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Secondary sexual characters and female quality in primates

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Abstract

Honest advertisement models of sexual selection propose that exaggerated secondary sexual ornaments are condition-dependent, and that only individuals with superior disease resistance will be able to express costly ornamentation. Studies of secondary sexual ornamentation and their maintenance by sexual selection tend to focus on males. However, females may also possess showy ornaments. We investigated whether female ornaments, in the form of sexual swellings, reliably signal female fitness in a semifree-ranging colony of mandrills (Mandrillus sphinx) at the Centre International de Recherches Médicales, Franceville (CIRMF), Gabon. We measured swelling height and width using photographs of periovulatory females over three mating seasons and compared swelling size with parasitism (using fecal analysis over one annual cycle), immune status (ratio of lymphocytes to neutrophils in blood smears made during captures), and genetic diversity (microsatellite heterozygosity). Swelling size varied by up to 10% between cycles in individual females, giving some support to the hypothesis that size differences may indicate the quality of individual swelling cycles. However, there was no significant difference in swelling size between conceptive and nonconceptive cycles. Measures of swelling size varied more between females than within females across swelling cycles, implying that swelling size was a relatively consistent characteristic of individual females. Swelling size was not significantly related to either general measures of parasitism and immune status, or to the closest available measures to each swelling cycle. Nor was swelling size significantly related to genetic diversity. The healthy, provisioned nature of the colony and problems associated with observational, correlational studies restrict interpretation of our data. However, in combination with previous findings that females of higher reproductive success do not show larger swellings, and that males do not allocate mating effort as a function of swelling size, these results imply that sexual swelling size does not indicate female quality in these semifree-ranging mandrills.

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References

  • Abernethy KA, White LJT, Wickings EJ (2002) Hordes of mandrills (Mandrillus sphinx): extreme group size and seasonal male presence. J Zool 258:131–137

    Article  Google Scholar 

  • Able DJ (1996) The contagion indicator hypothesis for parasite-mediated sexual selection. Proc Natl Acad Sci U S A 93:2229–2233

    Article  CAS  PubMed  Google Scholar 

  • Alberts SC, Altmann J, Wilson ML (1996) Mate guarding constrains foraging activity of male baboons. Anim Behav 51:1269–1277

    Article  Google Scholar 

  • Altmann SA (1962) A field study of the sociobiology of the rhesus monkey, Macaca mulatta. Ann NY Acad Sci 102:338–435

    CAS  PubMed  Google Scholar 

  • Altmann J, Altmann SA, Hausfater G, McCuskey S (1977) Life history of yellow baboons: physical development, reproductive parameters and infant mortality. Primates 18:315–330

    Article  Google Scholar 

  • Amos W, Worthington Wilmer J, Fullard K, Burg TM, Croxall JP, Bloch D, Coulson T (2001) The influence of parental relatedness on reproductive success. Proc R Soc Lond Ser B Biol Sci 268:2021–2027

    Article  CAS  Google Scholar 

  • Amundsen T (2000) Why are female birds ornamented? Trends Ecol Evol 15:149–155

    Article  PubMed  Google Scholar 

  • Andersson M (1994) Sexual selection. Princeton University Press, Princeton, New Jersey

    Google Scholar 

  • Aparicio JM, Cordero PJ, Veiga JP (2001) A test of the hypothesis of mate choice based on heterozygosity in the spotless starling. Anim Behav 62:1001–1006

    Article  Google Scholar 

  • Bentley-Condit VK, Smith EO (1997) Female reproductive parameters of Tana River yellow baboons. Int J Primatol 16:581–596

    Article  Google Scholar 

  • Bercovitch FB (1983) Time budgets and consortships in olive baboons (Papio anubis). Folia Primatol 41:180–190

    Google Scholar 

  • Bielert C, Anderson CM (1985) Baboon sexual swellings and male response: a possible operational mammalian supernormal stimulus and response interaction. Int J Primatol 6:377–393

    Google Scholar 

  • Bielert C, Girolami C (1986) Experimental assessments of behavioural and anatomical components of female chacma baboon (Papio ursinus) sexual attractiveness. Psychoneuroendocrinology 11:75–90

    Article  CAS  PubMed  Google Scholar 

  • Bielert C, van der Walt LA (1982) Male chacma baboon (Papio ursinus) sexual arousal: mediation by visual cues from female conspecifics. Psychoneuroendocrinology 7:31–48

