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

  • Lucie RigaillEmail author
  • James P. Higham
  • Sandra Winters
  • Cécile Garcia
Original Article


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.


Skin coloration Sexual communication Signal content Reproductive status Macaca fuscata 



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 information

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.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

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.


  1. Amundsen T (2000) Why are female birds ornamented? Trends Ecol Evol 15:149–155. CrossRefPubMedGoogle Scholar
  2. Amundsen T, Forsgren E (2001) Male mate choice selects for female coloration in a fish. P Natl Acad Sci USA 98:13155–13160. CrossRefGoogle Scholar
  3. Amundsen T, Forsgren E (2003) Male preference for colourful females affected by male size in a marine fish. Behav Ecol Sociobiol 54:55–64. CrossRefGoogle Scholar
  4. Anderson CM (1986) Female age: male preference and reproductive success in primates. Int J Primatol 7:305–326. CrossRefGoogle Scholar
  5. Andersson M, Simmons LW (2006) Sexual selection and mate choice. Trends Ecol Evol 21:296–302. CrossRefPubMedGoogle Scholar
  6. Andersson MB (1994) Sexual selection. Princeton University PressGoogle Scholar
  7. Baird TA (2004) Reproductive coloration in female collared lizards, Crotophytus collaris, stimulates courtship by males. Herpetologica 60:337–348. CrossRefGoogle Scholar
  8. Barlow GW (1973) Competition between color morphs of the polychromatic Midas cichlid Cichlasoma citrinellum. Science 179:806–807. CrossRefPubMedGoogle Scholar
  9. Barlow GW, Wallach SJ (1976) Colour and levels of aggression in the Midas cichlid. Anim Behav 24:814–817. CrossRefGoogle Scholar
  10. Bercovitch FB (1987) Female weight and reproductive condition in a population of olive baboons (Papio anubis). Am J Primatol 12:189–195CrossRefGoogle Scholar
  11. Bergman TJ, Ho L, Beehner JC (2009) Chest color and social status in male geladas (Theropithecus gelada). Int J Primatol 30:791–806. CrossRefGoogle Scholar
  12. Bradley BJ, Mundy NI (2008) The primate palette: the evolution of primate coloration. Evol Anthropol 17:97–111. CrossRefGoogle Scholar
  13. Burriss RP, Troscianko J, Lovell PG, Fulford AJC, Stevens M, Quigley R, Payne J, Saxton TK, Rowland HM (2015) Changes in women’s facial skin color over the ovulatory cycle are not detectable by the human visual system. PLoS One 10:e0130093. CrossRefPubMedPubMedCentralGoogle Scholar
  14. Clutton-Brock T (2007) Sexual selection in males and females. Science 318:1882–1885. CrossRefPubMedGoogle Scholar
  15. Clutton-Brock TH (2004) What is sexual selection? In: Kappeler PM, van Schaik CP (eds) Sexual selection in Primates: new and comparative perspectives. Cambridge University Press, Cambridge, pp 24–36CrossRefGoogle Scholar
  16. Darwin C (1871) The descent of man, and selection in relation to sex. J. Murray, LondonCrossRefGoogle Scholar
  17. David P, Heeb P (2009) Parasites and sexual selection. In: Thomas F, Guégan J-F, Renaud F (eds) Ecology and evolution of parasitism. Oxford University Press, Oxford, pp 31–47Google Scholar
  18. de Vries H, Stevens JMG, Vervaecke H (2006) Measuring and testing the steepness of dominance hierarchies. Anim Behav 71:585–592. CrossRefGoogle Scholar
  19. Deschner T, Heistermann M, Hodges K, Boesch C (2004) Female sexual swelling size, timing of ovulation, and male behavior in wild West African chimpanzees. Horm Behav 46:204–215. CrossRefPubMedGoogle Scholar
  20. Dixson AF (2012) Primate sexuality: comparative studies of the prosimians, monkeys, apes and human beings, 2nd edn. Oxford University Press, New YorkCrossRefGoogle Scholar
