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Sex Differences in the Development of Aggressive Behavior in Rhesus Macaques (Macaca mulatta)

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Abstract

Aggressive behavior plays a central role in primate life, having a crucial effect on their reproductive performance and survival and possibly affecting the formation and maintenance of social bonds. Although aggressive behavior might serve a different function in males and females, and sex differences in aggressive behavior seem to emerge early during development, very few studies have investigated whether aggressive patterns follow different developmental trajectories in male and female primates. However, the developmental perspective is crucial to understanding when differences in adults’ aggression emerge and which factors trigger them. We here analyzed aggressive interactions in rhesus macaques from birth to sexual maturation (before male dispersal), including male and female focal subjects. We further considered the partner’s sex, age, and rank, as well as maternal and paternal kinship, and used powerful multivariate statistical analysis. The probability to initiate aggression was largely similar for both sexes and throughout development. Both males and females were more aggressive toward partners of the same sex and similar age. In contrast, the probability of receiving aggression mostly differed between sexes across development and depended on the social context. The probability of receiving aggression increased through development. Finally, important developmental changes appeared between 2 and 3 yr of age, indicating that this period is crucial for the development of adult social roles. Our results suggest that aggressive behavior largely serves a similar function for both sexes during the first years of development, only partially anticipating adult aggressive patterns.

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References

  • Abondano, L. A., & Link, A. (2012). The social behavior of brown spider monkeys (Ateles hybridus) in a fragmented forest in Colombia. International Journal of Primatology, 33, 769–783.

    Article  Google Scholar 

  • Albers, M., & Widdig, A. (2013). The influence of kinship on familiar natal migrant rhesus macaques (Macaca mulatta). International Journal of Primatology, 34, 99–114.

    Article  PubMed Central  PubMed  Google Scholar 

  • Alexander, B. K., & Roth, E. M. (1971). The effects of acute crowding on aggressive behavior of Japanese monkeys. Behaviour, 39, 73–89.

    Article  CAS  PubMed  Google Scholar 

  • Altmann, J. (1974). Observational study of behavior sampling methods. Behaviour, 49, 227–267.

    Article  CAS  PubMed  Google Scholar 

  • Altmann, S. A. (1962). A field study of the sociobiology of rhesus monkeys, Macaca mulatta. Annals of the New York Academy of Sciences, 102, 338–435.

    Article  CAS  PubMed  Google Scholar 

  • Archer, J. (1994). Violence between men. In J. Archer (Ed.), Male violence (pp. 121–140). London and New York: Routledge.

    Google Scholar 

  • Archer, J., & Côté, S. (2005). Sex differences in aggressive behavior: A developmental and evolutionary perspective. In R. E. Tremblay, W. W. Hartup, & J. Archer (Eds.), Developmental origins of aggression (pp. 425–443). New York: Guilford Press.

    Google Scholar 

  • Arnold, K., & Whiten, A. (2003). Grooming interactions among the chimpanzees of the Budongo forest, Uganda: Tests of five explanatory models. Behaviour, 140, 519–552.

    Article  Google Scholar 

  • Asensio, N., Korstjens, A. H., Schaffner, C. M., & Aureli, F. (2008). Intragroup aggression, fission–fusion dynamics and feeding competition in spider monkeys. Behaviour, 145, 983–1001.

    Article  Google Scholar 

  • Baayen, H. (2008). Analyzing linguistic data: A practical introduction to statistics using R (1st ed.). Cambridge, UK: Cambridge University Press.

    Book  Google Scholar 

  • Barr, D. J., Levy, R., Scheepers, C., & Tily, H. J. (2013). Random effects structure for confirmatory hypothesis testing: Keep it maximal. Journal of Memory and Language, 68, 255–278.

    Article  Google Scholar 

  • Barrett, G. M., Shimizu, K., Bardi, M., Asaba, S., & Mori, A. (2002). Endocrine correlates of rank, reproduction, and female-directed aggression in male Japanese macaques (Macaca fuscata). Hormones and Behavior, 42, 85–96.

    Article  CAS  PubMed  Google Scholar 

  • Bates, D., Maechler, M., & Bolker, B. (2011). lme4: Linear mixed-effects models using S4 classes, R package version 0.999375-42. Available from: http://CRAN.R-project.org/package=lme4

  • Berard, J. D. (1990). Life history patterns of male rhesus macaques on Cayo Santiago. Oregon: University of Oregon.

    Google Scholar 

  • Bercovitch, F. B., & Berard, J. D. (1993). Life history costs and consequences of rapid reproductive maturation in female rhesus macaques. Behavioral Ecology and Sociobiology, 32, 103–109.

    Article  Google Scholar 

  • Bercovitch, F. B., & Goy, R. W. (1990). The socioendocrinology of reproductive development and reproductive success in macaques. In T. E. Ziegler & F. B. Bercovitch (Eds.), Socioendocrinology of primate reproduction (pp. 59–93). New York: Wiley Liss.

