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”.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alexander RD (1974) The evolution of social behavior. Annu Rev Ecol Syst 5:325–383
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
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
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
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
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
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
Balasubramaniam K, Dittmar K, Berman CM et al (2012a) Hierarchical steepness and phylogenetic models: phylogenetic signals in Macaca. Anim Behav 83:1207–1218
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
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
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
Berman CM, Thierry B (2010) Variation in kin bias: species differences and time constraints in macaques. Behaviour 147:1863–1887
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
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
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
Blomberg SP, Garland T (2002) Tempo and mode in evolution: phylogenetic inertia, adaptation and comparative methods. J Evol Biol 15:899–910
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
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
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
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
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
Bryden J, Funk S, Geard N et al (2011) Stability in flux: community structure in dynamic networks. J R Soc Interface 8:1031–1040
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
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
Caillaud D, Levrero F, Cristescu R et al (2006) Gorilla susceptibility to Ebola virus: the cost of sociality. Curr Biol 16:R489–R491
Camazine S, Deneubourg J-L, Franks NR et al. (2003) Self-organization in biological systems. Princeton University Press, Princeton, US
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
Cantor M, Shoemaker LG, Cabral RB et al (2015) Multilevel animal societies can emerge from cultural transmission. Nat Commun 6:8091
Chapais B (1988) Experimental matrilineal inheritance of rank in female Japanese macaques. Anim Behav 36:1025–1037
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
Cheney DL, Seyfarth RM (2009) Stress and coping mechanisms in female primates. Adv Study Behav 39:1–44
Cialdini RB, Goldstein NJ (2004) Social influence: compliance and conformity. Annu Rev Psychol 55:591–621
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
Clutton-Brock T (2002) Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296:69–72
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
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
Croft DP, James R, Krause J (2008) Exploring animal social networks. Princeton University Press, Princeton, US
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
Crook JH, Gartlan JS (1966) Evolution of primate societies. Nature 210:1200–1203
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
Dawkins R (2006) The selfish gene: 30th anniversary edition. Oxford University Press, Oxford, UK
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
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
Delm MM (1990) Vigilance for predators: detection and dilution effects. Behav Ecol Sociobiol 26:337–342
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
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
Dingemanse NJ, Kazem AJ, Réale D, Wright J (2010) Behavioural reaction norms: animal personality meets individual plasticity. Trends Ecol Evol 25:81–89
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
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
Duboscq J, Romano V, MacIntosh A, Sueur C (2016) Social information transmission in animals: lessons from studies of diffusion. Front Psychol 7:1147
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
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
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
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
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
Fisher DN, Rodríguez-Muñoz R, Tregenza T (2016) Wild cricket social networks show stability across generations. BMC Evol Biol 16:151
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
Foster W, Treherne J (1981) Evidence for the dilution effect in the selfish herd from fish predation on a marine insect. Nature 293:466
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
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
Frank SA (2007) All of life is social. Curr Biol 17:R648–R650
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
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
Galef BG, Whiskin EE (2008) ‘Conformity’ in Norway rats? Anim Behav 75:2035–2039. https://doi.org/10.1016/j.anbehav.2007.11.012
Goodall J (1986) Social rejection, exclusion, and shunning among the Gombe chimpanzees. Ethol Sociobiol 7:227–236
Granovetter MS (1973) The strength of weak ties. Am J Sociol 78:1360–1380. https://doi.org/10.1086/225469
Griffin AS (2004) Social learning about predators: a review and prospectus. Anim Learn Behav 32:131–140. https://doi.org/10.3758/BF03196014
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
Hamilton WD (1971) Geometry for the selfish herd. J Theor Biol 31:295–311. https://doi.org/10.1016/0022-5193(71)90189-5
Hariri AR, Mattay VS, Tessitore A et al (2002) Serotonin transporter genetic variation and the response of the human amygdala. Science 297:400–403
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
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
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
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
Hinde RA (1976) Interactions, relationships and social structure. Man 11:1–17
Hockings KJ (2009) Living at the interface: human–chimpanzee competition, coexistence and conflict in Africa. Interact Stud 10:183–205
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
Nakamura M, Hosaka K, Itoh N, Zamma K (eds) (2015) Mahale chimpanzees: 50 years of research. Cambridge University Press, UK
Huffman MA (2016) primate self-medication, passive prevention and active treatment-A brief review. Int J Multidiscip Stud 3(2):1–10
Hung AA, Plott CR (2001) Information cascades: replication and an extension to majority rule and conformity-rewarding institutions. Am Econ Rev 91:1508–1520
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
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
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
Kamilar JM, Cooper N (2013) Phylogenetic signal in primate behaviour, ecology and life history. Phil Trans R Soc B 368:20120341
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
Kappeler PM, van Schaik CP (2002) Evolution of primate social systems. Int J Primatol 23:707–740. https://doi.org/10.1023/A:1015520830318
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
Kelley JL, Morrell LJ, Inskip C et al (2011) Predation risk shapes social networks in fission–fusion populations. PLoS One 6:e24280
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
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
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
Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, Oxford, UK
Kulahci IG, Ghazanfar AA, Rubenstein DI (2018) Knowledgeable lemurs become more central in social networks. Curr Biol 28:1306–1310
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
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
