A vertical living: sexual selection strategies and upright locomotion

Ivan Norscia; Elisabetta Palagi

doi:10.1017/CBO9781139060059.006

3 - A vertical living: sexual selection strategies and upright locomotion

from Part I - Communication: from sociality to society

Published online by Cambridge University Press: 05 May 2016

Ivan Norscia and

Elisabetta Palagi

Foreword by

Alison Jolly and

Ian Tatterall

Afterword by

Michael Huffman

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Ivan Norscia: Affiliation:
Università degli Studi, Pisa
Elisabetta Palagi: Affiliation:
Università degli Studi, Pisa

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Summary

Could our vertical posture have influenced our sexual signals?…

Virtually all the sexual signals…are on the front of the body – the facial expressions, the lips, the beard, the nipples, the areolar signals, the breasts of the female, the pubic hair, the genitals themselves…The frontal approach means that the in-coming sexual signals and rewards are kept tightly linked with the identity signals from the partner.

Desmond Morris, 1967

Upright habits and their impact on sexual signalling

In a number of animal species, it is possible to observe that males and females strongly differ in specific morphological and/or behavioural traits. This phenomenon, called dimorphism, can be largely observed in primates showing male–female differences in parental investment, growth and developmental pattern, body and canine size, scent glands and scent marking behaviour, vocalisation and visual ornaments (e.g., skin colours, flanges and fur). Such sexually dimorphic features are defined as ‘secondary’ because they are under the hormonal control of primary sexual characters (reproductive organs). Therefore, secondary traits are not primarily involved in the production of offspring. Not only do they not appear to promote the survival of individuals but sometimes they appear to be detrimental to the animal which possesses them; for example, colourful ornaments (such as the notorious peacock tail) can increase animal visibility and predation probability and, consequently, reduce the chances of survival.

Since secondary sexual traits do not confer advantages or produce disadvantages, their evolutionary permanence is in apparent contrast with the classic natural selection theory proposed by Darwin in the Origin of Species (1859). Why have secondary sexual traits been selected, then? To explain this paradox, Darwin (1871) developed the theory of selection in relation to sex (sexual selection) which pivots around the fact that secondary sexual traits confer an advantage with respect of acquiring a mate by intimidating rivals and/or by attracting mates. In this respect, the race to maximise offspring production – promoted by sexual selection – is as important as the race to maximise survival chances – promoted by natural selection. According to a convincing recent theoretical synthesis, sexual selection is part of natural selection (Clutton-Brock, 2004) intended as a process aimed at increasing an animal's chance of surviving and producing the highest number of offspring.

Type: Chapter
Information: The Missing Lemur Link
An Ancestral Step in the Evolution of Human Behaviour
, pp. 54 - 74

DOI: https://doi.org/10.1017/CBO9781139060059.006 [Opens in a new window]

Publisher: Cambridge University Press

Print publication year: 2016

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References

Alexander, R. & Noonan, K. M. (1979). Concealment of ovulation, parental care, and human social evolution. In: Chagnon, N. and Irons, W. (eds), Evolutionary Biology and Human Social Behavior: An Anthropological Perspective. North Scituate, MA: Duxbury Press, pp. 436–453.

Andersson, M. (1994). Sexual Selection. Princeton University Press, Princeton. 624 p.

Archer, J. (2004). Sex differences in aggression in real-world settings: a meta-analytic review. Review of General Psychology, 4, 291–322.Google Scholar

Baer, D. & McEachron, D. L. (1982). A review of selected sociobiological principles: application to hominid evolution: I. The development of group social structure. Journal of Social and Biological Structures, 5, 69–90Google Scholar

Benshoof, L. & Thornhill, R. (1979). The evolution of monogamy and concealed ovulation in humans. Journal of Social and Biological Structures, 2, 95–106.Google Scholar

Berry, J. F. & Shine, R. (1980). Sexual size dimorphism and sexual selection in turtles (order Testudines). Oecologia (Berlin), 44, 185–191.Google Scholar

Brockman, D. K. (1999). Reproductive behavior of female Propithecus verreauxi at Beza Mahafaly, Madagascar. International Journal of Primatology, 20, 375–398.Google Scholar

Burley, N. (1981). Mate choice by multiple criteria in a monogamous species. American Naturalist, 117, 515–528.Google Scholar

Clutton-Brock, T. (2004). What is sexual selection? In: Kappeler, P. and Schaik, C. van (eds), Sexual Selection in Primates. pp. 24–36.