    Google Scholar 

  • Bercovitch, F. B., Sladky, K. K., Roy, M. M., & Goy, R. W. (1987). Intersexual aggression and male sexual activity in captive rhesus macaques. Aggressive Behavior, 13, 347–358.

    Article  Google Scholar 

  • Bercovitch, F. B., Widdig, A., Trefilov, A., Kessler, M. J., Berard, J. D., Schmidtke, J., Nürnberg, P., & Krawczak, M. (2003). A longitudinal study of age-specific reproductive output and body condition among male rhesus macaques, Macaca mulatta. Naturwissenschaften, 90, 309–312.

  • Berman, C. M., Rasmussen, K., & Suomi, S. J. (1997). Group size, infant development and social networks in free-ranging rhesus monkeys. Animal Behaviour, 53, 405–421.

    Article  Google Scholar 

  • Bernstein, I. S. (1976). Dominance, aggression and reproduction in primate societies. Journal of Theoretical Biology, 60, 459–472.

    Article  CAS  PubMed  Google Scholar 

  • Bernstein, I. S., & Ehardt, C. L. (1985a). Intragroup agonistic behavior in rhesus monkeys (Macaca mulatta). International Journal of Primatology, 6, 209–226.

    Google Scholar 

  • Bernstein, I. S., & Ehardt, C. L. (1985b). Agonistic aiding: Kinship, rank, age, and sex influences. American Journal of Primatology, 8, 37–52.

    Article  Google Scholar 

  • Bernstein, I. S., & Ehardt, C. L. (1985c). Age-sex differences in the expression of agonistic behavior in rhesus monkey (Macaca mulatta) groups. Journal of Comparative Psychology, 99, 115–132.

    Article  CAS  PubMed  Google Scholar 

  • Bernstein, I. S., & Ehardt, C. L. (1986). The influence of kinship and socialization on aggressive behaviour in rhesus monkeys (Macaca mulatta). Animal Behaviour, 34, 739–747.

    Article  Google Scholar 

  • Bernstein, I. S., & Gordon, T. P. (1974). The function of aggression in primate societies: Uncontrolled aggression may threaten human survival, but aggression may be vital to the establishment and regulation of primate societies and sociality. American Scientist, 62, 304–311.

    CAS  PubMed  Google Scholar 

  • Boesch, C. (2007). What makes us human (Homo sapiens)? The challenge of cognitive cross-species comparison. Journal of Comparative Psychology, 121, 227–240.

    Article  PubMed  Google Scholar 

  • Borries, C. (2000). Male dispersal and mating season influxes in Hanuman langurs living in multi-male groups. In P. M. Kappeler (Ed.), Primate males: Causes and consequences of variation in group composition (pp. 146–158). Cambridge, UK: Cambridge University Press.

    Google Scholar 

  • Bramblett, C. A. (1980). A model for development of social behavior in vervet monkeys. Developmental Psychobiology, 13, 205–223.

    Article  CAS  PubMed  Google Scholar 

  • Call, J., & Tomasello, M. (1996). The effect of humans on the cognitive development of apes. In A. E. Russon, K. A. Bard, & S. T. Parker (Eds.), Reaching into thought: The minds of the great apes (pp. 371–403). Cambridge, UK: Cambridge University Press.

    Google Scholar 

  • Campbell, C. J. (2003). Female-directed aggression in free-ranging Ateles geoffroyi. International Journal of Primatology, 24, 223–237.

    Article  Google Scholar 

  • Campbell, C. J. (2006). Lethal intragroup aggression by adult male spider monkeys (Ateles geoffroyi). American Journal of Primatology, 68, 1197–1201.

    Article  PubMed  Google Scholar 

  • Carpenter, C. R. (1940). A field study in Siam of the behavior and social relations of the gibbon (Hylobates lar). Comparative Psychology Monographs, 16, 1–212.

    Google Scholar 

  • Chapais, B. (1992). The role of alliances in social inheritance of rank among female primates. In A. H. Harcourt & F. B. M. de Waal (Eds.), Coalitions and alliances in humans and other animals (pp. 29–59). Oxford: Oxford University Press.

    Google Scholar 

  • Charpentier, M. J. E., Peignot, P., Hossaert-Mckey, M., & Wickings, E. J. (2007). Kin discrimination in juvenile mandrills, Mandrillus sphinx. Animal Behaviour, 73, 37–45.

    Article  Google Scholar 

  • Colvin, J. (1983). Familiarity, rank, and the structure of rhesus male peers networks. In R. A. Hinde (Ed.), Primate social relationships: An integrated approach (pp. 190–200). Oxford: Blackwell.

    Google Scholar 

  • Cords, M., Sheehan, M. J., & Ekernas, L. S. (2010). Sex and age differences in juvenile social priorities in female philopatric, nondespotic blue monkeys. American Journal of Primatology, 72, 193–205.

