Social attributes and associated performance measures in marmots: bigger male bullies and weakly affiliating females have higher annual reproductive success

Abstract

Studying the structure of social interactions is fundamental in behavioral ecology as social behavior often influences fitness and thus natural selection. However, social structure is often complex, and determining the most appropriate measures of variation in social behavior among individuals can be difficult. Social network analysis generates numerous, but often correlated, measures of individual connectedness derived from a network of interactions. We used measures of individual connectedness in networks of affiliative and agonistic interactions in yellow-bellied marmots, Marmota flaviventris, to first determine how variance was structured among network measures. Principal component analysis reduced our set of network measures to four “social attributes” (unweighted connectedness, affiliation strength, victimization, and bullying), which revealed differences between patterns of affiliative and agonistic interactions. We then used these extracted social attributes to examine the relationship between an individual’s social attributes and several performance measures: annual reproductive success, parasite infection, and basal stress. In male marmots, bullying was positively associated with annual reproductive success, while in females, affiliation strength was negatively associated with annual reproductive success. No other social attributes were significantly associated with any performance measures. Our study highlights the utility of considering multiple dimensions when measuring the structure and functional consequences of social behavior.

This is a preview of subscription content, access via your institution.

References

  1. Alexander RD (1974) The evolution of social behavior. Annu Rev Ecol Syst 5:325–383

    Article  Google Scholar 

  2. Altizer S, Nunn CL, Thrall PH, Gittleman JL, Antonovics J, Cunningham AA, Dobson AP, Ezenwa V, Jones KE, Pedersen AB, Poss M, Pulliam JRC (2003) Social organization and parasite risk in mammals: integrating theory and empirical studies. Annu Rev Ecol Evol Syst 34:517–547

    Article  Google Scholar 

  3. Anderson R, May RM (1991) Infectious disease of humans. Oxford University Press, Oxford

    Google Scholar 

  4. Armitage KB (1991a) Factors affecting corticosteroid concentrations in yellow-bellied marmots. Comp Biochem Physiol A 98:47–54

    PubMed  Article  CAS  Google Scholar 

  5. Armitage KB (1991b) Social and population dynamics of yellow-bellied marmots: results from long-term research. Annu Rev Ecol Syst 22:379–407

    Article  Google Scholar 

  6. Armitage KB (1998) Reproductive strategies of yellow-bellied marmots: energy conservation and differences between the sexes. J Mammal 79:385–393

    Article  Google Scholar 

  7. Armitage KB (2010) Individual fitness, social behavior, and population dynamics of yellow-bellied marmots. In: Billick I, Price MV (eds) The ecology of place: contributions of place-based research to ecological understanding. University of Chicago Press, Chicago, pp 134–154

    Google Scholar 

  8. Barrat A, Barthélemy M, Pastor-Satorras R, Vespignani A (2004) The architecture of complex weighted networks. Proc Natl Acad Sci USA 101:3747–3752

    PubMed  Article  CAS  Google Scholar 

  9. Barthélemy M, Barrat A, Pastor-Satorras R, Vespignani A (2005) Characterization and modeling of weighted networks. Phys A 346:34–43

    Article  Google Scholar 

  10. Bates D, Maechler M (2009) lme4: linear mixed-effects models using S4 classes. R package version 0.999375-32

  11. Blumstein DT, Patton ML, Saltzman W (2006) Faecal glucocorticoid metabolites and alarm calling in free-living yellow-bellied marmots. Biol Lett 2:29–32

    PubMed  Article  CAS  Google Scholar 

  12. Blumstein DT, Wey TW, Tang K (2009) A test of the social cohesion hypothesis: interactive female marmots remain at home. Proc R Soc Lond B 276:3007–3012

    Article  Google Scholar 

  13. Blumstein DT, Lea AJ, Olson LE, Martin J (2010) Heritability of anti-predatory traits: vigilance and locomotor performance in marmots. J Evol Biol 23:879–887

