Abstract
Reproductive skew models have been proposed as a unifying framework for understanding animal social systems, but few studies have investigated reproductive skew in a broad evolutionary context. We compiled data on the distribution of mating among males for 31 species of primates and calculated skew indices for each study. We analyzed the determinants of mating skew with phylogenetic comparative methods to investigate two models from reproductive skew theory, the concession model and the tug-of-war model. Mating skew decreased as the number of males increased in multimale groups, suggesting that monopolization of females becomes more difficult when there are more rivals, and therefore supporting the tug-of-war model. We predicted that single males are unable to monopolize receptive females as overlap in female receptivity increases (estrous synchrony) and, as a result, that mating skew decreases. However, we did not find any evidence for a link between female estrous synchrony and male mating skew. Finally, the concession model predicts high skew in male philopatric species relative to species in which males disperse, yet our measures of mating skew showed no significant associations with qualitative scores of male dispersal. More definitive tests of the concession model will require more quantitative measures of relatedness, which are presently unavailable for most primate species in our study. Overall, our results provide support for the tug-of-war model in primates, and the approach developed here can be applied to study comparative patterns of skew in other biological systems.


Similar content being viewed by others
References
Abouheif E (1999) A method for testing the assumption of phylogenetic independence in comparative data. Evol Ecol Res 1:895–909
Alberts SC, Altmann J, Wilson ML (1996) Mate guarding constrains foraging activity of male baboons. Anim Behav 51:1269–1277
Alberts SC, Watts HE, Altmann J (2003) Queuing and queue-jumping: long-term patterns of reproductive skew in male savannah baboons: Papio cynocephalus. Anim Behav 65:821–840
Altmann SA (1962) A field study of the sociobiology of the rhesus monkey, Macaca mulatta. Ann N Y Acad Sci 102:338–435
Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–265
Bennett NC, Faulkes CG (2000) African mole-rats: ecology and eusociality. Cambridge University Press, New York
Berard JD, Nurnberg P, Epplen JT, Schmidtre J (1994) Alternative reproductive tactics and reproductive success in male rhesus macaques. Behaviour 129:177–201
Bercovitch FB (1983) Time budgets and consortships in olive baboons (Papio anubis). Folia Primatol (Basel) 41:180–190
Bercovitch FB (1986) Male rank and reproductive activity in savanna baboons. Int J Primatol 7:533–550
Boesch C, Boesch-Achermann H (2000) The chimpanzees of the Tai Forest: behavioural ecology and evolution. Oxford University Press, Oxford
Boesch C, Kohou G, Nene H, Vigilant L (2006) Male competition and paternity in wild chimpanzees of the Tai forest. Am J Phys Anthropol 130:103–115
Bourke AFG (1997) Sociality and kin selection in insects. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach, 4th edn. Blackwell, Oxford, pp 203–227
Bradley BJ, Robbins MM, Williamson EA, Steklis HD, Steklis NG, Eckhardt N, Boesch C, Vigilant L (2005) Mountain gorilla tug-of-war: silverbacks have limited control over reproduction in multimale groups. Proc Natl Acad Sci U S A 102:9418–9423
Brereton AR (1994) Copulatory behavior in a free-ranging population of stumptail macaques (Macaca arctoides) in Mexico. Primates 35:113–122
Bulger JB (1993) Dominance rank and access to estrous females in male savanna baboons. Behaviour 127:67–103
