The redder the better? Information content of red skin coloration in female Japanese macaques

Abstract

Primates appear unusual among mammals in the expression of female colorful ornaments in the absence of sex role reversal. Most studies of female ornamentation in primates have focused on the sexual signaling function of female exaggerated ano-genital swellings in female-female competition and male attraction, but other female colorful ornaments, such as red skin coloration, may also contain information about reproductive status and individual characteristics. We analyzed variation in facial and hindquarter coloration (redness and luminance) according to the timing of the fertile phase (intra-cycle variation), the cycle number, whether the cycle was conceptive or non-conceptive (inter-cycle variation), and in relation to individual characteristics (social rank, parity, and body mass) in 12 captive female Japanese macaques (Macaca fuscata). While facial and hindquarter coloration did not accurately indicate the timing of the fertile phase, variation in hindquarter luminance signaled perceptible differences between pre- and post-ovulation stages. Hindquarters became less red, and faces were lighter as the number of consecutive cycles increased. Hindquarters were redder during non-conceptive cycles compared with conceptive ones. Individual variation in skin redness and luminance appeared perceptible under good light conditions. Higher-ranking females had darker hindquarters. We also found that variation in female skin coloration may contain information about differences in body mass but not in parity. Female skin coloration in Japanese macaques may thus be more indicative of inter-cycle variation and various specific female characteristics than the timing of the fertile phase. Our study provides insight into the potential information content of this signal and demonstrates the characteristics that males might be selecting for should males prefer redder females.

Significance statement

Primates are the most colorful group of mammals. Females of some primate species display red skin color that is suggested to play a role in mate attraction by reflecting reproductive status or individual characteristics. In Japanese macaques, a species lacking accurate behavioral and auditory indices of the probability of ovulation, female red skin coloration (face and hindquarters) may influence mating activity. Our study shows that this colorful trait does not contain information about the timing of the fertile phase and parity but may indicate inter-cycle differences and some female characteristics. Our findings add to a growing body of research on the possible roles and functions of female colorful ornaments in animal sexual communication.

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Acknowledgments

We thank Amélie Chimènes for her help with the preparation of the digital photography. We also thank The Center for Human Evolution Modeling Research of the Primate Research Institute and M.A. Huffman for use of the primate facilities. We thank Prof. David P. Watts and two anonymous reviewers for their constructive comments on earlier versions of this manuscript.

Funding

This work was financially supported by the Centre National de la Recherche Scientifique (France) to CG. LR is currently funded by the Human and Nature Interlaced Life Science Unit (Kyoto University, Japan) Research Coordination Alliance.

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Correspondence to Lucie Rigaill.

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The Center for Human Evolution Modeling Research of the Primate Research Institute reviewed and approved our research protocol in agreement with the Guidelines for the Care and Use of Nonhuman Primates of the Kyoto University Primate Research Institute.

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Communicated by D. P. Watts

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Rigaill, L., Higham, J.P., Winters, S. et al. The redder the better? Information content of red skin coloration in female Japanese macaques. Behav Ecol Sociobiol 73, 103 (2019). https://doi.org/10.1007/s00265-019-2712-x

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Keywords

  • Skin coloration
  • Sexual communication
  • Signal content
  • Reproductive status
  • Macaca fuscata