    Article  PubMed  Google Scholar 

  • Crockett, C. M., & Pope, T. R. (1993). Consequences of sex differences in dispersal for juvenile red howler monkeys. In M. E. Pereira & L. A. Fairbanks (Eds.), Juvenile primates: Life history, development and behavior (pp. 104–118). Chicago: University of Chicago Press.

    Google Scholar 

  • Crockford, C., Wittig, R. M., Mundry, R., & Zuberbühler, K. (2012). Wild chimpanzees inform ignorant group members of danger. Current Biology, 22, 142–146.

    Article  CAS  PubMed  Google Scholar 

  • Crockford, C., Wittig, R. M., Whitten, P. L., Seyfarth, R. M., & Cheney, D. L. (2008). Social stressors and coping mechanisms in wild female baboons (Papio hamadryas ursinus). Hormones and Behavior, 53, 254–265.

    Article  PubMed  Google Scholar 

  • Darwin, C. (1871). The descent of man and the selection in relation to sex. London: John Murray.

    Google Scholar 

  • Datta, S. (1988). The acquisition of dominance among free-ranging rhesus monkey siblings. Animal Behaviour, 36, 754–772.

    Article  Google Scholar 

  • Deag, J. M. (1977). Aggression and submission in monkey societies. Animal Behaviour, 25(Part 2), 465–474.

    Article  Google Scholar 

  • De Vries, H. (1998). Finding a dominance order most consistent with a linear hierarchy: A new procedure and review. Animal Behaviour, 55, 827–843.

    Article  PubMed  Google Scholar 

  • De Waal, F. B. M. (1989). Dominance “style” and primate social organization. In V. Standen & R. A. Foley (Eds.), Comparative socioecology (pp. 243–263). Oxford: Blackwell.

    Google Scholar 

  • De Waal, F. B. M., & Johanowicz, D. L. (1993). Modification of reconciliation behavior through social experience: An experiment with two macaque species. Child Development, 64, 897–908.

    Article  PubMed  Google Scholar 

  • De Waal, F. B. M., & Luttrell, L. M. (1989). Toward a comparative socioecology of the genus Macaca: Different dominance styles in rhesus and stumptail monkeys. American Journal of Primatology, 19, 83–109.

    Article  Google Scholar 

  • Dittus, W. P. J. (1977). The social regulation of population density and age-sex distribution in the toque monkey. Behaviour, 63, 281–322.

    Article  Google Scholar 

  • Dittus, W. P. J. (1979). The evolution of behaviors regulating density and age-specific sex ratios in a prmate population. Behaviour, 69, 265–301.

    Article  Google Scholar 

  • Dixson, A. F., & Nevison, C. M. (1997). The socioendocrinology of adolescent development in male rhesus monkeys (Macaca mulatta). Hormones and Behavior, 31, 126–135.

    Article  CAS  PubMed  Google Scholar 

  • Dobson, A. J. (2002). An introduction to generalized linear models (2nd ed.). Boca Raton, FL: CRC Press.

    Google Scholar 

  • Dunbar, R. I. M. (1988). Primate social systems. Ithaca, NY: Cornell University Press.

    Book  Google Scholar 

  • Eaton, G. G., Johnson, D. F., Glick, B. B., & Worlein, J. M. (1986). Japanese macaques (Macaca fuscata) social development: Sex differences in juvenile behavior. Primates, 27, 141–150.

    Article  Google Scholar 

  • Eaton, G. G., Modahl, K. B., & Johnson, D. F. (1981). Aggressive behavior in a confined troop of Japanese macaques: Effects of density, season, and gender. Aggressive Behavior, 7, 145–164.

    Article  Google Scholar 

  • Ekernas, L. S., & Cords, M. (2007). Social and environmental factors influencing natal dispersal in blue monkeys, Cercopithecus mitis stuhlmanni. Animal Behaviour, 73, 1009–1020.

    Article  Google Scholar 

  • Elo, A. E. (1978). The rating of chess players, past and present. New York: Arco.

    Google Scholar 

  • Fedigan, L. M., & Baxter, M. J. (1984). Sex differences and social organization in free-ranging spider monkeys (Ateles geoffroyi). Primates, 25, 279–294.

    Article  Google Scholar 

  • Feldblum, J. T., Wroblewski, E. E., Rudicell, R. S., Hahn, B. H., Paiva, T., Cetinkaya-Rundel, M., Pusey, A. E., & Gilby, I. C. (2014). Sexually coercive male chimpanzees sire more offspring. Current Biology, 24, 2855–2860.

  • Fox, J., & Weisberg, S. (2011). An R companion to applied regression, 2nd ed. Thousand Oaks, CA: SAGE. Available from: http://socserv.socsci.mcmaster.ca/jfox/Books/Companion

  • Fraser, O. N., Schino, G., & Aureli, F. (2008). Components of relationship quality in chimpanzees. Ethology, 114, 834–843.

