Sexual signalling in female crested macaques and the evolution of primate fertility signals

BMC Evolutionary Biology

Antje Engelhardt³  Dyah Perwitasari-Farajallah¹  Muhammad Agil⁴  Carina Saggau⁶  Michael Heistermann⁵  James P Higham² 

[1] Faculty of Mathematics & Natural Sciences, Bogor Agricultural University, Bogor, Indonesia;Department of Anthropology, New York University, 25 Waverly Place, New York, NY, 10003, USA;Courant Research Centre “Evolution of Social Behaviour”, Kellnerweg 6, Göttingen, 37077, Germany;Faculty of Veterinary Medicine, Bogor Agricultural University, Bogor, Indonesia;Reproductive Biology Unit, German Primate Centre, Kellnerweg 4, Göttingen, 37077, Germany;Jr Research Group on Sexual Selection, Reproductive Biology Unit, German Primate Centre, Kellnerweg 4, Göttingen, 37077, Germany

关键词: Primate;    Sexual swellings;    Sexual selection;    Fertility signals;   

Others  :  1141024
DOI  :  10.1186/1471-2148-12-89

 received in 2011-11-07, accepted in 2012-06-18,  发布年份 2012

【 摘 要 】

Background

Female signals of fertility have evolved in diverse taxa. Among the most interesting study systems are those of multimale multifemale group-living primates, where females signal fertility to males through multiple signals, and in which there is substantial inter-specific variation in the composition and reliability of such signals. Among the macaques, some species display reliable behavioural and/or anogenital signals while others do not. One cause of this variation may be differences in male competitive regimes: some species show marked sexual dimorphism and reproductive skew, with males fighting for dominance, while others show low dimorphism and skew, with males queuing for dominance. As such, there is variation in the extent to which rank is a reliable proxy for male competitiveness, which may affect the extent to which it is in females’ interest to signal ovulation reliably. However, data on ovulatory signals are absent from species at one end of the macaque continuum, where selection has led to high sexual dimorphism and male reproductive skew. Here we present data from 31 cycles of 19 wild female crested macaques, a highly sexually dimorphic species with strong mating skew. We collected measures of ovarian hormone data from faeces, sexual swelling size from digital images, and male and female behaviour.

Results

We show that both sexual swelling size and female proceptivity are graded-signals, but relatively reliable indicators of ovulation, with swelling size largest and female proceptive behaviours most frequent around ovulation. Sexual swelling size was also larger in conceptive cycles. Male mating behaviour was well timed to female ovulation, suggesting that males had accurate information about this.

Conclusion

Though probabilistic, crested macaque ovulatory signals are relatively reliable. We argue that in species where males fight over dominance, male dominance rank is surrogate for competitiveness. Under these circumstances it is in the interest of females to increase paternity concentration and assurance in dominants beyond levels seen in species where such competition is less marked. As such, we suggest that it may in part be variation in male competitive regimes that leads to the evolution of fertility signalling systems of different reliability.

【 授权许可】

   
2012 Higham et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1 .

Figure 2 .

Figure 3 .

