Mechanisms of network evolution: a focus on socioecological factors, intermediary mechanisms, and selection pressures

Abstract

Since group-living animals are embedded in a network of social interactions, socioecological factors may not only affect individual behavioral strategies but also the patterning of group-level social interactions, i.e., the network structure. These co-variations between socioecological factors, individual behavior, and group-level structure are important to study since ecological factors may strongly influence animal health outcomes and reproductive success. Besides factors such as social information and/or infectious agents, with far-reaching individual fitness consequences, seem independent of individuals’ own social interactions but directly affected by the topology of the social network. This paper reviews how socio-ecological pressures, i.e., causal factors (food distribution, predation, and infectious agent risk), via intermediary mechanisms (stress, information sharing, and mating system), may affect individual social behavior and consequently, social network topology. We also discuss how evolutionary driving forces, genetic (i.e., genes) and cultural (i.e., learned behavior) selection, may result in a specific composition of individuals’ social strategies that produce network topologies that might be optimized to specific socio-ecological conditions. We conclude that studies focusing on whether and how well networks resist changing conditions might provide a better understanding of the rules underlying individual behavior, which in turn influences network topology—a process we have called network evolution. Evolutionary processes may favor a group phenotypic composition, thus a network topology. This has been referred to as a “collective social niche construction”.

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References

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

    Article  Google Scholar 

  2. Allen B, Lippner G, Chen Y-T et al (2017) Evolutionary dynamics on any population structure. Nat Adv Online Publ. https://doi.org/10.1038/nature21723

    Article  Google Scholar 

  3. Amoroso CR, Frink AG, Nunn CL (2017) Water choice as a counterstrategy to faecally transmitted disease: an experimental study in captive lemurs. Behaviour 154:1239–1258

    Article  Google Scholar 

  4. Aplin LM, Farine DR, Morand-Ferron J, Sheldon BC (2012) Social networks predict patch discovery in a wild population of songbirds. In: Proceedings of the Royal Society of London B: Biological Sciences, rspb20121591

  5. Aplin LM, Farine D, Morand-Ferron J et al (2013) Individual personalities predict social behaviour in wild networks of great tits (Parus major). Ecol Lett 16:1365–1372

    Article  CAS  PubMed  Google Scholar 

  6. Aplin LM, Farine DR, Morand-Ferron J et al (2015) Experimentally induced innovations lead to persistent culture via conformity in wild birds. Nature 518:538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Arathi HS, Burns I, Spivak M (2000) Ethology of hygienic behaviour in the honey bee Apis mellifera L. (Hymenoptera: Apidae): behavioural repertoire of hygienic bees. Ethology 106:365–379. https://doi.org/10.1046/j.1439-0310.2000.00556.x

    Article  Google Scholar 

  8. Balasubramaniam K, Dittmar K, Berman CM et al (2012a) Hierarchical steepness and phylogenetic models: phylogenetic signals in Macaca. Anim Behav 83:1207–1218

    Article  Google Scholar 

  9. Balasubramaniam KN, Dittmar K, Berman CM et al (2012b) Hierarchical steepness, counter-aggression, and macaque social style scale. Am J Primatol 74:915–925. https://doi.org/10.1002/ajp.22044

    Article  PubMed  Google Scholar 

  10. Barr CS, Newman TK, Shannon C et al (2004) Rearing condition and rh5-HTTLPR interact to influence limbic-hypothalamic-pituitary-adrenal axis response to stress in infant macaques. Biol Psychiatry 55:733–738

    Article  CAS  PubMed  Google Scholar 

  11. Battesti M, Pasquaretta C, Moreno C et al (2015) Ecology of information: social transmission dynamics within groups of non-social insects. Proc R Soc Lond B Biol Sci 282:20142480. https://doi.org/10.1098/rspb.2014.2480

    Article  Google Scholar 

  12. Berman CM, Thierry B (2010) Variation in kin bias: species differences and time constraints in macaques. Behaviour 147:1863–1887

    Article  Google Scholar 

  13. Bijma P (2011) A general definition of the heritable variation that determines the potential of a population to respond to selection. Genetics 189:1347–1359

    Article  PubMed  PubMed Central  Google Scholar 

  14. Bijma P, Wade M (2008) The joint effects of kin, multilevel selection and indirect genetic effects on response to genetic selection. J Evol Biol 21:1175–1188

    Article  CAS  PubMed  Google Scholar 

  15. Bissonnette A, Franz M, Schülke O, Ostner J (2014) Socioecology, but not cognition, predicts male coalitions across primates. Behav Ecol 25:794–801. https://doi.org/10.1093/beheco/aru054

    Article  Google Scholar 

  16. Blomberg SP, Garland T (2002) Tempo and mode in evolution: phylogenetic inertia, adaptation and comparative methods. J Evol Biol 15:899–910

    Article  Google Scholar 

  17. Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745. https://doi.org/10.1111/j.0014-3820.2003.tb00285.x

    Article  Google Scholar 

  18. Bolt SL, Boyland NK, Mlynski DT et al (2017) Pair housing of dairy calves and age at pairing: effects on weaning stress, health, production and social networks. PLoS ONE 12:e0166926

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Borgeaud C, Sosa S, Bshary R et al (2016) Intergroup variation of social relationships in wild vervet monkeys: a dynamic network approach. Front Psychol 7:915. https://doi.org/10.3389/fpsyg.2016.00915

    Article  PubMed  PubMed Central  Google Scholar 

  20. Borgeaud C, Sosa S, Sueur C, Bshary R (2017) The influence of demographic variation on social network stability in wild vervet monkeys. Anim Behav 134:155–165. https://doi.org/10.1016/j.anbehav.2017.09.028