    Article  Google Scholar 

  • Gilby, I. C., & Wrangham, R. W. (2008). Association patterns among wild chimpanzees (Pan troglodytes schweinfurthii) reflect sex differences in cooperation. Behavioral Ecology and Sociobiology, 62, 1831–1842.

    Article  Google Scholar 

  • Glick, B. B., Eaton, G. G., Johnson, D. F., & Worlein, J. M. (1986). Development of partner preferences in Japanese macaques (Macaca fuscata): Effects of gender and kinship during the second year of life. International Journal of Primatology, 7, 467–479.

    Article  Google Scholar 

  • Goodall, J. (1986). The chimpanzees of Gombe: Patterns of behavior. Cambridge, MA: Belknap Press of Harvard University.

    Google Scholar 

  • Gould, L., Ziegler, T. E., & Wittwer, D. J. (2005). Effects of reproductive and social variables on fecal glucocorticoid levels in a sample of adult male ring-tailed lemurs (Lemur catta) at the Beza Mahafaly Reserve, Madagascar. American Journal of Primatology, 67, 5–23.

    Article  CAS  PubMed  Google Scholar 

  • Gouzoules, S., & Gouzoules, H. (1987). Kinship. In B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, & T. T. Struhsaker (Eds.), Primate societies (pp. 299–305). Chicago: University of Chicago Press.

    Google Scholar 

  • Ha, J. C., Alloway, H., & Sussman, A. (2011). Aggression in pigtailed macaque (Macaca nemestrina) breeding groups affects pregnancy outcome. American Journal of Primatology, 73, 1169–1175.

    Article  PubMed Central  PubMed  Google Scholar 

  • Hall, K. R. L. (1964). Aggression in monkey and ape societies. In J. D. Carthy & F. J. Ebling (Eds.), The natural history of aggression (pp. 51–64). London and New York: Academic Press. Available from: http://www.opus4.kobv.de/opus4-Fromm/frontdoor/index/index/docId/11379

  • Heesen, M., Rogahn, S., Macdonald, S., Ostner, J., & Schülke, O. (2014). Predictors of food-related aggression in wild Assamese macaques and the role of conflict avoidance. Behavioral Ecology and Sociobiology, 68, 1829–1841.

    Article  Google Scholar 

  • Higham, J. P., Heistermann, M., & Maestripieri, D. (2012). The endocrinology of male rhesus macaque social and reproductive status: A test of the challenge and social stress hypotheses. Behavioral Ecology and Sociobiology, 67, 19–30.

    Article  Google Scholar 

  • Honess, P. E., & Marin, C. M. (2006). Behavioural and physiological aspects of stress and aggression in nonhuman primates. Neuroscience & Biobehavioral Reviews, 30, 390–412.

    Article  CAS  Google Scholar 

  • Janson, C. H., & Van Schaik, C. P. (1988). Recognizing the many faces of primate food competition: Methods. Behaviour, 105, 165–186.

    Article  Google Scholar 

  • Janus, M. (1991a). Aggression in interactions of immature rhesus monkeys: Components, context and relation to affiliation levels. Animal Behaviour, 41, 121–134.

    Article  Google Scholar 

  • Janus, M. (1991b). Aggression in interactions of immature rhesus monkeys: Components, context and relation to affiliation level. Animal Behaviour, 41, 121–134.

    Article  Google Scholar 

  • Kapsalis, E., & Berman, C. M. (1996). Models of affiliative relationships among free-ranging rhesus monkeys (Macaca mulatta) I. Criteria for kinship. Behaviour, 133, 1209–1234.

    Article  Google Scholar 

  • Kaufman, A. B., & Rosenthal, R. (2009). Can you believe my eyes? The importance of interobserver reliability statistics in observations of animal behaviour. Animal Behaviour, 78, 1487–1491.

    Article  Google Scholar 

  • Koenig, A., Beise, J., Chalise, M. K., & Ganzhorn, J. U. (1998). When females should contest for food – testing hypotheses about resource density, distribution, size, and quality with Hanuman langurs (Presbytis entellus). Behavioral Ecology and Sociobiology, 42, 225–237.

    Article  Google Scholar 

  • Koyama, N. (1985). Playmate relationships among individuals of the Japanese monkey troop in Arashiyama. Primates, 26, 390–406.

    Article  Google Scholar 

  • Kulik, L., Amici, F., Langos, D., & Widdig, A. (2015). Sex differences in the development of social relationships in rhesus macaques (Macaca mulatta). International Journal of Primatology, 36, 353–376.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • Lambert, J. E. (2005). Competition, predation, and the evolutionary significance of the cercopithecine cheek pouch: The case of Cercopithecus and Lophocebus. American Journal of Physical Anthropology, 126, 183–192.

    Article  PubMed  Google Scholar 

  • Lambert, J. E., & Whitham, J. C. (2001). Cheek pouch use in Papio cynocephalus. Folia Primatologica, 72, 89–91.

    Article  CAS  Google Scholar 

  • Langos, D., Kulik, L., Mundry, R., & Widdig, A. (2013). The impact of paternity on male–infant association in a primate with low paternity certainty. Molecular Ecology, 22, 3638–3651.

