Individual, social, and sexual niche traits affect copulation success in a polygynandrous mating system

Behavioral Ecology and Sociobiology

Volumn 70, Issue 6, 2016, Pages 901-912

  Bar Ziv, Einat ^a   Ilany, Amiyaal ^b   Demartsev, Vlad ^a   Barocas, Adi ^c   Geffen, Eli ^a   Koren, Lee ^d  

^a TEL AVIV UNIVERSITY   (Israel)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF WYOMING   (United States)

^d BAR ILAN UNIVERSITY   (Israel)

Author keywords

Mate guarding; Mating strategy; Mating success; Mating system; Sexual network; Sexual niche; Social rank

Indexed keywords

COPULATION; MATE GUARDING; NICHE; POLYGAMY; REPRODUCTIVE STRATEGY; REPRODUCTIVE SUCCESS; SEX-RELATED DIFFERENCE; SEXUAL CONFLICT; SEXUAL SELECTION; SMALL MAMMAL; SOCIAL NETWORK;

ANIMALIA; PROCAVIA CAPENSIS; PROCAVIIDAE;

EID: 84962784424     PISSN: 03405443     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00265-016-2112-4     Document Type: Article

References (89)

1. Adrian O, Sachser N (2011) Diversity of social and mating systems in cavies: a review. J Mammal 92:39–53
2. Alberts SC, Buchan JC, Altmann J (2006) Sexual selection in wild baboons: from mating opportunities to paternity success. Anim Behav 72:1177–1196
3. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267
4. Andersson M (1994) Sexual selection. Princeton University Press, Princeton
5. Arnqvist G, Nilsson T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60:145–164
6. Ashby B, Gupta S (2013) Sexually transmitted infections in polygamous mating systems. Philos T Roy Soc B 368:20120048
7. Barnard CJ, Fitzsimons J (1988) Kin recognition and mate choice in mice: the effects of kinship, familiarity and social interference on intersexual interaction. Anim Behav 36:1078–1090
8. Barocas A, Ilany A, Koren L, Kam M, Geffen E (2011) Variance in centrality within rock hyrax social networks predicts adult longevity. PLoS One 6:e22375
9. Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368
10. Bateson M, Healy SD (2005) Comparative evaluation and its implications for mate choice. Trends Ecol Evol 20:659–664
11. Bel-Venner MC, Dray S, Allaine D, Menu F, Venner S (2008) Unexpected male choosiness for mates in a spider. Proc R Soc Lond B 275:77–82
12. Bergmuller R, Taborsky M (2010) Animal personality due to social niche specialisation. Trends Ecol Evol 25:504–511
13. Bowler M, Knogge C, Heymann EW, Zinner D (2012) Multilevel societies in New World primates? Flexibility may characterize the organization of Peruvian Red Uakaris (Cacajao calvus ucayalii). Int J Primatol 33:1110–1124
14. Buesching CD, Heistermann M, Hodges JK, Zimmermann E (1998) Multimodal oestrus advertisement in a small nocturnal prosimian, Microcebus murinus. Folia Primatol 69:295–308
15. Buss DM, Schmitt DP (1993) Sexual strategies theory: an evolutionary perspective on human mating. Psychol Rev 100:204–232
16. Butts C (2008) network: A package for managing relational data in R. J Stat Softw 24:2
17. 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
18. Clutton-Brock TH (1989) Mammalian mating systems. Proc R Soc Lond B 236:339–372
19. Clutton-Brock T (2007) Sexual selection in males and females. Science 318:1882–1885
20. Collet J, Richardson DS, Worley K, Pizzari T (2012) Sexual selection and the differential effect of polyandry. Proc Natl Acad Sci U S A 109:8641–8645
21. Coltman DW, Bancroft DR, Robertson A, Smith JA, Clutton-Brock TH, Pemberton JM (1999) Male reproductive success in a promiscuous mammal: behavioural estimates compared with genetic paternity. Mol Ecol 8:1199–1209
22. Dall’Olio S, Norscia I, Antonacci D, Palagi E (2012) Sexual signalling in Propithecus verreauxi: male “chest badge” and female mate choice. PLoS One 7:e37332
23. DeVries AC, Johnson CL, Carter CS (1997) Familiarity and gender influence social preferences in prairie voles (Microtus ochrogaster). Can J Zool 75:295–301
24. East ML, Burke T, Wilhelm K, Greig C, Hofer H (2003) Sexual conflicts in spotted hyenas: male and female mating tactics and their reproductive outcome with respect to age, social status and tenure. Proc R Soc Lond B 270:1247–1254
25. Edward DA, Chapman T (2011) The evolution and significance of male mate choice. Trends Ecol Evol 26:647–654
26. Emlen ST, Oring LW (1977) Ecology, sexual selection, and evolution of mating systems. Science 197:215–223
27. Fisher DO, Double MC, Blomberg SP, Jennions MD, Cockburn A (2006) Post-mating sexual selection increases lifetime fitness of polyandrous females in the wild. Nature 444:89–92
