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Behavioral Ecology and Sociobiology

, Volume 70, Issue 6, pp 901–912 | Cite as

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

  • Einat Bar Ziv
  • Amiyaal Ilany
  • Vlad Demartsev
  • Adi Barocas
  • Eli Geffen
  • Lee KorenEmail author
Original Article

Abstract

In polygynandrous mating systems, the factors that mediate copulation success and the use of alternative mating tactics, such as mate guarding, are still poorly understood. In the rock hyrax (Procavia capensis), both sexes mate annually with multiple partners during a single month. In order to examine the factors that drive copulation success, we used 494 mating-related observations that were collected over a decade. In our analysis, we used the traits of individual hyraxes as well as the traits of members of their sexual niche, which we defined as their local competitors and potential mates. Using individual traits, we found that overall, female hyraxes rejected copulation attempts more frequently than males, supporting predictions from sexual selection theory. Females who had been mothers in previous years were mate-guarded more by resident males. When we considered the traits of competitors and potential mates in individuals’ sexual niche, we found that when resident males had higher-ranking competitors, their copulation success decreased, irrespective of their own traits. Bachelor male copulation success was not influenced by their competitor’s social status. Female copulation success was positively affected by maternal status and by social network position. Females that were central in the social network and those that had central female competitors had higher copulation success, supporting the benefits of social cohesion and the importance of the social niche. Thus, our results suggest that in polygynandrous mating systems, copulation success is determined not only by individual quality but also by the social and sexual niches that the individual occupies.

Significance statement

Social networks describe with whom individuals consort. The complex patterns of sexual relationships in animal societies can also be expressed as networks of mating-related interactions. During our long-term study on the dynamic social relationships of wild rock hyraxes, we observed complex sexual interactions. Our results show that hyraxes choose mating partners from their available mate pool (or sexual niche) taking into account the traits of their actual mates, other potential mates, and those of their competitors. These findings suggest that the sexual niche, describing the subset of available mating partners, is important for mate choice, with significant implications to the study of sexual selection.

Keywords

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

Notes

Acknowledgments

We are obliged to the many research assistants, undergraduate students, field guides, and park rangers who helped us trap and mark the hyraxes over the last 15 years. We thank the Israeli Nature and Parks Authority (NPA) for permission to work at the Ein Gedi Nature Reserve and the Ein Gedi Field School for hospitality and logistic help. Comments from Ally Harari, Roi Dor, Richard Wagner, and two anonymous referees greatly improved the manuscript, as did editorial comments by Naomi Paz.

Compliance with ethical standards

Ethical statement

This study was supported by three grants from the Israel Science Foundation (577/99, 488/05, 461/09).

Conflict of interest

The authors declare no conflict of interests.

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Permits for capturing, handling, and marking the hyraxes were issued and reviewed annually by the Israeli Nature and Parks Authority (permit numbers: 1999/5983, 2000/8871, 2001/8871, 2002/14674, 2003/14674, 2004/17687, 2005/20737, 2007/27210, 2008/31138, 2009/32871, 2010/37520, 2011/38061, 2012/38400).