    Article  Google Scholar 

  21. Brent LJ, Heilbronner SR, Horvath JE, Gonzalez-Martinez J, Ruiz-Lambides A, Robinson AG et al. (2013) Genetic origins of social networks in rhesus macaques. Sci Rep 3:1042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Bryden J, Funk S, Geard N et al (2011) Stability in flux: community structure in dynamic networks. J R Soc Interface 8:1031–1040

    Article  PubMed  Google Scholar 

  23. Burk WJ, Steglich CE, Snijders TA (2007) Beyond dyadic interdependence: actor-oriented models for co-evolving social networks and individual behaviors. Int J Behav Dev 31:397–404

    Article  Google Scholar 

  24. Byrne RW, Whiten A, Henzi P (1990) Social relationships of mountain baboons—leadership and affiliation in a non-female-bonded monkey. Am J Primatol 20:313–329

    Article  Google Scholar 

  25. Caillaud D, Levrero F, Cristescu R et al (2006) Gorilla susceptibility to Ebola virus: the cost of sociality. Curr Biol 16:R489–R491

    Article  CAS  PubMed  Google Scholar 

  26. Camazine S, Deneubourg J-L, Franks NR et al. (2003) Self-organization in biological systems. Princeton University Press, Princeton, US

    Google Scholar 

  27. Cantor M, Whitehead H (2013) The interplay between social networks and culture: theoretically and among whales and dolphins. Phil Trans R Soc B 368:20120340

    Article  PubMed  Google Scholar 

  28. Cantor M, Shoemaker LG, Cabral RB et al (2015) Multilevel animal societies can emerge from cultural transmission. Nat Commun 6:8091

    Article  PubMed  PubMed Central  Google Scholar 

  29. Chapais B (1988) Experimental matrilineal inheritance of rank in female Japanese macaques. Anim Behav 36:1025–1037

    Article  Google Scholar 

  30. Charpentier MJE, Givalois L, Faurie C et al (2017) Seasonal glucocorticoid production correlates with a suite of small-magnitude environmental, demographic, and physiological effects in mandrills. Am J Phys Anthropol 165:20–33. https://doi.org/10.1002/ajpa.23329

    Article  PubMed  Google Scholar 

  31. Cheney DL, Seyfarth RM (2009) Stress and coping mechanisms in female primates. Adv Study Behav 39:1–44

    Article  Google Scholar 

  32. Cialdini RB, Goldstein NJ (2004) Social influence: compliance and conformity. Annu Rev Psychol 55:591–621

    Article  PubMed  Google Scholar 

  33. Claidière N, Messer EJE, Hoppitt W, Whiten A (2013) Diffusion dynamics of socially learned foraging techniques in squirrel monkeys. Curr Biol 23:1251–1255. https://doi.org/10.1016/j.cub.2013.05.036

    CAS  Article  PubMed  Google Scholar 

  34. Clutton-Brock T (2002) Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296:69–72

    Article  CAS  Google Scholar 

  35. Cremer S, Armitage SAO, Schmid-Hempel P (2007) Social Immunity. Curr Biol 17:R693–R702. https://doi.org/10.1016/j.cub.2007.06.008

    CAS  Article  PubMed  Google Scholar 

  36. Croft D, James R, Thomas P et al (2006) Social structure and co-operative interactions in a wild population of guppies (Poecilia reticulata). Behav Ecol Sociobiol 59:644–650

    Article  Google Scholar 

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

    Google Scholar 

  38. Croft DP, Krause J, Darden SK et al (2009) Behavioural trait assortment in a social network: patterns and implications. Behav Ecol Sociobiol 63:1495–1503

    Article  Google Scholar 

  39. Crook JH, Gartlan JS (1966) Evolution of primate societies. Nature 210:1200–1203

    Article  CAS  PubMed  Google Scholar 

  40. Dall SRX, Giraldeau L-A, Olsson O et al (2005) Information and its use by animals in evolutionary ecology. Trends Ecol Evol 20:187–193. https://doi.org/10.1016/j.tree.2005.01.010

    Article  PubMed  PubMed Central  Google Scholar 

  41. Dawkins R (2006) The selfish gene: 30th anniversary edition. Oxford University Press, Oxford, UK

    Google Scholar 

  42. de Waal FBM, Johanowicz DL (1993) Modification of reconciliation behavior through social experience: an experiment with two Macaque species. Child Dev 64:897–908. https://doi.org/10.1111/j.1467-8624.1993.tb02950.x

    Article  PubMed  Google Scholar 

  43. De Wilde TR, Ten Velden FS, De Dreu CK (2017) The neuropeptide oxytocin enhances information sharing and group decision making quality. Sci Rep 7:40622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Delm MM (1990) Vigilance for predators: detection and dilution effects. Behav Ecol Sociobiol 26:337–342

    Article  Google Scholar 

  45. Dickman AJ (2012) From cheetahs to chimpanzees: a comparative review of the drivers of human-carnivore conflict and human-primate conflict. Folia Primatol (Basel) 83:377–387

    Article  Google Scholar 

  46. Dindo M, Whiten A, de Waal FBM (2009) In-group conformity sustains different foraging traditions in Capuchin monkeys (Cebus apella). PLoS One 4:e7858. https://doi.org/10.1371/journal.pone.0007858

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. Dingemanse NJ, Kazem AJ, Réale D, Wright J (2010) Behavioural reaction norms: animal personality meets individual plasticity. Trends Ecol Evol 25:81–89

