Andersson, M. Sexual Selection (Princeton University Press, 1994).
van Schaik, C. P., van Noordwijk, M. A. & Nunn, C. L. Sex and social evolution in primates. In Comparative Primate Socioecology (ed. Lee, P. C.) 204–240 (Cambridge University Press, Cambridge, 2000).
Nunn, C. L. The evolution of exaggerated sexual swellings in primates and the graded signal hypothesis. Anim. Behav. 58, 246–299 (1999).
Google Scholar
Pagel, M. The evolution of conspicuous oestrous advertisement in Old World monkeys. Anim. Behav. 47, 1333–1341 (1994).
Google Scholar
Kücklich, M., Weiß, B. M., Birkemeyer, C., Einspanier, A. & Widding, A. Chemical cues of female fertility states in a non-human primate. Sci. Rep. 9, 131716 (2019).
Google Scholar
Maestripieri, D. & Roney, J. Primate copulation calls and postcopulatory female choice. Behav. Ecol. 16, 106–113 (2004).
Google Scholar
Semple, S. & McComb, K. Perception of female reproductive state from vocal cues in a mammal species. Proc. R Soc. Lond. B 267, 707–712 (2000).
Google Scholar
Street, S. E., Cross, C. P. & Brown, G. R. Exaggerated sexual swellings in female nonhuman primates are reliable signals of female fertility and body condition. Anim. Behav. 112, 203–212 (2016).
Google Scholar
Tiddi, B., Wheeler, B. C. & Heistermann, M. Female behavioral proceptivity functions as a probabilistic signal of fertility, not female quality, in a New World primate. Horm. Behav. 73, 148–155 (2015).
Google Scholar
Aujard, F., Heistermann, M., Thierry, B. & Hodges, J. K. Functional significance of behavioral, morphological, and endocrine correlates across the ovarian cycle in semifree ranging female Tonkean macaques. Am. J. Primatol. 46, 285–309 (1998).
Google Scholar
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).
Google Scholar
Heistermann, M. et al. Female ovarian cycle phase affects the timing of male sexual activity in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar. Am. J. Primatol. 70, 44–53 (2008).
Google Scholar
Garcia, C., Shimizu, K. & Huffman, M. Relationship between sexual interactions and the timing of the fertile phase in captive female Japanese macaques (Macaca fuscata). Am. J. Primatol. 71, 868–879 (2009).
Google Scholar
Heistermann, M. et al. Loss of oestrus, concealed ovulation and paternity confusion in free-ranging Hanuman langurs. Proc. Biol. Sci. B 268, 2445–2451 (2001).
Google Scholar
Ostner, J. et al. What Hanuman langur males know about female reproductive status. Am. J. Primatol. 68, 701–712 (2006).
Google Scholar
Bielert, C. & Anderson, C. M. Baboon sexual swellings and male response: A possible operational mammalian supernormal stimulus and response interaction. Int. J. Primatol. 6, 377–393 (1985).
Google Scholar
Brauch, K. et al. Female sexual behavior and sexual swelling size as potential cues for males to discern the female fertile phase in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar. Horm. Behav. 52, 375–383 (2007).
Google Scholar
Higham, J. P., MacLarnon, A. M., Ross, C., Heistermann, M. & Semple, S. Baboon sexual swellings: Information content of size and color. Horm. Behav. 53, 452–462 (2008).
Google Scholar
Higham, J. P., Semple, S., MacLarnon, A., Heistermann, M. & Ross, C. Female reproductive signals, and male mating behavior in the olive baboon. Horm. Behav. 55, 60–67 (2009).
Google Scholar
Thomas, M. L. Detection of female mating status using chemical signals and cues. Biol. Rev. Camb. Philos. Soc. 86, 1–13 (2011).
Google Scholar
Dixson, A. F. Primate Sexuality: Comparative Studies of the Prosimians, Monkeys, Apes and Human Beings (Oxford University Press, 2012).
