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

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.

[1]  D. V. Vuren,et al.  A 32-year demography of yellow-bellied marmots (Marmota flaviventris) , 1998 .

[2]  Isabelle M. Côté,et al.  Parasitism and group size in social animals: a meta-analysis , 1995 .

[3]  S. Creel,et al.  Social dominance and stress hormones , 2001 .

[4]  Sean F. Hanser,et al.  Social network theory: new insights and issues for behavioral ecologists , 2009, Behavioral Ecology and Sociobiology.

[5]  R S Morris,et al.  Social-network analysis of Mycobacterium bovis transmission among captive brushtail possums (Trichosurus vulpecula). , 2003, Preventive veterinary medicine.

[6]  D. Blumstein,et al.  Faecal glucocorticoid metabolites and alarm calling in free-living yellow-bellied marmots , 2006, Biology Letters.

[7]  R. A. Hinde,et al.  Interactions, Relationships and Social Structure , 1976 .

[8]  R. R. Krausz.  Living in Groups , 2013 .

[9]  Peter Amunga Mbati.  Parasites and the Behavior of Animals , 2002 .

[10]  R. E. Butterfield,et al.  Fitness consequences of social network position in a wild population of forked fungus beetles (Bolitotherus cornutus) , 2012, Journal of evolutionary biology.

[11]  Tina W. Wey,et al.  Social network analysis of animal behaviour: a promising tool for the study of sociality , 2008, Animal Behaviour.

[12]  K. Armitage.  Reproductive Strategies of Yellow-Bellied Marmots: Energy Conservation and Differences between the Sexes , 1998 .

[13]  J. Millspaugh,et al.  Use of fecal glucocorticoid metabolite measures in conservation biology research: considerations for application and interpretation. , 2004, General and comparative endocrinology.

[14]  K. Armitage.  Factors affecting corticosteroid concentrations in yellow-bellied marmots. , 1991, Comparative biochemistry and physiology. A, Comparative physiology.

[15]  A. Devries,et al.  Social modulation of stress responses , 2003, Physiology & Behavior.

[16]  D. McDonald,et al.  Predicting fate from early connectivity in a social network , 2007, Proceedings of the National Academy of Sciences.

[17]  N. Nelson,et al.  Social network structure and parasite infection patterns in a territorial reptile, the tuatara (Sphenodon punctatus). , 2010, International journal for parasitology.

[18]  J. House,et al.  Social relationships and health. , 1988, Science.

[19]  D. V. Vuren.  Ectoparasites, Fitness, and Social Behaviour of Yellow‐Bellied Marmots , 2010 .

[20]  Samuel R. Friedman,et al.  Social networks, risk-potential networks, health, and disease , 2001, Journal of Urban Health.

[21]  M. Newman.  Analysis of weighted networks. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[22]  D.,et al.  THE EVOLUTION OF SOCIAL BEHAVIOR , 2002 .

[23]  Bette A. Loiselle,et al.  Social networks in the lek-mating wire-tailed manakin (Pipra filicauda) , 2008, Proceedings of the Royal Society B: Biological Sciences.

[24]  J. Krause,et al.  Exploring Animal Social Networks , 2008 .

[25]  D. Blumstein,et al.  Rodent sociality and parasite diversity , 2007, Biology Letters.

[26]  Julian A. Drewe,et al.  The social network structure of a wild meerkat population: 2. Intragroup interactions , 2009, Behavioral Ecology and Sociobiology.

[27]  Tina W. Wey,et al.  Correlates and Consequences of Dominance in a Social Rodent , 2011 .

[28]  L. Freeman.  Centrality in social networks conceptual clarification , 1978 .

[29]  D. Blumstein,et al.  Applying the coalitionary-traits metric: sociality without cooperation in male yellow-bellied marmots , 2010 .

[30]  R. Sapolsky.  Social Status and Health in Humans and Other Animals , 2004 .

[31]  Richard James,et al.  Network structure and parasite transmission in a group living lizard, the gidgee skink, Egernia stokesii , 2009, Behavioral Ecology and Sociobiology.

[32]  K. Armitage.  SOCIAL AND POPULATION DYNAMICS OF YELLOW-BELLIED MARMOTS: Results from Long-Term Research , 1991 .