    Article  PubMed  Google Scholar 

  48. Domingue BW, Belsky DW, Fletcher JM et al (2018) The social genome of friends and schoolmates in the national longitudinal study of adolescent to adult health. Proc Natl Acad Sci 115:702–707. https://doi.org/10.1073/pnas.1711803115

    CAS  Article  PubMed  Google Scholar 

  49. Donaldson R, Finn H, Bejder L et al (2012) The social side of human-wildlife interaction: wildlife can learn harmful behaviours from each other. Anim Conserv 15:427–435

    Article  Google Scholar 

  50. Duboscq J, Romano V, MacIntosh A, Sueur C (2016) Social information transmission in animals: lessons from studies of diffusion. Front Psychol 7:1147

    Article  PubMed  PubMed Central  Google Scholar 

  51. Eldakar OT, Dlugos MJ, Wilcox RS, Wilson DS (2009) Aggressive mating as a tragedy of the commons in the water strider Aquarius remigis. Behav Ecol Sociobiol 64:25

    Article  Google Scholar 

  52. Farine DR, Montiglio P-O, Spiegel O (2015) From individuals to groups and back: the evolutionary implications of group phenotypic composition. Trends Ecol Evol 30:609–621

    Article  PubMed  PubMed Central  Google Scholar 

  53. Fincher CL, Thornhill R (2012) Parasite-stress promotes in-group assortative sociality: the cases of strong family ties and heightened religiosity. Behav Brain Sci 35:61–79. https://doi.org/10.1017/S0140525X11000021

    Article  PubMed  Google Scholar 

  54. Firth JA, Sheldon BC, Brent LJN (2017) Indirectly connected: simple social differences can explain the causes and apparent consequences of complex social network positions. Proc R Soc B 284:20171939. https://doi.org/10.1098/rspb.2017.1939

    Article  PubMed  Google Scholar 

  55. Fisher DN, McAdam AG (2017) Social traits, social networks and evolutionary biology. J Evol Biol n/a-n/a. https://doi.org/10.1111/jeb.13195

    Article  Google Scholar 

  56. Fisher DN, Rodríguez-Muñoz R, Tregenza T (2016) Wild cricket social networks show stability across generations. BMC Evol Biol 16:151

    Article  PubMed  PubMed Central  Google Scholar 

  57. Flack JC, Girvan M, de Waal FBM, Krakauer DC (2006) Policing stabilizes construction of social niches in primates. Nature 439:426–429. https://doi.org/10.1038/nature04326

    CAS  Article  PubMed  Google Scholar 

  58. Foster W, Treherne J (1981) Evidence for the dilution effect in the selfish herd from fish predation on a marine insect. Nature 293:466

    Article  Google Scholar 

  59. Foster EA, Franks DW, Morrell LJ et al (2012) Social network correlates of food availability in an endangered population of killer whales, Orcinus orca. Anim Behav 83:731–736. https://doi.org/10.1016/j.anbehav.2011.12.021

    Article  Google Scholar 

  60. Fowler JH, Dawes CT, Christakis NA (2009) Model of genetic variation in human social networks. Proc Natl Acad Sci 106:1720–1724. https://doi.org/10.1073/pnas.0806746106

    Article  PubMed  Google Scholar 

  61. Frank SA (2007) All of life is social. Curr Biol 17:R648–R650

    Article  CAS  PubMed  Google Scholar 

  62. Fruteau C, Voelkl B, Van Damme E, Noë R (2009) Supply and demand determine the market value of food providers in wild vervet monkeys. In: Proceedings of the National Academy of Sciences, pnas- 0812280106

  63. Fury CA, Ruckstuhl KE, Harrison PL (2013) Spatial and social sexual segregation patterns in Indo-Pacific Bottlenose Dolphins (Tursiops aduncus). PLoS One 8:e52987. https://doi.org/10.1371/journal.pone.0052987

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  64. Galef BG, Whiskin EE (2008) ‘Conformity’ in Norway rats? Anim Behav 75:2035–2039. https://doi.org/10.1016/j.anbehav.2007.11.012

    Article  Google Scholar 

  65. Goodall J (1986) Social rejection, exclusion, and shunning among the Gombe chimpanzees. Ethol Sociobiol 7:227–236

    Article  Google Scholar 

  66. Granovetter MS (1973) The strength of weak ties. Am J Sociol 78:1360–1380. https://doi.org/10.1086/225469

    Article  Google Scholar 

  67. Griffin AS (2004) Social learning about predators: a review and prospectus. Anim Learn Behav 32:131–140. https://doi.org/10.3758/BF03196014

    CAS  Article  Google Scholar 

  68. Griffin RH, Nunn CL (2012) Community structure and the spread of infectious disease in primate social networks. Evol Ecol 26:779–800. https://doi.org/10.1007/s10682-011-9526-2

    Article  Google Scholar 

  69. Hamilton WD (1971) Geometry for the selfish herd. J Theor Biol 31:295–311. https://doi.org/10.1016/0022-5193(71)90189-5

    CAS  Article  PubMed  Google Scholar 

  70. Hariri AR, Mattay VS, Tessitore A et al (2002) Serotonin transporter genetic variation and the response of the human amygdala. Science 297:400–403

    Article  CAS  PubMed  Google Scholar 

  71. Hartwell KS, Notman H, Bonenfant C, Pavelka MSM (2014) Assessing the occurrence of sexual segregation in Spider monkeys (Ateles geoffroyi yucatanensis), its mechanisms and function. Int J Primatol 35:425–444. https://doi.org/10.1007/s10764-013-9746-0

