Paternal care and the evolution of exaggerated sexual swellings in primates

Behavioral Ecology

Volumn 23, Issue 4, 2012, Pages 699-706

  Alberts, Susan C ^a,b   Fitzpatrick, Courtney L ^a  

^a DUKE UNIVERSITY   (United States)

^b INSTITUTE OF PRIMATE RESEARCH   (Kenya)

Author keywords

infanticide; parental care; primates; sexual swellings

Indexed keywords

EVOLUTIONARY BIOLOGY; FEMALE; INFANTICIDE; PATERNAL CARE; PRIMATE; PROBABILITY; SEXUAL SELECTION;

PRIMATES;

EID: 84862844816     PISSN: 10452249     EISSN: 14657279     Source Type: Journal    
DOI: 10.1093/beheco/ars052     Document Type: Article

References (82)

1. Alberts SC, Buchan JC, Altmann J. 2006. Sexual selection in wild baboons: from mating opportunities to paternity success. Anim Behav. 72:1177-1196. (Pubitemid 44634363)
2. Altmann J. 1980. Baboon mothers and infants. Cambridge (MA): Harvard University Press.
3. Bales KB. 1980. Cumulative scaling of paternalistic behavior in primates. Am Nat. 116:454-461.
4. Boggess J. 1984. Infant killing and male reproductive strategies in langurs (Presbytis entellus). In: Hausfater G, Hrdy SB, editors. Infanticide: comparative and evolutionary perspectives. New York: Aldine Publishing Company. p. 283-310.
5. Borries C, Koenig A. 2000. Infanticide in hanuman langurs: social organization, male migration, and weaning age. In: van Schaik CP, Janson CH, editors. Infanticide by males and its implications. Cambridge (UK): Cambridge University Press. p. 99-122.
6. Borries C, Launhardt K, Epplen C, Epplen JT, Winkler P. 1999. Males as infant protectors in hanuman langurs (Presbytis entellus) living in multimale groups-defence pattern, paternity and sexual behaviour. Behav Ecol Sociobiol. 46:350-356. (Pubitemid 129748806)
7. Brandt EM, Irons R, Mitchell G. 1970. Paternalistic behavior in 4 species of macaques. Brain Behav Evol. 3:415-420.
8. Brauch K, Pfefferle D, Hodges K, Mohle U, Fischer J, Heistermann M. 2007. Female sexual behavior and sexual swelling size as potential cues for males to discern the female fertile phase in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar. Horm Behav. 52:375-383. (Pubitemid 47267918)
9. Brault S, Caswell H. 1993. Pod-specific demography of killer whales (Orcinus orca). Ecology. 74:1444-1454. (Pubitemid 24429732)
10. Buchan JC, Alberts SC, Silk JB, Altmann J. 2003. True paternal care in a multi-male primate society. Nature. 425:179-181. (Pubitemid 37150895)
11. Bulger JB. 1993. Dominance rank and access to estrous females in male savanna baboons. Behaviour. 127:67-103. (Pubitemid 24416857)
12. Caswell H. 2001. Matrix population models: construction, analysis and interpretation. Sunderland (MA): Sinauer Associates.
13. Charpentier MJE, Van Horn RC, Altmann J, Alberts SC. 2008. Paternal effects on offspring fitness in a multimale primate society. Proc Natl Acad Sci USA. 105:1988-1992. (Pubitemid 351439452)
14. Clarke PMR, Henzi SP, Barrett L. 2009. Sexual conflict in chacma baboons, Papio hamadryas ursinus: absent males select for proactive females. Anim Behav. 77:1217-1225.
15. Clutton-Brock TH, Harvey PH. 1976. Evolutionary rules and primate societies. In: Bateson PPG, Hinde RA, editors. Growing points in ethology. Cambridge (UK): Cambridge University Press. p. 195-237.
16. Collins DA, Busse CD, Goodall J. 1984. Infanticide in two populations of savanna baboons. In: Hausfater G, Hrdy SB, editors. Infanticide: comparative and evolutionary perspectives. New York: Aldine Publishing Company. p. 193-216.
17. Crockett CM, Janson CH. 2000. Infanticide in red howlers: female group size, male membership, and a possible link to folivory. In: van Schaik CP, Janson CH, editors. Infanticide by males and its implications. Cambridge (UK): Cambridge University Press. p. 75-98.
18. Crockett CM, Sekulic R. 1984. Infanticide in red howler monkeys (Alouatta seniculus). In: Hausfater G, Hrdy SB, editors. Infanticide: comparative and evolutionary perspectives. New York: Aldine Publishing Company. p. 173-192.
