Sociability as a personality trait in animals: methods, causes and consequences.
behavioural syndromes
behavioural types
collective behaviour
division of labour
personality variation
repeatability
social networks
social structure
sociality
temperament
Journal
Biological reviews of the Cambridge Philosophical Society
ISSN: 1469-185X
Titre abrégé: Biol Rev Camb Philos Soc
Pays: England
ID NLM: 0414576
Informations de publication
Date de publication:
04 2022
04 2022
Historique:
revised:
27
11
2021
received:
05
04
2021
accepted:
30
11
2021
pubmed:
12
12
2021
medline:
3
5
2022
entrez:
11
12
2021
Statut:
ppublish
Résumé
Within animal populations there is variation among individuals in their tendency to be social, where more sociable individuals associate more with other individuals. Consistent inter-individual variation in 'sociability' is considered one of the major axes of personality variation in animals along with aggressiveness, activity, exploration and boldness. Not only is variation in sociability important in terms of animal personalities, but it holds particular significance for, and can be informed by, two other topics of major interest: social networks and collective behaviour. Further, knowledge of what generates inter-individual variation in social behaviour also holds applied implications, such as understanding disorders of social behaviour in humans. In turn, research using non-human animals in the genetics, neuroscience and physiology of these disorders can inform our understanding of sociability. For the first time, this review brings together insights across these areas of research, across animal taxa from primates to invertebrates, and across studies from both the laboratory and field. We show there are mixed results in whether and how sociability correlates with other major behavioural traits. Whether and in what direction these correlations are observed may differ with individual traits such as sex and body condition, as well as ecological conditions. A large body of evidence provides the proximate mechanisms for why individuals vary in their social tendency. Evidence exists for the importance of genes and their expression, chemical messengers, social interactions and the environment in determining an individual's social tendency, although the specifics vary with species and other variables such as age, and interactions amongst these proximate factors. Less well understood is how evolution can maintain consistent variation in social tendencies within populations. Shifts in the benefits and costs of social tendencies over time, as well as the social niche hypothesis, are currently the best supported theories for how variation in sociability can evolve and be maintained in populations. Increased exposure to infectious diseases is the best documented cost of a greater social tendency, and benefits include greater access to socially transmitted information. We also highlight that direct evidence for more sociable individuals being safer from predators is lacking. Variation in sociability is likely to have broad ecological consequences, but beyond its importance in the spread of infectious diseases, direct evidence is limited to a few examples related to dispersal and invasive species biology. Overall, our knowledge of inter-individual variation in sociability is highly skewed towards the proximate mechanisms. Our review also demonstrates, however, that considering research from social networks and collective behaviour greatly enriches our understanding of sociability, highlighting the need for greater integration of these approaches into future animal personality research to address the imbalance in our understanding of sociability as a personality trait.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
802-816Subventions
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/S009752/1
Pays : United Kingdom
Informations de copyright
© 2021 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.
Références
Abbey-Lee, R. N., Kreshchenko, A., Fernandez Sala, X., Petkova, I. & Løvlie, H. (2019). Effects of monoamine manipulations on the personality and gene expression of three-spined sticklebacks. The Journal of Experimental Biology 222, jeb211888.
Albery, G. F., Kirkpatrick, L., Firth, J. A. & Bansal, S. (2021a). Unifying spatial and social network analysis in disease ecology. Journal of Animal Ecology 90, 45-61.
Albery, G. F., Morris, A., Morris, S., Pemberton, J. M., Clutton-Brock, T. H., Nussey, D. H. & Firth, J. A. (2021b). Multiple spatial behaviours govern social network positions in a wild ungulate. Ecology Letters 24, 676-686.
Ansmann, I. C., Parra, G. J., Chilvers, B. L. & Lanyon, J. M. (2012). Dolphins restructure social system after reduction of commercial fisheries. Animal Behaviour 84, 575-581.
Aplin, L. M., Farine, D. R., Morand-Ferron, J., Cockburn, A., Thornton, A. & Sheldon, B. C. (2015). Experimentally induced innovations lead to persistent culture via conformity in wild birds. Nature 518, 538-541.
Aplin, L. M., Farine, D. R., Morand-Ferron, J., Cole, E. F., Cockburn, A. & Sheldon, B. C. (2013). Individual personalities predict social behaviour in wild networks of great tits (Parus major). Ecology Letters 16, 1365-1372.
Aplin, L. M., Farine, D. R., Morand-Ferron, J. & Sheldon, B. C. (2012). Social networks predict patch discovery in a wild population of songbirds. Proceedings of the Royal Society B: Biological Sciences 279, 4199-4205.