Cant MA (1998) A model for the evolution of reproductive skew without reproductive suppression. Anim Behav 55:163–169
Cant MA, Reeve HK (2002) Female control of the distribution of paternity in cooperative breeders. Am Nat 160:602–611
Charpentier M, Peignot P, Hossaert-McKey M, Gimenez O, Setchell JM, Wickings EJ (2005) Constraints on control: factors influencing reproductive success in male mandrills (Mandrillus sphinx). Behav Ecol 16:614–623
Clutton-Brock TH (1998) Reproductive skew, concessions and limited control. Trends Ecol Evol 13:288–292
Clutton-Brock TH, Brotherton PNM, Russell AF, O’Riain MJ, Gaynor D, Kansky R, Griffin A, Manser M, Sharpe L, McIlrath GM, Small T, Moss A, Monfort S (2001) Cooperation, control, and concession in meerkat groups. Science 291:478–481
Constable J, Ashley M, Goodall J, Pusey A (2001) Noninvasive paternity assignment in Gombe chimpanzees. Mol Ecol 10:1279–1300
Cords M (1984) Mating patterns and social structure in redtail monkeys (Cercopithecus ascanius). Z Tierpsychol 64:313–329
Cowlishaw G, Dunbar RIM (1991) Dominance rank and mating success in male primates. Anim Behav 41:1045–1056
Creel SR, Waser PM (1991) Failures of reproductive suppression in dwarf mongooses (Helogale parvula): accident or adaptation? Behav Ecol 2:7–15
Creel SR, Creel NM (2002) The African wild dog: behavior, ecology, and conservation. Princeton University Press, Princeton
Creel S, Creel NM, Mills MGL, Monfort SL (1997) Rank and reproduction in cooperatively breeding African wild dogs: behavioural and endocrine correlates. Behav Ecol 8:298–306
Curie-Cohen M, Yoshihara D, Luttrell L, Benforado K, MacCluer JW, Stone WH (1983) The effects of dominance on mating behavior and paternity in a captive troop of rhesus monkeys (Macaca mulatta). Am J Primatol 5:127–138
de Ruiter J, Geffen E (1998) Relatedness of matrilines, dispersing males and social groups in long-tailed macaques (Macaca fascicularis). Proc R Soc Lond B Biol Sci 265:79–87
de Ruiter JR, van Hooff JARAM, Scheffrahn W (1994) Social and genetic aspects of paternity in wild long-tailed macaques (Macaca fascicularis). Behaviour 129:203–224
Dixson AF (1998) Primate sexuality: comparative studies of the prosimians, monkeys, apes, and human beings. Cambridge University Press, Cambridge
Dunbar RIM (1988) Primate social systems. Cornell University Press, Ithaca
Dunbar RIM (1999) Male mating strategies: an optimal foraging problem. In: Kappeler P (ed) Primate males. Cambridge University Press, Cambridge, pp 259–268
Emlen ST (1997) Predicting family dynamics in social vertebrates. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach, 4th edn. Blackwell, Oxford, pp 228–253
Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223
Engelhardt A, Pfeifer J, Heistermann M, Niemitz C, van Hooff JA, Hodges JK (2004) Assessment of female reproductive status by male longtailed macaques, Macaca fascicularis, under natural conditions. Anim Behav 67:915–924
Engh AL, Funk SM, van Horn RC, Scribner KT, Bruford MW, Libants S, Szykman M, Smale L, Holekamp KE (2002) Reproductive skew among males in a female-dominated mammalian society. Behav Ecol 13:193–200
Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15
Field J, Solis CR, Queller DC, Strassmann JE (1998) Social and genetic structure of paper wasp cofoundress associations: tests of reproductive skew models. Am Nat 151:545–563
Freckleton RP (2000) Phylogenetic tests of ecological and evolutionary hypotheses: checking for phylogenetic independence. Funct Ecol 14:129–134
Garland T Jr, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18–32