28. Formica VA, Wood CW, Larsen WB, Butterfield RE, Augat ME, Hougen HY, Brodie ED III (2012) Fitness consequences of social network position in a wild population of forked fungus beetles (Bolitotherus cornutus). J Evol Biol 25:130–137
29. Gammell MP, De Vries H, Jennings DJ, Carlin CM, Hayden TJ (2003) David’s score: a more appropriate dominance ranking method than Clutton-Brock et al.’s index. Anim Behav 66:601–605
30. Garcia-Gonzalez F, Yasui Y, Evans JP (2014) Mating portfolios: bet-hedging, sexual selection and female multiple mating. Proc R Soc B 282:20150346
31. Georgiev AV, Russell AF, Thompson ME, Otali E, Muller MN, Wrangham RW (2014) The foraging costs of mating effort in male chimpanzees (Pan troglodytes schweinfurthii). Inter J Primatol 35:725–745
32. Glickman SE, Short RV, Renfree MB (2005) Sexual differentiation in three unconventional mammals: spotted hyenas, elephants and tammar wallabies. Horm Behav 48:403–417
33. Gowaty PA, Steinichen R, Anderson WW (2003) Indiscriminate females and choosy males: within- and between-species variation in Drosophila. Evolution 57:2037–2045
34. Hanken J, Sherman PW (1981) Multiple paternity in Belding’s ground squirrel litters. Science 212:351–353
35. Hanley JA, Negassa A, Edwardes MDD, Forrester JE (2003) Statistical analysis of correlated data using generalized estimating equations: an orientation. Am J Epidemiol 157:364–375
36. Hirsch BT, Maldonado JE (2011) Familiarity breeds progeny: sociality increases reproductive success in adult male ring-tailed coatis (Nasua nasua). Mol Ecol 20:409–419
37. Hoogland JL (1998) Why do female Gunnison’s prairie dogs copulate with more than one male? Anim Behav 55:351–359
38. Hoogland JL, Foltz DW (1982) Variance in male and female reproductive success in a harem-polygynous mammal, the black-tailed prairie dog (Sciuridae: Cynomys ludovicianus). Behav Ecol Sociobiol 11:155–163
39. Ilany A, Barocas A, Koren L, Kam M, Geffen E (2011) Do singing rock hyraxes exploit conspecific calls to gain attention? PLoS One 6:e28612
40. Ilany A, Barocas A, Kam M, Ilany T, Geffen E (2013a) The energy cost of singing in wild rock hyrax males: evidence for an index signal. Anim Behav 85:995–1001
41. Ilany A, Barocas A, Koren L, Kam M, Geffen E (2013b) Structural balance in the social networks of a wild mammal. Anim Behav 85:1397–1405
42. Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64
43. Jirotkul M (1999) Operational sex ratio influences female preference and male-male competition in guppies. Anim Behav 58:287–294
44. Kappeler PM, Schaffler L (2008) The lemur syndrome unresolved: extreme male reproductive skew in sifakas (Propithecus verreauxi), a sexually monomorphic primate with female dominance. Behav Ecol Sociobiol 62:1007–1015
45. Kappeler PM, Mass V, Port M (2009) Even adult sex ratios in lemurs: potential costs and benefits of subordinate males in Verreaux’s sifaka (Propithecus verreauxi) in the Kirindy Forest CFPF, Madagascar. Am J Phys Anthropol 140:487–497
46. Keeley ATH, Keeley BW (2004) The mating system of Tadarida brasiliensis (Chiroptera: Molossidae) in a large highway bridge colony. J Mammal 85:113–119
47. Kidd SA, Eskenazi B, Wyrobek AJ (2001) Effects of male age on semen quality and fertility: a review of the literature. Fertil Steril 75:237–248
48. Kokko H (1997) The lekking game: can female choice explain aggregated male displays? J Theor Biol 187:57–64
49. Kokko H, Brooks R, McNamara JM, Houston AI (2002) The sexual selection continuum. Proc R Soc Lond B 269:1331–1340
50. Koren L (2000) Hyrax socialization: first evidence for a matriarchal society. MSc-thesis, Tel-Aviv University
51. Koren L (2006) Vocalization as an indicator of individual quality in the rock hyrax. PhD-thesis, Tel-Aviv University
52. Koren L, Geffen E (2009a) Androgens and social status in female rock hyraxes. Anim Behav 77:233–238
53. Koren L, Geffen E (2009b) Complex call in male rock hyrax (Procavia capensis): a multi-information distributing channel. Behav Ecol Sociobiol 63:581–590
54. Koren L, Mokady O, Geffen E (2006) Elevated testosterone levels and social ranks in female rock hyrax. Horm Behav 49:470–477
55. Koren L, Mokady O, Geffen E (2008) Social status and cortisol levels in singing rock hyraxes. Horm Behav 54:212–216
56. Kvarnemo C, Forsgren E (2000) The influence of potential reproductive rate and variation in mate quality on male and female choosiness in the sand goby, Pomatoschistus minutus. Behav Ecol Sociobiol 48:378–384
57. Kvarnemo C, Simmons LW (2013) Polyandry as a mediator of sexual selection before and after mating. Philos T Roy Soc B 368:20120042