    PubMed  Article  CAS  Google Scholar 

  14. Bordes F, Blumstein DT, Morand S (2007) Rodent sociality and parasite diversity. Biol Lett 3:692–694

    PubMed  Article  Google Scholar 

  15. Borgatti SP, Everett MG, Freeman LC (2006) UCINET for Windows: software for social network analysis, 6139th edn. Analytic Technologies, Harvard

    Google Scholar 

  16. Cameron EZ, Setsaas TH, Linklater WL (2009) Social bonds between unrelated females increase reproductive success in feral horses. Proc Natl Acad Sci USA 106:13850–13853

    PubMed  Article  CAS  Google Scholar 

  17. Cheney D, Seyfarth R, Smuts B (1986) Social relationships and social cognition in nonhuman primates. Science 234:1361–1366

    PubMed  Article  CAS  Google Scholar 

  18. Cohen S, Kaplan JR, Cunnick JE, Manuck SB, Rabin BS (1992) Chronic social stress, affiliation, and cellular immune response in nonhuman primates. Psychol Sci 3:301–304

    Article  Google Scholar 

  19. Corner LAL, Pfeiffer DU, Morris RS (2003) Social-network analysis of Mycobacterium bovis transmission among captive brushtail possums (Trichosurus vulpecula). Prev Vet Med 59:147–167

    PubMed  Article  CAS  Google Scholar 

  20. Côté IM, Poulin R (1995) Parasitism and group size in social animals: a meta-analysis. Behav Ecol 6:159–165

    Article  Google Scholar 

  21. Creel S (2001) Social dominance and stress hormones. Trends Ecol Evol 16:491–497

    Article  Google Scholar 

  22. Croft DP, James R, Krause J (2008) Exploring animal social networks. Princeton University Press, Princeton

    Google Scholar 

  23. Csárdi G, Nepusz T (2009) iGraph library, 2nd edn. Free Software Foundation, Budapest

    Google Scholar 

  24. Das M, Penke ZP, van Hooff JARAM (1998) Postconflict affiliation and stress-related behavior of long-tailed macaque aggressors. Int J Primatol 19:53–71

    Article  Google Scholar 

  25. De Vries AC, Glasper ER, Detillion CE (2003) Social modulation of stress responses. Physiol Behav 79:399–407

    Article  Google Scholar 

  26. Engh AL, Siebert ER, Greenberg DA, Holekamp KE (2005) Patterns of alliance formation and postconflict aggression indicate spotted hyenas recognize third-party relationships. Anim Behav 69:209–217

    Article  Google Scholar 

  27. Flack JC, Girvan M, de Waal FBM, Krakauer DC (2006) Policing stabilizes construction of social niches in primates. Nature 439:426–429

    PubMed  Article  CAS  Google 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 25:130–137

    PubMed  Article  Google Scholar 

  29. Freeman LC (1979) Centrality in social networks: conceptual clarification. Soc Networks 1:215–239

    Article  Google Scholar 

  30. Friedman SR, Aral S (2001) Social networks, risk-potential networks, health, and disease. J Urban Health 78:411–418

    PubMed  Article  CAS  Google Scholar 

  31. Godfrey SS, Bull CM, James R, Murray K (2009) Network structure and parasite transmission in a group living lizard, the gidgee skink, Egernia stokesii. Behav Ecol Sociobiol 63:1045–1056

    Article  Google Scholar 

  32. Godfrey SS, Moore JA, Nelson NJ, Bull CM (2010) Social network structure and parasite infection patterns in a territorial reptile, the tuatara (Sphenodon punctatus). Int J Parasitol 40:1575–1585

    PubMed  Article  Google Scholar 

  33. Harrison A, Scantlebury M, Montgomery WI (2010) Body mass and sex-biased parasitism in wood mice Apodemus sylvaticus. Oikos 119:1099–1104

    Google Scholar 

  34. Hinde RA (1976) Interactions, relationships and social structure. Man 11:1–17

    Article  Google Scholar 

  35. House JS, Landis KR, Umberson D (1988) Social relationships and health. Science 241:540–545

    PubMed  Article  CAS  Google Scholar 

  36. Huang B, Wey TW, Blumstein DT (2011) Correlates and consequences of dominance in a social rodent. Ethology 117:573–585