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
Lloyd-Smith JO, Schreiber SJ, Kopp PE, Getz WM (2005) Superspreading and the effect of individual variation on disease emergence. Nature 438:355–359
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
Mann J, Stanton MA, Patterson EM et al (2012) Social networks reveal cultural behaviour in tool-using dolphins. Nat Commun 3:980
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
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
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
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
McPherson M, Smith-Lovin L, Cook JM (2001) Birds of a feather: homophily in social networks. Annu Rev Sociol 27:415–444
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
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
Morgan TJH, Laland KN (2012) The biological bases of conformity. Front Neurosci 6:87
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
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
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
Muthukrishna M, Henrich J (2016) Innovation in the collective brain. Phil Trans R Soc B 371:20150192
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
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
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
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
Newman ME (2002) Assortative mixing in networks. Phys Rev Lett 89:208701
Noë R, Hammerstein P (1995) Biological markets. Trends Ecol Evol 10:336–339. https://doi.org/10.1016/S0169-5347(00)89123-5
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
Nunn C, Altizer SM (2006) Infectious diseases in primates: behavior, ecology and evolution. Oxford University Press, Oxford, UK
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
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
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
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
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
Paterson JD, Wallis J (2005) Commensalism and conflict: the human-primate interface. American Society of Primatologists, Norman, Okla
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
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
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
Poirotte C, Massol F, Herbert A et al (2017) Mandrills use olfaction to socially avoid parasitized conspecifics. Sci Adv 3:e1601721
Pruitt JN, Goodnight CJ (2014) Site-specific group selection drives locally adapted group compositions. Nature 514:359
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
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
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
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
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
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
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
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
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
Saltz JB (2011) Natural genetic variation in social environment choice: context-dependent gene-environment correlation in Drosophila melanogaster. Evolution 65:2325–2334
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
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
Sarabian C, MacIntosh AJ (2015) Hygienic tendencies correlate with low geohelminth infection in free-ranging macaques. Biol Lett 11:20150757
Sarabian C, MacIntosh AJ (2016) Revulsion in chimpanzees: health maintenance through avoidance of biological contaminants. PeerJ (Preprints)
Sauro MD, Jorgensen RS, Teal Pedlow C (2003) Stress, glucocorticoids, and memory: a meta-analytic review. Stress 6:235–245
Van Schaik CP, Van Hooff JARAM (1983) On the ultimate causes of primate social systems. Behaviour 85(1):91–117
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
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
Seyfarth RM (1977) A model of social grooming among adult female monkeys. J Theor Biol 65:671–698
Shultz S, Opie C, Atkinson QD (2011) Stepwise evolution of stable sociality in primates. Nature 479:219–222
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
Sirviö J, Riekkinen P, Jäkälä P, Riekkinen PJ (1994) Experimental studies on the role of serotonin in cognition. Prog Neurobiol 43:363–379
Skyrms B, Pemantle R (2009) A dynamic model of social network formation. Adaptive networks. Springer, Berlin, Germany, pp 231–251
Soltis J, Boyd R, Richerson PJ (1995) Can group-functional behaviors evolve by cultural group selection?: an empirical test. Curr Anthropol 36:473–494
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
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
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
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
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
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
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
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
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
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
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
Tanaka I (1995) Matrilineal distribution of louse egg-handling techniques during grooming in free-ranging Japanese macaques. Am J Phys Anthropol 98:197–201
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
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
Thierry B, Singh M, Kaumanns W (2004) Macaque societies: a model for the study of social organization. Cambridge University Press, Cambridge, UK
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
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
Tkaczynski P, MacLarnon A, Ross C (2014) Associations between spatial position, stress and anxiety in forest baboons Papio anubis. Behav Processes 108:1–6
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
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
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
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
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
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
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
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
Watson KK, Ghodasra JH, Platt ML (2009) Serotonin transporter genotype modulates social reward and punishment in rhesus macaques. PLoS One 4:e4156
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
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
Whitehead H (2008) Analyzing animal societies: quantitative methods for vertebrate social analysis. University of Chicago Press, Chicago, US
Whiten A (2018) Social dynamics: knowledgeable lemurs gain status. Curr Biol 28:R344–R346
Whiten A, Goodall J, McGrew WC et al (1999) Cultures in chimpanzees. Nature 399:682–685
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
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
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
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
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
Wrangham R (1979) On the evolution of ape social systems. Inf Int Soc Sci Counc 18:336–368
Wrangham RW (1980) An ecological model of female-bonded primate groups. Behaviour 75:262–300
Yamagishi T, Hashimoto H (2016) Social niche construction. Curr Opin Psychol 8:119–124
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.
Author information
Authors and Affiliations
Corresponding author
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10329-018-0682-7