Dall'Olio, S., Norscia, I., Antonacci, D. & Palagi, E. (2012). Sexual signalling in Propithecus verreauxi: male ‘chest badge’ and female mate choice. PLoS ONE, 7(5), e37332. http://dx.doi.org/10.1371/journal.pone.0037332.Google Scholar

Darwin, C. (1859). On the Origin of Species by Means of Natural Selection. London: John Murray.

Darwin, C. (1871). The Descent of Man and Selection in Relation to Sex. London: John Murray.

Dixson, B. J. & Vasey, P. L. (2012). Beards augment perceptions of men's age, social status, and aggressiveness, but not attractiveness. Behavioral Ecology, 23, 481–490.Google Scholar

Dixson, B. J., Dixson, A. F., Bishop, P. & Parish, A. (2010). Human physique and sexual attractiveness in men and women: a New Zealand–U.S. comparative study. Archives of Sexual Behaviour, 39, 798–806.Google Scholar

Ellis, L., Hershberger, S., Field, E., et al. (2008). Sex Differences: Summarizing More than a Century of Scientific Research. New York: Taylor and Francis.

Feinberg, D. R., Jones, B. C., Law Smith, M. J., et al. (2006). Menstrual cycle, trait estrogen level, and masculinity preferences in the human voice. Hormones and Behavior, 49, 215–222.Google Scholar

Fisher, H. S., Swaisgood, R. R. & Fitch-Snyder, H. (2003). Countermarking by male pygmy lorises (Nycticebus pygmaeus): do females use odour cues to select mates with high competitive ability?Behavioral Ecology and Sociobiology, 53, 123–130.Google Scholar

Fleagle, J. G. (2013). Primate Adaptation and Evolution, 3rd ed. San Diego: Academic Press. 596 p.

Freeman, N. J., Pasternak, G. M., Rubi, T. L., Barrett, L. & Henzi, S. P. (2012). Evidence for scent marking in vervet monkeys?Primates, 53, 311–315.Google Scholar

Gangestad, S. W. & Thornhill, R. (2004). Females multiple mating and genetic benefits in humans: investigations of design. In: Kappeler, P. & Schaik, K. van (eds), Sexual Selection in Primates. pp. 90–113.

Gangestad, S. W. & Thornhill, R. (2008). Human oestrus. Proceedings of the Royal Society B: Biological Sciences, 275, 991–1000.Google Scholar

Gildersleeve, K., Haselton, M. G. & Fales, M. R. (2014). Do women's mate preferences change across the ovulatory cycle? A meta-analytic review. Psychological Bulletin, 140, 1205–1259.Google Scholar

Ghiglieri, M. P. (1989). Hominid socio-biology and hominid social evolution. In: Heltne, P. G. & Marquardt, L. A. (eds), Understanding Chimpanzees.Cambridge, MA: Harvard University Press, pp. 370–379.

González, G., Sorci, G., Smith, L. C. & de Lope, F. (2001). Testosterone and sexual signalling in male house sparrows (Passer domesticus). Behavioral Ecology and Sociobiology, 50, 557–562.Google Scholar

Goodall, J. (1968). The behavior of free-living chimpanzees in the Gombe Stream Reserve. Animal Behavior Monographs, 1, 165–311.Google Scholar

Goodall, J. (1986). The Chimpanzees of Gombe: Patterns of Behavior. Cambridge, MA: Harvard University Press.

Gordon, W. H., Andrew, R. J., Carini, L., et al. (1973). Primate communication and the gestural origin of language [and comments and reply]. Current Anthropology, 14, 5–24.Google Scholar

Guthrie, R. D. (1970). Evolution of human threat display organs. In: Dobzansky, T., Hecht, M. K. & Steers, W. C. (eds), Evolutionary Biology, New York: Appleton-Century-Crofts, pp. 257–302.

Hill, A. K., Hunt, J., Welling, L. L. M., et al. (2013). Quantifying the strength and form of sexual selection on men's traits. Evolution and Human Behavior, 34, 334–341.Google Scholar

Hrdy, S. B. (1997). Raising Darwin's consciousness: female sexuality and the prehominid origins of patriarchy. Human Nature, 8, 1–49.Google Scholar

Jablonski, N. G. & Chaplin, G. (1993). Origin of habitual terrestrial bipedalism in the ancestor of the Hominidae. Journal of Human Evolution, 24, 259–280.Google Scholar

Jolly, A. (1966). Lemur Behavior: A Madagascar Field Study. Chicago: University of Chicago Press.

