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Female fertile phase synchrony, and male mating and reproductive skew, in the crested macaque

  • 1.

    Darwin, C. The Descent of Man and the Selection in Relation to Sex (John Murray, London, 1871).

    Google Scholar 

  • 2.

    Miller, E. J., Eldridge, M. D. B., Cooper, D. W. & Herbert, C. A. Dominance, body size and internal relatedness influence male reproductive success in eastern grey kangaroos (Macropus giganteus). Reprod. Fertil. Dev. 22, 539–549 (2010).

    PubMed  Article  PubMed Central  Google Scholar 

  • 3.

    Hirsch, B. T. & Maldonado, J. E. Familiarity breeds progeny: Sociality increases reproductive success in adult male ring-tailed coatis (Nasua nasua). Mol. Ecol. 20, 409–419 (2011).

    PubMed  Article  PubMed Central  Google Scholar 

  • 4.

    Natoli, E., Schmid, M., Say, L. & Pontier, D. Male reproductive success in a social group of urban feral cats (Felis catus L.). Ethology 113, 283–289 (2007).

    Article  Google Scholar 

  • 5.

    Clutton-Brock, T. & Isvaran, K. Paternity loss in contrasting mammalian societies. Biol. Lett. 2, 513–516 (2006).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 6.

    Altmann, S. A. A field study of the sociobiology of rhesus monkeys, Macaca mulatta. Ann. N. Y. Acad. Sci. 102, 338–435 (1962).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 7.

    Kutsukake, N. & Nunn, C. L. Comparative tests of reproductive skew in male primates: The roles of demographic factors and incomplete control. Behav. Ecol. Sociobiol. 60, 695–706 (2006).

    Article  Google Scholar 

  • 8.

    Ostner, J., Nunn, C. L. & Schülke, O. Female reproductive synchrony predicts skewed paternity across primates. Behav Ecol 19, 1150–1158 (2008).

    PubMed  PubMed Central  Article  Google Scholar 

  • 9.

    Janson, C. & Verdolin, J. Seasonality of primate births in relation to climate. In Seasonality in Primates—Studies of Living and Extinct Human and Non-human Primates (eds Brockmann, D. K. & Van Schaik, C.) 308–351 (Cambridge University Press, Cambridge, 2005).

    Google Scholar 

  • 10.

    Gogarten, J. F. & Koenig, A. Reproductive seasonality is a poor predictor of receptive synchrony and male reproductive skew among nonhuman primates. Behav. Ecol. Sociobiol. 67, 123–134 (2012).

    Article  Google Scholar 

  • 11.

    Brockmann, D. K. & Van Schaik, C. P. Seasonality and reproductive function. In Seasonality in Primates: Studies of Living and Extinct Human and Non-human Primates (eds Brockmann, D. K. & Van Schaik, C. P.) 269–306 (Cambridge University Press, Cambridge, 2005).

    Google Scholar 

  • 12.

    Sterck, E. H. M., Watts, D. P. & van Schaik, C. P. The evolution of female social relationships in nonhuman primates. Behav. Ecol. Sociobiol. 41, 291–309 (1997).

    Article  Google Scholar 

  • 13.

    Nunn, C. L. The number of males in primate social groups: A comparative test of the socioecological model. Behav. Ecol. Sociobiol. 46, 1–13 (1999).

    Article  Google Scholar 

  • 14.

    Carnes, L. M., Nunn, C. L. & Lewis, R. J. Effects of the distribution of female primates on the number of males. PLoS One 6, 20 (2011).

    Google Scholar 

  • 15.

    Manson, J. H. Primate consortships: A critical review. Curr. Anthropol. 38(3), 353–374 (1997).

    Article  Google Scholar 

  • 16.

    Andersson, M. B. Sexual Selection (Princeton University Press, Princeton, 1994).

    Google Scholar 

  • 17.

    Fürtbauer, I., Heistermann, M., Schülke, O. & Ostner, J. Concealed fertility and extended female sexuality in a non-human primate (Macaca assamensis). PLoS One 6, e23105 (2011).

    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 18.

    Plavcan, J. M. Understanding dimorphism as a function of changes in male and female traits. Evol. Anthropol. Issues News Rev. 20, 143–155 (2011).

    Article  Google Scholar 

  • 19.

    Setchell, J. M., Charpentier, M. & Wickings, E. J. Mate guarding and paternity in mandrills: Factors influencing alpha male monopoly. Anim. Behav. 70, 1105–1120 (2005).

    Article  Google Scholar 

  • 20.

    Bradley, B. J. et al. Mountain gorilla tug-of-war: Silverbacks have limited control over reproduction in multimale groups. Proc. Natl. Acad. Sci. USA 102, 9418–9423 (2005).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 21.

