Familiarity affects the assessment of female facial signals of fertility by free-ranging male rhesus macaques

Proceedings of the Royal Society B: Biological Sciences

Volumn 278, Issue 1723, 2011, Pages 3452-3458

  Higham, James P ^a,b   Hughes, Kelly D ^c   Brent, Lauren J N ^d   Dubuc, Constance ^b,e   Engelhardt, Antje ^b   Heistermann, Michael ^b   Maestriperi, Dario ^a   Santos, Laurie R ^c   Stevens, Martin ^f  

^a UNIVERSITY OF CHICAGO   (United States)

^b GERMAN PRIMATE CENTER   (Germany)

^c YALE UNIVERSITY   (United States)

^d UNIVERSITY OF ROEHAMPTON   (United Kingdom)

^e UNIVERSITÉ DE MONTRÉAL   (Canada)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Cognition; Discrimination; Experience; Familiarity; Ovulation; Reproductive signals

Indexed keywords

COGNITION; FAMILIARITY; FECAL PELLET; FEMALE; GROUP BEHAVIOR; HORMONE; MALE; PRIMATE; REPRODUCTIVE CYCLE; REPRODUCTIVE STATUS; SENSORY SYSTEM; SIGNAL;

ANIMALIA; MACACA MULATTA; PRIMATES;

EID: 80053996286     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2011.0052     Document Type: Article

References (41)