Dulac, C. & Torello, A. T. Molecular detection of pheromone signals in mammals: From genes to behaviour. Nat. Rev. Neurosci. 4, 551–562 (2003).
Google Scholar
Gilad, Y., Wiebe, V., Prezeworski, M., Lancet, D. & Pääbo, S. Loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates. PLoS. Biol. 2, 0120–0125 (2004).
Google Scholar
Negus, V. The Comparative Anatomy and Physiology of the Nose and Paranasal Sinuses (Livingston, 1958).
Dominy, N. J. & Lucas, P. W. Ecological importance of trichromatic vision to primates. Nature 410, 363–366 (2001).
Google Scholar
Fornalé, F., Vaglio, S., Spiezio, C. & Prato Previde, E. Red-green colour vision in three catarrhine primates. Commun. Integr. Biol. 5, 583–589 (2012).
Google Scholar
Gerald, M. S. How color may guide the primate world: Possible relationships between sexual selection and sexual dichromatism. In Sexual Selection and Reproductive Competition in Primates: New Perspectives and Directions (ed. Jones, C. B.) (American Society of Primatologists, 2003).
Porter, R. H. & Moore, J. D. Human kin recognition by olfactory cues. Physiol. Behav. 27, 493–495 (1981).
Google Scholar
Geissman, T. & Hulftegger, A. M. Olfactory communication in gibbons? In Current Primatology: Social Development, Learning and Behaviour (eds Roeder, J. J. et al.) 199–206 (Université Louis Pasteur Press, 1994).
Wedekind, C., Seebeck, T., Bettens, F. & Paepke, A. J. MHC-dependent mate preferences in humans. Proc. Biol. Sci. B 260, 245–249 (1995).
Google Scholar
Wedekind, C. & Füri, S. Body odour preferences in men and women: Do they aim for specific MHC combinations or simply heterozygosity?. Proc. Biol. Sci. B 264, 1471–1479 (1997).
Google Scholar
Smith, T. et al. The existence of the vomeronasal organ in postnatal chimpanzees and evidence for its homology to that of humans. J. Anat. 198, 77–82 (2001).
Google Scholar
Jacob, S., McClintock, M. K., Zelano, B. & Ober, C. Paternally inherited HLA alleles are associated with women’s choice of male odor. Nat. Genet. 30, 175–179 (2002).
Google Scholar
Klailova, M. & Lee, P. C. Wild western lowland gorillas signal selectively using odor. PLoS ONE 9, e99554 (2014).
Google Scholar
Masi, S. & Bouret, S. Odor signals in wild western lowland gorillas: An involuntary and extra-group communication hypothesis. Physiol. Behav. 145, 123–126 (2015).
Google Scholar
Henkel, S. & Setchell, J. M. Group and kin recognition via olfactory cues in chimpanzees (Pan troglodytes). Proc. Biol. Sci. B 285, 20181527 (2018).
Weiß, B. M. et al. Chemical composition of axillary odorants reflects social and individual attributes in rhesus macaques. Behav. Ecol. Sociobiol. 72, 65 (2018).
Google Scholar
Jänig, S., Weiß, B. M., Birkemeyer, C. & Widding, A. Comprative chemical analysis of body odor in great apes. Am. J. Primatol. 81, e22976 (2019).
Google Scholar
Setchell, J. M. et al. Chemical composition of scent-gland secretions in an Old World monkey (Mandrillus sphinx): Influence of sex, male status, and individual identity. Chem. Sens. 35, 205–220 (2010).
Google Scholar
Vaglio, S. et al. Sternal gland scent-marking signals sex, age, rank and group identity in captive mandrills. Chem. Sens. 41, 177–186 (2016).
Clarke, P. M., Barrett, L. & Henzi, S. P. What role do olfactory cues play in chacma baboon mating?. Am. J. Primatol. 71, 493–502 (2009).
Google Scholar
Crawford, J. C., Boulet, M. & Drea, C. M. Smelling wrong: Hormonal contraception in lemurs alters critical female odour cues. Proc. Biol. Sci. B 278, 122–130 (2011).