    Article  Google Scholar 

  37. Keay JM, Singh J, Gaunt MC, Kaur T (2006) Fecal glucocorticoids and their metabolites as indicators of stress in various mammalian species: a literature review. J Zoo Wildl Med 37:234–244

    PubMed  Article  Google Scholar 

  38. Keeling MJ, Eames KTD (2005) Networks and epidemic models. J R Soc Interface 2:295–307

    PubMed  Article  Google Scholar 

  39. Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, New York

    Google Scholar 

  40. Lea AJ, Blumstein DT, Wey TW, Martin JGA (2010) Heritable victimization and the benefits of agonistic relationships. Proc Natl Acad Sci USA 107:21587–21592

    PubMed  Article  CAS  Google Scholar 

  41. Lusseau D, Whitehead H, Gero S (2008) Incorporating uncertainty into the study of animal social networks. Anim Behav 75:1809–1815

    Article  Google Scholar 

  42. Lusseau D, Barrett L, Henzi SP (2011) Formalising the multidimensional nature of social networks. arXiv:1101.3735v1

  43. Madden JR, Drewe JA, Pearce GP, Clutton-Brock TH (2009) The social network structure of a wild meerkat population: 2. Intragroup interactions. Behav Ecol Sociobiol 64:81–95

    Article  Google Scholar 

  44. McDonald DB (2007) Predicting fate from early connectivity in a social network. Proc Natl Acad Sci USA 104:10910–10914

    PubMed  Article  CAS  Google Scholar 

  45. Millspaugh JJ, Washburn BE (2004) Use of fecal glucocorticoid metabolite measures in conservation biology research: considerations for application and interpretation. Gen Comp Endocrinol 138:189–199

    PubMed  Article  CAS  Google Scholar 

  46. Moody J, White DR (2003) Structural cohesion and embeddedness: a hierarchical concept of social groups. Am Sociol Rev 68:103–127

    Article  Google Scholar 

  47. Moore J (2002) Parasites and the behavior of animals. Oxford University Press, New York

    Google Scholar 

  48. Newman MEJ (2004) Analysis of weighted networks. Phys Rev E 70:056131

    Article  CAS  Google Scholar 

  49. Nunn CL, Altizer S (2006) Infectious diseases in primates. Oxford University Press, New York

    Google Scholar 

  50. Olson LE, Blumstein DT (2010) Applying the coalitionary-traits metric: sociality without cooperation in male yellow-bellied marmots. Behav Ecol 21:957–965

    Article  Google Scholar 

  51. Ozgul A, Childs DZ, Oli MK, Armitage KB, Blumstein DT, Olson LE, Tuljapurkar S, Coulson T (2010) Coupled dynamics of body mass and population growth in response to environmental change. Nature 466:482–485

    PubMed  Article  CAS  Google Scholar 

  52. R Development Core Team (2009) R: a language and environment for statistical computer. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  53. Ryder TB, McDonald DB, Blake JG, Parker PG, Loiselle BA (2008) Social networks in the lek-mating wire-tailed manakin (Pipra filicauda). Proc R Soc Lond B 275:1367–1374

    Article  Google Scholar 

  54. Sapolsky RM (2004) Social status and health in humans and other animals. Annu Rev Anthropol 33:393–418

    Article  Google Scholar 

  55. Schwartz OA, Armitage KB, Van Vuren D (1998) A 32-year demography of yellow-bellied marmots (Marmota flaviventris). J Zool 246:337–346

    Article  Google Scholar 

  56. Sheriff MJ, Dantzer B, Delehanty B, Palme R, Boonstra R (2011) Measuring stress in wildlife: techniques for quantifying glucocorticoids. Physiol Ecol 166:869–887

    Google Scholar 

  57. Shine R (1989) Ecological causes for the evolution of sexual dimorphism: a review of the evidence. Q Rev Biol 64:419–461

