Paternity and relatedness in a polyandrous nonhuman primate: Testing adaptive hypotheses of male reproductive cooperation

Animal Behaviour

Volumn 82, Issue 3, 2011, Pages

  Díaz Muñoz, Samuel L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Alloparental care; Cooperation; Cooperative breeding; Cooperative polyandry; Geoffroy's tamarin; Male parental care; Paternity; Saguinus geoffroyi

Indexed keywords

ADAPTIVE RADIATION; ADULT; COMPETITION (ECOLOGY); DEMOGRAPHY; FITNESS; GENETIC ANALYSIS; LITTER; PARENT-OFFSPRING INTERACTION; PARENTAL CARE; PATERNITY; POLYANDRY; PRIMATE; REPRODUCTIVE BEHAVIOR; REPRODUCTIVE STRATEGY;

CALLITRICHIDAE; PRIMATES; SAGUINUS; SAGUINUS GEOFFROYI; SAGUINUS IMPERATOR;

EID: 80051663601     PISSN: 00033472     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anbehav.2011.06.013     Document Type: Article

References (77)

1. Altmann J. Observational study of behavior: sampling methods. Behaviour 1974, 49:227-266.
2. Arruda M.F., Araujo A., Sousa M.B.C., Albuquerque F.S., Albuquerque A.C.S.R., Yamamoto M.E. Two breeding females within free-living groups may not always indicate polygyny: alternative subordinate female strategies in common marmosets (Callithrix jacchus). Folia Primatologica 2005, 76:10-20.
3. ASAB/ABS Guidelines for the treatment of animals in behavioural research and teaching. Animal Behaviour 2006, 71:245-253.
4. Baker A.J., Dietz J.M., Kleiman D.G. Behavioural evidence for monopolization of paternity in multi-male groups of golden lion tamarins. Animal Behaviour 1993, 46:1091-1103.
5. Bateman A. Intra-sexual selection in Drosophila. Heredity 1948, 2:349-368.
6. Benirschke K., Brownhill L.E. Heterosexual cells in testes of chimeric marmoset monkeys. Cytogenetics 1963, 2:231-240.
7. Benirschke K., Anderson J., Brownhill L. Marrow chimerism in marmosets. Science 1962, 138:513-515.
8. Bezerra B.M., Da Silva Souto A., Schiel N. Infanticide and cannibalism in a free-ranging plurally breeding group of common marmosets (Callithrix jacchus). American Journal of Primatology 2007, 69:945-952.
9. Bohle U.R., Zischler H. Polymorphic microsatellite loci for the mustached tamarin (Saguinus mystax) and their cross-species amplification in other New World monkeys. Molecular Ecology Notes 2002, 2:1-3.
10. Canestrari D., Marcos J.M., Baglione V. Effect of parentage and relatedness on the individual contribution to cooperative chick care in carrion crows Corvus corone corone. Behavioral Ecology and Sociobiology 2005, 57:422-428.
11. Chao L. Evolution of polyandry in a communal breeding system. Behavioral Ecology 1997, 8:668-674.
12. Chen D., Tseng C., Tsai S., Wu T., Chang P., Sun C. Systematic analysis of stutters to enhance the accuracy of chimerism testing. Annals of Clinical and Laboratory Science 2008, 38:264-272.
13. Clutton-Brock T.H. Breeding together, kin selection and mutualism in cooperative vertebrates. Science 2002, 296:69-72.
14. Connor R., Smolker R., Richards A. Two levels of alliance formation among male bottlenose dolphins (Tursiops sp.). Proceedings of the National Academy of Sciences, U.S.A 1992, 89:987-990.
15. Crook J.H., Crook S.J. Tibetan polyandry: problems of adaptation and fitness. Human Reproductive Behavior 1988, 97-114. Cambridge University Press, Cambridge. L. Betzig, M.B. Mulder, P. Turke (Eds.).
16. Dawson, G. 1976. Behavioral ecology of the Panamanian tamarin Saguinus oedipus (Callitrichidae, Primates). Ph.D. thesis, Michigan State University.
17. Dawson G. Composition and stability of social groups of the tamarin, Saguinus oedipus geoffroyi, in Panama. The Biology and Conservation of the Callitrichidae 1978, 23-38. Smithsonian Institution Press, Washington, D.C. D.G. Kleiman (Ed.).
