Advertisement

Behavioral Ecology and Sociobiology

, Volume 54, Issue 4, pp 340–351 | Cite as

Size of sexual swellings reflects ovarian function in chimpanzees (Pan troglodytes)

  • Melissa A. Emery
  • Patricia L. Whitten
Original Article

Abstract

While many theories exist on the evolution of the sexual swelling signal in female primates, the significance of the very large and variable swellings found in some catarrhine primates is still debated. As suggested by Pagel [(1994) Anim Behav 47:1333–1341], these exaggerated and costly signals have the potential to provide information about differential female reproductive quality to males. While Domb [(2000) Department of Anthropology, Harvard University, Cambridge] and Domb and Pagel [(2001) Nature 410:204–206] propose that swellings serve to reliably indicate between-female fitness differences, we hypothesize that they may indicate current reproductive cycle quality, within or between females. This study examines the between-cycle relationship between ovarian function, gauged via fecal steroid analysis, and absolute size of sexual swellings, yielded through photogrammetric methods. Fourteen cycles from eight captive, group-living chimpanzees (Pan troglodytes) exhibited considerable variability both in ovarian steroid levels and maximum sexual swelling size. Nearly all measures of a female's maximal swelling in a cycle correlated with early follicular and early luteal estradiol averages and the duration of luteal progesterone elevation. Swelling area was also correlated with late follicular estradiol. Given past evidence that such measures of ovarian function predict conceptive success, these data strongly suggest that swellings could convey information to competing males about the fecundability of a potential mate.

Keywords

Sexual swellings Fecal steroids Ovarian hormones Chimpanzees 

Notes

Acknowledgements

Thanks to Jim Moore for his generosity in loaning M.A.E. the Nikon and Photoscale-2 photographic equipment used in this study. We also thank Katja Liebal for assistance in sample collection and Brian Hare, Signe Preuschoft, and Michael Seres, for introduction to the chimpanzees and for allowing collections during their studies. Elizabeth Russell provided valuable assistance in the Laboratory of Reproductive Ecology and Environmental Toxicology at Emory University. The authors are indebted to Cheryl Knott, Richard Wrangham, and Jeremy Dahl for helpful comments during planning stages, to C.K., R.W., Peter Ellison, David Pilbeam, Melissa Gerald, Martin Muller, Charles Nunn, and several anonymous reviewers for comments on the manuscript, and to Randall Collura and Ofer Bar-Yosef for use of their scanning equipment and expertise. This study was made possible by a NSF Graduate Research Fellowship, Mellon Foundation training grant (to M.A.E.), NIH Grant RR-00165 (to Yerkes), and Thomas Gordon and the animal care staff at the Yerkes Regional Primate Research Center field station. The Yerkes Primate Center and this research project are approved by the American Association for the Accreditation of Laboratory Animal Care.