Google Scholar
Scordato, E. S., Dubay, G. & Drea, C. M. Chemical composition of scent marks in the ringtailed lemur (Lemur catta): Glandular differences, seasonal variation, and individual signatures. Chem. Sens. 32, 493–504 (2007).
Google Scholar
Rahaman, H. & Parthasarathy, M. D. The role of olfactory signals in the mating behaviour of bonnet monkeys, Macaca radiata. Commun. Behav. Biol. 6, 97–104 (1971).
Google Scholar
Michael, R. P. & Keverne, E. B. Pheromones in the communication of sexual status in primates. Nature 218, 746–749 (1968).
Google Scholar
Michael, R. P. & Keverne, E. B. Primate sex pheromones of vaginal origin. Nature 225, 84–85 (1970).
Google Scholar
Michael, R. P. Hormonal steroids and sexual communication in primates. J. Steroid. Biochem. 6, 161–170 (1975).
Google Scholar
Goldfoot, D. A., Kravetz, M. A., Goy, R. W. & Freeman, S. K. Lack of effect of vaginal lavages and aliphatic acids on ejaculatory responses in rhesus monkeys: Behavioral and chemical analyses. Horm. Behav. 7, 1–27 (1976).
Google Scholar
Havlíček, J., Dvořáková, R., Bartoš, L. & Flegr, J. Non-advertised does not mean concealed: Body odour changes across the human menstrual cycle. Ethology 112, 81–90 (2006).
Google Scholar
Doty, R. L., Ford, M., Preti, G. & Huggins, G. R. Changes in the intensity and pleasantness of human vaginal odors during the menstrual cycle. Science 190, 1316–1318 (1975).
Google Scholar
Kuukasjarvi, S. et al. Attractiveness of women’s body odors over the menstrual cycle: The role of oral contraceptives and receiver sex. Behav. Ecol. 15, 579–584 (2004).
Google Scholar
Singh, D. & Bronstad, P. M. Female body odour is a potential cue to ovulation. Proc. R. Soc. Lond. B 268, 797–801 (2001).
Google Scholar
Cerda-Molina, A. L., Hernández-López, L., Rojas-Maya, S., Murcia-Mejía, C. & Mondragón-Ceballos, R. Male-induced sociosexual behaviour by vaginal secretions in Macaca arctoides. Int. J. Primatol. 27, 791–807 (2006).
Google Scholar
Robinson, J. G. Intrasexual competition and mate choice in primates. Am. J. Primatol. 3, 131–144 (1982).
Google Scholar
Penn, D. J. et al. Individual and gender fingerprints in human body odour. J. R. Soc. Interface 4, 331–340 (2007).
Google Scholar
Smith, T. & Abbott, D. Behavioral discrimination between circumgenital odor from peri-ovulatory dominant and anovulatory female common marmosets (Callithrix jacchus). Am. J. Primatol. 46, 265–284 (1998).
Google Scholar
Spence-Aizenberg, A., Kimball, B. A., Williams, L. E. & Fernandez-Duque, E. Chemical composition of glandular secretions from a pair-living monogamous primate: Sex, age, and gland differences in captive and wild owl monkeys (Aotus spp.). Am. J. Primatol. 80, e22730 (2018).
Google Scholar
Setchell, J. M. Sexual selection and the differences between the sexes in mandrills (Mandrillus sphinx). Yearb. Phys. Anthropol. 159, S105–S129 (2016).
Google Scholar
Higham, J. P., Heistermann, M., Ross, C., Semple, S. & MacIarnon, A. The timing of ovulation with respect to sexual swelling detumescence in wild olive baboons. Primates 49, 295–299 (2008).
Google Scholar
Hasson, O. Towards a general theory of biological signalling. J. Theor. Biol. 185, 139–156 (1997).
Google Scholar
Packer, C., Tatar, M. & Collins, A. Reproductive cessation in female mammals. Nature 392, 807–811 (1998).
