Abstract
The simplistic view of nocturnal prosimians as “solitary” primates leading impoverished social lives is now known to be incorrect. Although many prosimians are relatively nongregarious, they occupy varied and complex social networks which are maintained by means of olfactory and vocal signals, as well as by direct encounters during nocturnal activities (Charles-Dominique, 1977; Schilling, 1979; Bearder, 1986). Bearder has defined five types of social organization among the nocturnal primates, all of which involve varying degrees of home range overlap and range size differentials between the sexes (Figure 1). Mating systems may differ from social systems, however, as has been amply demonstrated by fieldwork on diurnal anthropoid species. Examples include the existence of monogamy and polyandry in some callitrichids (Sussman and Garber, 1987; Goldizen, 1987), and multi-male influxes into one male units in Erythrocebus patas and in various Cercopithecus species (Cords, 1986; 1988). Since, in some nocturnal prosimians, the home ranges of a number of females may overlap that of a single male (e.g., in Perodicticus potto: Type 2 system in Figure 1), it is tempting to speculate that the male may monopolize sexual access to these females, producing something akin to a polygynous “one-male group”. However, this review will present evidence that sperm competition (Parker, 1970) and sexual selection by female choice (Eberhard, 1985) have influenced the evolution of the genitalia and copulatory behavior in males of many nocturnal prosimian species. It will be argued that many of these animals have “dispersed” mating systems in which females are able to mate with a number of males during the peri-ovulatory phase of the ovarian cycle.
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References
Allen, M. L. and Lemmon, W. B., 1981, Orgasm in female primates. Am. J. Primatol. 1: 15–34.
Andrew, R. J. and Klopman, R. B., 1976, Urine-washing: comparative notes, in: R. D. Martin, G. A. Doyle and A. C. Walker, eds., Prosimian Behaviour, Duckworth, London.
Bancroft, J. H., 1989, Human Sexuality and its problems. (2nd Ed.) Churchill Livingstone, Edinburgh.
Barrett, E. B. M., 1985, The ecology of some nocturnal arboreal mammals in the rainforest of peninsula Malaysia. Ph.D. Thesis, University of Cambridge.
Beach, F. A., 1976, Sexual attractivity, proceptivity and receptivity in female mammals. Horm. Behav. 7: 105–138.
Beach, F. A. and Levinson, G., 1950, Effects of androgen on the glans penis and mating behaviour of castrated rats. J. Exp. Zool. 114: 159–171.
Bearder, S. K., 1986 Lorises, bushbabies and Tarsiers: diverse societies of solitary foragers, in, Primate Societies, B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham and T. T. Struhsaker eds., Chicago University Press, Chicago.
Bearder, S. K. and Doyle, G. A., 1974, Ecology of bushbabies, Galago senegalensis and Galago crassicaudatus with some notes on their behaviour in the field, in: Prosimian Biology, R. D. Martin, G. A. Doyle and A. C. Walker, eds., Duckworth: London.
Bearder, S. K., and Doyle, G. A., 1976, Ecology of bushbabies, Galago senegalensis and Galago crassicandatus, with some notes on their behaviour in the field, in: Prosimian Behaviour, R. D. Martin, G. A. Doyle and A. C. Walker, eds., Duckworth, London.
Blandau, R. J., 1945, On factors involved in sperm transport through the cervix uteri of the albino rat. Am. J. Anat. 73: 253–272.
Breed, W. G., 1981, Unusual anatomy of the male reproductive tract in Notomys alexis (Muridae). J. Mammal. 62: 373–375.
Charles-Dominique, P., 1972, Ecologie et vie sociale de Galago demidovii (Fischer, 1808, Prosimii). Z. Tierpsychol. Suppl. 9: 7–41.
Charles-Dominique, P., 1974, Vie sociale de Perodicticus potto (Primates, Lorisides). Etude de terrain en foret éqmatoriale de l’ouest African au Gabon. Mammalia 38: 355–379.
Charles-Dominique, P. 1977, Ecology and Behaviour of Nocturnal Primates, Duckworth, London
Charles-Dominique, P. and Hladik, C. M., 1971, Le lépilémur du sud de Madagascar: écologie, abmentation et vie sociale. Terre et Vie 25: 3–66.
Clark, A. B., 1982, Scent marks as social signals in Galago crassicaudatus. I. Sex and reproductive status as factors in signals and responses. J. Chem. Ecol. 8: 1133–1151.
Clark, A. B., 1985, Sociality in a nocturnal “solitary” prosimian: Galago crassicaudatus Int. J. Primatol. 6: 581–600.