Jones, B. C., Perrett, D. I., Little, A. C., et al. (2005). Menstrual cycle, pregnancy and oral contraceptive use alter attraction to apparent health in faces. Proceedings of the Royal Society B: Biological Sciences, 272, 347–354.Google Scholar

Kappeler, P. M. (1990). Social status and scent-marking behaviour in Lemur catta. Animal Behaviour, 40, 774–775.Google Scholar

Kappeler, P. M. & van Schaik, C. P. (2002). Evolution of primate social system. International Journal of Primatology, 23, 707–740.Google Scholar

Kappeler, P. M. & van Schaik, C. P. (2004). Sexual Selection in Primates. Cambridge University Press, 284 p.

Lassek, W. D. & Gaulin, S. J. C. (2009). Costs and benefits of fat-free muscle mass in men: relationship to mating success, dietary requirements, and natural immunity. Evolution and Human Behavior, 30, 322–328.Google Scholar

Lawler, R. R. (2007). Fitness and extra-group reproduction in male Verreaux's sifaka: an analysis of reproductive success from 1989–1999. American Journal of Physical Anthropology, 132, 267–277.Google Scholar

Lee, I. C., Pratto, F., & Johnson, B. T. (2011). Intergroup consensus/disagreement in support of group-based hierarchy: An examination of socio-structural and psycho-cultural factors. Psychological Bulletin, 137, 1029–1064.Google Scholar

Lerner, G. (1986). The Creation of Patriarchy. Oxford: Oxford University Press.

Leutenegger, W. & Kelly, J. T. (1977). Relationship of sexual dimorphism in canine size and body size to social, behavioral, and ecological correlates in anthropoid primates. Primates, 18, 117–136.Google Scholar

Lewis, R. J. (2002). Beyond dominance: the importance of leverage. Quarterly Review of Biology, 77, 149–164.Google Scholar

Lewis, R. J. (2005). Sex differences in scent-marking in sifaka: mating conflict or male services?American Journal of Physical Anthropology, 128, 389–398.Google Scholar

Lewis, R. J. (2009). Chest staining variation as a signal of testosterone levels in male Verreaux's sifaka. Physiology and Behavior, 96, 586–592.Google Scholar

Lewis, R. J. & Kappeler, P. M. (2005). Seasonality, body condition, and timing of reproduction in Propithecus verreauxi verreauxi in the Kirindy Forest. American Journal of Primatology, 67, 347–364.Google Scholar

Lewis, R. J. & van Schaik, C. P. (2007). Bimorphism in male Verreaux’ sifaka in the Kirindy forest of Madagascar. International Journal of Primatology, 28, 159–182.Google Scholar

Little, A. C., Jones, B. C. & Burriss, R. P. (2007). Preferences for masculinity in male bodies change across the menstrual cycle. Hormones and Behavior, 51, 633–639.Google Scholar

Lockwood, C. A., Menter, C. G., Moggi-Cecchi, J. & Keyser, A. W. (2007). Extended male growth in a fossil hominin specis. Science, 318, 1443–1446.Google Scholar

Maggioncalda, A. N., Sapolsky, R. M. & Czekala, N. M. (1999). Reproductive hormone profiles in captive male orangutans: implications for understanding developmental arrest. American Journal of Physical Anthropology, 109, 19–32.Google Scholar

Marlowe, F., Apicella, C. & Reed, D. (2005). Men's preference for women's profile waist-to-hip ratio in two societies. Evolution and Human Behavior, 26, 458–468.Google Scholar

Mertl-Millhollen, A. S. (2006). Scent marking as resource defense by female Lemur catta. American Journal of Primatology, 68, 605–621.Google Scholar

Møller, A. P. (1989). Natural and sexual selection on a plumage signal of status and on morphology in house sparrows, Passer domesticus. Journal of Evolutionary Biology, 2, 125–140Google Scholar

Møller, A. P., Soler, M. & Thornhill, R. (1995). Breast asymmetry, sexual selection, and human reproductive success. Ethology and Sociobiology, 16, 207–219.Google Scholar

Morris, M. (1967). The Naked Ape. London: Cape.