【 参考文献 】

• [1]Darwin C: The descent of man and selection in relation to sex. London: J. Murray; 1871.
• [2]Tannure-Nascimento IC, Nascimento FS, Zucchi R: The look of royalty: visual and odour signals of reproductive status in a paper wasp. Proc Roy Soc B 2008, 275:2555-2561.
• [3]Montgomerie R, Thornhill R: Fertility advertisement in birds: a means of inciting male-male competition? Ethology 1989, 81:209-220.
• [4]Charlton BD, Keating JL, Li RG, Yan H, Swaisgood RR: Female giant panda (Ailuropoda melanoleuca) chirps advertise the caller’s fertile phase. Proc Roy Soc B 2010, 277:1101-1106.
• [5]Clutton-Brock TH, Harvey PH: Evolutionary rules and primate societies. In Growing points in ethology. Edited by Bateson PPG, Hinde RA. Cambridge: Cambridge University Press; 1976:195-237.
• [6]Hamilton WJI: Significance of paternal investment by primates to the evolution of adult male–female associations. In Primate paternalism. Edited by Taub DM. New York: van Nostrand Reinhold; 1984:303-335.
• [7]Hrdy S: The women that never evolved. 2nd edition. Cambridge, MA: Harvard University Press; 1981.
• [8]Nunn C: The evolution of exaggerated sexual swellings in primates and the graded signal hypothesis. Anim Behav 1999, 58:229-246.
• [9]Pagel M: The evolution of conspicuous oestrus advertisement in Old World monkeys. Anim Behav 1994, 27:1-36.
• [10]Wrangham RW: An ecological model of female-bonded primate groups. Behaviour 1980, 75:262-300.
• [11]van Schaik CP: The ecology of social relationships amongst female primates. In Comparative socioecology: The behavioural ecology of humans and other mammals. Edited by Standen V, Foley RA. London: Blackwell Scientific Publications; 1989:195-218.
• [12]Sterck EHM, Watts DP, van Schaik CP: The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 1997, 41:291-309.
• [13]Deschner T, Heistermann M, Hodges K, Boesch C: Female sexual swelling size, timing of ovulation and male behavior in wild West African chimpanzees. Horm Behav 2004, 46:204-215.
• [14]Brauch K, Pfefferle D, Hodges K, Möhle U, Fischer J, Heistermann M: 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 2007, 52:375-383.
• [15]Higham JP, MacLarnon AM, Ross C, Heistermann M, Semple S: Baboon sexual swellings: Information content of size and color. Horm Behav 2008, 53:452-462.
• [16]Gesquiere LR, Wango EO, Alberts SC, Altmann J: Mechanisms of sexual selection: sexual swellings and estrogen concentrations as fertility indicators and cues for male consort decisions in wild baboons. Horm Behav 2007, 51:114-125.
• [17]Engelhardt A, Hodges JK, Niemitz C, Heistermann M: Female sexual behaviour, but not sex skin swelling, reliably indicates the timing of the fertile phase in wild long-tailed macaques (Macaca fasicularis). Horm Behav 2005, 47:195-204.
• [18]Fürtbauer I, Heistermann M, Schülke O, Ostner J: Concealed fertility and extended female sexuality in a non-human primate (Macaca assamensis). PLoS One 2011, 6:e23105.
• [19]Zuckerman S, Parkes AS: Observations on the secondary sexual charactersistics in monkeys. J Endocrinol 1939, 1:430-439.
• [20]Gillman J: The effect of multiple injections of progesterone on the turgescent perineum of the baboon (Papio porcarius). Endocrinology 1940, 26:1072-1077.
• [21]Michael RP, Zumpe D: A review of hormonal factors influencing the sexual and aggressive behavior of macaques. Am J Primatol 1993, 30:213-241.
• [22]Zehr JL, Maestripieri D, Wallen K: Estradiol increases female sexual initiation independent of male responsiveness in rhesus monkeys. Horm Behav 1998, 33:95-103.
• [23]Aujard F, Heistermann M, Thierry B, Hodges JK: The functional significance of behavioral, morphological, and endocrine correlates across the ovarian cycle in semifree ranging female Tonkean macaques. Am J Primatol 1998, 46:285-309.
