Abstract
Tamarins and marmosets (callitrichids) present an unusual opportunity for study of the determinants of primate social systems, because both the mating and infant care patterns of callitrichids are variable, even within individual populations. In this paper, I briefly describe three characteristics of callitrichid social systems that distinguish them from most other primates: extensive male parental care, helping by nonreproductive individuals, and variable mating patterns. I then discuss the evolution of these characteristics and of the frequent twinning exhibited by callitrichids. I suggest that an ancestor of modern callitrichids gave birth to a single offspring at a time, mated monogamously, and had significant paternal care. The idea that males of this ancestral form must have provided paternal care, even though only single infants were born, derives from a comparison of litter/mother weight ratios in modern primate species. Twinning perhaps then evolved because of a combination of dwarfing in the callitrichid lineage, leading to higher litter/mother weight ratios, and a high infant mortality rate, and because the extensive paternal care already present facilitated the raising of twins. I propose that the helping behavior of older offspring may have coevolved with twinning, because helpers would have increased the chances of survival of twins, and the presence of twins would have increased the benefits of helping. Finally, the high costs of raising twins and the variability of group compositions, especially the fact that some groups would not have had older offspring to serve as helpers, may have selected for facultative polyandry in saddle-back tamarins (Saguinus fuscicollis) and perhaps in other callitrichid species. Both helping and cooperative polyandry have been extensively studied in bird species, and I apply some of the conclusions of these studies to the discussion of the evolution of callitrichid social systems.
Similar content being viewed by others
References
Ashmole, P. (1963). The regulation of numbers of tropical oceanic birds.Ibis 103: 458–473.
Axelrod, R., and Hamilton, W. D. (1981). The evolution of cooperation.Science 211: 1390–1396.
Bearder, S. K. (1987). Lorises, bushbabies, and tarsiers: Diverse societies in solitary foragers. In Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R. W., and Struhsaker, T. T. (eds.),Primate Societies, Univ. of Chicago Press, Chicago, pp. 11–24.
Box, H. O. (1975). A social developmental study of young monkeys (Callithrix jacchus) within a captive family group.Primates 16: 419–435.
Brown, J. L. (1987).Helping and Communal Breeding in Birds: Ecology and Evolution, Princeton Univ. Press, Princeton.
Brown, J. L., Brown, E. R., Brown, S. D., and Dow, D. D. (1982). Helpers: Effects of experimental removal on reproductive success.Science 215: 421–422.
Brown, K., and Mack, D. S. (1978). Food sharing among captiveLeontopithecus rosalia.Folia Primatol. 29: 268–290.
Cebul, M. S., and Epple, G. (1984). Father-offspring relationships in laboratory families of saddle-back tamarins (Saguinus fuscicollis). In Taub, D. M. (ed.),Primate Paternalism, van Nostrand Reinhold, New York, pp. 1–19.
Chivers, D. J. (1974). The siamang in Malaya. InContributions to Primatology, Vol. 4, S. Karger, Basel.
Coates, A., and Poole, T. B. (1983). The behavior of the callitrichid monkey,Saguinus labiatus labiatus, in the laboratory.Int. J. Primatol. 4: 339–371.
Craig, J. L. (1980a). Pair and group breeding behaviour of a communal gallinule, the pukeko,Porphyrio p. melanotus.Anim. Behav. 28: 593–603.
Craig, J. L. (1980b). Breeding success of a communal gallinule.Behav. Ecol. Sociobiol. 6: 289–295.
Craig, J. L., and Jamieson, I. G. (1985). The relationships between presumed gamete contribution and parental investment in a communally breeding bird.Behav. Ecol. Sociobiol. 17: 207–211.
Curry, R. L. (1988). Influence of kinship on helping behavior in Galapagos mockingbirds.Behav. Ecol. Sociobiol. 22: 141–152.
Davies, N. B. (1983). Polyandry, cloaca pecking, and sperm competition in dunnocks.Nature, Lond., 302: 334–336.
Davies, N. B. (1985). Cooperation and conflict among dunnocks,Prunella modularis, in a variable mating system.Anim. Behav. 33: 628–648.