  21. Doutrelant C, Grégoire A, Grnac N et al (2008) Female coloration indicates female reproductive capacity in blue tits. J Evol Biol 21:226–233. CrossRefPubMedGoogle Scholar
  22. Dubuc C, Allen WL, Cascio J, Lee DS, Maestripieri D, Petersdorf M, Winters S, Higham JP (2015) Who cares? Experimental attention biases provide new insights into a mammalian sexual signal. Behav Ecol 27:68–74. CrossRefPubMedPubMedCentralGoogle Scholar
  23. Dubuc C, Allen WL, Maestripieri D, Higham JP (2014a) Is male rhesus macaque red color ornamentation attractive to females? Behav Ecol Sociobiol 68:1215–1224CrossRefGoogle Scholar
  24. 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 Macaca mulatta. Int J Primatol 30:777–789. CrossRefGoogle Scholar
  25. Dubuc C, Winters S, Allen WL, Brent LJN, Cascio J, Maestripieri D, Ruiz-Lambides AV, Widdig A, Higham JP (2014b) Sexually selected skin colour is heritable and related to fecundity in a non-human primate. Proc R Soc B 281:20141602. CrossRefPubMedGoogle Scholar
  26. Edward DA, Chapman T (2011) The evolution and significance of male mate choice. Trends Ecol Evol 26:647–654. CrossRefPubMedGoogle Scholar
  27. Fitzpatrick CL, Altmann J, Alberts SC (2015) Exaggerated sexual swellings and male mate choice in primates: testing the reliable indicator hypothesis in the Amboseli baboons. Anim Behav 104:175–185. CrossRefPubMedPubMedCentralGoogle Scholar
  28. Fooden J, Aimi M (2005) Systematic review of Japanese macaques, Macaca fuscata (Gray, 1870). Fieldiana Zool 104:1–198Google Scholar
  29. Fooden J, Aimi M (2003) Birth-season variation in Japanese macaques, Macaca fuscata. Primates 44:109–117. CrossRefPubMedGoogle Scholar
  30. Fujita S (2010) Interaction between male and female mating strategies and factors affecting reproductive outcome. In: Nakagawa N, Nakamichi M, Sugiura H (eds) The Japanese macaques. Springer Japan, Tokyo, pp 221–239CrossRefGoogle Scholar
  31. Fujita S, Sugiura H, Shimizu K, Mitsunaga F (2004) Hormone profiles and reproductive characteristics in wild female Japanese macaques (Macaca fuscata). Am J Primatol 64:367–375. CrossRefPubMedGoogle Scholar
  32. Galán P (2000) Females that imitate males: dorsal coloration varies with reproductive stage in female Podarcis bocagei (Lacertidae). Copeia 2000:819–825CrossRefGoogle Scholar
  33. Garcia C, Huffman MA, Shimizu K, Speakman JR (2011) Energetic consequences of seasonal breeding in female Japanese macaques (Macaca fuscata). Am J Phys Anthropol 146:161–170. CrossRefPubMedGoogle Scholar
  34. 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). Am J Primatol 71:868–879. CrossRefPubMedGoogle Scholar
  35. Griggio M, Devigili A, Hoi H, Pilastro A (2009) Female ornamentation and directional male mate preference in the rock sparrow. Behav Ecol 20:1072–1078. CrossRefGoogle Scholar
  36. Griggio M, Valera F, Casas A, Pilastro A (2005) Males prefer ornamented females: a field experiment of male choice in the rock sparrow. Anim Behav 69:1243–1250. CrossRefGoogle Scholar
  37. Grueter CC, Zhu P, Allen WL, Higham JP, Ren B, Li M (2015) Sexually selected lip colour indicates male group-holding status in the mating season in a multi-level primate society. R Soc Open Sci 2:150490. CrossRefPubMedPubMedCentralGoogle Scholar
  38. Hayakawa S (2007) Female defensibility in a small troops of Japanese macaques vis-à-vis nontroop males and copulation on the periphery of the troop. Int J Primatol 28:73–96CrossRefGoogle Scholar
  39. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Higham JP, Hughes KD, Brent LJN, Dubuc C, Engelhardt A, Heistermann M, Maestriperi D, Santos LR, Stevens M (2011) Familiarity affects the assessment of female facial signals of fertility by free-ranging male rhesus macaques. Proc R Soc Lond B 278:3452–3458. CrossRefGoogle Scholar
  41. Higham JP, MacLarnon AM, Ross C et al (2008) Baboon sexual swellings: information content of size and color. Horm Behav 53:452–462. CrossRefPubMedGoogle Scholar