Clark, W. Le Gros., 1959, The Antecedents of Man, Edinburgh Univ. Press, Edinburgh.
Clutton-Brock, T. H. and Harvey, P. H., 1976, Evolutionary rules and primate societies, in: Growing Points in Ethology, P. P. G. Bateson and R. A. Hinde, eds., Cambridge University Press, London.
Cords, M., 1986, Forest guenons and patas monkeys: male-male competition in one-male groups, in: Primate Societies, B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham and T. T. Struhsaker eds., University of Chicago Press, Chicago.
Cords, M., 1988, Mating systems of forest guenons: a preliminary review, in: A Primate Radiation: Evolutionary Biology of the African Guenons, A. Gautier-Hion, F. Boubiere, J. P. Gauter and J. Kingdom, eds., Cambridge University Press, Cambridge.
Darwin, C., 1871, The Descent of Man and Selection in Relation to Sex. John Murray, London.
De Ruiter, J. R. and Inoue, M., 1993, Paternity, male social rank and sexual behaviour. Primates 34: 553555.
Dewsbury, D. A., 1988, A test of the role of copulatory plugs in sperm competition in deer mice (Peromyscus maniculatus).
Dewsbury, D. A. and Hodges A. W., 1987, Copulatory behavior and related phenomena in spiny mice (Acomys cahirinus) and hopping mice (Notomys alexis), J. Mammal. 69: 49–57.
Dewsbury, D. A., and Pierce, J. D., 1989, Copulatory patterns of primates as viewed in broad mammalian perspective Am. J. Primatol. 17: 51–72.
Dixson, A. F., 1978, Effects of ovariectomy and estradiol replacement therapy upon the sexual and aggressive behavior of the greater galago (Galago crassicaudatus crassicaudatus). Horm. Behav. 10: 61–70.
Dixson, A. F., 1983, The hormonal control of sexual behaviour in primates. Oxford Rev. Repro. Biol. 5: 131–219.
Dixson, A. F., 1987a, Observations on the evolution of the genitalia and copulatory behaviour in male primates, J. Zool. Lond. 213: 423–443.
Dixson, A. F., 1987b, Baculum length and copulatory behavior in primates. Amer. J. Primatol. 13: 51–60.
Dixson, A. F., 1989, Effects of sexual selection upon the genitalia and copulatory behaviour in male galagos. Int. J. Primatol. 10: 47–55.
Dixson, A. F., 1990, The neuroendocrine control of sexual behaviour in female primates. Ann. Revs. Sex. Res. 1: 197–226.
Dixson, A. F., 1991a, Sexual selection, natural selection and copulatory patterns in male primates. Folia primatol. 57: 96–101.
Dixson, A. F., 1991b, Penile spines affect copulatory behaviour in a primate. (Callithrix jacchus). Physiol. Behav. 49: 557–562.
Dixson, A. F., Knight, J., Moore, H. D. M. and Carman, M., 1982, Observations on sexual development in male orang-utans (Pongo pygmaeus). Int. Z. Yrbk. 22: 222–227.
Dixson, A. F. and Mundy, N. 1994. Sexual behavior, sexual swelling and penile evolution in chimpanzees. (Pan troglodytes). Arch. Sex. Behavior. 23: 267–280.
Dixson, A. F. and Van Horn, R. N., 1977, Comparative studies of morphology and reproduction in two subspecies of the greater bushbaby, Galago crassicaudatus crassicaudatus and G. C. argentatus. J. Zool. Lond. 183, 517–526.
Doyle, G. A. Pelletier, A. and Bekker, T., 1967, Courtship mating and parturition in the lesser bushbaby (Galago senegalensis moholi) under semi-natural conditions. Folia Primatol. 7: 169–196.
Eaton, G. G., Slob, A. K. and Resko, J. A., 1973, Cycles of mating behaviour, oestogen and progesterone in the thick-tailed bushbaby Galago crassicaudatus crassicaudatus. under laboratory conditions. Anim. Behav. 21: 309–315.
Eberhard, W. G., 1985, Sexual Selection and Animal Genitalia, Harvard University Press, Harvard.
Eisenberg, J. F., Communication mechanisms and social integration in the black spider monkey, Ateles fusciceps robustus and related species. Smithson, Contr. Zool. 231: 1–108.
Evans, C. S. and Goy, R. W., 1968, Social behaviour and reproductive cycles in captive ring-tailed lemurs (Lemur catta). J. Zool. Lond. 156: 181–197.
Ewer, R. F., 1973, The Carnivores, Cornell Univ. Press, New York.
Foerg, R., 1982, Reproduction in Cheirogaleus medius, Folia primatol. 39: 49–62.