Muscarella, F. & Cunningham, M. R. (1996). The evolutionary significance and social perception of male pattern baldness and facial hair. Ethology and Sociobiology, 17, 99–117.Google Scholar

Nadler, R. D. (1995). Sexual behavior of orangutans (Pongo pygmaeus). In: Nadler, R. D., Galdikas, B. M. F, Sheeran, L. K and Rosen, N. (eds), The Neglected Ape. New York, NY: Plenum Press, pp. 2223–237.

Neave, N. & Shields, K. (2008). The effects of facial hair manipulation on female perceptions of attractiveness, masculinity, and dominance in male faces. Personality and Individual Differences, 45, 373–377.Google Scholar

Nishida, T. & Hiraiwa-Hasegawa, M. (1987). Chimpanzees and bonobos: Cooperative relationships among males. In: Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R. W. & Struhsaker, T. T. (eds), Primate Societies. Chicago: University of Chicago Press, pp. 165–177.

Nishida, T.Hiraiwa-Hasegawa, M., Hasegawa, T. & Takahata, Y. (1985). Group extinction and female transfer in wild chimpanzees in the Mahale National Park, Tanzania. Zeitschrift für Tierpsychologie, 67, 284–301.Google Scholar

Norscia, I. & Palagi, E. (2008). Berenty 2006: census of Propithecus verreauxi and possible evidence of population stress. International Journal of Primatology, 29, 1099–1115.Google Scholar

Norscia, I., Antonacci, D. & Palagi, E. (2009). Mating first, mating more: biological market fluctuation in a wild prosimian. PLoS ONE, 4(3), e4679. http://dx.doi.org/10.1371/ journal.pone.0004679.Google Scholar

Palagi, E., Telara, S. & Borgognini-Tarli, S. (2003). Sniffing behaviour in Lemur catta: seasonality, sex, and rank. International Journal of Primatology, 24, 335–350.Google Scholar

Palagi, E., Telara, S. & Borgognini-Tarli, S. (2004). Reproductive strategies in Lemur catta: the balance among sending, receiving, and countermarking scent signals. International Journal of Primatology, 25, 1019–1031Google Scholar

Penton-Voak, I. S., Perrett, D. I., Castles, D. L., et al. (1999). Menstrual cycle alters face preference. Nature, 399, 741–742.Google Scholar

Pisanski, K., Hahn, A. C., Fisher, C. I., et al. (2014). Changes in salivary estradiol predict changes in women's preferences for vocal masculinity. Hormones and Behavior, 66, 493–497.Google Scholar

Pochron, S. T. & Wright, P. C. (2003). Variability in adult group compositions of a prosimian primate. Behavioral Ecology and Sociobiology, 54, 285–293.Google Scholar

Pochron, S. T., Morelli, T. L., Terranova, P. et al. (2005). Patterns of male scent marking in Propithecus edwardsi of Ranomafana National Park, Madagascar. American Journal of Primatology, 65, 103–115.Google Scholar

Pond, C. M. & Mattacks, C. A. (1987). The anatomy of adipose tissue in captive Macaca monkeys and its implications for human biology. Folia Primatologica, 48, 164–185.Google Scholar

Porr, M. (2005). The making of the biface and the making of the individual. In: Gamble, C. S. & Porr, M. (eds), The Hominid Individual in Context: Archaeological investigations of Lower and Middle Palaeolithic landscapes, locales and artefacts. London/New York: Routledge, pp. 68–80.

Puts, D. A. (2005). Mating context and menstrual phase affect women's preferences for male voice pitch. Evolution and Human Behavior, 26, 388–397.Google Scholar

Puts, D. A. (2006). Cyclic variation in women's preferences for masculine traits: potential hormonal causes. Human Nature, 17, 114–127.Google Scholar

Puts, D. A. (2010). Beauty and the beast: Mechanisms of sexual selection in humans. Evolution and Human Behavior, 31, 157–175.Google Scholar

Puts, D. A., Hodges, C.Cárdenas, R. A. & Gaulin, S. J. C. (2007). Men's voices as dominance signals: vocal fundamental and formant frequencies influence dominance attributions among men. Evolution and Human Behavior, 28, 340–344.Google Scholar