    Article  Google Scholar 

  72. Heathcote RJP, Darden SK, Franks DW et al (2017) Fear of predation drives stable and differentiated social relationships in guppies. Sci Rep 7:41679. https://doi.org/10.1038/srep41679

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  73. Henrich J, Boyd R (1998) The evolution of conformist transmission and the emergence of between-group differences. Evol Hum Behav 19:215–241. https://doi.org/10.1016/S1090-5138(98)00018-X

    Article  Google Scholar 

  74. Henrich J, Gil-White FJ (2001) The evolution of prestige: freely conferred deference as a mechanism for enhancing the benefits of cultural transmission. Evol Hum Behav 22:165–196

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  76. Hockings KJ (2009) Living at the interface: human–chimpanzee competition, coexistence and conflict in Africa. Interact Stud 10:183–205

    Article  Google Scholar 

  77. Hoppitt WJE, Brown GR, Kendal R et al (2008) Lessons from animal teaching. Trends Ecol Evol 23:486–493. https://doi.org/10.1016/j.tree.2008.05.008

    Article  PubMed  Google Scholar 

  78. Nakamura M, Hosaka K, Itoh N, Zamma K (eds) (2015) Mahale chimpanzees: 50 years of research. Cambridge University Press, UK

    Google Scholar 

  79. Huffman MA (2016) primate self-medication, passive prevention and active treatment-A brief review. Int J Multidiscip Stud 3(2):1–10

    Article  Google Scholar 

  80. Hung AA, Plott CR (2001) Information cascades: replication and an extension to majority rule and conformity-rewarding institutions. Am Econ Rev 91:1508–1520

    Article  Google Scholar 

  81. Ilany A, Booms AS, Holekamp KE (2015) Topological effects of network structure on long-term social network dynamics in a wild mammal. Ecol Lett 18:687–695. https://doi.org/10.1111/ele.12447

    Article  PubMed  PubMed Central  Google Scholar 

  82. Isbell LA, Young TP (2002) Ecological models of female social relationships in primates: similarities, disparities, and some directions for future clarity. Behaviour 139:177–202

    Article  Google Scholar 

  83. Janson CH, Goldsmith ML (1995) Predicting group size in primates: foraging costs and predation risks. Behav Ecol 6:326–336. https://doi.org/10.1093/beheco/6.3.326

    Article  Google Scholar 

  84. Kamilar JM, Cooper N (2013) Phylogenetic signal in primate behaviour, ecology and life history. Phil Trans R Soc B 368:20120341

    Article  PubMed  Google Scholar 

  85. Kanngiesser P, Sueur C, Riedl K et al (2011) Grooming network cohesion and the role of individuals in a captive chimpanzee group. Am J Primatol 73:758–767. https://doi.org/10.1002/ajp.20914

    Article  PubMed  Google Scholar 

  86. Kappeler PM, van Schaik CP (2002) Evolution of primate social systems. Int J Primatol 23:707–740. https://doi.org/10.1023/A:1015520830318

    Article  Google Scholar 

  87. Kavaliers M, Colwell DD (1995) Discrimination by female mice between the odours of parasitized and non-parasitized males. Proc R Soc Lond B Biol Sci 261:31–35

    Article  CAS  Google Scholar 

  88. Kelley JL, Morrell LJ, Inskip C et al (2011) Predation risk shapes social networks in fission–fusion populations. PLoS One 6:e24280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. King AJ, Clark FE, Cowlishaw G (2011) The dining etiquette of desert baboons: the roles of social bonds, kinship, and dominance in co-feeding networks. Am J Primatol 73:768–774. https://doi.org/10.1002/ajp.20918

    Article  Google Scholar 

  90. King AJ, Wilson AM, Wilshin SD et al (2012) Selfish-herd behaviour of sheep under threat. Curr Biol 22:R561–R562. https://doi.org/10.1016/j.cub.2012.05.008

    CAS  Article  PubMed  Google Scholar 

  91. Kornienko O, Schaefer DR, Weren S et al (2016) Cortisol and testosterone associations with social network dynamics. Horm Behav. https://doi.org/10.1016/j.yhbeh.2016.01.013

    Article  PubMed  Google Scholar 

  92. Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, Oxford, UK

    Google Scholar 

  93. Kulahci IG, Ghazanfar AA, Rubenstein DI (2018) Knowledgeable lemurs become more central in social networks. Curr Biol 28:1306–1310

    Article  CAS  PubMed  Google Scholar 

  94. Leca J-B, Gunst N, Huffman MA (2007) Japanese macaque cultures: inter-and intra-troop behavioural variability of stone handling patterns across 10 troops. Behaviour 144:251–281

    Article  Google Scholar 

  95. Lesch K-P, Bengel D, Heils A et al (1996) Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 274:1527–1531

    Article  CAS  Google Scholar 

  96. Lihoreau M, Buhl J, Charleston MA et al (2015) Nutritional ecology beyond the individual: a conceptual framework for integrating nutrition and social interactions. Ecol Lett 18:273–286

    Article  PubMed  PubMed Central  Google Scholar 

  97. Lloyd-Smith JO, Schreiber SJ, Kopp PE, Getz WM (2005) Superspreading and the effect of individual variation on disease emergence. Nature 438:355–359

    Article  CAS  PubMed  Google Scholar 

  98. Lopes PC (2014) When is it socially acceptable to feel sick? Proc R Soc B Biol Sci 281(1788):20140218. https://doi.org/10.1098/rspb.2014.0218

    Article  Google Scholar 

  99. Mann J, Stanton MA, Patterson EM et al (2012) Social networks reveal cultural behaviour in tool-using dolphins. Nat Commun 3:980