  42. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  43. Hodges JK, Heistermann M (2011) Field endocrinology: monitoring hormonal changes in free-ranging primates. In: Setchell JM, Curtis DJ (eds) Field and laboratory methods in primatology: a practical guide. Cambridge University Press, Cambridge, pp 353–370CrossRefGoogle Scholar
  44. Hopkins J, Baudry G, Candolin U, Kaitala A (2015) I’m sexy and I glow it: female ornamentation in a nocturnal capital breeder. Biol Lett 11:20150599. CrossRefPubMedPubMedCentralGoogle Scholar
  45. Huffman MA (1992) Influences of female partner preference on potential reproductive outcome in Japanese macaques. Folia Primatol 59:77–88CrossRefGoogle Scholar
  46. Inoue E, Takenaka O (2008) The effect of male tenure and female mate choice on paternity in free-ranging Japanese macaques. Am J Primatol 70:62–68. CrossRefPubMedGoogle Scholar
  47. 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. CrossRefGoogle Scholar
  48. Isvaran K, Clutton-Brock T (2007) Ecological correlates of extra-group paternity in mammals. Proc R Soc Lond B 274:219–224. CrossRefGoogle Scholar
  49. Jawor JM, Gray N, Beall SM, Breitwisch R (2004) Multiple ornaments correlate with aspects of condition and behaviour in female northern cardinals, Cardinalis cardinalis. Anim Behav 67:875–882CrossRefGoogle Scholar
  50. Jessop TS, Chan R, Stuart-Fox D (2009) Sex steroid correlates of female-specific colouration, behaviour and reproductive state in Lake Eyre dragon lizards, Ctenophorus maculosus. J Comp Physiol A 195:619–630CrossRefGoogle Scholar
  51. Koyama N (1967) On dominance rank and kinship of a wild Japanese monkey troop in Arashiyama. Primates 8:189–216. CrossRefGoogle Scholar
  52. Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82:1–26. CrossRefGoogle Scholar
  53. Lande R (1980) Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34:292–305. CrossRefPubMedGoogle Scholar
  54. LeBas NR, Hockham LR, Ritchie MG (2003) Nonlinear and correlational sexual selection on ‘honest’ female ornamentation. Proc R Soc Lond B 270:2159–2165. CrossRefGoogle Scholar
  55. LeBas NR, Marshall NJ (2000) The role of colour in signalling and male choice in the agamid lizard Ctenophorus ornatus. Proc R Soc Lond B 267:445–452CrossRefGoogle Scholar
  56. Lukas D, Clutton-Brock T (2014) Costs of mating competition limit male lifetime breeding success in polygynous mammals. Proc R Soc B 281:20140418. CrossRefPubMedGoogle Scholar
  57. Martín J, López P (2009) Multiple color signals may reveal multiple messages in male Schreiber’s green lizards, Lacerta schreiberi. Behav Ecol Sociobiol 63:1743–1755. CrossRefGoogle Scholar
  58. 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. CrossRefGoogle Scholar
  59. Mennill DJ, Doucet SM, Montgomerie R, Ratcliffe LM (2003) Achromatic color variation in black-capped chickadees, Poecile atricapilla: black and white signals of sex and rank. Behav Ecol Sociobiol 53:350–357. CrossRefGoogle Scholar
  60. Mitani J, Call J, Kappeler PM et al (2012) The evolution of primate societies. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  61. Mori A (1979) Analysis of population changes by measurement of body weight in the Koshima troop of Japanese monkeys. Primates 20:371–397. CrossRefGoogle Scholar
  62. Muller MN, Thompson M, Wrangham RW (2006) Male chimpanzees prefer mating with old females. Curr Biol 16:2234–2238. CrossRefPubMedGoogle Scholar
  63. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142. CrossRefGoogle Scholar
  64. Nunn CL (1999) The evolution of exaggerated sexual swellings in primates and the graded-signal hypothesis. Anim Behav 58:229–246. CrossRefPubMedGoogle Scholar