Garland T Jr, Dickerman AW, Janis CM, Jones JA (1993) Phylogenetic analysis of covariance by computer simulation. Syst Biol 42:265–292
Girman DJ, Mills MGL, Geffen E, Wayne RK (1997) A molecular genetic analysis of social structure, dispersal, and interpack relationships of the African wild dog (Lycaon pictus). Behav Ecol Sociobiol 40:187–198
Griffin AS, Pemberton JM, Brotherton PNM, Gaynor D, Clutton-Brock TH (2003) A genetic analysis of cooperative breeding in meerkats (Suricata suricatta). Behav Ecol 14:472–480
Hager R (2003) Reproductive skew models applied to primates. In: Jones CB (ed) Sexual selection and reproductive competition in primates: new perspectives and directions. American Society of Primatologists, Norman, pp 65–101
Harcourt AH, Harvey PH, Larson SG, Short RV (1981) Testis weight, body weight and breeding system in primates. Nature 293:55–57
Harmon LJ, Losos JB (2005) The effect of intraspecific sample size on type I and type II error rates in comparative studies. Evolution 59:2705–2710
Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, Oxford
Harvey PH, Rambaut A (2000) Comparative analyses for adaptive radiations. Proc R Soc Lond B Biol Sci 355:1–7
Haydock J, Koenig WD (2002) Reproductive skew in the polygynandrous acorn woodpecker. Proc Natl Acad Sci USA 99:7178–7183
Heistermann M, Ziegler T, van Schaik CP, Launhardt K, Winkler P, Hodges JK (2001) Loss of oestrus, concealed ovulation and paternity confusion in free-ranging Hanuman langurs. Proc R Soc Lond B Biol Sci 268:2445–2451
Ims RA (1988) The potential for sexual selection in males: effect of sex ratio and spatio temporal distribution of receptive females. Evol Ecol 3:338–352
Inoue M, Mitsunaga F, Ohsawa H, Takenaka A, Sugiyama Y, Gaspard SA, Takenaka O (1991) Male mating behaviour and paternity discrimination by DNA fingerprinting in a Japanese macaque group. Folia Primatol 56:202–210
Inoue M, Mitsunaga F, Nozaki M, Ohsawa H, Takenaka A, Sugiyama Y, Shimizu K, Takenaka O (1993) Male dominance rank and reproductive success in an enclosed group of Japanese macaques: with special reference to post-conception mating. Primates 34:503–511
Jamieson IG (1997) Testing reproductive skew models in a communally breeding bird, the pukeko, Prophyrio porphyrio. Proc R Soc Lond B Biol Sci 264:335–340
Johnstone RA (2000) Models of reproductive skew: a review and synthesis. Ethology 106:5–26
Johnstone RA, Woodroffe R, Cant MA, Wright J (1999) Reproductive skew in multimember groups. Am Nat 153:315–331
Jones KE, Purvis A (1997) An optimum body size for mammals? Comparative evidence from bats. Funct Ecol 11:751–756
Keane B, Waser PM, Creel SR, Creel NM, Elliott LF, Minchella DJ (1994) Subordinate reproduction in dwarf mongooses. Anim Behav 47:65–75
Keller L, Reeve HK (1994) Partitioning of reproduction in animal societies. Trends Ecol Evol 9:98–102
Kokko H, Lindström J (1997) Measuring mating skew. Am Nat 149:794–799
Kokko H, Johnstone RA (1999) Social queuing in animal societies: a dynamic model of reproductive skew. Proc R Soc Lond B Biol Sci 265:571–578
Kokko H, Sutherland WJ, Lindström J, Reynolds JD, Mackenzie A (1998) Individual mating success, lek stability, and the neglected limitations of statistical power. Anim Behav 56:755–762
Kokko H, Mackenzie A, Reynolds JD, Lindström J, Sutherland WJ (1999) Measures of inequality are not equal. Am Nat 154:358–382
Langer P, Hogendoorn K, Keller L (2004) Tug-of-war over reproduction in a social bee. Nature 428:844–847
Launhardt K, Borries C, Hardt C, Epplen JT, Winkler P (2001) Paternity analysis of alternative male reproductive routes among the langurs (Semnopithecus entellus) of Ramnagar. Anim Behav 61:53–64