    Article  CAS  PubMed  Google Scholar 

  100. Maransky BP, Bildstein KL (2001) Follow your elders: age-related differences in the migration behavior of broad-winged hawks at Hawk Mountain Sanctuary, Pennsylvania. Wilson Bull 113:350–353

    Article  Google Scholar 

  101. Massen JJ, Koski SE (2014) Chimps of a feather sit together: chimpanzee friendships are based on homophily in personality. Evol Hum Behav 35:1–8

    Article  Google Scholar 

  102. McCowan B, Beisner BA, Capitanio JP et al (2011) Network stability is a balancing act of personality, power, and conflict dynamics in Rhesus Macaque societies. PLoS One 6:e22350. https://doi.org/10.1371/journal.pone.0022350

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  103. McFarland R, Murphy D, Lusseau D et al (2017) The ‘strength of weak ties’ among female baboons: fitness-related benefits of social bonds. Anim Behav 126:101–106

    Article  Google Scholar 

  104. McPherson M, Smith-Lovin L, Cook JM (2001) Birds of a feather: homophily in social networks. Annu Rev Sociol 27:415–444

    Article  Google Scholar 

  105. Migliano AB, Page AE, Gómez-Gardeñes J et al (2017) Characterization of hunter-gatherer networks and implications for cumulative culture. Nat Hum Behav 1:0043. https://doi.org/10.1038/s41562-016-0043

    Article  Google Scholar 

  106. Montiglio PO, McGlothlin JW, Farine DR (2018) Social structure modulates the evolutionary consequences of social plasticity: a social network perspective on interacting phenotypes. Ecol Evol 8(3):1451–1464

    Article  PubMed  Google Scholar 

  107. Morgan TJH, Laland KN (2012) The biological bases of conformity. Front Neurosci 6:87

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Morrell LJ, Croft DP, Dyer JRG et al (2008) Association patterns and foraging behaviour in natural and artificial guppy shoals. Anim Behav 76:855–864. https://doi.org/10.1016/j.anbehav.2008.02.015

    Article  Google Scholar 

  109. Moyers SC, Adelman JS, Farine DR et al (2018) Exploratory behavior is linked to stress physiology and social network centrality in free-living house finches (Haemorhous mexicanus). Horm Behav 102:105–113

    Article  PubMed  Google Scholar 

  110. Muehlenbein MP, Watts DP (2010) The costs of dominance: testosterone, cortisol and intestinal parasites in wild male chimpanzees. Biopsychosoc Med 4:21. https://doi.org/10.1186/1751-0759-4-21

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  111. Muthukrishna M, Henrich J (2016) Innovation in the collective brain. Phil Trans R Soc B 371:20150192

    Article  PubMed  Google Scholar 

  112. Nahallage CAD, Huffman MA (2007) Acquisition and development of stone handling behavior in infant Japanese macaques. Behaviour 144:1193–1215. https://doi.org/10.1163/156853907781890959

    Article  Google Scholar 

  113. Napper CJ, Hatchwell BJ (2016) Social dynamics in nonbreeding flocks of a cooperatively breeding bird: causes and consequences of kin associations. Anim Behav 122:23–35. https://doi.org/10.1016/j.anbehav.2016.09.008

    Article  Google Scholar 

  114. Naug D (2009) Structure and resilience of the social network in an insect colony as a function of colony size. Behav Ecol Sociobiol 63:1023–1028. https://doi.org/10.1007/s00265-009-0721-x

    Article  Google Scholar 

  115. Naug D, Smith B (2007) Experimentally induced change in infectious period affects transmission dynamics in a social group. Proc R Soc Lond B Biol Sci 274:61–65

    Article  Google Scholar 

  116. Newman ME (2002) Assortative mixing in networks. Phys Rev Lett 89:208701

    Article  CAS  PubMed  Google Scholar 

  117. Noë R, Hammerstein P (1995) Biological markets. Trends Ecol Evol 10:336–339. https://doi.org/10.1016/S0169-5347(00)89123-5

    Article  PubMed  Google Scholar 

  118. Nonacs P, Kapheim KM (2007) Social heterosis and the maintenance of genetic diversity. J Evol Biol 20:2253–2265. https://doi.org/10.1111/j.1420-9101.2007.01418.x

    CAS  Article  PubMed  Google Scholar 

  119. Nunn C, Altizer SM (2006) Infectious diseases in primates: behavior, ecology and evolution. Oxford University Press, Oxford, UK

    Google Scholar 

  120. Nunn CL, Jordán F, McCabe CM et al (2015) Infectious disease and group size: more than just a numbers game. Phil Trans R Soc B 370:20140111. https://doi.org/10.1098/rstb.2014.0111

    Article  PubMed  Google Scholar 

  121. Ohtsuki H, Hauert C, Lieberman E, Nowak MA (2006) A simple rule for the evolution of cooperation on graphs and social networks. Nature 441:502–505. https://doi.org/10.1038/nature04605

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  122. Page AE, Chaudhary N, Viguier S et al (2017) Hunter-gatherer social networks and reproductive success. Sci Rep 7:1153. https://doi.org/10.1038/s41598-017-01310-5

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  123. Pasquaretta C, Levé M, Claidière N et al (2014) Social networks in primates: smart and tolerant species have more efficient networks. Sci Rep 4:7600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Pasquaretta C, Battesti M, Klenschi E et al (2016) How social network structure affects decision-making in Drosophila melanogaster. Proc R Soc B 283:20152954. https://doi.org/10.1098/rspb.2015.2954