18. Dawson G. The use of time and space by the Panamanian tamarin, Saguinus oedipus. Folia Primatologica 1979, 31:253-284.
19. Dietz J.M., Baker A.J. Polygyny and female reproductive success in golden lion tamarins (Leontopithecus rosalia). Animal Behaviour 1993, 46:1067-1078.
20. Dickinson J.L. A test of the importance of direct and indirect fitness benefits for helping decisions in western bluebirds. Behavioral Ecology 2004, 15:233-238.
21. Digby L.J. Sexual behavior and extragroup copulations in a wild population of common marmosets (Callithrix jacchus). Folia Primatologica 1999, 70:136-145.
22. Digby L.J., Saltzman W. Is infanticide by females more common in the common marmoset (Callithrix jacchus)? Implications for how callitrichines balance cooperation and competition. American Journal of Physical Anthropology, Supplement 2005, 126. 95.
23. DuVal E.H. Adaptive advantages of cooperative courtship for subordinate male lance-tailed manakins. American Naturalist 2007, 169:423-432.
24. Epple G. The behavior of the marmoset monkeys (Callitrichidae). Primate Behavior 1975, Vol. 4:195-239. Academic Press, New York. L.A. Rosenblum (Ed.).
25. Escobar-Paramo P. Microsatellite primers for the wild brown capuchin monkey Cebus apella. Molecular Ecology 2000, 9:107-108.
26. Faaborg J., Parker P., Delay L., Devries T., Bednarz J., Paz S., Naranjo J., Waite T. Confirmation of cooperative polyandry in the Galapagos hawk (Buteo galapagoensis). Behavioral Ecology and Sociobiology 1995, 36:83-90.
27. Faulkes C.G., Arruda M.F., Monteiro da Cruz M.A.O. Genetic structure within and among populations of the common marmoset, Callithrix jacchus: implications for cooperative breeding. The Smallest Anthropoids: the Marmoset/Callimico Radiation 2009, 103-117. Springer, New York. S.M. Ford, L.M. Porter, L.C. Davis (Eds.).
28. Ford C.E., Evans E.P. Cytogenetic observations on XX/XY chimaeras and a reassessment of the evidence for germ cell chimaerism in heterosexual twin cattle and marmosets. Journal of Reproduction and Fertility 1977, 49:25-33.
29. Gannon W., Sikes R. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. Journal of Mammalogy 2007, 88:809-823.
30. Garber P.A. Proposed nutritional importance of plant exudates in the diet of the Panamanian tamarin, Saguinus oedipus geoffroyi. International Journal of Primatology 1984, 5:1-15.
31. Garber P.A. Phylogenetic approach to the study of tamarin and marmoset social systems. American Journal of Primatology 1994, 34:199-219.
32. Garber P.A., Encarnacion F., Moya L., Pruetz J.D. Demographic and reproductive patterns in moustached tamarin monkeys (Saguinus mystax): implications for reconstructing platyrrhine mating systems. American Journal of Primatology 1993, 29:235-254.
33. Garber P.A., Encarnacion F., Moya L., Pruetz J.D., Ique C. Social and seasonal influences on reproductive biology in male moustached tamarins (Saguinus mystax). American Journal of Primatology 1996, 38:29-46.
34. Gengozian N., Brewen J.G., Preston R.J., Batson J.S. Presumptive evidence for the absence of functional germ cell chimaerism in the marmoset. Journal of Medical Primatology 1980, 9:9-27.
35. Goldizen A.W. Facultative polyandry and the role of infant-carrying in wild saddle-back tamarins (Saguinus fuscicollis). Behavioral Ecology and Sociobiology 1987, 20:99-109.
36. Goldizen A.W. Social relationships in a cooperatively polyandrous group of tamarins (Saguinus fuscicollis). Behavioral Ecology and Sociobiology 1989, 24:79-89.