Davies, N. B. (1986). Reproductive success of dunnocks,Prunella modularis, in a variable mating system. I. Factors influencing provisioning rate, nestling weight and fledging success.J. Anim. Ecol. 55: 123–138.
Davies, N. B., and Lundberg, A. (1984). Food distribution and a variable mating system in the dunnock,Prunella modularis.J. Anim. Ecol. 53: 895–912.
Dawson, G. A. (1978). Composition and stability of social groups of the tamarin,Saguinus oedipus geoffroyi, in Panama: Ecological and behavioral implications. In Kleiman, D. G. (ed.),The Biology and Conservation of the Callitrichidae, Smithsonian Institution Press, Washington, D.C., pp. 23–37.
Dietz, J. M., and Kleiman, D. G. (1986). Reproductive parameters in groups of free-living golden lion tamarins.Primate Report 14: 77.
Dunbar, R. I. M. (1984).Reproductive decisions: An Economic Analysis of Gelada Baboon Social Strategies, Princeton Univ. Press, Princeton.
Eisenberg, J. F., Muckenhirn, N. A., and Rudran, R. (1972). The relation between ecology and social structure in primates.Science 176: 863–874.
Emlen, S. T. (1978). The evolution of cooperative breeding in birds. In Krebs. J. R., and Davies, N. B. (eds.),Behavioural Ecology: An Evolutionary Approach, Sinauer Associates, Sunderland, Massachusetts, pp. 245–281.
Emlen, S. T. (1981). Altruism, kinship, and reciprocity in the white-fronted bee-eater. In Alexander, R. D., and Tinkle, D. W. (eds.),Natural Selection and Social Behavior: Recent Research and New Theory, Chiron Press, New York, pp. 217–230.
Emlen, S. T. (1982). The evolution of helping. I. An ecological constraints model.Am. Nat. 119: 29–39.
Emlen, S. T. (1984). Cooperative breeding in birds and mammals. In Krebs, J. R., and Davies, N. B. (eds.),Behavioural Ecology, Sinauer Associates, Sunderland, Massachusetts, pp. 305–339.
Epple, G. (1972). Social behavior of laboratory groups ofS. fuscicollis. In Bridgewater, P. D. (ed.),Saving the Lion Marmoset, Proceedings of the WAPT Golden Lion Marmoset Conference, WAPT, Oglebay Park, Wheeling, West Virginia, pp. 50–58.
Epple, G. (1975). Parental behavior inSaguinus fuscicollis spp. (Calltrichidae).Folia Primatol. 24: 221–238.
Epple, G. (1978). Reproductive and social behavior of marmosets with special reference to captive breeding.Prim. Med. 10: 50–62.
Faaborg, J. (1986). Reproductive success and survivorship of the Galapagos hawkButeo galapagoensis: Potential costs and benefits of cooperative polyandry.Ibis 128: 337–347.
Faaborg, J., and Patterson, C. B. (1981). The characteristics and occurrence of cooperative polyandry.Ibis 123: 477–484.
Faaborg, J., de Vries, T. J., Patterson, C. B., and Griffin, C. R. (1980). Preliminary observations on the occurrence and evolution of polyandry in the Galapagos hawk (Buteo galapagoensis).Auk 97: 581–590.
Ford, S. M. (1980). Callitrichids as phyletic dwarfs, and the place of Callitrichidae in Platyrrhini.Primates 21: 31–43.
Fossey, D. (1983).Gorillas in the Mist, Houghton Mifflin Company, Boston.
Garber, P. A. (1986). Social organization and patterns of infant transport inSaguinus mystax in Amazonian Peru.Primate Report 14: 78.
Garber, P. A., Moya, L., and Malaga, C. (1984). A preliminary field study of the moustached tamarin monkey (Saguinus mystax) in northeastern Peru: Questions concerned with the evolution of a communal breeding system.Folia Primatol. 42: 17–32.