Google Scholar
Melnick, D. C. & Pearl, M. C. Cercopithecines in multimale groups: Genetic diversity and population structure. In Primate Societies (eds Smuts, B. B. et al.) 121–134 (University of Chicago Press, 1987).
Honoré, E. K. & Tardif, S. D. Reproductive biology of baboons. In The Baboon in Biomedical Research (eds VandeBerg, J. L. et al.) 89–110 (Springer-Verlag, 2009).
Pomerantz, O. & Terkel, J. Effects of positive reinforcement training techniques on the psychological welfare of zoo-housed chimpanzees (Pan troglodytes). Am. J. Primatol. 71, 687–695 (2009).
Google Scholar
Bercovitch, F. B. Reproductive Tactics in Adult Female and Adult Male Olive Baboons. (Ph.D. thesis, University of California, 1985).
Hendrickx, A. G. & Kraemer, D. C. Observation of the menstrual cycle, optimal mating time, and preimplantation embryos of the baboon. J. Reprod. Fert. S6, 119–128 (1969).
Koyama, T., De La Pena, A. & Hagino, N. Plasma estrogen, progestin, and luteinizing hormone during the normal menstrual cycle in the baboon: Role of luteinizing hormone. Am. J. Obstet. Gynecol. 127, 67–71 (1977).
Google Scholar
Shaikh, A. A., Celaya, C. L., Gomez, I. & Shaikh, S. A. Temporal relationship of hormonal peaks to ovulation and sex skin deturgescence in the baboon. Primates 23, 444–452 (1982).
Google Scholar
Vaglio, S. et al. Female copulation calls vary with male ejaculation in captive olive baboons. Behaviour 157, 807–822 (2020).
Google Scholar
Shambayati, B. Cytopathology (Oxford University Press, 2011).
Wilcox, A. J., Weingberg, C. R. & Baird, D. D. Timing of sexual intercourse in relation to ovulation: Effects on the probability of conception, survival of the pregnancy and sex of the baby. N. Engl. J. Med. 333, 189–194 (1995).
Google Scholar
Walker, D. & Vaglio, S. Sampling and analysis of animal scent signals. J. Vis. Exp. 168, e60902 (2021).
El‐Sayed, A. The Pherobase: Database of Pheromones and Semiochemicals. www.pherobase.com (2016).
Oksanen, J. et al. VEGAN: Community Ecology Package. R Package Version 2.5-5 (2019).
R Studio Team R Studio: Integrated Development for R (2019).
R Core Team R: A language and Environment for Statistical Computing (2018).
StataCorp. Stata Statistical Software, 16th Release (2019).
Mundry, R. & Sommer, C. Discriminant function analysis with nonindependent data: Consequences and an alternative. Anim. Behav. 74, 965–976 (2007).
Google Scholar
Venables, W. N. & Ripley, B. D. Modern Applied Statistics with S (Springer, 2002).
Breslow, N. E. & Clayton, D. G. Approximate inference in generalized linear mixed models. J. Am. Stat. Ass. 88, 9–25 (1993).
Google Scholar
Bell, B. A., Morgan, G. B., Schoeneberger, J. A. & Loudermilk, B. L. Dancing the sample size limbo with mixed models: How low can you go? SAS Global Forum, Paper 197 (2010).
Heymann, E. W. The neglected sense-olfaction in primate behavior, ecology, and evolution. Am. J. Primatol. 68, 519–524 (2006).
Google Scholar
Hayes, R., Morelli, T. & Wright, P. Anogenital gland secretions of Lemur catta and Propithecus verreauxi coquereli: A preliminary chemical examination. Am. J. Primatol. 63, 49–62 (2004).
Google Scholar
Janda, E. D., Perry, K., Hankinson, E., Walker, D. & Vaglio, S. Sex differences in scent-marking in captive red-ruffed lemurs. Am. J. Primatol. 81, 60–68 (2019).