Galdikas, B. M. F. 1985. Adult male sociality and reproductive tactics among orang-utans at Tajung, Puting. Folia primatol. 45: 9–24.
Goldfoot, D.A., Slob, A. K., Scheffler, G., Robinson, J. A., Wiegand, S. and Cords, J., 1975, Multiple ejaculations during prolonged sexual tests and lack of resultant serum testosterone increases in male stumptail macaques (M. arctoides). Arch. Sex. Behav. 4: 547–560.
Goldizen, A. W., 1987, Facultative polyandry and the role of infant carrying in wild saddleback tamarins (Saguinus fuscicollis), Behav. Ecol. Sociobiol. 20: 99–109.
Haddow, A. J. and Ellice, J. M., 1964, Studies on bushbabies (Galago spp.) with special reference to the epidemiology of yellow fever. Trans. Soc. Trop. Med. Hyg. 58: 521–538.
Harcourt, A. H., Harvey, P. H., Larson, S. G. and Short, R. V., 1981, Testis weight, body weight and breeding system in primates, Natural Lond. 293: 55–57.
Hart, B. L., 1978, Hormones, Spinal reflexes and sexual behaviour, in: Biological Determinants of Sexual Behaviour, J. B. Hutchison, ed., John Wiley and Sons, Chichester.
Harvey, P. H. and May, R. M., 1989, Out for the sperm count. Nature Lond. 337: 508–509.
Hill, W. C. O., 1953, Primates: Comparative Anatomy and Taxonomy Vol. I, Strepsirhini, Edinburgh University Press, Edinburgh.
Hill, W. C. O., 1958, External genitalia, in: Primatologia. Handbook of Primatology, Vol. 3, H. Hofer, A. H. Schultz and D. Starck, eds., S. Karger, Basel.
Hill, W. C. O., 1972, Evolutionary Biology of the Primates, Academic Press, London.
Hooper, E. and Musser, G., 1964, The glans penis in neotropical cricetines (Muridae) with comments on classification of muroid rodents. Misc. Publ. Mus. Zool. Univ. Mich. 123: 1–57.
Ioannou, J. M., 1966, The oestrous cycle of the potto, J. Reprod. Fertil. 11: 455–457.
Izard, M. K., 1990, Social influences on the reproductive success and reproductive endocrinology of prosimian primates, in: F. Bercovitch and T. Ziegler, eds. Socioendocrinology of Primate Reproduction, Wiley-Liss, New York.
Izard, M. K. and Rasmussen, D. T., 1985, Reproduction in the slender loris (Loris tardigradus malabaricus). Am. J. Primatol. 8: 153–165.
Jolly, A., 1966, Lemur Behavior, Chicago University Press, Chicago.
Kappeler, P.M., Reproduction in the crowned lemur (Lemur coronatus) in captivity, Am. J. Primatol. 12: 497–503.
Kingsley, S., 1982, Causes of non-breeding and the development of the secondary sexual characteristics in the male orang-utan: a hormonal study, in: L. E. M. de Boer, ed., The Orang-Utan: it’s Biology and Conservation, Dr. Junk, The Hague.
Klein, L. L., 1971, Observations on copulation and seasonal reproduction in two species of spider monkeys, Ateles belzebuth and A. geoffroyi. Folia primatol. 15: 233–248.
Koyama, N., 1988, Mating behavior of ring-tailed lemurs (Lemur catta) at Berenty, Madagascar. Primates, 29: 163–175.
Lebec, A., 1984, Relation entre le comportement agressif due microcébe måle, les autres comportements et la physiologie sexuelle. Role de quelques facteurs déterminants. Thése Zéme Cycle, Universié Paris VI.
Lipschitz, D. W., 1988, Endocrine factors determining female Galago senegalensis moholi. mating behaviour, M.Sc. Thesis, University of Witwatersrand.
Mackinnon, J. R., 1974, Behaviour and ecology of wild orang-utans (Pongo pygmaeus) Anim. Behav. 22: 374.
Manley, G. H., 1966, Reproduction in lorisoid primates, Symp. Zool. Soc. Lond. 15: 493–509.
Manley, G. H., 1967, Gestation periods in the Lorisidae, Int. Z. Ybk. 1: 80–81.
Martin, R. D., 1973, A review of the behavior and ecology of the lesser mouse lemur (Microcebus murinus J. F. Miller 1777), in: Michael J and J. H. Crook, eds., Ecology and Behaviour of Primates, R. P. Academic Press, London.
Martin, R. D., Dixson, A. F. and Wickings, E. J., 1992, Paternity in Primates, Genetic Tests and Theories. Karger, Basel.
