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Is male rhesus macaque red color ornamentation attractive to females?

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Abstract

Male sexually selected traits can evolve through different mechanisms: conspicuous and colorful ornaments usually evolve through intersexual selection, while weapons usually evolve through intra-sexual selection. Male ornaments are rare among mammals in comparison to birds, leading to the notion that female mate choice generally plays little role in trait evolution in this taxon. Supporting this view, when ornaments are present in mammals, they typically indicate social status and are products of male-male competition. This general mammalian pattern, however, may not apply to rhesus macaques (Macaca mulatta). Males of this species display conspicuous skin coloration, but this expression is not correlated to dominance rank and is therefore unlikely to have evolved due to male-male competition. Here, we investigate whether male color expression influences female proceptivity toward males in the Cayo Santiago free-ranging rhesus macaque population. We collected face images of 24 adult males varying in dominance rank and age at the peak of the mating season and modeled these to rhesus macaque visual perception. We also recorded female sociosexual behaviors toward these males. Results show that dark red males received more sexual solicitations, by more females, than pale pink ones. Together with previous results, our study suggests that male color ornaments are more likely to be a product of inter- rather than intra-sexual selection. This may especially be the case in rhesus macaques due to the particular characteristics of male-male competition in this species.

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References

  • Alberts SC, Buchan JC, Altmann J (2006) Sexual selection in wild baboons: from mating opportunities to paternity success. Anim Behav 72:1177–1196

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Amos W, Twiss S, Pomeroy P, Anderson S (1993) Male mating success and paternity in the grey seal, Halichoerus grypus, a study using DNA fingerprinting. Proc R Soc Lond B 252:199–207

    Article  CAS  Google Scholar 

  • Andersson M (1994) Sexual selection. Princeton University Press, New Jersey

    Google Scholar 

  • Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368

    Article  CAS  PubMed  Google Scholar 

  • Baulu J (1976) Seasonal sex skin coloration and hormonal fluctuations in free-ranging and captive monkeys. Horm Behav 7:481–494

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bercovitch FB, Nürnberg P (1996) Socioendocrine and morphological correlates of paternity in rhesus macaques (Macaca mulatta). J Reprod Fert 107:59–68

    Article  CAS  Google Scholar 

  • Bercovitch FB, Widdig A, Trefilov A, Kessler MJ, Berard JD, Schmidtke J, Nuernberg 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

    Article  CAS  PubMed  Google Scholar 

  • Bergman TJ, Beehner JC (2008) A simple method for measuring color in wild animals: validation and use on chest patch color in geladas (Theropithecus gelada). Biol J Linn Soc 94:231–240

    Article  Google Scholar 

  • Bergman TJ, Sheehan MJ (2013) Social knowledge and signals in primates. Am J Primatol 75:683–694

    Article  PubMed  Google Scholar 

  • Bergman TJ, Ho L, Beehner JC (2009) Chest color and social status in male geladas (Theropithecus gelada). Int J Primatol 30:791–806

    Article  Google Scholar 

  • Bielert CF, Goy RW (1973) Sexual behavior of male rhesus: effects of repeated ejaculation and partner's cycle stage. Horm Behav 4:109–122

    Article  Google Scholar 

  • Bowmaker JK, Dartnall HJA, Lythgoe JN, Mollon JD (1978) The visual pigments of rods and cones in the rhesus monkey, Macaca mulatta. J Physiol 274:329–348

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bradley BJ, Mundy NI (2008) The primate palette: the evolution of primate coloration. Evol Anthropol 17:97–111

    Article  Google Scholar 

  • Brill MH (1995) The relation between the color of the illuminant and the color of the illuminated object. Color Res Appl 20:70–75

    Article  Google Scholar 

  • Carpenter CR (1942) Sexual behavior of free ranging rhesus monkeys (Macaca mulatta). I. Specimens, procedures and behavioral characteristics of estrus. J Comp Psychol 33:113–142

    Article  Google Scholar 

  • Changizi MA, Zhang Q, Shimojo S (2006) Bare skin, blood and the evolution of primate color vision. Biol Lett 2:217–221

    Article  PubMed Central  PubMed  Google Scholar 

  • Chapais B (1983) Reproductive activity in relation to male dominance and the likelihood of ovulation in rhesus monkeys. Behav Ecol Sociobiol 12:215–228