[33]  Stanley Wasserman,et al.  Social Network Analysis: Methods and Applications , 1994, Structural analysis in the social sciences.

[34]  M. V. Price,et al.  The ecology of place : contributions of place-based research to ecological understanding , 2010 .

[35]  Jeanne Altmann,et al.  Social Bonds of Female Baboons Enhance Infant Survival , 2003, Science.

[36]  Z. Penke,et al.  Postconflict Affiliation and Stress-Related Behavior of Long-Tailed Macaque Aggressors , 1998, International Journal of Primatology.

[37]  R. Boonstra,et al.  Measuring stress in wildlife: techniques for quantifying glucocorticoids , 2011, Oecologia.

[38]  M. Keeling,et al.  Networks and epidemic models , 2005, Journal of The Royal Society Interface.

[39]  R. Shine.  Ecological Causes for the Evolution of Sexual Dimorphism: A Review of the Evidence , 1989, The Quarterly Review of Biology.

[40]  Daniel T Blumstein,et al.  A test of the social cohesion hypothesis: interactive female marmots remain at home , 2009, Proceedings of the Royal Society B: Biological Sciences.

[41]  A. Vespignani,et al.  The architecture of complex weighted networks. , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[42]  D. Krakauer,et al.  Policing stabilizes construction of social niches in primates , 2006, Nature.

[43]  J. Cacioppo,et al.  The relationship between social support and physiological processes: a review with emphasis on underlying mechanisms and implications for health. , 1996, Psychological bulletin.

[44]  Amanda J Lea,et al.  Heritable victimization and the benefits of agonistic relationships , 2010, Proceedings of the National Academy of Sciences.

[45]  W. Montgomery,et al.  Body mass and sex-biased parasitism in wood mice Apodemus sylvaticus , 2010 .

[46]  Elissa Z Cameron,et al.  Social bonds between unrelated females increase reproductive success in feral horses , 2009, Proceedings of the National Academy of Sciences.

[47]  T. Kaur,et al.  FECAL GLUCOCORTICOIDS AND THEIR METABOLITES AS INDICATORS OF STRESS IN VARIOUS MAMMALIAN SPECIES: A LITERATURE REVIEW , 2006, Journal of zoo and wildlife medicine : official publication of the American Association of Zoo Veterinarians.

[48]  Kay E. Holekamp,et al.  Patterns of alliance formation and postconflict aggression indicate spotted hyaenas recognize third-party relationships , 2005, Animal Behaviour.

[49]  S. Manuck,et al.  Chronic Social Stress, Affiliation, and Cellular Immune Response in Nonhuman Primates , 1992 .

[50]  J. Silk,et al.  The benefits of social capital: close social bonds among female baboons enhance offspring survival , 2009, Proceedings of the Royal Society B: Biological Sciences.

[51]  Nigel C. Bennett,et al.  Stress and the suppression of subordinate reproduction in cooperatively breeding meerkats , 2006, Proceedings of the National Academy of Sciences.

[52]  David Lusseau,et al.  Incorporating uncertainty into the study of animal social networks , 2008, Animal Behaviour.

[53]  Daniel T. Blumstein,et al.  Social cohesion in yellow-bellied marmots is established through age and kin structuring , 2010, Animal Behaviour.

[54]  Alessandro Vespignani,et al.  Characterization and modeling of weighted networks , 2005 .

[55]  Mary Poss,et al.  Social Organization and Parasite Risk in Mammals: Integrating Theory and Empirical Studies , 2003 .

[56]  D. Blumstein,et al.  Heritability of anti‐predatory traits: vigilance and locomotor performance in marmots , 2010, Journal of evolutionary biology.

[57]  David Lusseau,et al.  Formalising the multidimensional nature of social networks , 2011, ArXiv.

[58]  Peter K. McGregor,et al.  Analyzing Animal Societies: Quantitative Methods for Vertebrate Social Analysis , 2009 .

[59]  R. Seyfarth,et al.  Social relationships and social cognition in nonhuman primates. , 1986, Science.

[60]  D. R. White,et al.  Structural cohesion and embeddedness: A hierarchical concept of social groups , 2003 .

[61]  Arpat Ozgul,et al.  Coupled dynamics of body mass and population growth in response to environmental change , 2010, Nature.

[62]  Charles L. Nunn,et al.  Infectious Diseases in Primates , 2006 .