58. Lenton AP, Francesconi M (2011) Too much of a good thing? Variety is confusing in mate choice. Biol Lett 7:528–531
59. Massen JJM, Koski SE (2014) Chimps of a feather sit together: chimpanzee friendships are based on homophily in personality. Evol Hum Behav 35:1–8
60. McDonald GC, James R, Krause J, Pizzari T (2013) Sexual networks: measuring sexual selection in structured, polyandrous populations. Philos T Roy Soc B 368:20120356
61. McGlothlin JW, Neudorf DLH, Casto JM, Nolan V, Ketterson ED (2004) Elevated testosterone reduces choosiness in female dark-eyed juncos (Junco hyemalis): evidence for a hormonal constraint on sexual selection? Proc R Soc Lond B 271:1377–1384
62. Mendelssohn H (1965) Breeding in the Syrian hyrax. Int Zoo Yearb 5:116–125
63. Millar RP (1971) Reproduction in the rock hyrax (Procavia capensis). Zool Afr 3:243–261
64. Montiglio P-O, Ferrari C, Réale D (2013) Social niche specialization under constraints: personality, social interactions and environmental heterogeneity. Philos T Roy Soc B 368:20120343
65. Murray KL, Fleming TH (2008) Social structure and mating system of the buffy flower bat, Erophylla sezekorni (Chiroptera, Phyllostomidae). J Mammal 89:1391–1400
66. Neff BD, Svensson EI (2013) Polyandry and alternative mating tactics. Philos T Roy Soc B 368:20120045
67. Nutt KJ (2005) Philopatry of both sexes leads to the formation of multimale, multifemale groups in Ctenodactylus gundi (Rodentia: Ctenodactylidae). J Mammal 86:961–968
68. Oh KP, Badyaev AV (2010) Structure of social networks in a passerine bird: consequences for sexual selection and the evolution of mating strategies. Am Nat 176:E80–89
69. Parker GA, Birkhead TR (2013) Polyandry: the history of a revolution. Philos T Roy Soc B 368:20120335
70. Pizzari T, Wedell N (2013) The polyandry revolution. Philos T Roy Soc B 368:20120041
71. Sargent RC, Gross MR, Vandenberghe EP (1986) Male mate chice in fishes. Anim Behav 34:545–550
72. Schroeder J, Nakagawa S, Rees M, Mannarelli M-E, Burke T (2015) Reduced fitness in progeny from old parents in a natural population. Proc Natl Acad Sci U S A 112:4021–4025
73. Schwagmeyer PL, Parker GA (1987) Queuing for mates in thirteen-lined ground squirrels. Anim Behav 35:1015–1025
74. Semple S, McComb K (2000) Perception of female reproductive stale from vocal cues in a mammal species. Proc R Soc Lond B 267:707–712
75. Sherman PW (1989) Mate guarding as paternity insurance in Idaho ground squirrels. Nature 338:418–420
76. Sih A, Hanser SF, McHugh KA (2009) Social network theory: new insights and issues for behavioral ecologists. Behav Ecol Sociobiol 63:975–988
77. Simmons LW (2005) The evolution of polyandry: sperm competition, sperm selection, and offspring viability. Ann Rev Ecol Evol S 36:125–146
78. Slatyer RA, Mautz BS, Backwell PR, Jennions MD (2012) Estimating genetic benefits of polyandry from experimental studies: a meta-analysis. Biol Rev 87:1–33
79. Springer MS, Cleven GC, Madsen O, deJong WW, Waddell VG, Amrine HM, Stanhope MJ (1997) Endemic African mammals shake the phylogenetic tree. Nature 388:61–64
80. Taylor ML, Price TAR, Wedell N (2014) Polyandry in nature: a global analysis. Trends Ecol Evol 29:376–383
81. Thompson CL (2013) Non-monogamous copulations and potential within-group mating competition in white-faced Saki monkeys (Pithecia pithecia). Am J Primatol 75:817–824
82. Tregenza T, Wedell N (2002) Polyandrous females avoid costs of inbreeding. Nature 415:71–73
83. Wagner RH (1998) Hidden leks: sexual selection and the clustering of avian territories. Ornithol Monogr 49:123–145
84. Wagner RH, Schug MD, Morton ES (1996) Condition dependent control of paternity by female purple martins: implications for coloniality. Behav Ecol Sociobiol 38:379–389
85. Wey TW, Blumstein DT (2012) Social attributes and associated performance measures in marmots: bigger male bullies and weakly affiliating females have higher annual reproductive success. Behav Ecol Sociobiol 66:1075–1085
86. Wey TW, Burger JR, Ebensperger LA, Hayes LD (2013) Reproductive correlates of social network variation in plurally breeding degus (Octodon degus). Anim Behav 85:1407–1414
87. Wolff JO, Macdonald DW (2004) Promiscuous females protect their offspring. Trends Ecol Evol 19:127–134
88. Zeger SL, Liang KY (1986) Longitudinal data-analysis for discrete and continuous outcomes. Biometrics 42:121–130
89. Zeh JA, Zeh DW (2003) Toward a new sexual selection paradigm: polyandry, conflict and incompatibility. Ethology 109:929–950