• [24]Higham JP, Semple S, MacLarnon A, Heistermann M, Ross C: Female reproductive signaling, and male mating behavior, in the olive baboon. Horm Behav 2009, 55:60-67.
• [25]Bercovitch BF: Female co-operation, consortship maintenance, and male mating success in savanna baboons. Anim Behav 1995, 50:137-149.
• [26]Engelhardt A, Pfeifer J-B, Heistermann M, Niemitz C, van Hooff JARAM, Hodges JK: Assessment of female reproductive status by male longtailed macaques, Macaca fasicularus, under natural conditions. Anim Behav 2004, 67:915-924.
• [27]Emery Thompson M, Wrangham RW: Male mating interest varies with female fecundity in Pan troglodytes schweinfurthii of Kanyawara, Kibale National Park. Int J Primatol 2008, 29:885-905.
• [28]Heistermann M, Brauch K, Möhle U, Pfefferle D, Dittami J, Hodges K: Female ovarian cycle phase affects the timing of male sexual activity in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar. Am J Primatol 2008, 70:44-53.
• [29]Paul A, Kuester J, Timme A, Arnemann J: The association between rank, mating effort, and reproductive success in male Barbary macaques (Macaca sylvanus). Primates 1993, 34:491-502.
• [30]Kuemmerli R, Martin RD: Male and female reproductive success in Barbary macaques (Macaca sylvanus) in Gibraltar: No evidence for rank dependence. Int J Primatol 2005, 26:1229-1249.
• [31]Brauch K, Hodges JK, Engelhardt A, Fuhrmann K, Shaw E, Heistermann M: Sex-specific reproductive behaviours and paternity in free-ranging Barbary macaques (Macaca sylvanus). Behav Ecol Sociolbiol 2008, 62:1453-66.
• [32]Berard JD, Nürnberg P, Epplen JT, Schmidtke J: Alternative reproductive tactics and reproductive success in male rhesus macaques. Behaviour 1994, 129:177-201.
• [33]Widdig A, Bercovitch FB, Streich WJ, Nürnberg P, Krawczak M: A longitudinal analysis of reproductive skew in male rhesus macaques. Proc Roy Soc B 2004, 271:819-826.
• [34]Dubuc C, Muniz L, Heistermann M, Engelhardt A, Widdig A: Testing the Priority-of Access model in a seasonally breeding primate species (Macaca mulatta). Behav Ecol Sociobiol 2011, 65:1615-1627.
• [35]de Ruiter JR, Van Hooff JARAM, Scheffrahn W: Social and genetic aspects of paternity in wild long-tailed macaques (Macaca fascicularis). Behaviour 1994, 129:203-224.
• [36]Engelhardt A, Heistermann M, Hodges JK, Nürnberg P, Niemitz C: Determinants of male reproductive success in wild long-tailed macaques (Macaca fascicularis) – male monopolisation, female mate choice or post-copulatory mechanisms? Behav Ecol Sociobiol 2006, 59:740-52.
• [37]Plavcan JM: Sexual dimorphism in primate evolution. Am J Phys Anthropol 2001, 116:25-53.
• [38]van Noordwijk MA, van Schaik CP: Sexual selection and the careers of primate males: paternity concentration, dominance-acquisition tactics and transfer decisions. In Sexual selection in primates. Edited by Kappeler P, Schaik CP. Cambridge: Cambridge University Press; 2004:208-229.
• [39]Riley EP: The endemic seven: Four decades of research on the Sulawesi macaques. Evol Anthropol 2010, 19:22-36.
• [40]Neumann C, Assahad G, Hammerschmidt K, Perwitasari-Farajallah D, Engelhardt A: Loud calls in male crested macaques, Macaca nigra: a signal of dominance in a tolerant species. Anim Behav 2010, 79:187-193.
• [41]Collins NM, Sayer JA, Whitmore TC: The conservation Atlas of tropical forests: Asia and the Pacific. New York: Simon & Schuster; 1991.
• [42]Rosenbaum B, O’Brien TG, Kinnaird M, Supriatna J: Population densities of sulawesi crested black macaques ( Macaca nigra ) on Bacan and Sulawesi, Indonesia: effects of habitat disturbance and hunting. Am J Primatol 1998, 44:89-106.
• [43]O’Brien TG, Kinnaird MF: Behavior, diet, and movements of the sulawesi crested black macaque (Macaca nigra). Int J Primatol 1997, 18:321-351.
• [44]Kinnaird MF, O'Brien TG: A contextual analysis of the loud call of the Sulawesi crested black macaque, Macaca nigra. Tropic Biodiv 1999, 6:37-42.