Garnett, S. T. (1978). The behaviour patterns of the dusky moorhen,Gallinula tenebrosa Gould (Aves: Rallidae).Aust. Wildl. Res. 5: 363–384.
Garnett, S. T. (1980). The social organization of the dusky moorhen,Gallinula tenebrosa Gould (Aves: Rallidae).Aust. Wildl. Res. 7: 103–112.
Gartlan, S. (1969). Sexual and maternal behavior of the vervet monkey (Cercopithecus aethiops).J. Reprod. Fertil. (Suppl.) 6: 137–150.
Gaston, A. J. (1978). The evolution of group territorial behavior and cooperative breeding.Am. Nat. 112: 1091–1100.
Gengozian, N., Batson, J. S., and Smith, T. A. (1978). Breeding of marmosets in a colony environment.Prim. Med. 10: 71–78.
Goldizen, A. W. (1987a). Tamarins and marmosets: Communal care of offspring. In Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R. W., and Struhsaker, T. T. (eds.),Primate Societies, University of Chicago Press, Chicago, pp. 34–43.
Goldizen, A. W. (1987b). Facultative polyandry and the role of infant-carrying in wild saddleback tamarins (Saguinus fuscicollis).Behav. Ecol. Sociobiol. 20: 99–109.
Goldizen, A. W. (1988). Tamarin and marmoset mating systems: Unusual flexibility.Trends Ecol. Evol. 3: 36–40.
Goldizen, A. W. (1989). Social relationships in a cooperatively polyandrous group of tamarins (Saguinus fuscicollis).Behav. Ecol. Sociobiol. 24: 79–89.
Goldizen, A. W., and Terborgh, J. (1986). Cooperative polyandry and helping behavior in saddleback tamarins (Saguinus fuscicollis). In Else, J. G., and Lee, P. (eds.),Primate Ecology and Conservation, Proc. of the 10th Congress of the International Primatological Society, Vol. 2, Cambridge Univ. Press, Cambridge, pp. 191–198.
Goldizen, A. W., and Terborgh, J. (1989). Demography and dispersal patterns of a tamarin population: Possible causes of delayed breeding.Am. Nat. 134: 208–224.
Goldizen, A. W., Terborgh, J., Cornejo, F., Porras, D. T., and Evans, R. (1988). Seasonal food shortage, weight loss, and the timing of births in saddle-back tamarins (Saguinus fuscicollis).J. Anim. Ecol. 57: 893–901.
Goldstein, M. C. (1971). Stratification, polyandry, and family structure in Central Tibet.Southwest J. Anthropol. 27: 64–74.
Goss, C. M., Popejoy, L. T., II, Fusiler, J. L., and Smith, T. M. (1968). Observations on the relationships between embryological development, time of conception, and gestation. In Rosenblum, and Cooper (eds.),The Squirrel Monkey, Academic Press, New York, pp. 171–191.
Hamilton, W. D. (1964). The genetical evolution of social behavior. I, II..J. Theor. Biol. 7: 1–52.
Heinsohn, R. G., Cockburn, A., and Cunningham, R. B. (1988). Foraging, delayed maturation, and advantages of cooperative breeding in white-winged choughs,Corcorax melanorhamphos.Ethology 77: 177–186.
Hershkovitz, P. (1977).Living New World Monkeys (Platyrrhini), Vol. 1, University of Chicago Press, Chicago.
Hoage, R. J. (1978). Parental care inLeontopithecus rosalia rosalia: Sex and age differences in carrying behavior and the role of prior experience. In Kleiman, D. G. (ed.),The Biology and Conservation of the Callitrichidae, Smithsonian Institution Press, Washington, D.C., pp. 293–305.
Hubrecht, R. C. (1984). Field observations on group size and composition of the common marmoset (Callithrix jacchus jacchus), at Tapacura, Brazil.Primates 25: 13–21.
Hubrecht, R. C. (1985). Home-range size and use and territorial behavior in the common marmoset,Callithrix jacchus jacchus, at the Tapacura Field Station, Recife, Brazil.Int. J. Phimatol. 6: 533–550.