Masters, W. H. and Johnson, V. E., 1966, Human Sexual Response, Churchill, London.
Masters, J. C., Lumsden, W. H. R. and Young, D. A., 1988, Reproductive and dietary parameters in wild greater galago populations. Int. J. Primatol.
Matthews, M. K. and Adler, N. T., 1977, Facilitative and inhibitory influences of reproductive behavior on sperm transport in rats. J. comp. physiol. psychol. 91: 727–741.
Milton, K. M., 1985, Mating patterns of woolly spider monkeys, Brachyteles arachnoides: implications for female choice. Behav. Ecol. Sociobiol. 17: 53–59.
Moller, A. P., 1988, Ejaculate quality, testes size and sperm competition in primates, J. Human Evol. 17: 479–488.
Moller, A. P. 1989, Ejaculate quality, testes size and sperm production in mammals, Funct. Ecol. 3: 91–96.
Nadler, R. D., 1977, Sexual behavior of captive orang-utans. Arch. Sex. Behav. 6: 457–475.
Nash, L. T. and Harcourt, C. S., 1986, Social organization of galagos in Kenyan coastal forests: II. Galago garnettii Am. J. Primatol.10: 357–369.
Nishimura, A., 1988, Mating behavior of woolly monkeys, Lagothrix lagotricha, at La Macarena, Colombia. Field Stud. N. W. Monkeys 1: 19–27.
Pagés-Feuillade, E., 1988, Modalités de l’occupation de l’espace et relations inter-individuelles chez un prosimian malgache, Microcebus murinus. Folia Primatol. 50: 204–220.
Parker, G. A., 1970, Sperm competition and its evolutionary consequences in the insects, Biol. Rev. 45: 525–567.
Pereira, M. E., 1991, Asynchrony within estrous synchrony among ringtailed lemurs. (Primates: Lemuridae). Physiol. Behav. 49: 47–52.
Pereira, M. E., Sieligson, M. A. and Macedonia, J. M., 1988, The behavioral repertoire of the black and white ruffed lemur, Varecia variegata variegata. Folia Primatol. 51: 1–32.
Perret, M., 1986, Social influences on oestrous cycle length and plasma progesterone concentrations in the female lesser mouse lemur (Microcebus murinus). J. Reprod. Fertil. 77: 303–311.
Perret, M. 1992. Environmental and social determinants of sexual function in the male mouse lemur (Microcebus murinus). Folia Primatol. 59: 1–25.
Petter-Rousseaux, A., 1964, Reproductive Physiology and behaviour of the Lemuroidea, in: Evolutionary and Genetic Biology of Primates Vol. 2, in: J. Buettner-Janusch ed., Academic Press, New York.
Phoenix, C. H., Copenhaver, K. H. and Brenner, R. M. 1976, Scanning electron microscopy of penile papillae in intact and castrated rats. Horm. Behav. 7: 217–227.
Pfaff, D. W., 1980, Estrogens and Brain Function, Springer, New York.
Pollock, J. I., 1979, Spatial distribution and ranging behavior in lemurs, in: G. A. Doyle and R. D. Martin, eds., The Study of Prosimian Behavior, Academic Press, New York.
Ramakrishna, P. A. and Prasad, M. R. N., 1967, Changes in the male reproductive organs of Loris tardigradus lydekkerianus (Cabrera). Folia Primatol. 5: 176–189.
Richard, A., 1976, Patterns of mating behaviour in propithecus verreaxi verreauxi, in: A. Doyle and A. C. Walker eds., Prosimian Behaviour, R. D. Martin, G. Duckworth, London.
Rodriquez-Sierra, J. F., Crowley, W. R. and Komisaruk, B. R., 1975, Vaginal stimulation in rats induces prolonged lordosis responsiveness and sexual receptivity, J. Comp. Physiol. Psychol. 89: 79–85.
Roosmalen, M. G. M. Van and Klein, L. L., 1988, The spider monkeys, genus Ateles, in Ecology and Behavior of Neotropical Primates, Vol. 2, R. A. Mittermeier, A. B. Rylands, A. Coimbra-Filho and A. B. Fonseca, eds., World Wildlife Fund, Washington D. C.
Saayman, G. S., 1970, The menstrual cycle and sexual behaviour in a troop of free-ranging chacma baboons (Papio ursinus). Folia primatol. 12: 81–110.
Sachs, B. D., 1982, Role of the rat’s striated penile muscles in penile reflexes, copulation and induction of pregnancy. J. Reprod. Fertil. 66: 433–443.