    Article  PubMed Central  PubMed  Google Scholar 

  • Lindburg, D. G. (1969). Rhesus monkeys: Mating season mobility of adult males. Science, 166, 1176–1178.

    Article  CAS  PubMed  Google Scholar 

  • Link, A., Di Fiore, A., & Spehar, S. N. (2009). Female-directed aggression and social control in spider monkeys. In M. N. Muller & R. W. Wrangham (Eds.), Sexual coercion in primates and humans: An evolutionary perspective on male aggression against females (pp. 157–183). Cambridge, MA: Harvard University Press.

    Google Scholar 

  • Lonsdorf, E. V., Markham, A. C., Heintz, M. R., Anderson, K. E., Ciuk, D. J., Goodall, J., & Murray, C. M. (2014). Sex differences in wild chimpanzee behavior emerge during infancy. PLoS ONE, 9, e99099.

  • Lorenz, K. (1966). On aggression. London and New York: Psychology Press.

    Google Scholar 

  • Majolo, B., Ventura, R., & Koyama, N. F. (2005). Sex, rank and age differences in the Japanese macaque (Macaca fuscata yakui) participation in inter-group encounters. Ethology, 111, 455–468.

    Article  Google Scholar 

  • Markham, A. C., Lonsdorf, E. V., Pusey, A. E., & Murray, C. M. (2015). Maternal rank influences the outcome of aggressive interactions between immature chimpanzees. Animal Behaviour, 100, 192–198.

    Article  PubMed  Google Scholar 

  • Marriott, B. M., Roemer, J., & Sultana, C. (1989). An overview of the food intake patterns of the Cayo Santiago rhesus monkeys (Macaca mulatta): Report of a pilot study. Puerto Rico Health Sciences Journal, 8, 87–94.

    CAS  PubMed  Google Scholar 

  • Mitchell, G. (1979). Behavioral sex differences in nonhuman primates. New York: Van Nostrand Reinhold.

    Google Scholar 

  • Muller, M. N., & Mitani, J. C. (2005). Conflict and cooperation in wild chimpanzees. Advances in the Study of Behavior, 35, 275–331.

    Article  Google Scholar 

  • Mundry, R. (2014). Statistical issues and assumptions of phylogenetic generalized least squares. In L. Z. Garamszegi (Ed.), Modern phylogenetic comparative methods and their application in evolutionary biology (pp. 131–153). Berlin and Heidelberg: Springer-Verlag. Available from: http://link.springer.com/chapter/10.1007/978-3-662-43550-2-6.

  • Nakamichi, M. (1989). Sex differences in social development during the first 4 years in a free-ranging group of Japanese monkeys, Macaca fuscata. Animal Behaviour, 38, 737–748.

    Article  Google Scholar 

  • Nakamichi, M. (2001). Mother-offspring relationship in macaques. In T. Matsuzawa (Ed.), Primate origins of human cognition and behavior (pp. 418–440). Tokyo: Springer-Verlag. Available from: http://link.springer.com/chapter/10.1007/978-4-431-09423-4-21.

  • Neumann, C., Duboscq, J., Dubuc, C., Ginting, A., Irwan, A. M., Agil, M., Widdig, A., & Engelhardt, A. (2011). Assessing dominance hierarchies: Validation and advantages of progressive evaluation with Elo-rating. Animal Behaviour, 82, 911–921.

  • Nishida, T. (1979). The social structure of chimpanzees at the Mahale Mountains. In D. A. Hamburg & E. R. McCown (Eds.), The great apes (pp. 73–121). Menlo Park, CA: Benjamin Cummings.

    Google Scholar 

  • Nürnberg, P., Sauermann, U., Kayser, M., Lanfer, C., Manz, E., Widdig, A., Berard, J., Bercovitch, F. B., Kessler, M., Schmidtke, J., & Krawczak, M. (1998). Paternity assessment in rhesus macaques (Macaca mulatta): Multilocus DNA fingerprinting and PCR marker typing. American Journal of Primatology, 44, 1–18.

  • Ostner, J., Heistermann, M., & Schülke, O. (2008). Dominance, aggression and physiological stress in wild male Assamese macaques (Macaca assamensis). Hormones and Behavior, 54, 613–619.

    Article  PubMed  Google Scholar 

  • Owens, N. W. (1975). Social play behaviour in free-living baboons, Papio anubis. Animal Behaviour, 230(Part 2), 387–408.

    Article  Google Scholar 

  • Pereira, M. E. (1995). Development and social dominance among group-living primates. American Journal of Primatology, 37, 143–175.

    Article  Google Scholar 

  • Pereira, M. E., & Fairbanks, L. A. (Eds.). (1993). Juvenile primates: Life history, development and behavior. Chicago: University of Chicago Press.

    Google Scholar 

  • Pereira, M. E., & Kappeler, P. M. (1997). Divergent systems of agonistic behaviour in Lemurid primates. Behaviour, 134, 225–274.