References

  1. Adrian O, Sachser N (2011) Diversity of social and mating systems in cavies: a review. J Mammal 92:39–53CrossRefGoogle Scholar
  2. Alberts SC, Buchan JC, Altmann J (2006) Sexual selection in wild baboons: from mating opportunities to paternity success. Anim Behav 72:1177–1196CrossRefGoogle Scholar
  3. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267CrossRefPubMedGoogle Scholar
  4. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  5. Arnqvist G, Nilsson T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60:145–164CrossRefPubMedGoogle Scholar
  6. Ashby B, Gupta S (2013) Sexually transmitted infections in polygamous mating systems. Philos T Roy Soc B 368:20120048CrossRefGoogle Scholar
  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 36:1078–1090CrossRefGoogle Scholar
  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:e22375CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368CrossRefPubMedGoogle Scholar
  10. Bateson M, Healy SD (2005) Comparative evaluation and its implications for mate choice. Trends Ecol Evol 20:659–664CrossRefPubMedGoogle Scholar
  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 275:77–82CrossRefGoogle Scholar
  12. Bergmuller R, Taborsky M (2010) Animal personality due to social niche specialisation. Trends Ecol Evol 25:504–511CrossRefPubMedGoogle Scholar
  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 33:1110–1124CrossRefPubMedPubMedCentralGoogle Scholar
  14. Buesching CD, Heistermann M, Hodges JK, Zimmermann E (1998) Multimodal oestrus advertisement in a small nocturnal prosimian, Microcebus murinus. Folia Primatol 69:295–308CrossRefGoogle Scholar
  15. Buss DM, Schmitt DP (1993) Sexual strategies theory: an evolutionary perspective on human mating. Psychol Rev 100:204–232CrossRefPubMedGoogle Scholar
  16. Butts C (2008) network: A package for managing relational data in R. J Stat Softw 24:2Google Scholar
  17. Clarke PMR, Henzi SP, Barrett L (2009) Sexual conflict in chacma baboons, Papio hamadryas ursinus: absent males select for proactive females. Anim Behav 77:1217–1225CrossRefGoogle Scholar
  18. Clutton-Brock TH (1989) Mammalian mating systems. Proc R Soc Lond B 236:339–372CrossRefPubMedGoogle Scholar
  19. Clutton-Brock T (2007) Sexual selection in males and females. Science 318:1882–1885CrossRefPubMedGoogle Scholar
  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 109:8641–8645CrossRefPubMedPubMedCentralGoogle Scholar
  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 8:1199–1209CrossRefPubMedGoogle Scholar
  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:e37332CrossRefPubMedPubMedCentralGoogle Scholar
  23. DeVries AC, Johnson CL, Carter CS (1997) Familiarity and gender influence social preferences in prairie voles (Microtus ochrogaster). Can J Zool 75:295–301CrossRefGoogle Scholar
  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 270:1247–1254CrossRefGoogle Scholar
  25. Edward DA, Chapman T (2011) The evolution and significance of male mate choice. Trends Ecol Evol 26:647–654CrossRefPubMedGoogle Scholar
  26. Emlen ST, Oring LW (1977) Ecology, sexual selection, and evolution of mating systems. Science 197:215–223CrossRefPubMedGoogle Scholar
  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 444:89–92CrossRefPubMedGoogle Scholar
  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 25:130–137CrossRefPubMedGoogle Scholar
  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 66:601–605CrossRefGoogle Scholar
  30. Garcia-Gonzalez F, Yasui Y, Evans JP (2014) Mating portfolios: bet-hedging, sexual selection and female multiple mating. Proc R Soc B 282:20150346CrossRefGoogle Scholar
  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 35:725–745CrossRefGoogle Scholar
  32. Glickman SE, Short RV, Renfree MB (2005) Sexual differentiation in three unconventional mammals: spotted hyenas, elephants and tammar wallabies. Horm Behav 48:403–417CrossRefPubMedGoogle Scholar
  33. Gowaty PA, Steinichen R, Anderson WW (2003) Indiscriminate females and choosy males: within- and between-species variation in Drosophila. Evolution 57:2037–2045CrossRefPubMedGoogle Scholar
  34. Hanken J, Sherman PW (1981) Multiple paternity in Belding’s ground squirrel litters. Science 212:351–353CrossRefPubMedGoogle Scholar