19. Dahl JF, Nadler RD, Collins DC. 1991. Monitoring the ovarian cycles of Pan troglodytes and P. paniscus-a comparative approach. Am J Primatol. 24:195-209.
20. Daspre A, Heistermann M, Hodges JK, Lee PC, Rosetta L. 2009. Signals of female reproductive quality and fertility in colony-living baboons (Papio h. anubis) in relation to ensuring paternal investment. Am J Primatol. 71:529-538.
21. Deschner T, Heistermann M, Hodges K, Boesch C. 2003. Timing and probability of ovulation in relation to sex skin swelling in wild West African chimpanzees, Pan troglodytes verus. Anim Behav. 66: 551-560. (Pubitemid 37105972)
22. Deschner T, Heistermann M, Hodges K, Boesch C. 2004. Female sexual swelling size, timing of ovulation, and male behavior in wild West African chimpanzees. Horm Behav. 46:204-215. (Pubitemid 38901040)
23. Dixson AF. 1983. Observations on the evolution and behavioral significance of sexual skin in female primates. Adv Study Behav. 13:63-106.
24. Domb LG, Pagel M. 2001. Sexual swellings advertise female quality in wild baboons. Nature. 410:204-206. (Pubitemid 32216591)
25. Drea CM. 2005. Bateman revisited: the reproductive tactics of female primates. Integr Comp Biol. 45:915-923. (Pubitemid 43098223)
26. Dunbar RIM. 1987. Demography and reproduction. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT, editors. Primate societies. Chicago (IL): University of Chicago Press. p. 240-249.
27. Emery MA, Whitten PL. 2003. Size of sexual swellings reflects ovarian function in chimpanzees (Pan troglodytes). Behav Ecol Sociobiol. 54:340-351. (Pubitemid 37144018)
28. Engelhardt A, Hodges JK, Niemitz C, Heistermann M. 2005. Female sexual behavior, but not sex skin swelling, reliably indicates the timing of the fertile phase in wild long-tailed macaques (Macaca fascicularis). Horm Behav. 47:195-204. (Pubitemid 40138833)
29. Fernandez-Duque E, Valeggia CR, Mendoza SP. 2009. The biology of paternal care inhuman and nonhuman primates. Annu Rev Anthropol. 38:115-130.
30. Fossey D. 1984. Infanticide in mountain gorillas (Gorilla gorilla beringei) with comparative notes on chimpanzees. In: Hausfater G, Hrdy SB, editors. Infanticide: comparative and evolutionary perspectives. New York: Aldine Publishing Company. p. 217-236.
31. Gesquiere LR, Wango EO, Alberts SC, Altmann J. 2007. Mechanisms of sexual selection: sexual swellings and estrogen concentrations as fertility indicators and cues for male consort decisions in wild baboons. Horm Behav. 51:114-125. (Pubitemid 44838637)
32. Hamilton WJ III. 1984. Significance of paternal investment by primates to the evolution of adult male-female associations. In: Taub DM, editor. Primate paternalism. New York: Van Nostrand Reinhold. p. 309-335.
33. Higham JP, Heistermann M, Ross C, Semple S, MacLarnon A. 2008a. The timing of ovulation with respect to sexual swelling detumescence in wild olive baboons. Primates 49:295-299.
34. Higham JP, MacLarnon AM, Ross C, Heistermann M, Semple S. 2008b. Baboon sexual swellings: information content of size and color. Horm Behav. 53:452-462.
35. Hrdy SB. 1981. The woman that never evolved. Cambridge (MA): Harvard University Press.
36. Hrdy SB, Whitten PL. 1987. Patterning of sexual activity. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT, editors. Primate societies. Chicago (IL): University of Chicago Press. p. 370-384.
37. Huchard E, Alvergne A, Fejan D, Knapp LA, Cowlishaw G, Raymond M. 2010. More than friends? Behavioural and genetic aspects of heterosexual associations in wild chacma baboons. Behav Ecol Sociobiol. 64:769-781.
38. Huchard E, Courtiol A, Benavides JA, Knapp LA, Raymond M, Cowlishaw G. 2009. Can fertility signals lead to quality signals? Insights from the evolution of primate sexual swellings. Proc R Soc B Biol Sci. 276:1889-1897.
39. Kleiman DG, Malcolm JR. 1981. The evolution of male parental investment in mammals. In: Gubernik DJ, Klopfer PH, editors. Parental care in mammals. New York: Plenum Publishing Corporation. p. 347-387.