    Nunn, C. L. The evolution of exaggerated sexual swellings in primates and the graded-signal hypothesis. Anim. Behav. 58(2), 229–246 (1999).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 22.

    Rodriguez-Llanes, J. M., Verbeke, G. & Finlayson, C. Reproductive benefits of high social status in male macaques (Macaca). Anim. Behav. 78, 643–649 (2009).

    Article  Google Scholar 

  • 23.

    Paul, A., Kuester, J., Timme, A. & Arnemann, J. The association between rank, mating effort and reproductive success in male Barbary macaques (Macaca sylvanus). Primates 34, 491–502 (1993).

    Article  Google Scholar 

  • 24.

    Kümmerli, R. & Martin, R. D. Male and female reproductive success in Macaca sylvanus in Gibraltar: No evidence for rank dependence. Int. J. Primatol. 26, 1229–1249 (2005).

    ADS  Article  Google Scholar 

  • 25.

    Brauch, K. et al. Sex-specific reproductive behaviours and paternity in free-ranging Barbary macaques (Macaca sylvanus). Behav. Ecol. Sociobiol. 62, 1453–1466 (2008).

    Article  Google Scholar 

  • 26.

    Berard, J. D., Nurnberg, P., Epplen, J. T. & Schmidtke, J. Alternative reproductive tactics and reproductive success in male rhesus macaques. Behaviour 129, 177–201 (1994).

    Article  Google Scholar 

  • 27.

    Widdig, A. et al. A longitudinal analysis of reproductive skew in male rhesus macaques. Proc. Biol. Sci. 271, 819–826 (2004).

    PubMed  PubMed Central  Article  Google Scholar 

  • 28.

    Dubuc, C., Muniz, L., Heistermann, M., Engelhardt, A. & Widdig, A. Testing the priority-of-access model in a seasonally breeding primate species. Behav. Ecol. Sociobiol. 65, 1615–1627 (2011).

    PubMed  PubMed Central  Article  Google Scholar 

  • 29.

    de Ruiter, J. R., van Hooff, J. A. R. A. M. & Scheffrahn, W. Social and genetic aspects of paternity in wild long-tailed macaques (Macaca fascicularis). Behaviour 129, 204–224 (1994).

    Article  Google Scholar 

  • 30.

    Engelhardt, A., Heistermann, M., Hodges, J. K., Nuernberg, P. & Niemitz, C. Determinants of male reproductive success in wild long-tailed macaques (Macaca fascicularis)—male monopolisation, female mate choice or post-copulatory mechanisms?. Behav. Ecol. Sociobiol. 59, 740–752 (2006).

    Article  Google Scholar 

  • 31.

    Plavcan, J. M. & van Schaik, C. P. Intrasexual competition and body weight dimorphism in anthropoid primates. Am. J. Phys. Anthropol. 103, 37–68 (1997).

    CAS  PubMed  Article  Google Scholar 

  • 32.

    Plavcan, J. M., van Schaik, C. P. & Kappeler, P. M. Competition, coalitions and canine size in primates. J. Hum. Evol. 28, 245–276 (1995).

    Article  Google Scholar 

  • 33.

    Groves, C. Primate Taxonomy (Smithsonian Books, Washington, 2001).

    Google Scholar 

  • 34.

    Thierry, B., Iwaniuk, A. N. & Pellis, S. M. The influence of phylogeny on the social behaviour of macaques (Primates: Cercopithecidae, genus Macaca). Ethology 106, 713–728 (2000).

    Article  Google Scholar 

  • 35.

    Duboscq, J. et al. Social tolerance in wild female crested macaques (Macaca nigra) in Tangkoko-Batuangus Nature Reserve, Sulawesi, Indonesia. Am. J. Primatol. 75, 361–375 (2013).

    PubMed  PubMed Central  Article  Google Scholar 

  • 36.

    Plavcan, J. M., van Schaik, C. P. & McGraw, W. S. Seasonality, social organization, and sexual dimorphism in primates. In Seasonality in Primates: Studies of Living and Extinct Human and Non-Human Primates (eds van Schaik, C. P. & Brockman, D. K.) 401–442 (Cambridge University Press, Cambridge, 2005). https://doi.org/10.1017/CBO9780511542343.015.

    Google Scholar 

  • 37.

    Marty, P. R., Hodges, K., Agil, M. & Engelhardt, A. Alpha male replacements and delayed dispersal in crested macaques (Macaca nigra). Am. J. Primatol. 79, e22448 (2017).

    Article  Google Scholar 

  • 38.