References

  1. Aidara D, Badawi M, Zahiri-Tagret C, Robyn C (1981) Changes in concentrations of serum prolactin, FSH, oestradiol and progesterone and of the sex skin during the menstrual cycle in the mangabey monkey (Cercocebus atys lunulatus). J Reprod Fertil 62:475–481PubMedGoogle Scholar
  2. Akman M, Erden H, Bener F, Liu J, Bahceci M (2002) Can luteal phase estradiol levels predict the pregnancy outcome in in vitro fertilization cycles of good responders whose excess embyros yield blastocysts? Fertil Steril 77:638–639. DOI 10.1016/S0015-0282(01)03209-5Google Scholar
  3. Altmann J, Altmann SA, Hausfater G, McCuskey SA (1977) Life history of yellow baboons: physical development, reproductive parameters, and infant mortality. Primates 18:315–330Google Scholar
  4. Amundsen T, Forsgren E (2001) Male mate choice selects for female coloration in a fish. Proc Natl Acad Sci USA 98:13155–13160. DOI 10.1073/pnas.211439298CrossRefPubMedGoogle Scholar
  5. Amundsen T, Forsgren E (2003) Male preference for colourful females affected by male size in a marine fish. Behav Ecol Sociobiol (in press). DOI 10.1007/s00265-003-0593-4Google Scholar
  6. Anderson CM, Bielert CF (1994) Adolescent exaggeration in female Catarrhine primates. Primates 35:283–300Google Scholar
  7. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  8. Bahr NI, Palme R, Mohle U, Hodges JK, Heistermann M (2000) Comparative aspects of the metabolism and excretion of cortisol in three individual nonhuman primates. Gen Comp Endocrinol 117:427–438. DOI 10.1006/gcen.1999.7431CrossRefPubMedGoogle Scholar
  9. Berger J, Peacock M (1988) Variability in size-weight relationships of Bison bison. J Mammal 69:618–624Google Scholar
  10. Berglund A, Rosenqvist G, Bernet P (1997) Ornamentation predicts reproductive success in female pipefish. Behav Ecol Sociobiol 34:435–442Google Scholar
  11. Bielert C, Anderson CM (1985) Baboon sexual swellings and male response: a possible operational mammalian supernormal stimulus and response interaction. Int J Primatol 6:377–393Google Scholar
  12. Boesch C, Boesch-Achermann H (2000) The chimpanzees of the Tai Forest. Oxford University Press, OxfordGoogle Scholar
  13. Brockman DK, Whitten PL (1996) Reproduction in free-ranging Propithecus verreauxi: estrus and the relationship between multiple partner matings and fertilization. Am J Phys Anthropol 100:57–69CrossRefPubMedGoogle Scholar
  14. Brockman DK, Whitten PL, Russell E, Richard AF, Izard MK (1995) Application of fecal steroid techniques to the reproductive endocrinology of female Verreaux's sifaka (Propithecus verreauxi). Am J Primatol 36:313–325Google Scholar
  15. Byers JA (1998) American pronghorn: social adaptations and the ghosts of predators past. University of Chicago Press, ChicagoGoogle Scholar
  16. Carlisle KS, Brenner RM, Montagna W (1981) Hormonal regulation of sex skin in Macaca nemestrina. Biol Reprod 25:1053–1063PubMedGoogle Scholar
  17. Cedard L, Guichard A, Janssens Y, G. T, Boyer P, Zorn JR (1987) Progesterone and estradiol in saliva after in vitro fertilization and embryo transfer. Fertil Steril 47:278–283PubMedGoogle Scholar
  18. Clutton-Brock TH, Harvey PH (1976) Evolutionary rules and primate societies. In: Bateson PPG, Hinde RA (eds) Growing points in ethology, 6th edn. Cambridge University Press, Cambridge, pp 195–237Google Scholar
  19. Cuadrado M (1998) The use of yellow spot colors as a sexual receptivity signal in females of Chamaeleo chamaeleon. Herpetology 54:395–402Google Scholar
  20. Dahl JF, Nadler RD (1992) Genital swelling in females of the monogamous gibbon Hylobates (H.) lar. Am J Phys Anthropol 89:101–108PubMedGoogle Scholar
  21. Dahl JF, Nadler RD, Collins DC (1991) Monitoring the ovarian cycles of Pan troglodytes and P. paniscus: a comparative approach. Am J Primatol 24:195–209Google Scholar
  22. Dixson AF (1983) Observations on the evolution and behavioral significance of "sexual skin" in female primates. Adv Stud Behav 13:63–106Google Scholar
  23. Dixson AF (1998) Primate sexuality: comparative studies of the prosimians, monkeys, apes, and human beings. Oxford University Press, OxfordGoogle Scholar
  24. Dixson AF, Mundy NJ (1994) Sexual behavior, sexual swelling, and penile evolution in chimpanzees (Pan troglodytes). Arch Sex Behav 23:267–280PubMedGoogle Scholar