    CAS  Article  PubMed  Google Scholar 

  125. Paterson JD, Wallis J (2005) Commensalism and conflict: the human-primate interface. American Society of Primatologists, Norman, Okla

    Google Scholar 

  126. Pearce E, Wlodarski R, Machin A, Dunbar RI (2017) Variation in the β-endorphin, oxytocin, and dopamine receptor genes is associated with different dimensions of human sociality. Proc Natl Acad Sci 114(20):5300–5305

    Article  CAS  PubMed  Google Scholar 

  127. Perrin N, Petit EJ, Menard N (2012) Social systems: demographic and genetic issues. Mol Ecol 21:443–446. https://doi.org/10.1111/j.1365-294X.2011.05404.x

    Article  PubMed  Google Scholar 

  128. Pike TW, Laland KN (2010) Conformist learning in nine-spined sticklebacks’ foraging decisions. Biol Lett 6:466–468. https://doi.org/10.1098/rsbl.2009.1014

    Article  PubMed  PubMed Central  Google Scholar 

  129. Poirotte C, Massol F, Herbert A et al (2017) Mandrills use olfaction to socially avoid parasitized conspecifics. Sci Adv 3:e1601721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Pruitt JN, Goodnight CJ (2014) Site-specific group selection drives locally adapted group compositions. Nature 514:359

    Article  CAS  PubMed  Google Scholar 

  131. Puga-Gonzalez I, Ostner J, Schülke O et al (2018) Mechanisms of reciprocity and diversity in social networks: a modeling and comparative approach. Behav Ecol 29:745–760

    Article  Google Scholar 

  132. Réale D, Dingemanse NJ, Kazem AJ, Wright J (2010) Evolutionary and ecological approaches to the study of personality. Philos Trans R Soc B Biol Sci 365:3937–3946

    Article  Google Scholar 

  133. Riley EP (2007) The human-macaque interface: conservation implications of current and future overlap and conflict in Lore Lindu National Park, Sulawesi, Indonesia. Am Anthropol 109:473–484

    Article  Google Scholar 

  134. Romano V, Duboscq J, Sarabian C et al (2016) Modeling infection transmission in primate networks to predict centrality-based risk. Am J Primatol 78:767–779. https://doi.org/10.1002/ajp.22542

    Article  PubMed  Google Scholar 

  135. Romano V, Shen M, Pansanel J, MacIntosh AJJ, Sueur C (2018) Social transmission in networks: global efficiency peaks with intermediate levels of modularity. Behav Ecol Sociobiol 72:154. https://doi.org/10.1007/s00265-018-2564-9

    Article  Google Scholar 

  136. Rommeck I, Capitanio JP, Strand SC, McCowan B (2011) Early social experience affects behavioral and physiological responsiveness to stressful conditions in infant rhesus macaques (Macaca mulatta). Am J Primatol 73:692–701

    Article  PubMed  PubMed Central  Google Scholar 

  137. Rosengaus RB, Traniello JF (2001) Disease susceptibility and the adaptive nature of colony demography in the dampwood termite Zootermopsis angusticollis. Behav Ecol Sociobiol 50:546–556. https://doi.org/10.1007/s002650100394

    Article  Google Scholar 

  138. Rushmore J, Caillaud D, Matamba L et al (2013) Social network analysis of wild chimpanzees provides insights for predicting infectious disease risk. J Anim Ecol 82:976–986. https://doi.org/10.1111/1365-2656.12088

    Article  PubMed  Google Scholar 

  139. Sah P, Leu ST, Cross PC, et al (2017) Unraveling the disease consequences and mechanisms of modular structure in animal social networks. Proc Natl Acad Sci 114(16):4165–4170

    Article  CAS  PubMed  Google Scholar 

  140. Saltz JB (2011) Natural genetic variation in social environment choice: context-dependent gene-environment correlation in Drosophila melanogaster. Evolution 65:2325–2334

    Article  PubMed  Google Scholar 

  141. Saltz JB, Foley BR (2011) Natural genetic variation in social niche construction: social effects of aggression drive disruptive sexual selection in Drosophila melanogaster. Am Nat 177:645–654

    Article  PubMed  Google Scholar 

  142. Santostefano F, Wilson AJ, Araya-Ajoy YG, Dingemanse NJ (2016) Interacting with the enemy: indirect effects of personality on conspecific aggression in crickets. Behav Ecol 27:1235–1246

    Article  Google Scholar 

  143. Sarabian C, MacIntosh AJ (2015) Hygienic tendencies correlate with low geohelminth infection in free-ranging macaques. Biol Lett 11:20150757

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Sarabian C, MacIntosh AJ (2016) Revulsion in chimpanzees: health maintenance through avoidance of biological contaminants. PeerJ (Preprints)

  145. Sauro MD, Jorgensen RS, Teal Pedlow C (2003) Stress, glucocorticoids, and memory: a meta-analytic review. Stress 6:235–245

    Article  CAS  PubMed  Google Scholar 

  146. Van Schaik CP, Van Hooff JARAM (1983) On the ultimate causes of primate social systems. Behaviour 85(1):91–117

    Article  Google Scholar 

  147. Schaik CPV, Kappeler PM (1997) Infanticide risk and the evolution of male–female association in primates. Proc R Soc Lond B Biol Sci 264:1687–1694. https://doi.org/10.1098/rspb.1997.0234

    Article  Google Scholar 

  148. Schülke O, Bhagavatula J, Vigilant L, Ostner J (2010) Social bonds enhance reproductive success in male macaques. Curr Biol 20:2207–2210. https://doi.org/10.1016/j.cub.2010.10.058

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  149. Seyfarth RM (1977) A model of social grooming among adult female monkeys. J Theor Biol 65:671–698