Sachs, B. D. and Meisel, R. L., 1988, The physiology of male sexual behavior, in: E. Knobil and J. Neill eds., The Physiology of Reproduction, Vol. 2, Raven Press, New York.
Schilling, A. 1979, Olfactory communication in Prosimians, in: The Study of Prosimian Behavior, G. A. Doyle and R. D. Martin, eds., Academic Press, New York.
Schilling, A. and Evans, C., 1994, Vomerolfaction capacity in lemuroids, in: L. Alterman, G. A. Doyle and M. K. Izard (eds.). Creatures of the Dark: the Nocturnal Prosimians. Plenum, New York.
Schilling, A. and Perret, M., 1987, Chemical signals and reproductive capacity in a male prosimian primate (Microcebus murinus). Chem. Senses 12: 143–158.
Shideler, S. E., Lindburg, D. G. and Lasley, B. L., 1983, Estrogen-behavior correlates in the reproductive physiology and behavior of the ruffed lemur (Lemur variegatus), Horm. Behav. 17: 249–263.
Shinoda, A., Kraemer, G. W. and Goy, R. W., 1991, Effects of estrogen on activity in rhesus monkeys, in: A. Ehara, T. Kimura, O. Takenaka and M. Iwamoto, eds., Primatology Today, Elsevier, Amsterdam.
Short, R. V., 1979, Sexual selection and its component parts, somatic and genital selection, as illustrated by man and the great apes. Adv. Study Behav. 9: 131–158.
Sterling, E. J., 1992, Feeding behavior of the aye-aye (Daubentonia madagascariensis) on Nosy Mangabe, Madagascar. Paper read at the XIVth Congress of the International Primatological Society, Strasbourg, August 1992.
Sussman, R. W. and Garber, P. A., 1987, A new interpretation of the social organization and the mating system of the Callitrichidae, Int. J. Primatol. 8: 73–92.
Van Horn R. and Resko, J. A., 1977, The reproductive cycle of the ring-tailed lemur (Lemur catta): sex steriod levels and sexual receptivity under controlled photosperiods. Endocrinology 101: 1579–1586.
Verrell, P. A., 1992, Primate penile morphologies and social systems: further evidence for an association. Folia primatol. 59: 114–120.
Voss, R., 1979, Male accessory glands and the evolution of copulatory plugs in rodents, Occ. Pap. Mus. Zool. Univ. Mich. 689: 1–17.
Wallach, S. J. R. and Hart, B. L., 1983, The role of the striated penile muscles of the male rat in seminal plug dislodgement and deposition. Physiol. Behav. 31: 815–821.
Wallen, K., 1982, Influence of female hormonal state upon rhesus monkey sexual behavior varies with space for social interactions. Science, 217: 375–377.
Wnite, F. J., 1991, Social organization, reeding ecology and reproductive strategy of ruffed lemurs, Varecia variegata. in: A. Ehara, T. Kimura, O. Takenaka and M. Iwamoto, eds., Primatology Today, Elsevier, Amsterdam.
Wickings, E. J. and Dixson, A. F., 1992, Testicular function, secondary sexual development and social status in male mandrills (Mandrillus sphinx). Physiol. Behav. 52: 909–916.
Wickings, E. J., Bossi, T. and Dixson, A. F., 1993, Reproductive success in the mandrill (Mandrillus sphinx); correlations of male dominance and mating success with paternity as determined by DNA fingerprinting. J. Zool. Lond. 231: 563–574
Wright, P. C., Izard, M. K. and Simons, E. L., 1986a, Reproductive cycles in Tarsius bancanus, Am. J. Primatol. 11: 207–215.
Wright, P. C., Toyama, T. M. and Simons, E. I., 1986b, Courtship and copulation in Tarsius bancanus. Folia primatol. 46: 142–148.
Young, W. C., 1961, The hormones and mating behavior, in: Sex and Internal Secretions, Vol. 2, W. C. Young, ed., Williams and Wilkins, Baltimore.
Zimmerman, E., 1988, Reproduction, physical growth and behavioral development in slow loris (Nycticebus coucang, Lorisidae). Hum. Evol. 4: 171–179.
Zimmerman, E., Zimmerman, P. and Zimmerman, A., 1979, Sociale communikation bei plumploris (Nycticebus coucang). Z. Des Kolner Zoo 22: 25–36.
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Dixson, A.F. (1995). Sexual Selection and the Evolution of Copulatory Behavior in Nocturnal Prosimians. In: Alterman, L., Doyle, G.A., Izard, M.K. (eds) Creatures of the Dark. Springer, Boston, MA. https://doi.org/10.1007/978-1-4757-2405-9_7
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