  25. Domb L (2000) Sexual swellings in wild baboons (Papio cynocephalus anubis) at Gombe National Park, Tanzania. PhD thesis, Department of Anthropology, Harvard University, Cambridge, Mass.Google Scholar
  26. Domb LG, Pagel MD (2001) Sexual swellings advertise female quality in wild baboons. Nature 410:204–206. DOI 10.1038/35065597CrossRefPubMedGoogle Scholar
  27. Ellison PT, Panter-Brick C, Lipson SF, O'Rourke MT (1993) The ecological context of human ovarian function. Hum Reprod 8:2248–2258PubMedGoogle Scholar
  28. Furuichi T (1987) Sexual swelling, receptivity and grouping of wild pygmy chimpanzee females at Wamba, Zaire. Primates 28:309–318Google Scholar
  29. Gillman J (1940) The effect of multiple injections of progesterone on the turgescent perineum of the baboon (Papio porcarius). Endocrinology 26:1072–1077Google Scholar
  30. Gillman J, Stein HB (1941) A quantitative study of the inhibition of oestradiol benzoate by progesterone in the baboon (Papio porcarius). Endocrinology 28:274–282Google Scholar
  31. Girolami L, Bielert C (1987) Female perineal swelling and its effects on male sexual arousal: an apparent sexual releaser in the chacma baboon (Papio ursinus). Int J Primatol 8:651–661Google Scholar
  32. Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Belknap, CambridgeGoogle Scholar
  33. Graham CE (1981) Menstrual cycle of the great apes. In: Graham CE (ed) Reproductive biology of the great apes. Academic, New York, pp 1–43Google Scholar
  34. Graham CE (1982) Ovulation time: a factor in ape fertility assessment. Am J Primatol [Suppl] 1:51–55Google Scholar
  35. Graham CE, Warner H, Misener J, Collins DC, Preedy JRK (1977) The association between basal body temperature, sexual swelling and urinary gonadal hormone levels in the menstrual cycle of the chimpanzee. J Reprod Fertil 50:23–28PubMedGoogle Scholar
  36. Hamilton WJ (1984) Significance of paternal investment by primates to the evolution of adult male-female associations. In: Taub DM (ed) Primate paternalism. Van Nostrand Reinhold, New York, pp 309–335Google Scholar
  37. Harlow SD, Baird DD, Weinberg CR, Wilcox AJ (2000) Urinary oestrogen patterns in long follicular phases. Hum Reprod 15:11–16CrossRefGoogle Scholar
  38. Heistermann M, Tari S, Hodges JK (1993) Measurement of faecal steroids for monitoring ovarian function in New World primates, Callitrichidae. J Reprod Fertil 99:243–251PubMedGoogle Scholar
  39. Heistermann M, Möle U, Vervaecke H, van Elsacker L, Hodges JK (1996) Application of urinary and fecal steroid measurements for monitoring ovarian function and pregnancy in the bonobo (Pan paniscus) and evaluation of perineal swelling patterns in relation to endocrine events. Biol Reprod 55:844–853PubMedGoogle Scholar
  40. Hrdy SB (1981) The woman that never evolved. Harvard University Press, Cambridge, Mass.Google Scholar
  41. Jacobsen J (1991) Photoscale-2. Arcata, Calif.Google Scholar
  42. Kato J, Onouchi T, Oshima K (1980) The presence of progesterone receptors in the sexual skin of the monkey. Steroids 36:743–749CrossRefPubMedGoogle Scholar
  43. Knott CD (1999) Reproductive physiological and behavioral responses of orangutans in Borneo to fluctuations in food availability. PhD thesis, Department of Anthropology, Harvard University, Cambridge, Mass.Google Scholar
  44. Krohn PL, Zuckerman S (1937) Water metabolism in relation to the menstrual cycle. J Physiol (Lond) 88:369–387Google Scholar
  45. Lenton EA, Gelsthorp CH, Harper R (1988) Measurement of progesterone in saliva: assessment of the normal fertile range using spontaneous conception cycles. Clin Endocrinol 38:637–646Google Scholar
  46. Li H, Nakajima S, Chen J, Todd H, JW O, BL L (2001) Differences in hormonal characteristics of conceptive versus nonconceptive cycles. Fertil Steril 75:549–553. DOI 10.1016/S0015-0282(00)01765-9CrossRefPubMedGoogle Scholar
  47. Lipson SF, Ellison PT (1996) Comparison of salivary steroid profiles in naturally occurring conception and non-conception cycles. Hum Reprod 11:2090–2096PubMedGoogle Scholar
  48. Masters A, Markham R (1991) Assessing reproductive status in orangutans by using urinary estrone. Zoo Biol 10:197–208Google Scholar
  49. Matsumoto-Oda A (1998) Injuries to the sexual skin of female chimpanzees at Mahale and their effect on behaviour. Folia Primatol 69:400–404Google Scholar
  50. Matsumoto-Oda A (1999) Mahale chimpanzees: grouping patterns and cycling females. Am J Primatol 47:197–207. DOI 10.1002/(SICI)1098-2345(1999)47:3197:AID-AJP23.0.Co;2-3Google Scholar