    Article  CAS  PubMed  Google Scholar 

  • Bielert C, Girolami L, Jowell S (1989) An experimental examination of the colour component in visually mediated sexual arousal of the chacma baboons (Papio ursinus). J Zool 219:569–579

    Article  Google Scholar 

  • Brown JL (1997) A theory of mate choice based on heterozygosity. Behav Ecol 8:60–65

    Google Scholar 

  • Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Ann Rev Ecolog Syst 18:237–268

    Article  Google Scholar 

  • Charpentier M, Setchell JM, Prugnolle F, Knapp LA, Wickings EJ, Peignot P, Hossaert-McKey M (2005) Genetic diversity and reproductive success in mandrills (Mandrillus sphinx). Proc Natl Acad Sci U S A 102:16723–16728

    Article  CAS  PubMed  Google Scholar 

  • Cohen J (1988) Statistical power analysis for the behavioral sciences. Lawrence Erlbaum, New Jersey

    Google Scholar 

  • Cotton S, Fowler K, Pomiankowski A (2004) Do sexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap hypothesis? Proc Biol Sci 271:771–783

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Dewsbury DA (1982) Ejaculate cost and male choice. Am Nat 119:601–610

    Article  Google Scholar 

  • Ditchkoff SS, Lochmiller RL, Masters RE, Hoofer ST, van den Bussche RA (2001) Major-histocompatibility-complex-associated variation in secondary sexual traits of white-tailed deer (Odocoileus virginianus): evidence for good-genes advertisement. Evolution 55:616–625

    Article  CAS  PubMed  Google Scholar 

  • Dixson AF (1983) Observations on the evolution and behavioural significance of ‘sexual skin’ in female primates. Adv Study Behav 13:63–106

    Google Scholar 

  • Dixson AF (1998) Primate sexuality: comparative studies of the prosimians, monkeys, apes and human beings. Oxford University Press, Oxford

    Google Scholar 

  • Domb LG, Pagel M (2001) Sexual swellings advertise female quality in wild baboons. Nature 410:204–206

    Article  CAS  PubMed  Google Scholar 

  • Domb LG, Pagel M (2002) Reply: significance of primate sexual swellings. Nature 420:143

    Article  CAS  Google Scholar 

  • Drews C (1996) Contexts and patterns of injuries in free-ranging male baboons (Papio cynocephalus). Behaviour 133:443–474

    Google Scholar 

  • Edwards SV, Hedrick PW (1998) Evolution and ecology of MHC molecules: from genomics to sexual selection. Trends Ecol Evol 13:305–311

    Article  Google Scholar 

  • Emery MA, Whitten PL (2003) Size of sexual swellings reflects ovarian function in chimpanzees (Pan troglodytes). Behav Ecol Sociobiol 54:340–351

    Article  Google Scholar 

  • Erdfelder E, Faul F, Buchner A (1996) GPOWER: a general power analysis program. Behav Res Meth Instrum Comput 28:1–11

    Google Scholar 

  • Foerster K, Delhey K, Johnsen A, Lifjeld JT, Kempenaers B (2003) Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425:714–717

    Article  CAS  PubMed  Google Scholar 

  • Grubb P (1973) Distribution, divergence and speciation of the drill and mandrill. Folia Primatol 20:161–177

    Article  CAS  PubMed  Google Scholar 

  • Gustafsson L, Qvanstroem A, Sheldon B (1995) Trade-offs between life history traits and a secondary sexual character in male collared flycatchers. Nature 375:311–313

    Article  CAS  Google Scholar 

  • Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites. Science 218:384–387

    Article  CAS  PubMed  Google Scholar 

  • Harrison MJS (1988) The mandrills in Gabon’s rain forest: ecology, distribution and status. Oryx 22:218–228

    Article  Google Scholar 

  • Hoffman JI, Boyd IL, Amos W (2004) Exploring the relationship between parental relatedness and male reproductive success in the Antarctic fur seal Arctocephalus gazella. Evolution 58:2087–2099

    Article  PubMed  Google Scholar 

  • Hoglund J, Sheldon BC (1998) The cost of reproduction and sexual selection. Oikos 83:478–483

    Article  Google Scholar 

  • Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64

    Article  CAS  PubMed  Google Scholar 

  • Johnstone RA (1995) Sexual selection, honest advertisement and the handicap principle—reviewing the evidence. Biol Rev 70:1–65