40. Kuester J, Paul A. 1992. Influence of male competition and female mate choice on male mating success in Barbary macaques (Macaca sylvanus). Behaviour. 120:192-217.
41. Kuester J, Paul A. 1996. Female-female competition and male mate choice in Barbary macaques (Macaca sylvanus). Behaviour. 133: 763-790.
42. Le Gouar PJ, Schekkerman H, van der Jeugd HP, Boele A, van Harxen R, Fuchs P, Stroeken P, van Noordwijk AJ. 2011. Long-term trends in survival of a declining population: the case of the little owl (Athene noctua) in the Netherlands. Oecologia. 166:369-379.
43. Lehmann J, Fickenscher G, Boesch C. 2006. Kin biased investment in wild chimpanzees. Behaviour. 143:931-955. (Pubitemid 44583539)
44. Leland L, Struhsaker TT, Butynski TM. 1984. Infanticide by adult males in three primate species of Kibale Forest, Uganda: a test of hypotheses. In: Hausfater G, Hrdy SB, editors. Infanticide: comparative and evolutionary perspectives. New York: Aldine Publishing Company. p. 151-172.
45. McDonald DB. 1993. Demographic consequences of sexual selection in the long-tailed manakin. Behav Ecol. 4:297-309.
46. Ménard N, ScheffrahnW, Vallet D, Vidane C, Reber C. 1992. Application of blood protein electrophoresis and DNA fingerprinting to the analysis of paternity and social characteristics of wild Barbary macaques. In: Martin RD, Dixson AF, Wickings EJ, editors. Paternity in primates: genetic tests and theories. Basel (Switzerland): Karger. p. 155-174.
47. Mohle U, Heistermann M, Dittami J, Reinberg V, Wallner B, Hodges JK. 2005. Patterns of anogenital swelling size and their endocrine correlates during ovulatory cycles and early pregnancy in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar. Am J Primatol. 67:279. (Pubitemid 43095999)
48. Moscovice LR, Di Fiore A, Crockford C, Kitchen DM, Wittig R, Seyfarth RM, Cheney DL. 2010. Hedging their bets? Male and female chacma baboons form friendships based on likelihood of paternity. Anim Behav. 79:1007-1015.
49. Moscovice LR, Heesen M, Di Fiore A, Seyfarth RM, Cheney DL. 2009. Paternity alone does not predict long-term investment in juveniles by male baboons. Behav Ecol Sociobiol. 63:1471-1482.
50. Nguyen N, Van Horn RC, Alberts SC, Altmann J. 2009. " Friendships" between new mothers and adult males: adaptive benefits and determinants in wild baboons (Papio cynocephalus). Behav Ecol Sociobiol. 63:1331-1344.
51. van Noordwijk M. 1985. Sexual behaviour of Sumatran long-tailed macaques. Ethology. 70:277-296.
52. Nunn CL. 1999. The evolution of exaggerated sexual swellings in primates and the graded-signal hypothesis. Anim Behav. 58: 229-246. (Pubitemid 29400913)
53. Pagel M. 1994. Evolution of conspicuous advertisement in old world monkeys. Anim Behav. 47:1333-1341.
54. Palombit RA, Cheney DL, Fischer J, Johnson S, Rendall D, Seyfarth RM, Silk JB. 2000. Male infanticide and defense of infants in chacma baboons. In: van Schaik CP, Janson CH, editors. Infanticide by males and its implications. Cambridge (UK): Cambridge University Press. p. 123-152.
55. Palombit RA, Seyfarth RM, Cheney DL. 1997. The adaptive value of 'friendships' to female baboons: experimental and observational evidence. Anim Behav. 54:599-614. (Pubitemid 27413941)
56. Petrie M. 1994. Improved growth and survival of offspring of peacocks with more elaborate trains. Nature. 371:598-599. (Pubitemid 24315738)
57. Petrie M, Halliday T, Sanders C. 1991. Peahens prefer peacocks with more elaborate trains. Anim Behav. 41:323-331.
58. Petrie M, Williams A. 1993. Peahens lay more eggs for peacocks with larger trains. Proc R Soc Lond Ser B Biol Sci. 251:127-131.
59. Reichert KE, Heistermann M, Hodges JK, Boesch C, Hohmann G. 2002. What females tell males about their reproductive status: are morphological and behavioural cues reliable signals of ovulation in bonobos (Pan paniscus)? Ethology. 108:583-600. (Pubitemid 34749689)
60. Rosenbaum S, Silk JB, Stoinski TS. 2011. Male-immature relationships in multi-male groups of mountain gorillas (Gorilla beringei beringei). Am J Primatol. 73:356-365.