  51. McArthur JW, Beitins IZ, Gorman A, Collins DC, Preedy JRK, Graham CE (1981) The interrelationship between sex skin swelling and the urinary excretion of LH, estrone, and pregnanediol by the cycling female chimpanzee. Am J Primatol 1:265–270Google Scholar
  52. Milgrom E (1990) Steroid hormones. In: Baulieu E-E, Kelly PA (eds) Hormones: from molecules to disease. Chapman & Hall, New York, pp 387–438Google Scholar
  53. Milton K, Demment MW (1988) Digestion and passage kinetics of chimpanzees fed high and low fiber diets and comparison with human data. J Nutr 118:1082–1088PubMedGoogle Scholar
  54. Moore J, Jacobsen J (1992) Remote morphometry. Am J Phys Anthropol [Suppl] 14:126–127Google Scholar
  55. Nadler RD, Collins DC (1991) Copulatory frequency, urinary pregnanediol, and fertility in great apes. Am J Primatol 24:167–179Google Scholar
  56. Nadler RD, Graham CE, Collins DC, Gould KG (1979) Plasma gonadotropins, prolactin, gonadal steroids and genital swelling during the menstrual cycle of lowland gorillas. Endocrinology 105:290–296PubMedGoogle Scholar
  57. Nadler RD, Graham CE, Gosselin RE, Collins DC (1985) Serum levels of gonadotropins and gonadal steroids, including testosterone, during the menstrual cycles of the chimpanzee (Pan troglodytes). Am J Primatol 9:273–284Google Scholar
  58. Nakamura M (1990) Cloacal protuberance and copulatory behavior of the Alpine Accentor Prunella collaris. Auk 107:284–295Google Scholar
  59. Noordwijk MA van (1985) Sexual behavior of Sumatran long-tailed macaques (Macaca fasciciularis). Z Tierpsychol 70:277–296Google Scholar
  60. Nunn CL (1999) The evolution of exaggerated sexual swellings in primates and the graded-signal hypothesis. Anim Behav 58:229–246. DOI 10.1006/anbe.1999.1159CrossRefPubMedGoogle Scholar
  61. 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 12:646–654CrossRefGoogle Scholar
  62. Onouchi T, Kato J (1983) Estrogen receptors and the estrogen-inducible progestin receptors in the sexual skin of the monkey. J Steroid Biochem 18:145–151CrossRefPubMedGoogle Scholar
  63. Ozasa H, Gould KG (1982) Demonstration and characterization of estrogen receptor in chimpanzee sex skin: correlation between nuclear receptor levels and degree of swelling. Endocrinology 111:125–131PubMedGoogle Scholar
  64. Pagel M (1994) The evolution of conspicuous oestrous advertisement in Old World monkeys. Anim Behav 47:1333–1341CrossRefGoogle Scholar
  65. Perez LE, Czekala NM, Weisenseel KA, Lasley BL (1988) Excretion of radiolabeled estradiol metabolites in the slow loris (Nycticebus coucang). Am J Primatol 16:321–330Google Scholar
  66. Shideler SE, Ortuno AM, Moran FM, Moorman EA, Lasley BL (1993) Simple extraction and enzyme immunoassays for estrogen and progesterone metabolites in the feces of Macaca fascicularis during nonreceptive and conceptive ovarian cycles. Biol Reprod 48:1290–1298PubMedGoogle Scholar
  67. Sillen-Tullberg B, Møller AP (1993) The relationship between concealed ovulation and mating systems in anthropoid primates: a phylogenetic analysis. Am Nat 141:1–25CrossRefGoogle Scholar
  68. Stallmann R, Froehlich J (2000) Primate sexual swellings as coevolved signal systems. Primates 41:1–16Google Scholar
  69. Stavisky RC (1994) Socioendocrinology: noninvasive techniques for monitoring reproductive function in captive and free ranging primates. Diss Abstr Int A55:1018Google Scholar
  70. Stavisky RC, Russell E, Stallings J, Smith EO, Worthman C, Whitten P (1995) Fecal steroid analysis of ovarian cycles in free-ranging baboons. Am J Primatol 36:285–297Google Scholar
  71. Steinetz BG, Ducrot C, Randolph C, Mahoney CJ (1992) Determination of the time of ovulation in chimpanzees by measurement of LH, estrone sulfate, and pregnanediol 3 alpha-glucuronide in urine: comparison with serum hormone patterns. J Med Primatol 21:239–245PubMedGoogle Scholar
  72. Tenaza RR (1989) Female sexual swellings in the Asian colobine Simias concolor. Am J Primatol 17:81–86Google Scholar
  73. Thomson JA, Hess DL, Dahl KD, Iliff-Sizemore SA, Stouffer RL, Wolf DP (1992) The Sulawesi crested black macaque (Macaca nigra) menstrual cycle: changes in perineal tumescence and serum estradiol, progesterone, follicle-stimulating hormone, and luteinizing hormone levels. Biol Reprod 46:879–884PubMedGoogle Scholar