Google Scholar
Smith, T., Tomlinson, A., Mlotkiewicz, J. & Abbott, D. Female marmoset monkeys (Callithrix jacchus) can be identified from the chemical composition of their scent marks. Chem. Sens. 26, 449–458 (2001).
Google Scholar
Hurst, J. L., Robertson, D., Tolladay, U. & Beynon, J. Proteins in urine scent marks of male house mice extend the longevity of olfactory signals. Anim. Behav. 55, 1289–1297 (1998).
Google Scholar
Belcher, A. M. et al. Proteins: biologically relevant components of the scent marks of a primate (Saguinus fuscicollis). Chem. Sens. 15, 431–446 (1990).
Google Scholar
Doty, R. L. Olfactory communication in humans. Chem. Sens. 6, 351–376 (1981).
Google Scholar
Curtis, R. F., Ballantine, J. A., Keverne, E. B., Bonsall, R. W. & Michael, R. P. Identification of primate sexual pheromones and the properties of synthetic attractants. Nature 232, 396–398 (1971).
Google Scholar
Jha, S. K., Marina, N., Liu, C. & Hayashi, K. Human body odor discrimination by GC-MS spectra data mining. Anal. Methods 7, 9549–9561 (2015).
Google Scholar
Balcerzak, L., Gibka, J., Sikora, M., Kula, J. & Strub, D. J. Minor constituents of essential oils and aromatic extracts. Oximes derived from natural flavor and fragrance raw materials: Sensory evaluation, spectral and gas chromatographic characteristics. Food Chem. 301, 125283 (2019).
Google Scholar
Baker, M. Fur rubbing: use of medicinal plants by capuchin monkeys (Cebus capucinus). Am. J. Primatol. 38, 263–270 (1996).
Google Scholar
Wyatt, T. Pheromones and Animal Behaviour. Chemical Signal and Signatures (Cambridge University Press, 2014).
DelBarco-Trillo, J., Harelimana, I. H., Goodwin, T. E. & Drea, C. M. Chemical differences between voided and bladder urine in the aye-aye (Daubentonia madagascariensis): Implications for olfactory communication studies. Am. J. Primatol. 75, 695–702 (2013).
Google Scholar
Smith, T. Individual olfactory signatures in common marmosets (Callithrix jacchus). Am. J. Primatol. 68, 585–604 (2006).
Google Scholar
Drea, C. M. Design, delivery and perception of conditiondependent chemical signals in strepsirrhine primates: Implications for human olfactory communication. Phil. Trans. R. Soc. B 375, 20190264 (2020).
Google Scholar
Poirier, A. C. et al. On the trail of primate scent signals: A field analysis of callitrichid scent-gland secretions by portable gas chromatography-mass spectrometry. Am. J. Primatol. 1, e23236 (2021).
Mason, R. T. & Parker, M. R. Social behaviour and pheromonal communication in reptiles. J. Comp. Physiol. A 196, 729–749 (2010).
Google Scholar
Shirasu, M. & Touhara, K. The scent of disease: Volatile organic compounds of the human body related to disease and disorder. J. Biochem. 150, 257–266 (2011).
Google Scholar
Rivera, A. J., Stumpf, R. M., Wilson, B., Leigh, S. & Salyers, A. A. Baboon vaginal microbiota: An overlooked aspect of primate physiology. Am. J. Primatol. 72, 467–474 (2010).
Google Scholar
Pener, M. P. & Simpson, S. J. Locust phase polyphenism: An update. Adv. Insect Physiol. 36, 1–272 (2009).
Google Scholar
Andersson, J., Borg-Karlson, A. K. & Wiklund, C. Antiaphrodisiacs in pierid butterflies: A theme with variation!. J. Chem. Ecol. 29, 1489–1499 (2003).
Google Scholar
Ramirez, S. R. et al. Asynchronous diversification in a specialized plant-pollinator mutualism. Science 333, 1742–1746 (2011).
Google Scholar
Rigaill, L., Higham, J. P., Lee, P. C., Blin, A. & Garcia, C. Multimodal sexual signaling and mating behavior in olive baboons (Papio anubis). Am. J. Primatol. 75, 774–787 (2013).