  35. Hanley JA, Negassa A, Edwardes MDD, Forrester JE (2003) Statistical analysis of correlated data using generalized estimating equations: an orientation. Am J Epidemiol 157:364–375CrossRefPubMedGoogle Scholar
  36. Hirsch BT, Maldonado JE (2011) Familiarity breeds progeny: sociality increases reproductive success in adult male ring-tailed coatis (Nasua nasua). Mol Ecol 20:409–419CrossRefPubMedGoogle Scholar
  37. Hoogland JL (1998) Why do female Gunnison’s prairie dogs copulate with more than one male? Anim Behav 55:351–359CrossRefPubMedGoogle Scholar
  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 11:155–163CrossRefGoogle Scholar
  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:e28612CrossRefPubMedPubMedCentralGoogle Scholar
  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 85:995–1001CrossRefGoogle Scholar
  41. Ilany A, Barocas A, Koren L, Kam M, Geffen E (2013b) Structural balance in the social networks of a wild mammal. Anim Behav 85:1397–1405CrossRefGoogle Scholar
  42. Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64CrossRefPubMedGoogle Scholar
  43. Jirotkul M (1999) Operational sex ratio influences female preference and male-male competition in guppies. Anim Behav 58:287–294CrossRefPubMedGoogle Scholar
  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 62:1007–1015CrossRefGoogle Scholar
  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 140:487–497Google Scholar
  46. Keeley ATH, Keeley BW (2004) The mating system of Tadarida brasiliensis (Chiroptera : Molossidae) in a large highway bridge colony. J Mammal 85:113–119CrossRefGoogle Scholar
  47. Kidd SA, Eskenazi B, Wyrobek AJ (2001) Effects of male age on semen quality and fertility: a review of the literature. Fertil Steril 75:237–248CrossRefPubMedGoogle Scholar
  48. Kokko H (1997) The lekking game: can female choice explain aggregated male displays? J Theor Biol 187:57–64CrossRefGoogle Scholar
  49. Kokko H, Brooks R, McNamara JM, Houston AI (2002) The sexual selection continuum. Proc R Soc Lond B 269:1331–1340CrossRefGoogle Scholar
  50. Koren L (2000) Hyrax socialization: first evidence for a matriarchal society. MSc-thesis, Tel-Aviv UniversityGoogle Scholar
  51. Koren L (2006) Vocalization as an indicator of individual quality in the rock hyrax. PhD-thesis, Tel-Aviv UniversityGoogle Scholar
  52. Koren L, Geffen E (2009a) Androgens and social status in female rock hyraxes. Anim Behav 77:233–238CrossRefGoogle Scholar
  53. Koren L, Geffen E (2009b) Complex call in male rock hyrax (Procavia capensis): a multi-information distributing channel. Behav Ecol Sociobiol 63:581–590CrossRefGoogle Scholar
  54. Koren L, Mokady O, Geffen E (2006) Elevated testosterone levels and social ranks in female rock hyrax. Horm Behav 49:470–477CrossRefPubMedGoogle Scholar
  55. Koren L, Mokady O, Geffen E (2008) Social status and cortisol levels in singing rock hyraxes. Horm Behav 54:212–216CrossRefPubMedGoogle Scholar
  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 48:378–384CrossRefGoogle Scholar
  57. Kvarnemo C, Simmons LW (2013) Polyandry as a mediator of sexual selection before and after mating. Philos T Roy Soc B 368:20120042CrossRefGoogle Scholar
  58. Lenton AP, Francesconi M (2011) Too much of a good thing? Variety is confusing in mate choice. Biol Lett 7:528–531CrossRefPubMedPubMedCentralGoogle Scholar
  59. Massen JJM, Koski SE (2014) Chimps of a feather sit together: chimpanzee friendships are based on homophily in personality. Evol Hum Behav 35:1–8CrossRefGoogle Scholar
  60. McDonald GC, James R, Krause J, Pizzari T (2013) Sexual networks: measuring sexual selection in structured, polyandrous populations. Philos T Roy Soc B 368:20120356CrossRefGoogle Scholar
  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 271:1377–1384CrossRefGoogle Scholar
  62. Mendelssohn H (1965) Breeding in the Syrian hyrax. Int Zoo Yearb 5:116–125CrossRefGoogle Scholar
  63. Millar RP (1971) Reproduction in the rock hyrax (Procavia capensis). Zool Afr 3:243–261CrossRefGoogle Scholar
  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 368:20120343CrossRefGoogle Scholar