37. Goldizen A.W. Tamarin and marmoset mating systems: unusual flexibility. Trends in Ecology & Evolution 1998, 3:36-40.
38. Goldizen A.W., Mendelson J., VanVlaardingen M., Terborgh J. Saddle-back tamarin (Saguinus fuscicollis) reproductive strategies: evidence from a thirteen-year study of a marked population. American Journal of Primatology 1996, 38:57-83.
39. Goldizen A., Buchan J.C., Putland D.A., Goldizen A.R., Krebs E.A. Patterns of mate-sharing in a population of Tasmanian native hens Gallinula mortierii. Ibis 2000, 142:40-47.
40. Hamilton W.D. The genetical evolution of social behaviour II. Journal of Theoretical Biology 1964, 7:17-52.
41. Hampton S.H. Germ cell chimerism in male marmosets. American Journal of Physical Anthropology 1973, 38:265-268.
42. Harcourt A., Purvis A., Liles L. Sperm competition: mating system, not breeding season, affects testes size of primates. Functional Ecology 1995, 9:468-476.
43. Haydock J., Koenig W.D. Reproductive skew in the polygynandrous acorn woodpecker. Proceedings of the National Academy of Sciences, U.S.A 2002, 99:7178-7183.
44. Heinsohn R., Ebert D., Legge S., Peakall R. Genetic evidence for cooperative polyandry in reverse dichromatic Eclectus parrots. Animal Behaviour 2007, 74:1047-1054.
45. Huck M., Löttker P., Heymann E.W. The many faces of helping: possible costs and benefits of infant carrying and food transfer in wild moustached tamarins (Saguinus mystax). Behaviour 2004, 141:915-934.
46. Huck M., Löttker P., Böhle U., Heymann E.W. Paternity and kinship patterns in polyandrous moustached tamarins (Saguinus mystax). American Journal of Physical Anthropology 2005, 127:449-464.
47. Huck M., Löttker P., Heymann E.W. Characterization and social correlates of fecal testosterone and cortisol excretion in wild male Saguinus mystax. International Journal of Primatology 2005, 26:159-179.
48. Hrdy S.B. Mothers and Others: the Evolutionary Origins of Mutual Understanding 2009, Belknap Press, Cambridge, Massachusetts.
49. Kalinowski S.T., Wagner A.P., Taper M.L. ML-Relate: a computer program for maximum likelihood estimation of relatedness and relationship. Molecular Ecology Notes 2006, 6:576-579.
50. Kalinowski S.T., Taper M.L., Marshall T.C. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molecular Ecology 2007, 16:1099-1106.
51. Kleiman D.G. Monogamy in mammals. Quarterly Review of Biology 1977, 52:39-69.
52. Kleiman D.G. The development of pair preferences in the lion tamarins (Leontopithecus rosalia): male competition or female choice?. Biology and Behavior of Marmosets Proceedings of the Marmoset Workshop, Gottingen, W-Germany, September 2-5, 1977 (German Edition) 1978, 203-207. H. Rothe, Gottingen. H. Rothe, H.J. Wolters, J. Hearn (Eds.).
53. Kohda M., Heg D., Makino Y., Takeyama T., Shibata J., Watanabe K., Munehara H., Hori M., Awata S. Living on the wedge, female control of paternity in a cooperatively polyandrous cichlid. Proceedings of the Royal Society B 2009, 276:4207-4214.
54. Krakauer A.H. Kin selection and cooperative courtship in wild turkeys. Nature 2005, 434:69-72.
55. Levine N.E., Silk J.B. Why polyandry fails: sources of instability in polyandrous marriages. Current Anthropology 1997, 38:375-398.
56. Neyman P. Aspects of ecology and social organization of free ranging cotton-top tamarins (Saguinus oedipus) and the conservation status of the species. The Biology and Conservation of the Callitrichidae 1978, 39-72. Smithsonian Institution Press, Washington, D.C. D.G. Kleiman (Ed.).
57. Nievergelt C.M., Digby L.J., Ramkrishnan U., Woodruff D.S. Genetic analysis of group composition and breeding system in a wild common marmoset (Callithrix jacchus) population. International Journal of Primatology 2000, 21:1-20.