Google Scholar
Candolin, U. The use of multiple cues in mate choice. Biol. Rev. Camb. Philos. Soc. 78, 575–595 (2003).
Google Scholar
Johnstone, R. A., Reynolds, J. D. & Deutsch, J. C. Mutual mate choice and sex differences in choosiness. Evolution 50, 1382–1391 (1996).
Google Scholar
Johnstone, R. A. Multiple displays in animal communication: “Backup signals” and “multiple messages”. Phil. Trans. R. Soc. B 351, 329–338 (1996).
Google Scholar
Greene, L. K. et al. Mix it and fix it: Functions of composite olfactory signals in ring-tailed lemurs. R. Soc. Open Sci. 3, 160076 (2016).
Google Scholar
Mitro, S., Gordon, A. R., Olsson, M. J. & Lundström, J. N. The smell of age: Perception and discrimination of body odors of different ages. PLoS ONE 7(5), e38110 (2012).
Google Scholar
Beauchamp, G. K. & Yamazaki, K. Chemical signalling in mice. Biochem. Soc. Trans. 31, 147–151 (2003).
Google Scholar
Kean, E. F., Muller, C. T. & Chadwick, E. A. Otter scent signals age, sex, and reproductive status. Chem. Sens. 36, 555–564 (2011).
Google Scholar
MacDonald, E. A., Fernandez-Duque, E., Evans, S. & Hagey, L. R. Sex, age, and family differences in the chemical composition of owl monkey (Aotus nancymaae) subcaudal scent secretions. Am. J. Primatol. 70, 12–18 (2007).
Google Scholar
Osada, K. et al. The scent of age. Proc. R. Soc. Lond. B 270, 929–933 (2003).
Google Scholar
White, A. M., Swaisgood, R. R. & Zhang, H. Chemical communication in the giant panda (Ailuropoda melanoleuca): The role of age in the signaller and assessor. J. Zool. 259, 171–178 (2006).
Google Scholar
Anderson, C. M. Female age: Male preference and reproductive success in primates. Int. J. Primatol. 7, 305–326 (1986).
Google Scholar
Cant, A. C. & Young, A. J. Resolving social conflict among females without overt aggression. Phil. Trans. R. Soc. B 368, 20130076 (2013).
Google Scholar
Alberts, S. C., Altmann, J. & Wilson, M. L. Mate guarding constrains foraging activity of male baboons. Anim. Behav. 51, 1269–1277 (1996).
Google Scholar
Brennan, P. A. & Kendrick, K. M. Mammalian social odours: attraction and individual recognition. Phil. Trans. R. Soc. B 361, 2061–2078 (2006).
Google Scholar
Wyatt, T. Pheromones and Animal Behaviour (Cambridge University Press, 2003).
Thom, M. D. & Hurst, J. L. Individual recognition by scent. Ann. Zool. Fenn. 41, 765–787 (2004).
Setchell, J. M., Lee, P. C., Wickings, E. J. & Dixson, A. F. Growth and ontogeny of sexual size dimorphism in the mandrill (Mandrillus sphinx). Am. J. Phys. Anthropol. 115, 349–360 (2001).
Google Scholar
Palagi, E. & Dapporto, L. Beyond odor discrimination: Demonstrating individual recognition by scent in Lemur catta. Chem. Sens. 31, 437–443 (2006).
Google Scholar
Epple, G., Kuderling, I. & Belcher, A. M. Some communicatory functions of scent marking in the cotton-top tamarin Saguinus oedipus oedipus. J. Chem. Ecol. 14, 503–515 (1988).
Google Scholar
Laska, M., Genzel, D. & Wieser, A. The number of functional olfactory receptor genes and the relative size of olfactory brain structures are poor predictors of olfactory discrimination performance with enantiomers. Chem. Sens. 30, 171–175 (2005).
Google Scholar
Source: Ecology - nature.com