    PubMed  Article  CAS  Google Scholar 

  58. Sih A, Hanser SF, McHugh KA (2009) Social network theory: new insights and issues for behavioral ecologists. Behav Ecol Sociobiol 63:975–988

    Article  Google Scholar 

  59. Silk JB, Alberts SC, Altmann J (2003) Social bonds of female baboons enhance infant survival. Science 302:1231–1234

    PubMed  Article  CAS  Google Scholar 

  60. Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, Wittig RM, Seyfarth RM, Cheney DL (2009) The benefits of social capital: close social bonds among female baboons enhance offspring survival. Proc R Soc Lond B 276:3099–3104

    Article  Google Scholar 

  61. SPSS Inc (2007) SPSS 16.0 Graduate Student Version, 1602nd edn. SPSS, Chicago

    Google Scholar 

  62. Uchino BN, Cacioppo JT, Kiecolt-Glaser JK (1996) The relationship between social support and physiological processes: a review with emphasis on underlying mechanisms and implications for health. Psychol Bull 119:488–531

    PubMed  Article  CAS  Google Scholar 

  63. Van Vuren D (1996) Ectoparasites, fitness, and social behavior of yellow-bellied marmots. Ethology 102:686–694

    Article  Google Scholar 

  64. Wasserman S, Faust K (1994) Social network analysis: methods and applications. Cambridge University Press, New York

    Google Scholar 

  65. Wey TW, Blumstein DT (2010) Social cohesion in yellow-bellied marmots is established through age and kin structuring. Anim Behav 79:1343–1352

    Article  Google Scholar 

  66. Wey T, Blumstein DT, Shen W, Jordán F (2008) Social network analysis of animal behaviour: a promising tool for the study of sociality. Anim Behav 75:333–344

    Article  Google Scholar 

  67. Whitehead H (2008) Analyzing animal societies: quantitative methods for vertebrate social analysis. University of Chicago Press, Chicago

    Google Scholar 

  68. Young AJ, Carlson AA, Monfort SL, Russell AF, Bennett NC, Clutton-Brock TH (2006) Stress and the suppression of subordinate reproduction in cooperatively breeding meerkats. Proc Natl Acad Sci USA 103:12005–12010

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was funded by the US Department of Education GAANN Fellowship, National Science Foundation (NSF) GK-12 Fellowship, UCLA Chancellor’s Prize, RMBL Snyder Graduate Research Fellowship, Homes O. Miller Fellowship, and Bartholomew Research Grant (to TWW); the UCLA Academic Senate and Division of Life Sciences, National Geographic Society, and NSF-IDBR-0754247 (to DTB); and NSF-DBI 0242960, 0731346 (to the RMBL). We are also grateful to the many field and lab assistants for data collection; Lucretia E. Olson and Amanda J. Lea for genetic analyses; Rebecca N. Booth and the University of Washington Center for Conservation Biology for radioimmunoassay of hormone extractions; Johannes Foufopolous, Laura Ramos, and Dirk Van Vuren for advice on parasites; the UCLA ATS statistical consultants, especially Xiao Chen and Phil Ender, for help on statistical analysis; and Jennifer E. Smith, Amanda J. Lea, Rick Grannis, Peter Nonacs, Gerald Wilkinson, F. Stephen Dobson, and an anonymous reviewer for constructive feedback on earlier versions of the manuscript.

Ethical standards

The research was conducted in compliance with US regulations, under research protocol ARC no. 2001-191-01, approved by the University of California at Los Angeles Animal Research Committee on 13 May 2002 and renewed annually. Live animals were trapped under permits issued by the Colorado Division of Wildlife.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Tina W. Wey.

Additional information

Communicated by G. Wilkinson

Appendices

Appendix 1

Table 7

Table 7 Correlations among network measures

Appendix 2

Table 8 Correlations among social factors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Wey, T.W., Blumstein, D.T. 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 (2012). https://doi.org/10.1007/s00265-012-1358-8

Download citation

Keywords

  • Affiliation
  • Agonism
  • Social behavior
  • Performance measures
  • Animal social networks