    Article  Google Scholar 

  • Clutton-Brock TH (1988) Reproductive success. In: Clutton-Brock TH (ed) Reproductive success: studies of individual variation in contrasting breeding systems. University of Chicago Press, Chicago, pp 472–485

    Google Scholar 

  • Clutton-Brock TH, Huchard E (2013) Social competition and selection in males and females. Philos Trans R Soc B 5:20130074

  • Clutton-Brock T, McAuliffe K (2009) Female mate choice in mammals. Quart Rev Biol 84:3–27

    Article  PubMed  Google Scholar 

  • Coltman DW, Bancroft DR, Robertson A, Smith JA, Pemberton JM (1999) Male reproductive success in a promiscuous mammal: behavioural estimates compared with genetic paternity. Mol Ecol 8:1199–1209

    Article  CAS  PubMed  Google Scholar 

  • Coyne SP (2011) Alternative mating strategies among males in a social group of rhesus macaques (Macaca mulatta) on Cayo Santiago. MA thesis, University of Chicago

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

    Book  Google Scholar 

  • Dixson AF (2012) Primate sexuality: comparative studies of prosimians, monkeys, apes, and human beings, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • Dubuc C, Brent LJN, Accamando AK, Gerald MS, MacLarnon A, Semple S, Heistermann M, Engelhardt A (2009) Sexual skin color contains information about the timing of the fertile phase in free-ranging rhesus macaques. Int J Primatol 30:777–789

    Article  Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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? Horm Behav 61:696–705

    Article  PubMed Central  PubMed  Google Scholar 

  • Dubuc C, Coyne SP, Maestripieri D (2013) Effect of mating activity and dominance rank on male masturbation among free-ranging male rhesus macaques. Ethology 119:1–8

    Google Scholar 

  • Dubuc C, Ruiz-Lambides A, Widdig A (2014) Variance in male lifetime reproductive success and estimation of the degree of polygyny in a primate. Behav Ecol. doi:10.1093/beheco/aru052

  • Emlen DJ (2008) The evolution of animal weapons. Annu Rev Evol Ecol Syst 39:387–413

    Article  Google Scholar 

  • Engelhardt A, Neumann C, Heistermann M, Perwitasari-Farajallah D (2008) Sex skin coloration in male Sulawesi crested black macaques (Macaca nigra). Primate Eye 96:337

    Google Scholar 

  • Folstad I, Karter AJ (1992) Parasites, bright males and the immunocompetence handicap. Am Nat 2:603–622

    Article  Google Scholar 

  • Gerald MS (2001) Primate color predicts social status and aggressive outcome. Anim Behav 61:559–566

    Article  Google Scholar 

  • Gerald MS, Ayala J, Ruiz-Lambides A, Waitt C, Weiss A (2010) Do females pay attention to secondary sexual coloration in vervet monkeys (Chlorocebus aethiops)? Naturwissenschaften 97:89–96

    Article  CAS  PubMed  Google Scholar 

  • Higham JP (2006) The reproductive ecology of female olive baboons (Papio hamdryas anubis) at Gashaka-Gumti National Park, Nigeria. PhD thesis, Roehampton University

  • Higham JP, Brent LJN, Dubuc C, Accamando AK, Engelhardt A, Gerald MS, Heistermann M, Stevens M (2010) Color signal information content and the eye of the beholder: a case study in the rhesus macaque. Behav Ecol 21:739–746

    Article  PubMed Central  PubMed  Google Scholar 

  • Higham JP, Hughes KD, Brent LJN, Dubuc C, Engelhardt A, Heistermann M, Maestripieri D, Santos LR, Stevens M (2011) Familiarity affects assessment of facial signals of female fertility by free-ranging male rhesus macaques. Proc R Soc Lond B 278:3452–3458

    Article  Google Scholar 

  • Higham JP, Pfefferle D, Heistermann M, Maestripieri D, Stevens M (2013) Signaling in multiple modalities in male rhesus macaques: sex skin coloration and barks in relation to androgen levels, social status, and mating behavior. Behav Ecol Sociobiol 67:1457–1469

    Article  Google Scholar 

  • Hill GE, McGraw KJ (2006) Bird coloration. Harvard University Press, Cambridge, Volume II. Function and evolution

    Google Scholar 

  • Hoffman CL, Ruiz-Lambides AV, Davila E, Maldonado E, Gerald MS, Maestripieri D (2008) Sex differences in survival costs of reproduction in a promiscuous primate. Behav Ecol Sociobiol 62:1711–1718

