86. Widdig A, Streich WJ, Nürnberg P, Croucher PJP, Bercovitch FB, Krawczak M, (2006b) Paternal kin bias in the agonistic interventions of adult female rhesus macaques (Macaca mulatta). Behavioral Ecology and Sociobiology, 61, 205-214.
87. Zehr JL, Tannenbaum PL, Jones B, Wallen K, (2000) Peak occurrence of female sexual initiation predicts day of conception in rhesus monkeys (Macaca mulatta). Reproduction Fertility and Development, 12, 397-404.
88. Zehr JL, Meter PEV, Wallen K, (2005) Factors regulating the timing of puberty onset in female rhesus monkeys (Macaca mulatta): role of prenatal androgens, social rank, and adolescent body weight. Biology of Reproduction, 72, 1087-1094.