Arlinghaus, R., Laskowski, K. L., Alós, J., Klefoth, T., Monk, C. T., Nakayama, S. & Schröder, A. (2017). Passive gear-induced timidity syndrome in wild fish populations and its potential ecological and managerial implications. Fish and Fisheries 18, 360-373.
Aujnarain, A. B., Luo, O. D., Taylor, N., Lai, J. K. Y. & Foster, J. A. (2018). Effects of exercise and enrichment on behaviour in CD-1 mice. Behavioural Brain Research 342, 43-50.
Barnard, C. J. & Sibly, R. M. (1981). Producers and scroungers: a general model and its application to captive flocks of house sparrows. Animal Behaviour 29, 543-550.
Bauer, U., Federle, W., Seidel, H., Grafe, T. U. & Ioannou, C. C. (2015). How to catch more prey with less effective traps: explaining the evolution of temporarily inactive traps in carnivorous pitcher plants. Proceedings of the Royal Society B: Biological Sciences 282, 20142675.
Bazazi, S., Ioannou, C. C., Simpson, S. J., Sword, G. A., Torney, C. J., Lorch, P. D. & Couzin, I. D. (2010). The social context of cannibalism in migratory bands of the mormon cricket. PLoS One 5, e15118.
Bell, A. M., Hankison, S. J. & Laskowski, K. L. (2009). The repeatability of behaviour: a meta-analysis. Animal Behaviour 77, 771-783.
Benítez, M. E., Sosnowski, M. J., Tomeo, O. B. & Brosnan, S. F. (2018). Urinary oxytocin in capuchin monkeys: validation and the influence of social behavior. American Journal of Primatology 80, e22877.
Berger, S., Gureczny, S., Reisinger, S. N., Horvath, O. & Pollak, D. D. (2019). Effect of chronic corticosterone treatment on depression-like behavior and sociability in female and male C57BL/6N mice. Cell 8, 1018.
Bergmüller, R. & Taborsky, M. (2010). Animal personality due to social niche specialisation. Trends in Ecology & Evolution 25, 504-511.
Beshers, S. N. & Fewell, J. H. (2001). Models of division of labor in social insects. Annual Review of Entomology 46, 413-440.
Best, E. C., Blomberg, S. P. & Goldizen, A. W. (2015). Shy female kangaroos seek safety in numbers and have fewer preferred friendships. Behavioral Ecology 26, 639-646.
Bevan, P. A., Gosetto, I., Jenkins, E. R., Barnes, I. & Ioannou, C. C. (2018). Regulation between personality traits: individual social tendencies modulate whether boldness and leadership are correlated. Proceedings of the Royal Society B: Biological Sciences 285, 20180829.
Bierbach, D., Laskowski, K. L. & Wolf, M. (2017). Behavioural individuality in clonal fish arises despite near-identical rearing conditions. Nature Communications 8, 15361.
Blaszczyk, M. B. (2017). Consistency in social network position over changing environments in a seasonally breeding primate. Behavioral Ecology and Sociobiology 72, 11.
Block, J. (1995). A contrarian view of the five-factor approach to personality description. Psychological Bulletin 117, 187-215.
Blumstein, D. T., Petelle, M. B. & Wey, T. W. (2013). Defensive and social aggression: repeatable but independent. Behavioral Ecology 24, 457-461.
Blumstein, D. T., Williams, D. M., Lim, A. N., Kroeger, S. & Martin, J. G. A. (2018). Strong social relationships are associated with decreased longevity in a facultatively social mammal. Proceedings of the Royal Society B: Biological Sciences 285, 20171934.
Bond, C. M., Johnson, J. C., Chaudhary, V., McCarthy, E. M., McWhorter, M. L. & Woehrle, N. S. (2020). Perinatal fluoxetine exposure results in social deficits and reduced monoamine oxidase gene expression in mice. Brain Research 1727, 146282.
Boon, A. K., Réale, D. & Boutin, S. (2007). The interaction between personality, offspring fitness and food abundance in North American red squirrels. Ecology Letters 10, 1094-1104.
Bowen, M. T., Carson, D. S., Spiro, A., Arnold, J. C. & McGregor, I. S. (2011). Adolescent oxytocin exposure causes persistent reductions in anxiety and alcohol consumption and enhances sociability in rats. PLoS One 6, e27237.
Brenner, R. G., Oliveri, A. N., Sinnott-Armstrong, W. & Levin, E. D. (2020). Effects of sub-chronic methylphenidate on risk-taking and sociability in zebrafish (Danio rerio). Naunyn-Schmiedeberg's Archives of Pharmacology 393, 1373-1381.