Li Q, Zhang Y (2005) Phylogenetic relationships of the macaques (Cercopithecidae: Macaca), inferred from mitochondrial DNA sequences. Biochem Genet 43:375–386
Lindenfors P, Froberg L, Nunn CL (2004) Females drive primate social evolution. Proc R Soc Lond B Biol Sci 271(Suppl):S101–S103
Lukas D, Reynolds V, Boesch C, Vigilant L (2005) To what extent does living in a group mean living with kin? Mol Ecol 14:2181–2196
Magrath RD, Heinsohn RG (2000) Reproductive skew in birds: models, problems and prospects. J Avian Biol 31:247–258
Magrath RD, Heinsohn RG, Johnstone RA (2004) Reproductive skew. In: Koenig WD, Dickinson JL (eds) Ecology and evolution of cooperative breeding in birds. Cambridge University Press, Cambridge, pp 157–176
Matsubara M (2003) Costs of mate guarding and opportunistic mating among wild male Japanese macaques. Int J Primatol 24:1057–1075
McClintock MK (1981) Social control of the ovarian cycle and the function of estrous synchrony. Am Zool 21:243–256
McClintock MK (1983) Pheromonal regulation of the ovarian cycle: enhancement, suppression and synchrony. Academic, New York
McMillan C (1989) Male age, dominance, and mating success among rhesus monkeys. Am J Phys Anthropol 80:83–89
McRae SB (1996) Family values: costs and benefits of communal nesting in the moorhe. Anim Behav 52:225–245
Mitani JC, Gros-Louis J, Manson JH (1996) Number of males in primate groups: comparative tests of competing hypotheses. Am J Primatol 38:315–332
Moller AP, Ninni P (1998) Sperm competition and sexual selection: a meta-analysis of paternity studies of birds. Behav Ecol Sociobiol 43:345–358
Morales CJ, Melnick DJ (1998) Phylogenetic relationships of the macaques (Cercopithecidae: Macaca), as revealed by high resolution restriction site mapping of mitochondrial ribosomal genes. J Hum Evol 34:1–23
Morin PA, Moore JJ, Chakraborty R, Jin L, Goodall J, Woodruff DS (1994) Kin selection, social structure, gene flow, and the evolution of chimpanzees. Science 265:1193–1201
Nishida T (1983) Alpha status and agonistic alliance in wild chimpanzees. Primates 24:318–336
Nishida T (1997) Sexual behavior of adult male chimpanzees of the Mahale Mountains National Park, Tanzania. Primates 38:379–398
Noe R (1992) Alliance formation among male baboons: shopping for profitable partners. In: Harcourt AH, de Waal FBM (eds) Coalitions and alliances in humans and other animals. Oxford University Press, Oxford, pp 284–321
Nonacs P (2000) Measuring and using skew in the study of social behavior and evolution. Am Nat 156:577–589
Nonacs P (2001) A life-history approach to group living and social contracts between individuals. Ann Zool Fenn 38:239–254
Nonacs P (2003) Measuring the reliability of skew indices: is there one best index? Anim Behav 65:615–627
Nunn CL (1999a) The number of males in primate social groups: a comparative test of the socioecological model. Behav Ecol Sociobiol 46:1–13
Nunn CL (1999b) The evolution of exaggerated sexual swellings in primates and the graded signal hypothesis. Anim Behav 58:229–246
Nunn CL, Barton RA (2000) Allometric slopes and independent contrasts: a comparative test of Kleiber’s law in primate ranging patterns. Am Nat 156:519–533
Nunn CL, Barton RA (2001) Comparative methods for studying primate adaptation and allometry. Evol Anthropol 10:81–98
Ohsawa H, Inoue M, Takenaka O (1993) Mating strategy and reproductive success of male patas monkeys (Erythrocebus patas). Primates 34:533–544
Packer C (1979) Male dominance and reproductive activity in Papio anubis. Anim Behav 37:37–45