    Kerhoas, D., Perwitasari-Farajallah, D., Agil, M., Widdig, A. & Engelhardt, A. Social and ecological factors influencing offspring survival in wild macaques. Behav. Ecol. 25, 1164–1172 (2014).

    PubMed  PubMed Central  Article  Google Scholar 

  • 39.

    Neumann, C., Assahad, G., Hammerschmidt, K., Perwitasari-Farajallah, D. & Engelhardt, A. Loud calls in male crested macaques, Macaca nigra: A signal of dominance in a tolerant species. Anim. Behav. 79, 187–193 (2010).

    Article  Google Scholar 

  • 40.

    Martinez-Iñigoa, L., Agil, M., Engelhardt, A., Pilot, M. & Majolo, B. Resource and mate defence influence the outcome of intergroup encounters in wild crested macaques (Macaca nigra). Primate Eye 123, 48–49 (2017).

    Google Scholar 

  • 41.

    Higham, J. P. et al. Sexual signalling in female crested macaques and the evolution of primate fertility signals. BMC Evol. Biol. 12, 89–99 (2012).

    PubMed  PubMed Central  Article  Google Scholar 

  • 42.

    Engelhardt, A. & Perwitasari-Farajallah, D. Reproductive biology of Sulawesi crested black macaques (Macaca nigra). Folia Primatol. (Basel) 79, 326 (2008).

    Google Scholar 

  • 43.

    Marty, P. R., Hodges, K., Agil, M. & Engelhardt, A. Determinants of immigration strategies in male crested macaques (Macaca nigra). Sci. Rep. 6, 32028 (2016).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 44.

    Wigby, S. & Chapman, T. Sperm competition. Curr. Biol. 14, R100–R103 (2004).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 45.

    Tregenza, T. & Wedell, N. Benefits of multiple mates in the cricket gryllus bimaculatus. Evolution 52, 1726–1730 (1998).

    PubMed  Article  PubMed Central  Google Scholar 

  • 46.

    Clutton-Brock, T. H. Reproductive skew, concessions and limited control. Trends Ecol. Evol. 13, 288–292 (1998).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 47.

    Alberts, S. C., Buchan, J. C. & Altmann, J. Sexual selection in wild baboons: From mating opportunities to paternity success. Anim. Behav. 72, 1177–1196 (2006).

    Article  Google Scholar 

  • 48.

    Boesch, C., Kohou, G., Néné, H. & Vigilant, L. Male competition and paternity in wild chimpanzees of the Taï forest. Am. J. Phys. Anthropol. 130, 103–115 (2006).

    PubMed  Article  PubMed Central  Google Scholar 

  • 49.

    Higham, J. P., Heistermann, M. & Maestripieri, D. The energetics of male-male endurance rivalry in free-ranging rhesus macaques, Macaca mulatta. Anim. Behav. 81, 1001–1007 (2011).

    Article  Google Scholar 

  • 50.

    Muniz, L. et al. Male dominance and reproductive success in wild white-faced capuchins (Cebus capucinus) at Lomas Barbudal, Costa Rica. Am. J. Primatol. 72, 1118–1130 (2010).

    PubMed  Article  PubMed Central  Google Scholar 

  • 51.

    Strier, K. B., Chaves, P. B., Mendes, S. L., Fagundes, V. & Di Fiore, A. Low paternity skew and the influence of maternal kin in an egalitarian, patrilocal primate. Proc. Natl. Acad. Sci. 108, 18915–18919 (2011).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 52.

    Daspre, A., Heistermann, M., Hodges, J. K., Lee, P. C. & Rosetta, L. Signals of female reproductive quality and fertility in colony-living baboons (Papio hanubis) in relation to ensuring paternal investment. Am. J. Primatol. 71, 529–538 (2009).

    PubMed  Article  PubMed Central  Google Scholar 

  • 53.

    Weingrill, T., Lycett, J. E., Barrett, L., Hill, R. A. & Henzi, S. P. Male consortship behaviour in chacma baboons: The role of demographic factors and female conceptive probabilities. Behaviour 140, 405–427 (2003).

    Article  Google Scholar 

  • 54.

    Engelhardt, A. et al. Assessment of female reproductive status by male longtailed macaques, Macaca fascicularis, under natural conditions. Anim. Behav. 67, 915–924 (2004).

    Article  Google Scholar 

  • 55.

    Higham, J. P., Semple, S., MacLarnon, A., Heistermann, M. & Ross, C. Female reproductive signaling, and male mating behavior, in the olive baboon. Horm. Behav. 55, 60–67 (2009).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 56.

    Schülke, O. & Ostner, J. Male reproductive skew, paternal relatedness, and female social relationships. Am. J. Primatol. 70, 695–698 (2008).