    Article  Google Scholar 

  • Perry, S. (1996). Female-female social relationships in wild white-faced capuchin monkeys, Cebus capucinus. American Journal of Primatology, 40, 167–182.

    Article  Google Scholar 

  • Pusey, A. E., & Packer, C. (1987). Dispersal and philopatry. In B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, & T. T. Struhsaker (Eds.), Primate societies (pp. 250–266). Chicago: University of Chicago Press.

    Google Scholar 

  • Quinn, G. P., & Keough, M. J. (2002). Experimental design and data analysis for biologists (1st ed.). Cambridge, UK: Cambridge University Press.

    Book  Google Scholar 

  • Rajpurohit, L. S., & Sommer, V. (1993). Juvenile male emigration from natal one-male troops in hanuman langurs. In M. E. Pereira & L. A. Fairbanks (Eds.), Juvenile primates: Life history, development and behavior (pp. 86–103). Chicago: University of Chicago Press.

    Google Scholar 

  • Raleigh, M. J., Flannery, J. W., & Ervin, F. R. (1979). Sex differences in behavior among juvenile vervet monkeys (Cercopithecus aethiops sabaeus). Behavioral and Neural Biology, 26, 455–465.

    Article  Google Scholar 

  • Rawlins, R. G., & Kessler, M. J. (Eds.). (1986). The Cayo Santiago macaques: History, behavior and biology. Albany: State University of New York Press.

    Google Scholar 

  • R Core Team. (2014). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available from: http://www.R-project.org/

  • Reinhardt, V. (1987). Are male rhesus monkeys more aggressive than females? Primates, 28, 123–125.

    Article  Google Scholar 

  • Roney, J. R., & Maestripieri, D. (2005). Social development and affiliation. In D. Maestripieri (Ed.), Primate psychology (pp. 171–204). Cambridge, MA: Harvard University Press.

    Google Scholar 

  • Rowell, T. E., & Chism, J. (1986). The ontogeny of sex differences in the behavior of patas monkeys. International Journal of Primatology, 7, 83–107.

    Article  Google Scholar 

  • Rudran, R. (1978). Sociobiology of the blue monkeys (Cercopithecus mitis stuhlmanni) of the Kibale Forest, Uganda. Smithsonian Contributions to Zoology, 249, 1–88.

    Google Scholar 

  • Sapolsky, R. M. (2005). The influence of social hierarchy on primate health. Science, 308, 648–652.

    Article  CAS  PubMed  Google Scholar 

  • Schielzeth, H. (2010). Simple means to improve the interpretability of regression coefficients. Methods in Ecology and Evolution, 1, 103–113.

    Article  Google Scholar 

  • Schielzeth, H., & Forstmeier, W. (2009). Conclusions beyond support: Overconfident estimates in mixed models. Behavioral Ecology, 20, 416–420.

    Article  PubMed Central  PubMed  Google Scholar 

  • Seyfarth, R. M. (1976). Social relationships among adult female baboons. Animal Behaviour, 24, 917–938.

    Article  Google Scholar 

  • Seyfarth, R. M. (1980). The distribution of grooming and related behaviours among adult female vervet monkeys. Animal Behaviour, 28, 798–813.

    Article  Google Scholar 

  • Silk, J. B. (2007). The adaptive value of sociality in mammalian groups. Philosophical Transactions of the Royal Society B: Biological Sciences, 362, 539–559.

    Article  Google Scholar 

  • Silk, J. B., Alberts, S. C., & Altmann, J. (2004). Patterns of coalition formation by adult female baboons in Amboseli, Kenya. Animal Behaviour, 67, 573–582.

    Article  Google Scholar 

  • Silk, J. B., & Boyd, R. (1983). Female cooperation, competition, and mate choice in matrilineal macaque groups. In S. K. Wasser (Ed.), Social behavior of female vertebrates (pp. 315–347). New York: Academic Press.

    Google Scholar 

  • Silk, J. B., Samuels, A., & Rodman, P. S. (1981). The influence of kinship, rank, and sex on affiliation and aggression between adult female and immature bonnet macaques (Macaca radiata). Behaviour, 78, 111–137.

    Article  Google Scholar 

  • Silk, J. B., Seyfarth, R. M., & Cheney, D. L. (1999). The structure of social relationships among female savanna baboons in Moremi Reserve, Botswana. Behaviour, 136, 679–703.

    Article  Google Scholar 

  • Slater, K. Y., Schaffner, C. M., & Aureli, F. (2008). Female-directed male aggression in wild Ateles geoffroyi yucatanensis. International Journal of Primatology, 29, 1657–1669.

    Article  Google Scholar 

  • Slater, K. Y., Schaffner, C. M., & Aureli, F. (2009). Sex differences in the social behavior of wild spider monkeys (Ateles geoffroyi yucatanensis). American Journal of Primatology, 71, 21–29.