Paul A (1997) Breeding seasonality affects the association between dominance and reproductive success in non-human male primates. Folia Primatol 68:344–349
Paul A, Kuester J (1996) Differential reproduction in male and female Barbary macaques. In: Fa JE, Lindburg DG (eds) Evolution and ecology of macaque societies. Cambridge University Press, Cambridge, pp 293–317
Pawlowski B, Lowen CB, Dunbar RIM (1998) Neocortex size, social skills and mating success in primates. Behaviour 135:357–368
Pemberton JM, Albon SD, Guinness FE, Clutton-Brock TH, Dover G (1992) Behavioral estimates of male mating success tested by DNA fingerprinting in a polygynous mammal. Behav Ecol 3:66–75
Pereira ME (1991) Asynchrony within estrous synchrony among ringtailed lemurs (Primates: Lemuridae). Physiol Behav 49:47–52
Perry S (1997) Male–female social relationships in wild white-faced capuchins (Cebus capucinus). Behaviour 134:477–510
Pope (1990) The reproductive consequences of male cooperation in the red howler monkey: paternity exclusion in multi-male and single-male troops using genetic markers. Behav Ecol Sociobiol 27:439–446
Possamai CB, Young RJ, de Oliveira RCR, Mendes SL, Strier KB (2005) Age-related variation in copulations of male northern muriquis (Brachyteles hypoxanthus). Folia Primatol 76:33–36
Price T (1997) Correlated evolution and independent contrasts. Philos Trans R Soc Lond B Biol Sci 352:519–529
Purvis A (1995) A composite estimate of primate phylogeny. Philos Trans R Soc Lond B Biol Sci 348:405–421
Purvis A, Rambaut A (1995) Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data. Comput Appl Biosci 11:247–251
Purvis A, Webster AJ (1999) Phylogenetically independent comparisons and primate phylogeny. In: Lee PC (ed) Comparative primate socioecology. Cambridge University Press, Cambridge, pp 44–70
Ragsdale JE (1999) Reproductive skew theory extended: the effect of resource inheritance on social organization. Evol Ecol Res 1:859–874
Reeve HK, Emlen ST (2000) Reproductive skew and group size: an N-person staying incentive model. Behav Ecol 11:640–647
Reeve HK, Keller L (2001) Tests of reproductive-skew models in social insects. Ann Rev Entomol 46:347–385
Reeve HK, Emlen ST, Keller L (1998) Reproductive sharing in animal societies: reproductive incentives or incomplete control by dominant breeders? Behav Ecol 9:267–278
Reeve HK, Starks PT, Peters JM, Nonacs P (2000) Genetic support for the evolutionary theory of reproductive transactions in social wasps. Proc R Soc Lond B Biol Sci 267:75–79
Reeve J, Abouheif E (1999) Phylogenetic Independence. Indexed at J Felsenstein’s site for phylogenetic analysis software (http://evolution.genetics.washington.edu/phylip/software.html)
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
Ridley M (1986) The number of males in a primate troop. Anim Behav 34:1848–1858
Robbins MM (1999) Male mating patterns in wild multimale mountain gorilla groups. Anim Behav 57:1013–1020
Robbins AM, Robbins MM (2005) Fitness consequences of dispersal decisions for male mountain gorillas (Gorilla beringei beringei). Behav Ecol Sociobiol 58:295–309
Samuel A, Silk JB, Rodman PS (1984) Changes in the dominance rank and reproductive behaviour of male bonnet macaques (Macaca radiata). Anim Behav 32:994–1003
Say L, Pontier D, Natoli E (2001) Influence of oestrus synchronization on male reproductive success in the domestic cat (Felis catus L.). Proc R Soc Lond B Biol Sci 268:1049–1053
Seppä P, Queller DC, Strassmann JE (2002) Reproduction in foundress associations of the social wasp, Polistes carolina: conventions, competition, and skew. Behav Ecol 13:531–542