  65. O’Neill AC, Fedigan LM, Ziegler TE (2004) Relationship between ovarian cycle phase and sexual behavior in female Japanese macaques (Macaca fuscata). Am J Phys Anthropol 125:352–362. CrossRefPubMedGoogle Scholar
  66. Osorio D, Vorobyev M (2005) Photoreceptor sectral sensitivities in terrestrial animals: adaptations for luminance and colour vision. Proc R Soc Lond B 272:1745–1752. CrossRefGoogle Scholar
  67. Petersdorf M, Dubuc C, Georgiev AV, Winters S, Higham JP (2017) Is male rhesus macaque facial coloration under intrasexual selection? Behav Ecol 28:1472–1481. CrossRefPubMedPubMedCentralGoogle Scholar
  68. Pflüger LS, Valuch C, Gutleb DR, Ansorge U, Wallner B (2014) Colour and contrast of female faces: attraction of attention and its dependence on male hormone status in Macaca fuscata. Anim Behav 94:61–71. CrossRefGoogle Scholar
  69. Pilastro A, Griggio M, Matessi G (2003) Male rock sparrows adjust their breeding strategy according to female ornamentation: parental or mating investment? Anim Behav 66:265–271CrossRefGoogle Scholar
  70. Pinheiro J, Bates D, DebRoy S et al (2014) nlme: linear and nonlinear mixed effects models. R package version 3.1–117, = nlme
  71. Pryke SR, Andersson S, Lawes MJ, Piper SE (2002) Carotenoid status signaling in captive and wild red-collared widowbirds: independent effects of badge size and color. Behav Ecol 13:622–631. CrossRefGoogle Scholar
  72. Rhodes L, Argersinger ME, 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 colour in intact male rhesus macaques. J Reprod Fertil 111:51–57. CrossRefPubMedGoogle Scholar
  73. Rigaill L, Higham JP, Lee PC et al (2013) Multimodal sexual signaling and mating behavior in olive baboons (Papio anubis). Am J Primatol 75:774–787. CrossRefPubMedGoogle Scholar
  74. Rigaill L, MacIntosh AJJ, Higham JP et al (2015) Multimodal advertisement of pregnancy in free-ranging female Japanese macaques (Macaca fuscata). PLoS One 10:e0135127. CrossRefPubMedPubMedCentralGoogle Scholar
  75. Rigaill L, MacIntosh AJJ, Higham JP et al (2017) Testing for links between face color and age, dominance status, parity, weight, and intestinal nematode infection in a sample of female Japanese macaques. Primates 58:83–91. CrossRefPubMedGoogle Scholar
  76. Setchell JM, Charpentier MJE, Bedjabaga I-B, Reed P, Wickings EJ, Knapp LA (2006a) Secondary sexual characters and female quality in primates. Behav Ecol Sociobiol 61:305–315. CrossRefGoogle Scholar
  77. 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. CrossRefPubMedGoogle Scholar
  78. Setchell JM, Wickings EJ (2005) Dominance, status signals and coloration in male mandrills (Mandrillus sphinx). Ethology 111:25–50. CrossRefGoogle Scholar
  79. Setchell JM, Wickings JE (2006) Mate choice in male mandrills (Mandrillus sphinx). Ethology 112:91–99. CrossRefGoogle Scholar
  80. Setchell JM, Wickings JE (2004a) Sexual swelling in mandrills (Mandrillus sphinx): a test of the reliable indicator hypothesis. Behav Ecol 15:438–445. CrossRefGoogle Scholar
  81. Setchell JM, Wickings JE (2004b) Social and seasonal influences on the reproductive cycle in female mandrills (Mandrillus sphinx). Am J Phys Anthropol 125:73–84. CrossRefPubMedGoogle Scholar
  82. Setchell JM, Wickings EJ, Knapp LA (2006b) Signal content of red facial coloration in female mandrills (Mandrillus sphinx). Proc R Soc Lond B 273:2395–2400. CrossRefGoogle Scholar
  83. Sheehan MJ, Bergman TJ (2015) Is there an evolutionary trade-off between quality signaling and social recognition? Behav Ecol 27:2–13CrossRefGoogle Scholar
  84. Siddiqi A, Cronin TW, Loew ER et al (2004) Interspecific and intraspecific views of color signals in the strawberry poison frog Dendrobates pumilio. J Exp Biol 207:2471–2485. CrossRefPubMedGoogle Scholar
  85. Soltis J, Mitsunaga F, Shimizu K et al (1997) Sexual selection in Japanese macaques II: female mate choice and male-male competition. Anim Behav 54:737–746CrossRefGoogle Scholar