    Article  CAS  PubMed  Google Scholar 

  • Keller L, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241

    Article  Google Scholar 

  • Kim C-Y, Lee H-S, Han S-C, Heo J-D, Kwon M-S, Ha C-S, Han S-S (2005) Hematological and serum biochemical values in cynomolgus monkeys anesthetized with ketamine hydrochloride. J Med Primatol 34:96–100

    Article  CAS  PubMed  Google Scholar 

  • Kokko H, Brooks R, McNamara JM, Houston AI (2002) The sexual selection continuum. Proc R Soc Lond B Biol Sci 269:1331–1340

    Article  Google Scholar 

  • Marshall RC, Buchanan KL, Catchpole CK (2003) Sexual selection and individual genetic diversity in a songbird. Proc R Soc Lond B Biol Sci 270:S248–S250

    Google Scholar 

  • Marson J, Gervais D, Meuris S, Cooper RW, Jouannet P (1989) Influence of ejaculation frequency on semen characteristics in chimpanzees (Pan troglodytes). J Reprod Fertil 85:43–45

    Article  CAS  PubMed  Google Scholar 

  • Mitton JB, Schuster WSF, Cothran EG, de Fries JC (1993) Correlation between the individual heterozygosity of parents and their offspring. Heredity 71:59–63

    PubMed  Google Scholar 

  • Moller AP, Saino N (1994) Parasites, immunology of hosts, and host sexual selection. J Parasitol 80:850–858

    Article  CAS  PubMed  Google Scholar 

  • Møller AP, Christe P, Lux E (1999) Parasitism, host immune function, and sexual selection. Q Rev Biol 74:3–20

    Article  PubMed  Google Scholar 

  • Müller G, Ward PI (1995) Parasitism and heterozygosity influence the secondary sexual characters of the European minnow, Phoxinus phoxinus (L) (Cyprinidae). Ethology 100:309–319

    Article  Google Scholar 

  • Norris K, Evans MR (2000) Ecological immunology: life history trade-offs and immune defence in birds. Behav Ecol 11:19–26

    Article  Google Scholar 

  • Nunn CL (1999) The evolution of exaggerated sexual swellings in primates and the graded signal hypothesis. Anim Behav 58:299–246

    Article  Google Scholar 

  • Nunn CL, Altizer S (2006) Infectious diseases in primates: behavior, ecology and evolution. Oxford University Press, Oxford

    Google Scholar 

  • Nunn CL, van Schaik CP, Zinner D (2001) Do exaggerated sexual swellings function in female mating competition in primates? A comparative test of the reliable indicator hypothesis. Behav Ecol 12:646–654

    Article  Google Scholar 

  • Pagel M (1994) The evolution of conspicuous oestrous advertisement in old world monkeys. Anim Behav 47:1333–1341

    Article  Google Scholar 

  • Penn DJ, Potts WK (1999) The evolution of mating preferences and major histocompatibility complex genes. Am Nat 153:145–164

    Article  Google Scholar 

  • Preston BT, Stevenson IR, Pemberton JM, Wilson K (2001) Dominant rams lose out by sperm depletion: a waning success in siring counters a ram’s high score in competition for ewes. Nature 409:681–682

    Article  CAS  PubMed  Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Scribner KT, Smith MH, Johns PE (1989) Environmental and genetic components of antler growth in white-tailed deer. J Mammal 70:284–291

    Article  Google Scholar 

  • Setchell JM (1999) Socio-sexual development in the male mandrill (Mandrillus sphinx). University of Cambridge, Cambridge, UK

    Google Scholar 

  • Setchell JM, Wickings EJ (2004a) Sexual swellings in mandrills (Mandrillus sphinx): a test of the reliable indicator hypothesis. Behav Ecol 15:438–445

    Article  Google Scholar 

  • Setchell JM, Wickings EJ (2004b) Social and seasonal influences on the reproductive cycle in female mandrills (Mandrillus sphinx). Am J Phys Anthropol 125:73–84

    Article  PubMed  Google Scholar 

  • Setchell JM, Tshipamba P, Bourry O, Rouquet P, Wickings EJ, Knapp LA (2006) Haematology of a semi-free-ranging colony of mandrills (Mandrillus sphinx). Int J Primatol (in press)

  • Shaikh AA, Celaya CL, Gomez I, Schaik SA (1982) Temporal relationship of hormonal peaks to ovulation and sex skin deturgescence in the baboon. Primates 23:444–452