  74. Tutin CEG (1980) Reproductive behavior of wild chimpanzees in the Gombe National Park, Tanzania. J Reprod Fertil [Suppl] 28:43–57Google Scholar
  75. Wallis J (1985) Synchrony of estrous swelling in captive group-living chimpanzees (Pan troglodytes). Int J Primatol 6:335–350Google Scholar
  76. Wallis J (1992) Chimpanzee genital swelling and its role in the pattern of sociosexual behavior. Am J Primatol 28:101–113Google Scholar
  77. Wallis J (1997) A survey of reproductive parameters in the free-ranging chimpanzees of Gombe National Park. J Reprod Fertil 109:297–307PubMedGoogle Scholar
  78. Wallis J, Goodall J (1993) Anogenital swelling in pregnant chimpanzees of Gombe National Park. Am J Primatol 31:89–98Google Scholar
  79. Wasser SK (1996) Reproductive control in wild baboons measured by fecal steroids. Biol Reprod 55:393–399PubMedGoogle Scholar
  80. Wasser SK, Monfort SL, Southers J, Wildt DE (1994) Excretion rates and metabolites of oestradiol and progesterone in baboon (Papio cynocephalus cynocephalus) faeces. J Reprod Fertil 101:213–220PubMedGoogle Scholar
  81. Weiss S (2002) Reproduction signals of female lizards: pattern of trait expression and male response. Ethology 108:793-–813. DOI 10.1046/j.1439-0310.2002.00819.xCrossRefGoogle Scholar
  82. West NB, Carlisle KS, Brenner RM (1990) Progesterone treatment suppresses estrogen receptors in the sex skin of Macaca nemestrina. J Steroid Biochem 35:481–485CrossRefPubMedGoogle Scholar
  83. Whitten PL, Russell E (1996) Informational content of sexual swellings and fecal steroids in sooty mangabeys (Cercocebus torquatus atys). Am J Primatol 40:67–82CrossRefGoogle Scholar
  84. Whitten PL, Brockman DK, Stavisky RC (1998a) Recent advances in noninvasive techniques to monitor hormone-behavior interactions. Yrbk Phys Anthropol 41:1–23CrossRefGoogle Scholar
  85. Whitten PL, Stavisky RC, Aureli F, Russell E (1998b) Response of fecal cortisol to stress in captive chimpanzees (Pan troglodytes). Am J Primatol 44:57–69CrossRefPubMedGoogle Scholar
  86. Wood JW (1994) Dynamics of human reproduction: biology, biometry, demography. Aldine, New YorkGoogle Scholar
  87. Worthman CM, Stallings JF, Hofman LF (1990) Sensitive salivary estradiol assay for monitoring ovarian function. J Clin Chem 36:1769–1773Google Scholar
  88. Worthman CM, Jenkins CL, Stallings JF, Lai D (1993) Attenuation of nursing-related ovarian suppression and high fertility in well-nourished, intensively breast-feeding Amele women of lowland Papua New Guinea. J Biosoc Sci 25:425–443PubMedGoogle Scholar
  89. Wrangham RW (1993) The evolution of sexuality in chimpanzees and bonobos. Hum Nat 4:47–79Google Scholar
  90. Wrangham RW (2000) Why are male chimpanzees more gregarious than mothers? A scramble competition hypothesis. In: Kappeler PM (ed) Primate males: causes and consequences of variation in group composition, 21st edn. Cambridge University Press, Cambridge, pp 248–258Google Scholar
  91. Wrangham RW (2001) Costs and benefits of female sexual attractiveness in chimpanzees and bonobos: a scramble competition hypothesis. In: Boesch C, Hohman G, Marchant LF (eds) Behavioral variation in chimpanzees and bonobos. Cambridge University Press, CambridgeGoogle Scholar
  92. Young WC, Yerkes RM (1943) Factors influencing the reproductive cycle in the chimpanzee; the period of adolescent sterility and related problems. Endocrinology 33:121–154Google Scholar
  93. Yovich JL, Edirisinghe WR, Cummins JM (1991) Evaluation of luteal support therapy in arandomized controlled study within a gamete intrafallopian transfer program. Fertil Steril 55:131–139PubMedGoogle Scholar
  94. Ziegler TE, Sholl SA, Scheffler G, Haggery MA, Lasley BL (1989) Excretion of estrone, estradiol, and progesterone in the urine and feces of the female cotton-top tamarin (Saguinus oedipus oedipus). Am J Primatol 17:185–195Google Scholar
  95. Zinner D, Alberts SC, Nunn CL, Altmann J (2002) Significance of primate sexual swellings. Nature 420:142–143. DOI 10.1038/420142aCrossRefPubMedGoogle Scholar
  96. Zuckerman S, Parkes AS (1939) Observations on the secondary sexual characters in monkeys. J Endocrinol 1:430–439Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  1. 1.Department of AnthropologyHarvard UniversityCambridgeUSA
  2. 2.Department of AnthropologyEmory UniversityAtlantaUSA

Personalised recommendations