• [45]Hodges JK, Heistermann M: Field Endocrinology: monitoring hormonal changes in free-ranging primates. In Field and Laboratory methods in primatology (2ndEd). Edited by Setchell J, Curtis D. Cambridge: Cambridge University Press; 2011:282-294.
• [46]Heistermann M, Finke M, Hodges JK: Assessment of female reproductive status in captive-housed Hanuman langurs (Presbytis entellus) by measurement of urinary and fecal steroid excretion patterns. Am J Primatol 1995, 37:275-284.
• [47]Schwarzenberger E, Möstl E, Palme R, Bamberg E: Faecal steroid analysis for noninvasive monitoring of reproductive status in farm, wild and zoo animals. Anim Reprod Sci 1996, 42:515-526.
• [48]Heistermann M, Uhrigshardt J, Husung A, Kaumanns A, Hodges JK: Measurement of faecal steroid metabolites in the lion-tailed macaque (Macaca silenus): A non-invasive tool for assessing female ovarian function. Primate Report 2001, 59:27-42.
• [49]Möhle U, Heistermann M, Dittami J, Reinberg V, Hodges JK: Patterns of anogenital swelling size and their endocrine correlates during ovulatory cycles and early pregnancy in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar. Am J Primatol 2005, 66:351-368.
• [50]Heistermann M, Ziegler T, van Schaik CP, Launhardt K, Winkler P, Hodges JK: Loss of oestrus, concealed ovulation and paternity confusion in free-ranging Hanuman langurs. Proc Roy Soc B 2001, 268:2445-2451.
• [51]O'Neill AC, Fedigan LM, Ziegler TE: Relationship between ovarian cycle phase and sexual behavior in female Japanese macaques (Macaca fuscata). Am J Phys Anthropol 2004, 125:352-362.
• [52]Heistermann M, Hodges JK: Endocrine monitoring of the ovarian cycle and pregnancy in the saddle-back tamarin (Saguinus fuscicollis) by measurement of steroid conjugates in urine. Am J Primatol 1995, 35:117-127.
• [53]Domb LG, Pagel M: Sexual swellings advertise female quality in wild baboons. Nature 2001, 410:204-206.
• [54]Altmann J: Observational study of behavior: sampling methods. Behavior 1974, 49:227-267.
• [55]Shideler SE, Orturo AM, Moran FM, Moorman EA, Lasley BL: Simple extraction and enzyme immunoassays for estrogen and progesterone metabolites in the feces of Macaca fascicularis during non-conceptive and conceptive ovarian cycles. Biol Reprod 1993, 48:1290-1298.
• [56]Higham JP, Brent LJN, Dubuc C, Accamando AK, Engelhardt A, Gerald MS, Heistermann M, Stevens M: Color signal information content and the eye of the beholder: a case study in the rhesus macaque. Behav Ecol 2010, 21:739-746.
• [57]Dubuc C, Brent LJN, Accamando AK, Gerald MS, MacLarnon A, Semple S, Heistermann M, Engelhardt A: Sexual skin color contains information about the timing of the fertile phase in free-ranging rhesus macaques. Int J Primatol 2009, 30:777-789.
• [58]Hadidian J, Bernstein IS: Female reproductive cycles and birth data from an Old World monkey colony. Primates 1979, 20:429-442.
• [59]Bates D, Maechler M, Bolker B: lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-42; 2011. http://CRAN.R-project.org/package=lme4 webcite
• [60]Hadfield JD: MCMC Methods for Multi-Response Generalized Linear Mixed Models: The MCMCglmm R Package. J Stat Softw 2010, 33:1-22.
• [61]Weingrill T, Lycett JE, Barrett L, Hill RA, Henzi SP: Male consortship behaviour in chacma baboons: The role of demographic factors and female conceptive probabilities. Behaviour 2003, 140:405-427.
• [62]Higham JP, Hughes KD, Brent LJN, Dubuc C, Engelhardt A, Heistermann M, Maestripieri D, Santos LR, Stevens M: Familiarity affects assessment of facial signals of female fertility by free-ranging male rhesus macaques. Proc Roy Soc B 2011, 278:3452-3458.
• [63]Manson JH: Do Female Rhesus Macaques Choose Novel Males? Am J Primatol 1995, 37:285-296.
• [64]Paul A: Sexual selection and mate choice. Int J Primatol 2002, 23:877-904.