    PubMed  Article  PubMed Central  Google Scholar 

  • 57.

    Schülke, O. & Ostner, J. Ecological and social influences on sociality. In The evolution of Primate Societies (eds Mitani, J. C. et al.) 193–219 (University of Chicago Press, Chicago, 2012).

    Google Scholar 

  • 58.

    Higham, J. P. et al. Female fertile phase synchrony, and male mating and reproductive skew, in the crested macaque. Dryad, Dataset. https://doi.org/10.5061/dryad.rfj6q578x. (2021).

  • 59.

    Rosenbaum, B., O’Brien, T. G., Kinnaird, M. & Supriatna, J. Population densities of Sulawesi crested black macaques (Macaca nigra) on Bacan and Sulawesi, Indonesia: Effects of habitat disturbance and hunting. Am. J. Primatol. 44, 89–106 (1998).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 60.

    Collins, N. M. The Conservation Atlas of Tropical Forests: Asia and the Pacifics (Springer, Berlin, 1991).

    Google Scholar 

  • 61.

    O’Brien, T. G. & Kinnaird, M. F. Behavior, diet, and movements of the Sulawesi crested black macaque (Macaca nigra). Int. J. Primatol. 18, 321–351 (1997).

    Article  Google Scholar 

  • 62.

    Kinnaird, M. F. & O’Brien, T. G. A contextual analysis of the loud call of the Sulawesi crested black macaque, Macaca nigra. Trop. Biodivers. 20, 37–42 (1999).

    Google Scholar 

  • 63.

    Neumann, C. et al. Assessing dominance hierarchies: Validation and advantages of progressive evaluation with Elo-rating. Anim. Behav. 82, 911–921 (2011).

    Article  Google Scholar 

  • 64.

    Hadidian, J. & Bernstein, I. S. Female reproductive cycles and birth data from an Old World monkey colony. Primates 20, 429–442 (1979).

    Article  Google Scholar 

  • 65.

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

    CAS  Article  Google Scholar 

  • 66.

    Danish, L. M. & Palombit, R. A. “Following”, an alternative mating strategy used by male olive baboons (Papio hamadryas anubis): Quantitative behavioral and functional description. Int. J. Primatol. 35, 394–410 (2014).

    Article  Google Scholar 

  • 67.

    Hodges, J. K. & Heistermann, M. Field Endocrinology: Monitoring Hormonal Changes in Free-Ranging Primates 353–370 (Cambridge University Press, Cambridge, 2011).

    Google Scholar 

  • 68.

    Heistermann, M. et al. Loss of oestrus, concealed ovulation and paternity confusion in free-ranging Hanuman langurs. Proc. Biol. Sci. 268, 2445–2451 (2001).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 69.

    Engelhardt, A., Hodges, J. K., Niemitz, C. & Heistermann, M. Female sexual behavior, but not sex skin swelling, reliably indicates the timing of the fertile phase in wild long-tailed macaques (Macaca fascicularis). Horm. Behav. 47, 195–204 (2005).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 70.

    Nsubuga, A. M. et al. Factors affecting the amount of genomic DNA extracted from ape faeces and the identification of an improved sample storage method. Mol. Ecol. 13, 2089–2094 (2004).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 71.

    Engelhardt, A., Muniz, L., Perwitasari-Farajallah, D. & Widdig, A. Highly polymorphic microsatellite markers for the assessment of male reproductive skew and genetic variation in Critically Endangered crested macaques (Macaca nigra). Int. J. Primatol. 38, 672–691 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  • 72.

    Taberlet, P. et al. Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Res. 24, 3189–3194 (1996).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 73.

    Taberlet, P. & Luikart, G. Non-invasive genetic sampling and individual identification. Biol. J. Linn. Soc. 68, 41–55 (1999).

    Article  Google Scholar 

  • 74.

    Arandjelovic, M. et al. Two-step multiplex polymerase chain reaction improves the speed and accuracy of genotyping using DNA from noninvasive and museum samples. Mol. Ecol. Resour. 9, 28–36 (2009).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 75.

    Kalinowski, S. T., Taper, M. L. & Marshall, T. C. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol. Ecol. 16, 1099–1106 (2007).

    PubMed  Article  Google Scholar 

  • 76.

    Hadfield, J. D. MCMC methods for multi-response generalized linear mixed models: The MCMCglmm package. J. Stat. Softw. 33, 1–25 (2010).

    Article  Google Scholar 

  • 77.

    Nonacs, P. Measuring the reliability of skew indices: Is there one best index? Anim. Behav. 65, 615–627 (2003).

    Article  Google Scholar 


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