58. Ohno S., Gropp A. Embryological basis for germ cell chimerism in mammals. Cytogenetics 1965, 4:251-261.
59. Orians G.H. On the evolution of mating systems in birds and mammals. American Naturalist 1969, 103:589-604.
60. Packer C., Gilbert D., Pusey A., O'Brien S. A molecular genetic analysis of kinship and cooperation in African lions. Nature 1991, 351:562-565.
61. Porter L.M., Garber P.A. Social behavior of callimicos: mating strategies and infant care. The Smallest Anthropoids: the Marmoset/Callimico Radiation 2009, 119-133. Springer, New York. S.M. Ford, L.M. Porter, L.C. Davis (Eds.).
62. Price E., McGrew W. Departures from monogamy in colonies of captive cotton-top tamarins. Folia Primatologica 1991, 57:16-27.
63. Queller D.C., Goodnight K.F. Estimating relatedness using genetic-markers. Evolution 1989, 43:258-275.
64. R Development Core Team R: a Language and Environment for Statistical Computing 2009, R Foundation for Statistical Computing, Vienna, http://www.R-project.org.
65. Ross C.N., French J.A., Ortić G. Germ-line chimerism and paternal care in marmosets (Callithrix kuhlii). Proceedings of the National Academy of Sciences, U.S.A 2007, 104:6278-6282.
66. Rothe H., Koenig A. Sex ratio in newborn common marmosets (Callithrix jacchus): no indication for a functional germ cell chimerism. Zeitschrift für Säugetierkunde 1991, 56:318-320.
67. Rousset F. GENEPOP'007: a complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources 2008, 8:103-106.
68. Rylands A.B., Groves C.P., Mittermeier R.A., Cortés-Ortiz l, Hines J.H.H. Taxonomy and distributions of mesoamerican primates. New Perspectives in the Study of Mesoamerican Primates: Distribution, Ecology, Behavior, and Conservation 2005, 29-79. Springer, New York. P.A. Garber, A. Estrada, M.S.M. Pavelka (Eds.).
69. Schaffner C.M., French J.A. Behavioral and endocrine responses in male marmosets to the establishment of multimale breeding groups: evidence for non-monopolizing facultative polyandry. International Journal of Primatology 2004, 25:709-732.
70. Signer E.N., Anzenberger G., Jeffreys A.J. Chimaeric and constitutive DNA fingerprints in the common marmoset (Callithrix jacchus). Primates 2000, 41:49-61.
71. Smith E. Is Tibetan polyandry adaptive?. Human Nature 1998, 9:225-261.
72. Suarez, S. S. 2007. Paternity, relatedness and socio-reproductive behavior in a population of wild red-bellied tamarins (Saguinus labiatus). Ph.D. thesis, New York University.
73. Sussman R.W., Garber P.A. A new interpretation of the social organization and mating system of the Callitrichidae. International Journal of Primatology 1987, 8:73-92.
74. Terborgh J., Goldizen A. On the mating system of the cooperatively breeding saddle-backed tamarin (Saguinus fuscicollis). Behavioral Ecology and Sociobiology 1985, 16:293-299.
75. Thyagarajan B., Young S., Floodman S., Peterson R., Wang X. Systematic analysis of interference due to stutter in estimating chimerism following hematopoietic cell transplantation. Journal of Clinical Laboratory Analysis 2009, 23:308-313.
76. Windfelder T.L. Observations on the birth and subsequent care of twin offspring by a lone pair of wild emperor tamarins (Saguinus imperator). American Journal of Primatology 2000, 52:107-113.
77. Yamamoto M.E., Arruda M.F., Alencar A.I., Cordeiro de Sousa M.B., Araújo A. Mating systems and female-female competition in the common marmoset, Callithrix jacchus. The Smallest Anthropoids: the Marmoset/Callimico Radiation 2009, 119-133. Springer, New York. S.M. Ford, L.M. Porter, L.C. Davis (Eds.).