61. Van Schaik CP. 2000. Infanticide by male primates: the sexual selection hypothesis revisited. In: van Schaik CP, Janson CH, editors. Infanticide by males and its implications. Cambridge (UK): Cambridge University Press. p. 27-60.
62. Van Schaik CP, Paul A. 1996. Male care in primates: does it ever reflect paternity? Evol Anthropol. 5:152-156.
63. Sergio F, Tavecchia G, Blas J, Lopez L, Tanferna A, Hiraldo F. 2011. Variation in age-structured vital rates of a long-lived raptor: implications for population growth. Basic Appl Ecol. 12:107-115.
64. Setchell JM, Wickings EJ. 2004. Sexual swelling in mandrills (Mandrillus sphinx): a test of the reliable indicator hypothesis. Behav Ecol. 15:438-445. (Pubitemid 38751701)
65. Sim IMW, Rebecca GW, Ludwig SC, Grant MC, Reid JM. 2011. Characterizing demographic variation and contributions to population growth rate in a declining population. J Anim Ecol. 80: 159-170.
66. Small MF. 1990. Promiscuity in Barbary macaques (Macaca sylvanus). Am J Primatol. 20:267-282.
67. Smuts BB. 1985. Sex and friendship in baboons. Hawthorne (NY): Aldine.
68. Snowden CT, Suomi SJ. 1982. Paternal behavior in primates. In: Fitzgerald HE, Mullins JA, Gage P, editors. Child nurturance, vol 3: studies of development in nonhuman primates. New York: Plenum Press. p. 63-108.
69. Steenbeek R. 2000. Infanticide by males and female choice in wild Thomas's langurs. In: van Schaik CP, Janson CH, editors. Infanticide by males and its implications. Cambridge (UK): Cambridge University Press. p. 153-177.
70. Strier KB. 1996. Male reproductive strategies in new world primates. Hum Nat. 7:105-123. (Pubitemid 126313439)
71. Taub DM. 1980. Female choice and mating strategies among wild Barbary macaques (Macaca sylvanus L.). In: Lindburg DG, editor. The macaques: studies in ecology, behavior and evolution. New York: Van Nostrand Reinhold. p. 287-344.
72. Vogel C, Loch H. 1984. Reproductive parameters, adult male replacements, and infanticide among free-ranging langurs (Presbytis entellus) at Jodhpur (Rajasthan), India. In: Hausfater G, Hrdy SB, editors. Infanticide: comparative and evolutionary perspectives. New York: Aldine Publishing Company. p. 237-256.
73. Warren Y, Williamson EA. 2001. Carriage of infants by a silverback mountain gorilla. Folia Primatol. 72:245-247. (Pubitemid 33072766)
74. Weingrill T, Lycett JE, Barrett L, Hill RA, Henzi SP. 2003. Male consortship behaviour in chacma baboons: the role of demographic factors and female conceptive probabilities. Behaviour. 140:405-427. (Pubitemid 36784771)
75. Whitten PL. 1987. Infants and adult males. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT, editors. Primate societies. Chicago (IL): University of Chicago Press. p. 343-357.
76. Whitten PL, Russell E. 1996. Information content of sexual swellings and fecal steroids in sooty mangabeys (Cercocebus torquatus atys). Am J Primatol. 40:67-82. (Pubitemid 26351377)
77. Wildt DE, Doyle LL, Stone SC, Harrison RM. 1977. Correlation of perineal swelling with serum ovarian hormone levels, vaginal cytology, and ovarian follicular development during the baboon reproductive cycle. Primates. 18:261-270.
78. Wisdom MJ, Mills LS, Doak DF. 2000. Life stage simulation analysis: estimating vital-rate effects on population growth for conservation. Ecology. 81:628-641. (Pubitemid 30437989)
79. Wroblewski EE. 2010. Paternity and father-offspring relationships in wild chimpanzees, Pan troglodytes schweinfurthii [PhD Dissertation]. [Minneapolis (MN)]: University of Minnesota.
80. Xiang ZF, Sayers K, Grueter CC. 2009. Direct paternal care in blackand-white snub-nosed monkeys. J Zool. 278:157-162.
81. Zhao Q, Pan WS. 2006. Male-immature interactions seem to depend on group composition in white-headed langur (Trachypithecus leucocephalus). Acta Ethol. 9:91-94. (Pubitemid 44819354)
82. Zinner D, Alberts SC, Nunn CL, Altmann J. 2002. Significance of primate sexual swelling. Nature. 420:142-143.