    Article  PubMed  Google Scholar 

  • Strier, K. B., Dib, L. T., & Figueira, J. E. C. (2002). Social dynamics of male muriquis (Brachyteles arachnoides hypoxanthus). Behaviour, 139, 315–342.

    Article  Google Scholar 

  • Struhsaker, T. T., & Leland, L. (1976). Socioecology of five sympatric monkey species in the Kibale Forest, Uganda. New York: Academic Press.

    Google Scholar 

  • Suomi, S. J. (2005). Mother-infant attachment, peer relationships, and the development of social networks in rhesus monkeys. Human Development, 48, 67–79.

    Article  Google Scholar 

  • Thierry, B. (1990). Feedback loop between kinship and dominance: The macaque model. Journal of Theoretical Biology, 145, 511–522.

    Article  CAS  PubMed  Google Scholar 

  • Thierry, B., Singh, M., & Kaumanns, W. (Eds.). (2004). Macaque societies: A model for the study of social organization. Cambridge, UK: Cambridge University Press.

    Google Scholar 

  • Tinbergen, N. (1968). On war and peace in animals and man: An ethologist’s approach to the biology of aggression. Science, 160, 1411–1418.

    Article  CAS  PubMed  Google Scholar 

  • Trivers, R. L. (1972). Parental investment and sexual selection. In B. Campbell (Ed.), Sexual selection and the descent of man (pp. 139–179). Chicago: Aldine.

    Google Scholar 

  • Valero, A., Schaffner, C. M., Vick, L. G., Aureli, F., & Ramos-Fernandez, G. (2006). Intragroup lethal aggression in wild spider monkeys. American Journal of Primatology, 68, 732–737.

    Article  PubMed  Google Scholar 

  • Van Roosmalen, M. G. M., & Klein, L. L. (1988). The spider monkeys, genus Ateles. In R. A. Mittermeier, A. B. Rylands, C. A. F. Filho, & G. A. B. da Fonseca (Eds.), Ecology and behavior of neotropical primates, Vol. 2 (pp. 455–537). Washington, DC: World Wildlife Fund.

  • Van Schaik, C. P. (1983). Why are diurnal primates living in groups? Behaviour, 87, 102–144.

    Google Scholar 

  • Van Schaik, C. P. (1989). The ecology of social relationships amongst female primates. In V. Standen & R. A. Foley (Eds.), Comparative socioecology: The behavioural ecology of humans and other mammals (pp. 195–218). Oxford: Blackwell.

    Google Scholar 

  • Van Schaik, C. P., & Kappeler, P. M. (1997). Infanticide risk and the evolution of male–female association in primates. Proceedings of the Royal Society of London B: Biological Sciences, 264, 1687–1694.

    Article  Google Scholar 

  • Walters, J. R., & Seyfarth, R. M. (1987). Conflict and cooperation. In B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, & T. T. Struhsaker (Eds.), Primate societies (pp. 306–317). Chicago: University of Chicago Press.

    Google Scholar 

  • Watts, D. P. (2000a). Grooming between male chimpanzees at Ngogo, Kibale National Park. II. Influence of male rank and possible competition for partners. International Journal of Primatology, 21, 211–238.

    Article  Google Scholar 

  • Watts, D. P. (2000b). Grooming between male chimpanzees at Ngogo, Kibale National Park. I. Partner number and diversity and grooming reciprocity. International Journal of Primatology, 21, 189–210.

    Article  Google Scholar 

  • Widdig, A. (2007). Paternal kin discrimination: The evidence and likely mechanisms. Biological Reviews, 82, 319–334.

    Article  PubMed  Google Scholar 

  • Widdig, A. (2013). The impact of male reproductive skew on kin structure and sociality in multi-male groups. Evolutionary Anthropology, 22, 239–250.

    Article  PubMed  Google Scholar 

  • Widdig, A., Kessler, M. J., Bercovitch, F., Berard, J. D., Duggleby, C., Nürnberg, P., Rawlins, R. G., Sauermann, U., Wang, Q., Krawczak, M., & Schmidtke, J. (2015a). Genetic studies on the Cayo Santiago rhesus macaques: A review of 40 years of research. American Journal of Primatologyhttp://onlinelibrary.wiley.com/doi/10.1002/ajp.22424/abstract  

  • Widdig, A., Langos, D., & Kulik, L. (2015b). Sex differences in kin bias at maturation: Male rhesus macaques prefer paternal kin prior to natal dispersal. American Journal of Primatology. Available from: http://onlinelibrary.wiley.com/doi/10.1002/ajp.22401/abstract

  • Widdig, A., Nürnberg, P., Krawczak, M., Streich, W. J., & Bercovitch, F. B. (2001). Paternal relatedness and age proximity regulate social relationships among adult female rhesus macaques. Proceedings of the National Academy of Sciences of the USA, 98, 13769–13773.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Widdig, A., Nürnberg, P., Krawczak, M., Streich, W. J., & Bercovitch, F. B. (2002). Affiliation and aggression among adult female rhesus macaques: A genetic analysis of paternal cohorts. Behaviour, 139, 371–391.