    Article  CAS  Google Scholar 

  • Sheridan L, Pomiankowski A (1997) Fluctuating asymmetry, spot asymmetry and inbreeding depression in the sexual coloration of male guppy fish. Heredity 79:515–523

    Article  Google Scholar 

  • Snowdon CT (2004) Sexual selection and communication. In: Kappeler PK, van Schaik CP (eds) Sexual selection in primates: new and comparative perspectives. Cambridge University Press, Cambridge, pp 57–70

    Google Scholar 

  • Stallmann RR, Froehlich JW (2000) Primate sexual swellings as coevolved signal systems. Primates 41:1–16

    Google Scholar 

  • Stuart MD, Strier KB (1995) Primates and parasites: a case for a multidisciplinary approach. Int J Primatol 16:577–593

    Google Scholar 

  • van Oosterhout C, Trigg RE, Carvalho GR, Magurran AE, Hauser L, Shaw PW (2003) Inbreeding depression and genetic load of sexually selected traits: how the guppy lost its spots. J Evol Biol 16:273–281

    Article  PubMed  Google Scholar 

  • von Schantz T, Wittzell H, Goransson G, Grahn M, Persson K (1996) MHC genotype and male ornamentation: genetic evidence for the Hamilton–Zuk model. Proc R Soc Lond Ser B Biol Sci 263:265–271

    Google Scholar 

  • von Schantz T, Wittzell H, Goransson G, Grahn M (1997) Mate choice, male condition-dependent ornamentation and MHC in the pheasant. Hereditas 127:133–140

    Article  Google Scholar 

  • Wedell N, Gage MJG, Parker GA (2002) Sperm competition, male prudence and sperm-limited females. Trends Ecol Evol 17:313–320

    Article  Google Scholar 

  • Weingrill T, Lycett JE, Barrett L, Hill RA, Henzi SP (2003) Male consortship behaviour in chacma baboons: the role of demographic factors and female conceptive probabilities. Behaviour 140:405–427

    Article  Google Scholar 

  • Wildt DE, Doyle U, Stone SC, Harrison RM (1977) Correlation of perineal swelling with serum ovarian hormone levels, vaginal cytology and ovarian follicular development during the baboon reproductive cycle. Primates 18:261–270

    Article  CAS  Google Scholar 

  • Zahavi A (1975) Mate selection—a selection for handicap. J Theor Biol 53:205–214

    Article  CAS  PubMed  Google Scholar 

  • Zinner D, Alberts SC, Nunn CL, Altmann J (2002) Significance of primate sexual swellings. Nature 420:142–143

    Article  CAS  PubMed  Google Scholar 

  • Zuk M (1992) The role of parasites in sexual selection: current evidence and future directions. Adv Study Behav 21:39–68

    Article  Google Scholar 

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Acknowledgements

We wish to thank CIRMF for making the study possible. We particularly thank the past and present staff of the Primate Centre and the LAM at CIRMF. We thank Benoît Goossens and Aurelie Gauthier for help with fecal sampling, and Charlie Nunn and three anonymous reviewers for comments that greatly improved the manuscript. The CIRMF is financed by the Gabonese government, Total Gabon, and the Ministére Français des Affaires Etrangéres. This study was funded by a Leverhulme Trust project grant (award no. F/01576/B).

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Authors and Affiliations

  1. Department of Biological Anthropology, University of Cambridge, Downing Street, Cambridge, CB2 3DZ, UK

    Joanna M. Setchell & Leslie A. Knapp

  2. Centre International de Recherches Médicales, BP 769, Franceville, Gabon

    Joanna M. Setchell, Marie J. E. Charpentier & E. Jean Wickings

  3. Centre d’Ecologie Fonctionnelle et Evolutive UMR 5175, CNRS, 1919 Route de Mende, 34293, Montpellier Cedex 5, France

    Marie J. E. Charpentier

  4. Duke University, Science Drive, Biological Building 020, P.O. 90338, Durham, NC, 27708, USA

    Marie J. E. Charpentier

  5. Field Veterinary Program, Wildlife Conservation Society, New York, NY, USA

    Issa-Ben Bedjabaga & Patricia Reed

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  1. Joanna M. Setchell
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Correspondence to Joanna M. Setchell.

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Communicated by C. Nunn

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Setchell, J.M., Charpentier, M.J.E., Bedjabaga, IB. et al. Secondary sexual characters and female quality in primates. Behav Ecol Sociobiol 61, 305–315 (2006). https://doi.org/10.1007/s00265-006-0260-7

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