Setchell JM, Charpentier M, Wickings EJ (2005) Mate guarding and paternity in mandrills: factors influencing alpha male monopoly. Anim Behav 70:1105–1120
Shively C, Smith DG (1985) Social status and reproductive success of male Macaca fascicularis. Am J Primatol 9:129–135
Shuster SM, Wade MJ (2003) Mating systems and mating strategies. Princeton University Press, Princeton
Smith DG (1981) The association between rank and reproductive success of male rhesus monkeys. Am J Primatol 1:83–90
Smith RJ, Cheverud JM (2002) Scaling of sexual dimorphism in body mass: a phylogenetic analysis of Rensch’s rule in primates. Int J Primatol 23:1095–1135
Soltis J, Mitsunaga F, Shimizu K, Nozaki M, Yanagihara Y, Domingo-Roura X, Takenaka O (1997) Sexual selection in Japanese macaques II: female mate choice and male–male competition. Anim Behav 54:737–746
Strier KB, Dib LT, Figueira JEC (2002) Social dynamics of male muriquis (Brachyteles arachnoids hypoxanthus). Behaviour 139:315–342
Struhsaker TT, Pope TR (1991) Mating system and reproductive success: a comparison of two African forest monkeys (Colobus badius and Cercopithecus ascanius). Behaviour 117:182–205
Takahashi H (2004) Do males have a better chance of mating when the number of estrous females is equal to or greater than the males’ ordinal rank? Testing the hypothesis in Japanese macaques. Am J Primatol 63:95–102
Tsuji K, Tsuji N (1998) Indices of reproductive skew depend on average reproductive success. Evol Ecol 12:141–152
Tsuji K, Kasuya E (2001) What do indices of reproductive skew measure? Am Nat 158:155–165
van Noordwijk MA, van Schaik CP (2004) Sexual selection and the careers of primate males: paternity concentration, dominance acquisition tactics and transfer decisions. In: Kappeler PM, van Schaik CP (eds) Sexual selection in primates: a comparative perspective. Cambridge University Press, Cambridge, pp 208–229
van Schaik CP, van Noordwijk MA, Nunn CL (1999) Sex and social evolution in primates. In: Lee P (ed) Comparative socioecology of primates. Cambridge University Press, Cambridge, pp 204–240
Vehrencamp SL (1983a) A model for the evolution of despotic versus egalitarian societies. Anim Behav 31:667–682
Vehrencamp SL (1983b) Optimal skew in cooperative societies. Am Zool 23:327–355
Vigilant L, Hofreiter M, Siedel H, Boesch C (2001) Paternity and relatedness in wild chimpanzee communities. Proc Natl Acad Sci U S A 98:12890–12895
Watts DP (1998) Coalitionary mate guarding by male chimpanzees at Ngogo, Kibale National Park, Uganda. Behav Ecol Sociobiol 44:43–55
Widdig A, Bercovitch FB, Streich WJ, Sauermann U, Nuernberg P, Krawczak M (2004) A longitudinal analysis of reproductive skew in male macaques. Proc R Soc Lond B Biol Sci 271:819–826
Williams DA (2004) Female control of reproductive skew in cooperatively breeding brown jays (Cyanocorax morio). Behav Ecol Sociobiol 55:370–380
Acknowledgements
We thank Bill McGrew and Mandy Korstjens for providing unpublished data and Martha Robbins, Oliver Schülke, Julia Ostner, Daichi Saito, Peter Kappeler, and three reviewers for helpful comments. This study was supported by Japan Society for the Promotion of Science (JSPS) Research Fellowships to N.K. and National Science Foundation (NSF) funding (no. DEB-0212096) to C.N.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated By P. Kappeler
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kutsukake, N., Nunn, C.L. Comparative tests of reproductive skew in male primates: the roles of demographic factors and incomplete control. Behav Ecol Sociobiol 60, 695–706 (2006). https://doi.org/10.1007/s00265-006-0213-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00265-006-0213-1