Ingram, J. C. (1977). Interactions between parents and infants, and the development of independence in the common marmoset (Callithrix jacchus).Anim. Behav. 25: 811–827.
Izawa, K. (1978). A field study of the ecology and behavior of the black-mantle tamarin (Saguinus nigricollis).Primates 19: 241–274.
Jamieson, I. G., and Craig, J. L. (1987). Dominance and mating in a communal polygynandrous bird: Cooperation or indifference towards mating competitors?Ethology 75: 317–327.
Kirkwood, J. K., and Underwood, S. J. (1984). Energy requirements of captive cotton-top tamarins (Saguinus oedipus oedipus).Folia Primatol. 42: 180–187.
Kleiman, D. G. (1977). Monogamy in mammals.Q. Rev. Biol. 52: 39–69.
Koenig, W. D., and Mumme, R. L. (1987).Population Ecology of the Cooperatively Breeding Acorn Woodpecker, Princeton Univ. Press. Princeton.
Koenig, W. E., Mumme, R. L., and Pitelka, F. A. (1983). Female roles in cooperatively breeding acorn woodpeckers. In Wasser, S. K. (ed.),Social Behavior of Female Vertebrates, Academic Press, New York, pp. 235–261.
Lancaster, J. B. (1971). Play mothering: The relationships between juvenile females and young infants among free-ranging vervet monkeys (Cercopithecus aethiops).Folia Primatol. 15: 161–182.
Leutenegger, W. (1973). Maternal-fetal weight relationships in primates.Folia Primatol. 20: 280–293.
Leutenegger, W. (1979). Evolution of litter size in primates.Am. Nat. 114: 525–531.
Leutenegger, W. (1980). Monogamy in callitrichids: A consequence of phyletic dwarfism?Int. J. Primatol. 1: 95–98.
Ligon, J. D. (1981). Demographic patterns and communal breeding in the green woodhoopoe,Phoeniculus purpureus. In Alexander, R. D., and Tinkle, D. W. (eds.),Natural Selection and Social Behavior: Recent Research and New Theory, Chiron Press, New York, pp. 231–243.
Maynard Smith, J., and Ridpath, M. G. (1972). Wife sharing in the Tasmanian native hen (Tribonyx mortierii): A case of kinship selection?.Am. Nat. 106: 447–452.
McGrew, W. C. (1988). Parental division of infant caretaking varies with family composition in cotton-top tamarins.Anim. Behav. 36: 285–310.
Neyman, P. F. (1978). Aspects of the ecology and social organization of free-ranging cottontop tamarins (Saguinus oedipus) and the conservation status of the species. In Kleiman, D. G. (ed.),The Biology and Conservation of the Callitrichidae, Smithsonian Institution Press, Washington, D.C., pp. 39–71.
Nicolson, N. A. (1987). Infants, mothers, and other females. In Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R. W., and Struhsaker, T. T. (eds.),Primates Societies, Univ. of Chicago Press, Chicago, pp. 330–342.
Nishida, T. (1983). Alloparental behavior in wild chimpanzees of the Mahale Mountains, Tanzania.Folia Primatol. 41: 1–33.
Rabenold, K. N. (1985). Cooperation in breeding by nonreproductive wrens: Kinship, reciprocity, and demography.Behav. Ecol. Sociobiol. 17: 1–17.
Reyer, H.-U. (1980). Flexible helper structure as an ecological adaptation in the pied kingfisher (Ceryle rudis rudis L.).Behav. Ecol. Sociobiol. 6: 219–227.
Richard, A. F. (1987). Malagasy prosimians: Female dominance. In Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R. W., and Struhsaker, T. T. (eds.),Primate Societies, Univ. of Chicago Press, Chicago, pp. 25–33.
Ridpath, M. G. (1972a). The Tasmanian native hen,Tribonyx mortierii. I. Patterns of behaviour.CSIRO Wildlife Res. 17: 1–51.
Ridpath, M. G. (1977b). The Tasmanian native hen,Tribonyx mortierii. II. The individual, the group, and the population.CSIRO Wildlife Res. 17: 53–90.