Brent, L. J. N., Heilbronner, S. R., Horvath, J. E., Gonzalez-Martinez, J., Ruiz-Lambides, A., Robinson, A. G., Skene, J. H. P. & Platt, M. L. (2013). Genetic origins of social networks in rhesus macaques. Scientific Reports 3, 1042.
Brodin, T., Fogarty, S., Sih, A. & Cote, J. (2019). Personality-dependent survival of the invasive mosquitofish: being social can be deadly. Aquatic Invasions 14, 465-477.
Buffington, S. A., Di Prisco, G. V., Auchtung, T. A., Ajami, N. J., Petrosino, J. F. & Costa-Mattioli, M. (2016). Microbial reconstitution reverses maternal diet-induced social and synaptic deficits in offspring. Cell 165, 1762-1775.
Caine, N. G., Earle, H. & Reite, M. (1983). Personality traits of adolescent pig-tailed monkeys (Macaca nemestrina): an analysis of social rank and early separation experience. American Journal of Primatology 4, 253-260.
Capitanio, J. P., Mendoza, S. P. & Bentson, K. L. (2004). Personality characteristics and basal cortisol concentrations in adult male rhesus macaques (Macaca mulatta). Psychoneuroendocrinology 29, 1300-1308.
Carter, A. J., Feeney, W. E., Marshall, H. H., Cowlishaw, G. & Heinsohn, R. (2013). Animal personality: what are behavioural ecologists measuring? Biological Reviews 88, 465-475.
Carter, C. S., Grippo, A. J., Pournajafi-Nazarloo, H., Ruscio, M. G. & Porges, S. W. (2008). Oxytocin, vasopressin and sociality. In Advances in Vasopressin and Oxytocin - From Genes to Behaviour to Disease (eds I. D. Neumann and B. R. Landgraf), pp. 331-336. Elsevier, Oxford.
Cattelan, S., Lucon-Xiccato, T., Pilastro, A. & Griggio, M. (2017). Is the mirror test a valid measure of fish sociability? Animal Behaviour 127, 109-116.
Chiara, V., Ramon Portugal, F. & Jeanson, R. (2019). Social intolerance is a consequence, not a cause, of dispersal in spiders. PLoS Biology 17, e3000319.
Clarke, A. S. & Schneider, M. L. (1993). Prenatal stress has long-term effects on behavioral responses to stress in juvenile rhesus monkeys. Developmental Psychobiology 26, 293-304.
Colin, C. & Desor, D. (1986). Differenciations comportementales dans des groupes de rats soumis a une difficulte d'acces a la nourriture. Behavioural Processes 13, 85-100.
Corner, L. A. L., Pfeiffer, D. U. & Morris, R. S. (2003). Social-network analysis of Mycobacterium bovis transmission among captive brushtail possums (Trichosurus vulpecula). Preventive Veterinary Medicine 59, 147-167.
Côté, I. M. & Poulinb, R. (1995). Parasitism and group size in social animals: a meta-analysis. Behavioral Ecology 6, 159-165.
Cote, J. & Clobert, J. (2007). Social personalities influence natal dispersal in a lizard. Proceedings of the Royal Society B: Biological Sciences 274, 383-390.
Cote, J., Dreiss, A. & Clobert, J. (2008). Social personality trait and fitness. Proceedings of the Royal Society B: Biological Sciences 275, 2851-2858.
Cote, J., Fogarty, S., Weinersmith, K., Brodin, T. & Sih, A. (2010). Personality traits and dispersal tendency in the invasive mosquitofish (Gambusia affinis). Proceedings of the Royal Society B: Biological Sciences 277, 1571-1579.
Croft, D. P., Krause, J., Darden, S. K., Ramnarine, I. W., Faria, J. J. & James, R. (2009). Behavioural trait assortment in a social network: patterns and implications. Behavioral Ecology and Sociobiology 63, 1495-1503.
Dall, S. R. X., Bell, A. M., Bolnick, D. I. & Ratnieks, F. L. W. (2012). An evolutionary ecology of individual differences. Ecology Letters 15, 1189-1198.
Dammhahn, M., Dingemanse, N. J., Niemelä, P. T. & Réale, D. (2018). Pace-of-life syndromes: a framework for the adaptive integration of behaviour, physiology and life history. Behavioral Ecology and Sociobiology 72, 62.
Dhellemmes, F., Finger, J.-S., Laskowski, K. L., Guttridge, T. L. & Krause, J. (2020). Comparing behavioural syndromes across time and ecological conditions in a free-ranging predator. Animal Behaviour 162, 23-33.
Dimitriadou, S., Croft, D. P. & Darden, S. K. (2019). Divergence in social traits in Trinidadian guppies selectively bred for high and low leadership in a cooperative context. Scientific Reports 9, 17194.