    Article  CAS  PubMed  Google Scholar 

  150. Shultz S, Opie C, Atkinson QD (2011) Stepwise evolution of stable sociality in primates. Nature 479:219–222

    Article  CAS  PubMed  Google Scholar 

  151. Silk JB, Alberts SC, Altmann J (2003) Social bonds of female baboons enhance infant survival. Science 302:1231–1234. https://doi.org/10.1126/science.1088580

    CAS  Article  PubMed  Google Scholar 

  152. Sirviö J, Riekkinen P, Jäkälä P, Riekkinen PJ (1994) Experimental studies on the role of serotonin in cognition. Prog Neurobiol 43:363–379

    Article  PubMed  Google Scholar 

  153. Skyrms B, Pemantle R (2009) A dynamic model of social network formation. Adaptive networks. Springer, Berlin, Germany, pp 231–251

    Google Scholar 

  154. Soltis J, Boyd R, Richerson PJ (1995) Can group-functional behaviors evolve by cultural group selection?: an empirical test. Curr Anthropol 36:473–494

    Article  Google Scholar 

  155. Southwick CH, Siddiqi MF (1994) Primate commensalism: the rhesus monkey in India. Société nationale de protection de la nature et d’acclimatation de France, Paris

    Google Scholar 

  156. Sparrowe RT, Liden RC, Wayne SJ, Kraimer ML (2001) Social networks and the performance of individuals and groups. Acad Manage J 44:316–325. https://doi.org/10.2307/3069458

    Article  Google Scholar 

  157. Sterck EHM, Watts DP, van Schaik CP (1997) The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291–309. https://doi.org/10.1007/s002650050390

    Article  Google Scholar 

  158. Street SE, Navarrete AF, Reader SM, Laland KN (2017) Coevolution of cultural intelligence, extended life history, sociality, and brain size in primates. Proc Natl Acad Sci 114:7908–7914

    Article  CAS  Google Scholar 

  159. Sueur C (2012) Social network, information flow and decision-making efficiency: a comparison of humans and animals. In: Social networking and community behavior modeling: qualitative and quantitative measures. IGI Global, Hershey, US, pp 164–177

    Google Scholar 

  160. Sueur C, Deneubourg J-L, Petit O, Couzin ID (2010) Differences in nutrient requirements imply a non-linear emergence of leaders in animal groups. PLoS Comput Biol 6:e1000917. https://doi.org/10.1371/journal.pcbi.1000917

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  161. Sueur C, King AJ, Conradt L et al (2011a) Collective decision-making and fission–fusion dynamics: a conceptual framework. Oikos 120:1608–1617. https://doi.org/10.1111/j.1600-0706.2011.19685.x

    Article  Google Scholar 

  162. Sueur C, Petit O, De Marco A et al (2011b) A comparative network analysis of social style in macaques. Anim Behav 82:845–852. https://doi.org/10.1016/j.anbehav.2011.07.020

    Article  Google Scholar 

  163. Sueur C, Deneubourg J-L, Petit O (2012) From social network (centralized vs. decentralized) to collective decision-making (unshared vs. shared consensus). PLoS One 7:e32566. https://doi.org/10.1371/journal.pone.0032566

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  164. Sueur C, King AJ, Pelé M, Petit O (2013) Fast and accurate decisions as a result of scale-free network properties in two primate species. In: Gilbert T, Kirkilionis M, Nicolis G (eds) Proceedings of the European Conference on Complex Systems 2012. Springer Proceedings in Complexity. Springer International Publishing, pp 579–584

    Google Scholar 

  165. Surbeck M, Deschner T, Weltring A, Hohmann G (2012) Social correlates of variation in urinary cortisol in wild male bonobos (Pan paniscus). Horm Behav 62:27–35. https://doi.org/10.1016/j.yhbeh.2012.04.013

    CAS  Article  PubMed  Google Scholar 

  166. Tanaka I (1995) Matrilineal distribution of louse egg-handling techniques during grooming in free-ranging Japanese macaques. Am J Phys Anthropol 98:197–201

    Article  CAS  PubMed  Google Scholar 

  167. Tavares SB, Samarra FIP, Miller PJO (2017) A multilevel society of herring-eating killer whales indicates adaptation to prey characteristics. Behav Ecol. https://doi.org/10.1093/beheco/arw179

    Article  Google Scholar 

  168. Thierry B, Iwaniuk AN, Pellis SM (2000) The Influence of phylogeny on the social behaviour of macaques (Primates: Cercopithecidae, genus Macaca). Ethology 106:713–728

    Article  Google Scholar 

  169. Thierry B, Singh M, Kaumanns W (2004) Macaque societies: a model for the study of social organization. Cambridge University Press, Cambridge, UK

    Google Scholar 

  170. Thierry B, Aureli F, Nunn CL, et al (2008) A comparative study of conflict resolution in macaques: insights into the nature of trait covariation. Anim Behav 75:847–860. https://doi.org/10.1016/j.anbehav.2007.07.006

    Article  Google Scholar 

  171. Thornhill R, Fincher CL, Aran D (2009) Parasites, democratization, and the liberalization of values across contemporary countries. Biol Rev 84:113–131. https://doi.org/10.1111/j.1469-185X.2008.00062.x

    Article  PubMed  Google Scholar 

  172. Tkaczynski P, MacLarnon A, Ross C (2014) Associations between spatial position, stress and anxiety in forest baboons Papio anubis. Behav Processes 108:1–6