1. Charlton, B. D., Keating, J. L., Li, R. G., Yan, H. & Swaisgood, R. R. 2010 Female giant panda (Ailuropoda melanoleuca) chirps advertise the caller's fertile phase. Proc. R. Soc. B 277, 1101-1106. (doi:10.1098/rspb.2009.1431)
2. Tannure-Nascimento, I. C., Nascimento, F. S. & Zucchi, R. 2008 The look of royalty: visual and odour signals of reproductive status in a paper wasp. Proc. R. Soc. B 275, 2555-2561. (doi:10.1098/rspb.2008.0589)
3. Higham, J. P., MacLarnon, A. M., Ross, C., Heistermann, M. & Semple, S. 2008 Baboon sexual swellings: information content of size and color. Horm. Behav. 53, 452-462. (doi:10.1016/j.yhbeh.2007.11.019)
4. Cheney, D. L. & Seyfarth, R. M. 2007 Baboon metaphysics: the evolution of a social mind. Chicago, IL: University of Chicago Press.
5. Dixson, A. F. 1998 Primate sexuality: comparative studies of prosimians, monkeys, apes, and human beings. Oxford, UK: Oxford University Press.
6. Roberts, S. C., Havlicek, J., Flegr, J., Hruskova, M., Little, A. C., Jones, B. C., Perrett, D. I. & Petrie, M. 2004 Female facial attractiveness increases during the fertile phase of the menstrual cycle. Proc. R. Soc. Lond. B 271, S270-S272. (doi:10.1098/rsbl.2004.0174)
7. Dubuc, C., Brent, L. J. N., Accamando, A. K., Gerald, M. S., MacLarnon, A., Semple, S., Heistermann, M. & Engelhardt, A. 2009 Sexual skin color contains information about the timing of the fertile phase in freeranging rhesus macaques. Int. J. Primatol. 30, 777-789. (doi:10.1007/s10764-009-9369-7)
8. Higham, J.P., Brent, L.J.N., Dubuc, C., Accamando, A.K., Engelhardt, A., Gerald, M.S., 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. (doi:10.1093/beheco/arq047)
9. Bercovitch, B. F. 1995 Female co-operation, consortship maintenance, and male mating success in savanna baboons. Anim. Behav. 50, 137-149. (doi:10.1006/anbe.1995.0227)
10. Nunn, C. 1999 The evolution of exaggerated sexual swellings in primates and the graded signal hypothesis. Anim. Behav. 58, 229-246. (doi:10.1006/anbe.1999.1159)
11. Van Schaik, C. P. & Paul, A. 1996 Male care in primates: does it ever reflect paternity? Evol. Anthropol. 5, 152-156. (doi:10.1002/(SICI)1520-6505(1996)5:5,152::AIDEVAN3.3.0.CO;2-H)
12. Berard, J. 1999 Afour-year study of the association between male dominance rank, residency status, and reproductive activity in rhesus macaques (Macaca mulatta). Primates 40, 159-175. (doi:10.1007/BF02557708)
13. Deaner, R. O., Khera, A. V. & Platt, M. L. 2005 Monkeys pay per view: adaptive valuation of social images by rhesus macaques. Curr. Biol. 15, 543-548. (doi:10.1016/j.cub.2005.01.044)
14. Bercovitch, F. B. 1997 Reproductive strategies of rhesus macaques. Primates 38, 247-263. (doi:10.1007/BF02381613)
15. Engelhardt, A., Hodges, J. K. & Heistermann, M. 2007 Post-conception mating in wild long-tailed macaques (Macaca fasicularis): characterization, endocrine correlates and functional significance. Horm. Behav. 51, 3-10. (doi:10.1016/j.yhbeh.2006.06.009)
16. Weingrill, T., Lycett, J. E., Barrett, L., Hill, R. A. & Henzi, S. P. 2003 Male consortship behaviour in chacma baboons: the role of demographic factors and female conceptive probabilities. Behaviour 140, 405-427. (doi:10.1163/156853903321826701)
17. Waitt, C., Gerald, M. S., Little, A. C. & Kraiselburd, E. 2006 Selective attention toward female secondary sexual color in male rhesus macaques. Am. J. Primatol. 68, 738-744. (doi:10.1002/ajp.20264)
18. Rawlins, R. G. & Kessler, M. J. (eds) 1986 The Cayo Santiago macaques: history, behavior and biology. Albany, NY: SUNY.
19. Hoffman, C. L., Ruiz-Lambides, A. V., Davila, E., Maldonado, E., Gerald, M. S. & Maestripieri, D. 2008 Sex differences in survival costs of reproduction in a promiscuous primate. Behav. Ecol. Sociobiol. 62, 1711-1718. (doi:10.1007/s00265-008-0599-z)
20. Stevens, M., Stoddard, M. C. & Higham, J. P. 2009 Studying primate color: towards visual system-dependent methods. Int. J. Primatol. 30, 893-917. (doi:10.1007/s10764-009-9356-z)
21. Jeffcoate, S. L. 1983 Use of rapid hormone assays in the prediction of ovulation. In Ovulation: methods for its prediction and detection (ed. S. L. Jeffcoate), pp. 67-82. Chichester, UK: Wiley.
22. Heistermann, M., Uhrigshardt, J., Husung, A., Kaumanns, A. & Hodges, J. K. 2001 Measurement of faecal steroid metabolites in the lion-tailed macaque (Macaca silenus): a non-invasive tool for assessing female ovarian function. Primate Rep. 59, 27-42.
23. Wasser, S. K., Monfort, S. L., Southers, J. & Wildt, D. E. 1994 Excretion rates and metabolites of oestradiol and progesterone in baboon (Papio cynocephalus cynocephalus) faeces. J. Reprod. Fertil. 101, 213-220. (doi:10.1530/jrf.0.1010213)
24. Wilcox, A. J., Weinberg, C. R. & Baird, D. 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. N. Engl. J. Med. 333, 1517-1522. (doi:10.1056/NEJM199512073332301)
25. Vorobyev, M. & Osorio, D. 1998 Receptor noise as a determinant of colour thresholds. Proc. R. Soc. Lond. B 265, 351-358. (doi:10.1098/rspb.1998.0302)
26. Fantz, R. 1965 Visual perception from birth as shown by pattern selectivity. Ann. NY Acad. Sci. 118, 793-814. (doi:10.1111/j.1749-6632.1965.tb40152.x)
27. Preacher, K. J. 2001 Calculation for the chi-square test: an interactive calculation tool for chi-square tests of goodness of fit and independence (computer software). See http://www.quantpsy.org.
28. Keverne, E. B. 1976 Sexual receptivity and attractiveness in the rhesus monkey. Adv. Study Behav. 7, 155-200. (doi:10.1016/S0065-3454(08)60167-9)
29. Michael, R. P. & Keverne, E. B. 1968 Pheromones in the communication of sexual status in primates. Nature 218, 746-749. (doi:10.1038/218746a0)
30. Gobbini, M. I. & Haxby, J. V. 2007 Neural systems for recognition of familiar faces. Neuropsychologia 45, 32-41. (doi:10.1016/j.neuropsychologia.2006.04.015)
31. Gobbini, M. I., Lebenluft, E., Santiago, N. & Haxby, J. V. 2004 Social and emotional attachment in the neural representation of faces. Neuroimage 22, 1628-1635. (doi:10.1016/j.neuroimage.2004.03.049)
32. Rhodes, L., Argersinger, M. E., Gantert, L. T., Friscino, B. H., Hom, G., Pikounis, B., Hess, D. L. & Rhodes, W. L. 1997 Effects of administration of testosterone, dihydrotestosterone, oestrogen and fadrozole, and aromatase inhibitor, on sex skin colour in intact male rhesus macaques. J. Reprod. Fertil. 111, 51-57. (doi:10.1530/jrf.0.1110051)
33. Gillmann, J. 1940 The effect of multiple injections of progesterone on the turgescent perineum of the baboon (Papio porcarius). Endocrinology 26, 1072-1077. (doi:10.1210/endo-26-6-1072)
34. 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. (doi:10.1016/j.yhbeh.2004.03.013)
35. Grammer, K. & Thornhill, R. 1994 Human (Homo sapiens) facial attractiveness and sexual selection: the role of symmetry and averageness. J. Comp. Psychol. 3, 233-242. (doi:10.1037/0735-7036.108.3.233)
36. Law-Smith, M. J. et al. 2006 Facial appearance is a cue to oestrogen levels in women. Proc. R. Soc. B 273, 135-140. (doi:10.1098/rspb.2005.3296)
37. Török, J., Hegyi, G. & Garamszegi, L. Z. 2003 Depigmented wing patch size is a condition-dependent indicator of viability in male collared flycatchers. Behav. Ecol. 14, 382-388. (doi:10.1093/beheco/14.3.382)
38. Pagel, M. 1994 The evolution of conspicuous oestrus advertisement in Old World monkeys. Anim. Behav. 27, 1-36.
39. Domb, L. G. & Pagel, M. 2001 Sexual swellings advertise female quality in wild baboons. Nature 410, 204-206. (doi:10.1038/35065597)
40. Pipitone, R. N. & Gallup, G. G. 2008 Women's voice attractiveness varies across the menstrual cycle. Evol. Hum. Behav. 29, 268-274. (doi:10.1016/j.evolhumbehav.2008.02.001)
41. Havlicek, J., Dvorakova, R., Bartos, L. & Flegr, J. 2006 Non-advertized does not mean concealed: body odour changes across the human menstrual cycle. Ethology 112, 81-90. (doi:10.1111/j.1439-0310.2006.01125.x)