    Article  PubMed Central  PubMed  Google Scholar 

  • Inoue M, Mitsunaga F, Nozaki M, Ohsawa H, Takenaka A, Sugiyama Y, Shimizu K, Takenaka O (1993) Male dominance rank and reproductive success in an enclosed group of Japanese macaques with special reference to post-conception mating. Primates 34:503–511

    Article  Google Scholar 

  • Ives HE (1912) Studies in the photometry of lights of different colors. I. Spectral luminosity curves obtained by the equality of brightness photometer under similar conditions. Phil Mag 24:149–188

    Article  CAS  Google Scholar 

  • Jones JH (2011) Primates and the evolution of long, slow life histories. Curr Biol 21:R708–R717

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kamilar JM, Heesy CP, Bradley BJ (2013) Did trichromatic color vision and red hair color co-evolve in primates? Am J Primatol 75:740–751

    Article  PubMed  Google Scholar 

  • Khan SA, Levine WJ, Dobson SD, Kralik JD (2011) Red signals dominance in male rhesus macaques. Psychol Sci 22:1001–1003

    Article  PubMed  Google Scholar 

  • Manson JH (1992) Measuring female mate choice in Cayo Santiago rhesus macaques. Anim Behav 44:405–416

    Article  Google Scholar 

  • Manson JH (1995) Do female rhesus macaques choose novel males? Am J Primatol 37:285–296

    Article  Google Scholar 

  • Manson JH (1996) Male dominance and mount series duration in Cayo Santiago rhesus macaques. Anim Behav 51:1219–1231

    Article  Google Scholar 

  • Martin P, Bateson P (1986) Measuring behavior: an introductory guide. Cambridge University Press, Cambridge

    Google Scholar 

  • Marty JS, Higham JP, Gadsby EL, Ross C (2009) Dominance, coloration and social and sexual behavior in male drills (Mandrillus leucophaeus). Int J Primatol 30:807–823

    Article  Google Scholar 

  • Michael RP, Zumpe D (1970) Sexual initiating behavior by female rhesus monkeys (Macaca mulatta) under laboratory conditions. Behaviour 36:168–186

    Article  Google Scholar 

  • Muller MN, Emery Thompson M, Kahlenberg S, Wrangham RW (2011) Sexual coercion by male chimpanzees shows that female choice may be more apparent than real. Behav Ecol Sociobiol 65: 921–933

  • Osorio D, Vorobyev M (2005) Photoreceptor spectral sensitivities in terrestrial animals: adaptations for luminance and color vision. Proc R Soc Lond B 272:1745–1752

    Article  CAS  Google Scholar 

  • Paul A (2002) Sexual selection and mate choice. Int J Primatol 23:877–904

    Article  Google Scholar 

  • Plavcan JM (2001) Sexual dimorphism in primate evolution. Am J Phys Anthropol 116:25–53

    Article  Google Scholar 

  • Pradhan GR, van Schaik CP (2009) Why do females find ornaments attractive? The coercion‐avoidance hypothesis. Biol J Linn Soc 96:372–382

    Article  Google Scholar 

  • Rawlins RG, Kessler MJ (1986) The Cayo Santiago macaques: history, behavior, and biology. SUNY Press, Albany

    Google Scholar 

  • Rhodes L, Argersinger LT, Gantert LT, Friscino BH, Hom G, Pikounis B, Hess DL, Rhodes WL (1997) Effects of administration of testosterone, dihydrotestosterone, oestrogen and fadrozole, an aromatase inhibitor, on sex skin color in intact male rhesus macaques. J Reprod Fertil 111:51–57

    Article  CAS  PubMed  Google Scholar 

  • Setchell JM (2005) Do female mandrills prefer brightly colored males? Int J Primatol 26:715–735

    Article  Google Scholar 

  • Setchell JM, Dixson AF (2001) Changes in the secondary sexual adornments of male mandrills (Mandrillus sphinx) are associated with gain and loss of alpha status. Horm Behav 39:177–184

    Article  CAS  PubMed  Google Scholar 

  • Setchell JM, Wickings EJ (2005) Dominance, status signals and coloration in male mandrills (Mandrillus sphinx). Ethology 111:25–50

    Article  Google Scholar 

  • Silk J, Short J, Roberts J, Kusnitz J (1993) Gestation length in rhesus macaques (Macaca mulatta). Int J Primatol 14:95–104