    Article  Google Scholar 

  • Widdig, A., Streich, W. J., Nürnberg, P., Croucher, P. J.,  Bercovitch, F. B., & Krawczak, M. (2006). Paternal kin bias in the agonistic interventions of adult female rhesus macaques (Macaca mulatta). Behavioral Ecology and Sociobiology, 61, 205–214.

  • Wilson, A. P., & Boelkins, R. C. (1970). Evidence for seasonal variation in aggressive behaviour by Macaca mulatta. Animal Behaviour, 18(Part 4), 719–724.

    Article  CAS  PubMed  Google Scholar 

  • Wilson, M. L., & Wrangham, R. W. (2003). Intergroup relations in chimpanzees. Annual Review of Anthropology, 32, 363–392.

    Article  Google Scholar 

  • Wittig, R. M., Crockford, C., Weltring, A., Deschner, T., & Zuberbühler, K. (2015). Single aggressive interactions increase urinary glucocorticoid levels in wild male chimpanzees. PLoS ONE, 10, e0118695.

    Article  PubMed Central  PubMed  Google Scholar 

  • Wolfheim, J. H. (1977). Sex differences in behavior in a group of captive juvenile talapoin monkeys (Miopithecus talapoin). Behaviour, 63, 110–127.

    Article  Google Scholar 

  • Worlein, J. M., Eaton, G. G., Johnson, D. F., & Glick, B. B. (1988). Mating season effects on mother-infant conflict in Japanese macaques, Macaca fuscata. Animal Behaviour, 36, 1472–1481.

    Article  Google Scholar 

  • Wrangham, R. W. (1980). An ecological model of female-bonded primate groups. Behaviour, 75, 262–299.

    Article  Google Scholar 

  • Wrangham, R. W., Clark, A. P., & Isabirye-Bosuta, G. (1992). Female social relationships and social organisation of Kibale Forest chimpanzees. In Topics in primatology (pp. 81–98). Tokyo: Tokyo University Press.

    Google Scholar 

  • Young, G. H., Jr., Coehlo, A. M., & Bramblett, C. A. (1982). The development of grooming, sociosexual behavior, play and aggression in captive baboons in their first two years. Primates, 23, 511–519.

    Article  Google Scholar 

  • Zehr, J. L., Meter, P. E. V., & 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.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank the CPRC for allowing us to conduct this study and providing support throughout. We are especially grateful to the staff of the Cayo Santiago Field Station, including Edgar Davila, Julio Resto, Giselle Caraballo Cruz, and Angelina Ruiz, for their cooperation during observations and DNA collection. We also thank Joyce Moewius, Akie Yanagie, Klaus Leipholz, and Margaret Chiavetta for their help with data and sample collection. We are also grateful to Fred Bercovitch, Matt Kessler, John Berard, Michael Krawczak, Peter Nürnberg, and Jörg Schmidtke, who started the genetic data base of the Cayo Santiago population, mainly funded by the National Science Foundation, National Institutes of Health, and the German Research Foundation (DFG). We would further like to thank Andrea Trefilov, Elisabeth Kirst, Peter Nürnberg, Petra Otremba, Marion Nagy, Laura Muniz, and Stefanie Bley for their help in improving and extending the genetic database, and Linda Vigilant for allowing us laboratory access. Moreover, we thank Roger Mundry for statistical advice, Hagen Stenzel for writing a number of macros for data analysis, and Brigitte Weiß for helpful discussion and comments on a previous version of the manuscript. The editor and two anonymous reviewers provided very helpful comments on an earlier version of the manuscript. The population of Cayo Santiago was supported by grant number 8P40 OD012217-25 from the National Center for Research Resources (NCRR), the Office of Research Infrastructure Programs (ORIP) of the National Institutes of Health, and the Medical Sciences Campus of the University of Puerto Rico. The content of this publication is solely the responsibility of the authors and does not necessarily represent the official views of NCRR or ORIP. We conducted this project within the Jr. Research Group of Primate Kin Selection, an Emmy-Noether Group funded by the German Research Foundation (DFG) (grant numbers WI 1801/1-1, 1-2, 2-1, 3-1 awarded to A. Widdig). Further funding was provided by a PhD grant of the University of Leipzig (awarded to L. Kulik and D. Langos) and the KKGS Stiftung, Elsa-Neumann Stiftung, and the DAAD (awarded to D. Langos). We are grateful to the Max-Planck Institute for Evolutionary Anthropology, Leipzig, for their logistic support and for hosting the Jr. Research Group of Primate Kin Selection.

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Kulik, L., Amici, F., Langos, D. et al. Sex Differences in the Development of Aggressive Behavior in Rhesus Macaques (Macaca mulatta). Int J Primatol 36, 764–789 (2015). https://doi.org/10.1007/s10764-015-9853-1

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