Riedman, J. L. (1982). The evolution of alloparental care and adoption in mammals and birds.Quart. Rev. Biol. 57: 405–435.
Rodman, P. S., and Mitani, J. C. (1987). Orangutans: Sexual dimorphism in a solitary species. In Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R. W., and Struhsaker, T. T. (eds.),Primate Societies, Univ. of Chicago Press, Chicago, pp. 146–154.
Rylands, A. B. (1985). Infant-carrying in a wild marmoset group,Callithrix humeralifer: Evidence for a polyandrous mating system.A Primatologia No Brazil 2: 131–144.
Selander, R. K. (1964). Speciation in wrens of the genusCampylorhynchus.Univ. Calif. Publ. Zool. 74: 257–273.
Skutch, A. F. (1935). Helpers at the nest.Auk 52: 257–273.
Snowdon, C. T., and Soini, P. (In press). The tamarins: GenusSaguinus. In Mittermeier, R. A., and Coimbra-Filho, A. F. (eds.),Ecology and Behavior of Neotropical Primates, Academia Brasileira de Ciencias, Rio de Janeiro.
Soini, P. (1987). Sociosexual behavior of a free-rangingCebuella pygmaea (Callitrichidae, Platyrrhini) troop during postpartum estrus of its reproductive female.Am. J. Primatol. 13: 223–230.
Stacey, P. B. (1979a). Habitat saturation and communal breeding in the acorn woodpecker.Anim. Behav. 27: 1153–1166.
Stacey, P. B. (1979b). Kinship, promiscuity and communal breeding in the acorn woodpecker.Behav. Ecol. Sociobiol. 6: 53–66.
Sussman, R. W., and Kinzey, W. G. (1984). The ecological role of the Callitrichidae.Am. J. Phys. Anthrop. 64: 419–449.
Symington, M. M. (1987). Sex ratio and maternal rank in wild spider monkeys: When daughters disperse.Behav. Ecol. Sociobiol. 20: 421–425.
Tardif, S. D., Carson, R. L., and Gangaware, B. L. (1986). Comparison of infant care in family groups of the common marmoset (Callithrix jacchus) and the cotton-top tamarin (Saguinus oedipus).Am. J. Primatol. 11: 103–110.
Tardif, S. D., Richter, C. B., and Carson, R. L. (1984). Effects of sibling-rearing experience on future reproductive success in two species of Callitrichidae.Am. J. Primatol. 6: 377–380.
Terborgh, J., and Goldizen, A. W. (1985). On the mating system of the cooperatively breeding saddle-back tamarin (Saguinus fuscicollis).Behav. Ecol. Sociobiol. 16: 293–299.
Trivers, R. L. (1971). The evolution of reciprocal altruism.Q. Rev. Biol. 46: 35–57.
Vogt, J. L., Carlson, H., and Menzel, E. (1978). Social behavior of a marmoset (Saguinus fuscicollis) group. I: Parental care and infant development.Primates 19: 715–726.
Wolfe, L. G., Deinhardt, F., Ogden, J. D., Adams, J. R., and Fisher, L. E. (1975). Reproduction of wild-caught and laboratory-born marmoset species used in biomedical research (Saguinus sp.,Callithrix jacchus).Lab. Anim. Sci. 25: 802–813.
Woolfenden, G. E., and Fitzpatrick, J. W. (1978). The inheritance of territory in group-breeding birds.Bioscience 28: 104–108.
Woolfenden, G. E., and Fitzpatrick, J. W. (1984).The Florida Scrub Jay: Demography of a Cooperative-Breeding Bird, Princeton Univ. Press, Princeton.
Wright, P. C. (1984). Biparental care inAotus trivirgatus andCallicebus moloch. In Small, M. F. (ed.),Female Primates: Studies by Women Primatologists, Alan R. Liss, New York, pp. 59–75.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Goldizen, A.W. A comparative perspective on the evolution of tamarin and marmoset social systems. International Journal of Primatology 11, 63–83 (1990). https://doi.org/10.1007/BF02193696
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02193696