    Article  Google Scholar 

  • Soltis J (2004) Mating systems. In: Thierry B, Singh M, Kaumanns W (eds) Macaque societies: a model for the study of social organization. New York, Cambridge University Press, pp 135–151

  • Stephen ID, Coetzee V, Law Smith MJ, Perrett DI (2009) Skin blood perfusion and oxygenation color affect perceived human health. PLoS ONE 4:e5083

    Article  PubMed Central  PubMed  Google Scholar 

  • Stevens M, Párraga CA, Cuthill IC, Partridge JC, Troscianko T (2007) Using digital photography to study animal coloration. Biol J Linn Soc 90:211–237

    Article  Google Scholar 

  • Stevens M, Stoddard MC, Higham JP (2009) Studying primate color: towards visual system-dependent methods. Int J Primatol 30:893–917

    Article  Google Scholar 

  • Trivers RL (1972) Parental investment and sexual selection, 1871–1971. In: Campbell B (ed) Sexual selection and the descent of man. Heinemann, London, pp 136–179

    Google Scholar 

  • van Noordwijk MA, van Schaik CP (2004) Sexual selection and the careers of primate males: paternity concentration, dominance acquisition tactics and transfer decisions. In: Kappeler PM, van Schaik CP (eds) Sexual selection in primates: new and comparative perspectives. Cambridge University Press, Cambridge, pp 208–229

    Chapter  Google Scholar 

  • Vandenbergh JG (1965) Hormonal basis of sex skin in male rhesus monkeys. Gen Comp Endocr 5:31–34

    Article  Google Scholar 

  • Waitt C, Little AC, Wolfensohn S, Honess P, Brown AP, Buchanan-Smith HM, Perrett DI (2003) Evidence from rhesus macaques suggests that male coloration plays a role in female primate mate choice. Proc R Soc Lond B 270:144–146

    Article  Google Scholar 

  • Wallen K, Winston LA, Gaventa S, Davis-SaSilva M, Collins DC (1984) Periovulatory changes in female sexual behavior and patterns of ovarian steroid secretion in group-living rhesus monkeys. Horm Behav 18:431–450

    Article  CAS  PubMed  Google Scholar 

  • Wingfield JC, Hegner RE, Dufty AMJ, Ball GF (1990) The “challenge hypothesis”: theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat 136:829–846

    Article  Google Scholar 

  • Zumpe D, Michael RP (1970) Redirected aggression and gonadal hormones in captive rhesus monkeys (Macaca mulatta). Anim Behav, 18:11–19

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Acknowledgments

We thank the Caribbean Primate Research Center for permission to conduct this study, Julie Cascio for assistance in data collection, Tara Mandalaywala for logistic support, Sean Coyne and Greg Ruber for sharing valuable behavioral observations, Geoff Gallice for advice to CD on image capture in the field, and five anonymous reviewers for their fruitful comments on an earlier version of the manuscript. This project was funded by NIH (to DM), intramural funds from NYU (to JPH), and FQRSC (to CD). The population of Cayo Santiago was supported by grant number 2P40RR03640-25 from the National Center for Research Resources (NCRR) and the Office of Research Infrastructure Programs (ORIP) of NIH. The content of this publication is solely the responsibility of the authors and does not necessarily represent the official views of NCRR, ORIP or NIH.

Ethical standards

The investigation was approved by the IACUC of the University of Puerto Rico, Medical Sciences Campus (protocol no. A0100108).

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Authors and Affiliations

  1. Center for the Study of Human Origins, Department of Anthropology, New York University, 25 Waverly Place, New York City, NY, 10003, USA

    Constance Dubuc, William L. Allen & James P. Higham

  2. Institute for Mind and Biology, University of Chicago, Chicago, USA

    Constance Dubuc & Dario Maestripieri

  3. Department of Comparative Human Development, University of Chicago, Chicago, USA

    Dario Maestripieri

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  1. Constance Dubuc
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  2. William L. Allen
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  3. Dario Maestripieri
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  4. James P. Higham
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Correspondence to Constance Dubuc.

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Communicated by E. Huchard

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Dubuc, C., Allen, W.L., Maestripieri, D. et al. Is male rhesus macaque red color ornamentation attractive to females?. Behav Ecol Sociobiol 68, 1215–1224 (2014). https://doi.org/10.1007/s00265-014-1732-9

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  • DOI: https://doi.org/10.1007/s00265-014-1732-9

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