    Article  PubMed  Google Scholar 

  173. Traulsen A, Nowak MA (2006) Evolution of cooperation by multilevel selection. Proc Natl Acad Sci 103:10952–10955. https://doi.org/10.1073/pnas.0602530103

    CAS  Article  PubMed  Google Scholar 

  174. van de Waal E, Borgeaud C, Whiten A (2013) Potent social learning and conformity shape a wild primate’s foraging decisions. Science 340:483–485

    Article  CAS  Google Scholar 

  175. van Hoof JA (2000) 16• Relationships among non-human primate males: a deductive framework. In: Primate males: Causes and consequences of variation in group composition. Cambridge University Press, Cambridge, UK, pp 183–191

    Google Scholar 

  176. van Schaik CP (1989) The ecology of social relationships amongst female primates. In: Standen V, Foley RA (eds) Comparative socioecology. Blackwell, Oxford, UK, pp 195–218

    Google Scholar 

  177. van Schaik CP, Isler K, Burkart JM (2012) Explaining brain size variation: from social to cultural brain. Trends Cogn Sci 16:277–284. https://doi.org/10.1016/j.tics.2012.04.004

    Article  PubMed  Google Scholar 

  178. VanderWaal KL, Obanda V, Omondi GP et al (2016) The “strength of weak ties” and helminth parasitism in giraffe social networks. Behav Ecol 27:1190–1197. https://doi.org/10.1093/beheco/arw035

    Article  Google Scholar 

  179. Verderane MP, Izar P, Visalberghi E, Fragaszy DM (2013) Socioecology of wild bearded capuchin monkeys (Sapajus libidinosus): an analysis of social relationships among female primates that use tools in feeding. Behaviour 150:659–689

    Article  Google Scholar 

  180. Viblanc VA, Pasquaretta C, Sueur C et al (2016) Aggression in Columbian ground squirrels: relationships with age, kinship, energy allocation, and fitness. Behav Ecol 27:1716–1725. https://doi.org/10.1093/beheco/arw098

    Article  Google Scholar 

  181. Watson KK, Ghodasra JH, Platt ML (2009) Serotonin transporter genotype modulates social reward and punishment in rhesus macaques. PLoS One 4:e4156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  182. Watson SK, Reamer LA, Mareno MC et al (2017) Socially transmitted diffusion of a novel behavior from subordinate chimpanzees. Am J Primatol n/a-n/a. https://doi.org/10.1002/ajp.22642

    Article  Google Scholar 

  183. Wei W, Qi X-G, Guo S-T et al (2012) Market powers predict reciprocal grooming in golden snub-nosed monkeys (Rhinopithecus roxellana). PLoS One 7:e36802. https://doi.org/10.1371/journal.pone.0036802

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  185. Whiten A (2018) Social dynamics: knowledgeable lemurs gain status. Curr Biol 28:R344–R346

    Article  CAS  PubMed  Google Scholar 

  186. Whiten A, Goodall J, McGrew WC et al (1999) Cultures in chimpanzees. Nature 399:682–685

    Article  CAS  Google Scholar 

  187. Whiten A, Horner V, de Waal FBM (2005) Conformity to cultural norms of tool use in chimpanzees. Nature 437:737–740. https://doi.org/10.1038/nature04047

    CAS  Article  PubMed  Google Scholar 

  188. Whiten A, Ayala FJ, Feldman MW, Laland KN (2017) The extension of biology through culture. Proc Natl Acad Sci 114:7775–7781. https://doi.org/10.1073/pnas.1707630114

    CAS  Article  Google Scholar 

  189. Williams JR, Insel TR, Harbaugh CR, Carter CS (1994) Oxytocin administered centrally facilitates formation of a partner preference in female prairie voles (Microtus ochrogaster). J Neuroendocrinol 6:247–250

    Article  CAS  PubMed  Google Scholar 

  190. Wilson AJ, Gelin U, Perron M-C, Réale D (2009) Indirect genetic effects and the evolution of aggression in a vertebrate system. Proc R Soc Lond B Biol Sci 276:533–541

    Article  Google Scholar 

  191. Wittig RM, Crockford C, Weltring A, Langergraber KE, Deschner T, Zuberbühler K (2016) Social support reduces stress hormone levels in wild chimpanzees across stressful events and everyday affiliations. Nat Commun 7:13361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  192. Wrangham R (1979) On the evolution of ape social systems. Inf Int Soc Sci Counc 18:336–368

    Article  Google Scholar 

  193. Wrangham RW (1980) An ecological model of female-bonded primate groups. Behaviour 75:262–300

    Article  Google Scholar 

  194. Yamagishi T, Hashimoto H (2016) Social niche construction. Curr Opin Psychol 8:119–124

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank Andrew J.J. MacIntosh and Jean-Louis Deneubourg for our numerous discussions on this topic. We thank David N. Fisher and Krishna Balasubramanian for their useful comments on the paper. We thank Joanna Munro for English editing service. C.S. is funded by an ANR programme Blanc grant (HANC, ANR-15-CE36-0005-01) and a CNRS PICS programme (exchange with Japan, n°7455). V.R. is an International Research Fellow from the Japan Society for the Promotion of Science (JSPS). I.P.G. was supported by a post-doctoral research grant from the National Council of Science and Technology (CONACyT), Mexico.

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Sueur, C., Romano, V., Sosa, S. et al. Mechanisms of network evolution: a focus on socioecological factors, intermediary mechanisms, and selection pressures. Primates 60, 167–181 (2019). https://doi.org/10.1007/s10329-018-0682-7

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Keywords

  • Group-living trade-off, cultural evolution
  • Sociality
  • Fitness
  • Multi-level selection
  • Cultural brain hypothesis