  65. Murray KL, Fleming TH (2008) Social structure and mating system of the buffy flower bat, Erophylla sezekorni (Chiroptera, Phyllostomidae). J Mammal 89:1391–1400CrossRefGoogle Scholar
  66. Neff BD, Svensson EI (2013) Polyandry and alternative mating tactics. Philos T Roy Soc B 368:20120045CrossRefGoogle Scholar
  67. Nutt KJ (2005) Philopatry of both sexes leads to the formation of multimale, multifemale groups in Ctenodactylus gundi (Rodentia : Ctenodactylidae). J Mammal 86:961–968CrossRefGoogle Scholar
  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:E80–89CrossRefPubMedGoogle Scholar
  69. Parker GA, Birkhead TR (2013) Polyandry: the history of a revolution. Philos T Roy Soc B 368:20120335CrossRefGoogle Scholar
  70. Pizzari T, Wedell N (2013) The polyandry revolution. Philos T Roy Soc B 368:20120041CrossRefGoogle Scholar
  71. Sargent RC, Gross MR, Vandenberghe EP (1986) Male mate chice in fishes. Anim Behav 34:545–550CrossRefGoogle Scholar
  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 112:4021–4025CrossRefPubMedPubMedCentralGoogle Scholar
  73. Schwagmeyer PL, Parker GA (1987) Queuing for mates in thirteen-lined ground squirrels. Anim Behav 35:1015–1025CrossRefGoogle Scholar
  74. Semple S, McComb K (2000) Perception of female reproductive stale from vocal cues in a mammal species. Proc R Soc Lond B 267:707–712CrossRefGoogle Scholar
  75. Sherman PW (1989) Mate guarding as paternity insurance in Idaho ground squirrels. Nature 338:418–420CrossRefPubMedGoogle Scholar
  76. Sih A, Hanser SF, McHugh KA (2009) Social network theory: new insights and issues for behavioral ecologists. Behav Ecol Sociobiol 63:975–988CrossRefGoogle Scholar
  77. Simmons LW (2005) The evolution of polyandry: sperm competition, sperm selection, and offspring viability. Ann Rev Ecol Evol S 36:125–146CrossRefGoogle Scholar
  78. Slatyer RA, Mautz BS, Backwell PR, Jennions MD (2012) Estimating genetic benefits of polyandry from experimental studies: a meta-analysis. Biol Rev 87:1–33CrossRefPubMedGoogle Scholar
  79. Springer MS, Cleven GC, Madsen O, deJong WW, Waddell VG, Amrine HM, Stanhope MJ (1997) Endemic African mammals shake the phylogenetic tree. Nature 388:61–64CrossRefPubMedGoogle Scholar
  80. Taylor ML, Price TAR, Wedell N (2014) Polyandry in nature: a global analysis. Trends Ecol Evol 29:376–383CrossRefPubMedGoogle Scholar
  81. Thompson CL (2013) Non-monogamous copulations and potential within-group mating competition in white-faced Saki monkeys (Pithecia pithecia). Am J Primatol 75:817–824CrossRefPubMedGoogle Scholar
  82. Tregenza T, Wedell N (2002) Polyandrous females avoid costs of inbreeding. Nature 415:71–73CrossRefPubMedGoogle Scholar
  83. Wagner RH (1998) Hidden leks: sexual selection and the clustering of avian territories. Ornithol Monogr 49:123–145CrossRefGoogle Scholar
  84. Wagner RH, Schug MD, Morton ES (1996) Condition dependent control of paternity by female purple martins: implications for coloniality. Behav Ecol Sociobiol 38:379–389CrossRefGoogle Scholar
  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 66:1075–1085CrossRefGoogle Scholar
  86. Wey TW, Burger JR, Ebensperger LA, Hayes LD (2013) Reproductive correlates of social network variation in plurally breeding degus (Octodon degus). Anim Behav 85:1407–1414CrossRefPubMedPubMedCentralGoogle Scholar
  87. Wolff JO, Macdonald DW (2004) Promiscuous females protect their offspring. Trends Ecol Evol 19:127–134CrossRefPubMedGoogle Scholar
  88. Zeger SL, Liang KY (1986) Longitudinal data-analysis for discrete and continuous outcomes. Biometrics 42:121–130CrossRefPubMedGoogle Scholar
  89. Zeh JA, Zeh DW (2003) Toward a new sexual selection paradigm: polyandry, conflict and incompatibility. Ethology 109:929–950CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Einat Bar Ziv
    • 1
  • Amiyaal Ilany
    • 2
  • Vlad Demartsev
    • 1
  • Adi Barocas
    • 3
  • Eli Geffen
    • 1
  • Lee Koren
    • 4
    Email author
  1. 1.Department of ZoologyTel Aviv UniversityTel AvivIsrael
  2. 2.Department of BiologyUniversity of PennsylvaniaPhiladelphiaUSA
  3. 3.Department of Zoology and Physiology and Program in EcologyUniversity of WyomingLaramieUSA
  4. 4.The Mina and Everard Goodman Faculty of Life SciencesBar-Ilan UniversityRamat-GanIsrael

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