  86. Stevens M, Stoddard MC, Higham JP (2009) Studying primate color: towards visual system-dependent methods. Int J Primatol 30:893–917. CrossRefGoogle Scholar
  87. Street SE, Cross CP, Brown GR (2016) Exaggerated sexual swellings in female nonhuman primates are reliable signals of female fertility and body condition. Anim Behav 112:203–212. CrossRefGoogle Scholar
  88. Takeshita RSC, Bercovitch FB, Huffman MA, Mouri K, Garcia C, Rigaill L, Shimizu K (2014) Environmental, biological, and social factors influencing fecal adrenal steroid concentrations in female Japanese macaques (Macaca fuscata). Am J Primatol 76:1084–1093. CrossRefPubMedGoogle Scholar
  89. Thompson CW, Moore MC (1991) Throat colour reliably signals status in male tree lizards, Urosaurus ornatus. Anim Behav 42:745–753. CrossRefGoogle Scholar
  90. Thrall PH, Antonovics J, Dobson AP (2000) Sexually transmitted diseases in polygynous mating systems: prevalence and impact on reproductive success. Proc R Soc Lond B 267:1555–1563CrossRefGoogle Scholar
  91. Torres R, Velando A (2005) Male preference for female foot colour in the socially monogamous blue-footed booby, Sula nebouxii. Anim Behav 69:59–65. CrossRefGoogle Scholar
  92. van Schaik CP (2000) Social counter strategies against infanticide by males in primates and other mammals. In: Kappeler PM (ed) Primate males: causes and consequences of variation in group composition. Cambridge University Press, Cambridge, pp 34–52Google Scholar
  93. van Schaik CP, Hodges JK, Nunn CL (2000) Paternity confusion and the ovarian cycles of female primates. In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 361–387CrossRefGoogle Scholar
  94. van Schaik CP, Pradhan GR, van Noordwijk MA (2004) Mating conflict in primates: infanticide, sexual harassment and female sexuality. In: Kappeler P, van Schaik CP (eds) Sexual selection in Primates: new and comparative perspectives. Cambridge University Press, Cambridge, pp 131–150CrossRefGoogle Scholar
  95. Volpato GL, Luchiari AC, Duarte CRA, Barreto RE, Ramanzini GC (2003) Eye color as an indicator of social rank in the fish Nile tilapia. Braz J Med Biol Res 36:1659–1663. CrossRefPubMedGoogle Scholar
  96. Vorobyev M, Osorio D (1998) Receptor noise as a determinant of colour thresholds. Proc R Soc Lond B 265:351–358. CrossRefGoogle Scholar
  97. Waitt C, Gerald MS, Little AC, Kraiselburd E (2006) Selective attention toward female secondary sexual color in male rhesus macaques. Am J Primatol 68:738–744. CrossRefPubMedGoogle Scholar
  98. 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:S144–S146. CrossRefGoogle Scholar
  99. Weiss SL (2002) Reproductive signals of female lizards: pattern of trait expression and male response. Ethology 108:793–813. CrossRefGoogle Scholar
  100. Weiss SL (2016) Ornamentation, age, and survival of female striped plateau lizards, Sceloporus virgatus. Sci Nat 103:16CrossRefGoogle Scholar
  101. Weiss SL, Kennedy EA, Bernhard JA (2009) Female-specific ornamentation predicts offspring quality in the striped plateau lizard, Sceloporus virgatus. Behav Ecol 20:1063–1071. CrossRefGoogle Scholar
  102. Wilcox A, Weingberg C, Baird D (1995) Timing of sexual intercourse in relation to ovulation: effects on the probability of conception, survival of the pregnancy and sex of the baby. New Engl J Med 333:189–194CrossRefGoogle Scholar
  103. Zinner D, Alberts SC, Nunn CL, Altmann J (2002) Significance of primate sexual swellings. Nature 420:142–143CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Primate Research InstituteKyoto UniversityInuyamaJapan
  2. 2.Department of Anthropology, Center for the Study of Human OriginsNew York UniversityNew YorkUSA
  3. 3.UMR 7206CNRS-Muséum National d’Histoire Naturelle-Université Paris DiderotParisFrance

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