Puts, D. A., Jones, B. C. & DeBruine, L. M. (2012). Sexual selection on human faces and voices. Journal of Sex Research, 49, 227–243.Google Scholar

Puts, D. A., Bailey, D. H., Cárdenas, R. A., et al. (2013). Women's attractiveness changes with estradiol and progesterone across the ovulatory cycle. Hormones and Behavior, 63, 13–19.Google Scholar

Richard, A. F. (1992). Aggressive competition between males, female-controlled polygyny and sexual monomorphism in a Malagasy primate, Propithecus verreauxi. Journal of Human Evolution, 22, 395–406.Google Scholar

Roney, J. R., Simmons, Z. L. & Gray, P. B. (2011). Changes in estradiol predict within-women shifts in attraction to facial cues of men's testosterone. Psychoneuroendocrinology, 36, 742–749.Google Scholar

Rosvall, K. A. (2011). Intrasexual competition in females: evidence for sexual selection?Behavioral Ecology, 22, 1131–1140.Google Scholar

Sell, A., Cosmides, L., Tooby, J., et al. (2009). Human adaptations for the visual assessment of strength and fighting ability from the body and face. Proceedings of the Royal Society B: Biological Sciences, 276, 575–584.Google Scholar

Singh, D. & Young, R. K. (1995). Body weight, waist-to-hip ratio, breasts, and hips: role in judgments of female attractiveness and desirability for relationships. Ethology and Sociobiology, 16, 483–507.Google Scholar

Sterelny, K. (2007). Social intelligence, human intelligence and niche construction. Philosophical Transactions of the Royal Society B: Biological Sciences, 362, 719–730.Google Scholar

Stirling, I. (1975). Factors affecting the evolution of social behavior in the Pinnipedia. Rapports et Procès-Verbaux des Rèunions du Conseil Permanent International pour l'Exploration de la Mer, 169, 205–212.Google Scholar

Strassman, B. I. (1981). Sexual selection, paternal care, and concealed ovulation in humans. Ethology and Sociobiology, 2, 31–40.Google Scholar

Swaddle, J. P. & Cuthill, I. C. (1994). Female zebra finches prefer males with symmetric chest plumage. Proceedings of the Royal Society B: Biological Sciences, 258, 267–271.Google Scholar

Symons, D. (1979). The Evolution of Human Sexuality. New York: Oxford University Press.

Szalay, F. S. & Costello, R. K. (1991). Evolution of permanent estrus displays in hominids. Journal of Human Evolution, 20, 439–464.Google Scholar

Utami, Atmoko, S. & van Hooff, J. A. R. A. M. (2004). Alternative male reproductive strategies: male bimaturism in orangutans. In: Kappeler, P. M. & Schaik, C. P. van (eds), Sexual Selection in Primates: New and Comparative Perspectives. Cambridge University Press, pp. 196–207.

Utami, S. S., Goossens, B, Bruford, M. W., de Ruiter, J. R. & van Hooff, J. A. R. A. M. (2002). Male bimaturism and reproductive success in Sumatran orang-utans. Behavioral Ecology, 13, 643–652.Google Scholar

van Rhijn, J. G. (1973). Behavioural dimorphism in male ruffs, Philomacus pugnax (L.). Behaviour, 47, 153–229.Google Scholar

Veiga, J. P. & Puerta, P. (1996). Nutritional constraints determine the expression of a sexual trait in the house sparrow, Passer domesticus. Proceedings of the Royal Society of London: Biological Sciences, 263, 229–234.Google Scholar

Welling, L. L., Jones, B. C., DeBruine, L. M., et al. (2007). Raised salivary testosterone in women is associated with increased attraction to masculine faces. Hormones and Behavior, 52, 156–161.Google Scholar

Wolff, S. E. & Puts, D. A. (2010). Vocal masculinity is a robust dominance signal in men. Behavioral Ecology and Sociobiology, 64, 1673–1683.Google Scholar

Wood, B. A., Li, Y. & Willoughby, C. (1991). Intraspecific variation and sexual dimorphism in cranial and dental variables among higher primates and their bearing on the hominid fossil record. Journal of Anatomy, 174, 185–205.Google Scholar

Zahavi, A. (2007). Sexual selection, signal selection and the handicap principle. In: Jamieson, B. G. M. (ed.), Reproductive Biology and Phylogeny of Birds. Enfield, New Hampshire:Science Publishers, pp. 143–160.

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