Dingemanse, N. J., Van der Plas, F., Wright, J., Réale, D., Schrama, M., Roff, D. A., Van der Zee, E. & Barber, I. (2009). Individual experience and evolutionary history of predation affect expression of heritable variation in fish personality and morphology. Proceedings of the Royal Society B: Biological Sciences 276, 1285-1293.
Dochtermann, N. A., Schwab, T. & Sih, A. (2014). The contribution of additive genetic variation to personality variation: heritability of personality. Proceedings of the Royal Society of London B: Biological Sciences 282, 20142201.
Drewe, J. A. (2010). Who infects whom? Social networks and tuberculosis transmission in wild meerkats. Proceedings of the Royal Society B: Biological Sciences 277, 633-642.
Duffield, C. & Ioannou, C. C. (2017). Marginal predation: do encounter or confusion effects explain the targeting of prey group edges? Behavioral Ecology 28, 1283-1292.
Farhat, S. M., Mahboob, A., Iqbal, G. & Ahmed, T. (2017). Aluminum-induced cholinergic deficits in different brain parts and its implications on sociability and cognitive functions in mouse. Biological Trace Element Research 177, 115-121.
Firth, J. A., Cole, E. F., Ioannou, C. C., Quinn, J. L., Aplin, L. M., Culina, A., McMahon, K. & Sheldon, B. C. (2018). Personality shapes pair bonding in a wild bird social system. Nature Ecology & Evolution 2, 1696-1699.
Firth, J. A. & Sheldon, B. C. (2016). Social carry-over effects underpin trans-seasonally linked structure in a wild bird population. Ecology Letters 19, 1324-1332.
Firth, J. A., Sheldon, B. C. & Farine, D. R. (2016). Pathways of information transmission among wild songbirds follow experimentally imposed changes in social foraging structure. Biology Letters 12, 20160144.
Firth, J. A., Voelkl, B., Crates, R. A., Aplin, L. M., Biro, D., Croft, D. P. & Sheldon, B. C. (2017). Wild birds respond to flockmate loss by increasing their social network associations to others. Proceedings of the Royal Society B: Biological Sciences 284, 20170299.
Fischer, S., Bohn, L., Oberhummer, E., Nyman, C. & Taborsky, B. (2017). Divergence of developmental trajectories is triggered interactively by early social and ecological experience in a cooperative breeder. Proceedings of the National Academy of Sciences 114, E9300-E9307.
Fisher, D. N. & McAdam, A. G. (2017). Social traits, social networks and evolutionary biology. Journal of Evolutionary Biology 30, 2088-2103.
Fogarty, S., Cote, J. & Sih, A. (2011). Social personality polymorphism and the spread of invasive species: a model. The American Naturalist 177, 273-287.
Formica, V., Wood, C., Cook, P. & Brodie, E. III (2017). Consistency of animal social networks after disturbance. Behavioral Ecology 28, 85-93.
Franks, V. R., Andrews, C. E., Ewen, J. G., McCready, M., Parker, K. A. & Thorogood, R. (2020). Changes in social groups across reintroductions and effects on post-release survival. Animal Conservation 23, 443-454.
Freund, J., Brandmaier, A. M., Lewejohann, L., Kirste, I., Kritzler, M., Krüger, A., Sachser, N., Lindenberger, U. & Kempermann, G. (2013). Emergence of individuality in genetically identical mice. Science 340, 756-759.
Gilbert, C., McCafferty, D., Le Maho, Y., Martrette, J.-M., Giroud, S., Blanc, S. & Ancel, A. (2010). One for all and all for one: the energetic benefits of huddling in endotherms. Biological Reviews 85, 545-569.
Ginelli, F., Peruani, F., Pillot, M., Chaté, H., Theraulaz, G. & Bon, R. (2015). Intermittent collective dynamics emerge from conflicting imperatives in sheep herds. Proceedings of the National Academy of Sciences 112, 12729-12734.
Godfrey, S. S., Bull, C. M., James, R. & Murray, K. (2009). Network structure and parasite transmission in a group living lizard, the gidgee skink, Egernia stokesii. Behavioral Ecology and Sociobiology 63, 1045-1056.
Gosling, S. D. & John, O. P. (1999). Personality dimensions in nonhuman animals a cross-species review. Current Directions in Psychological Science 8, 69-75.
Halloy, J., Sempo, G., Caprari, G., Rivault, C., Asadpour, M., Tache, F., Said, I., Durier, V., Canonge, S. & Ame, J. M. (2007). Social integration of robots into groups of cockroaches to control self-organized choices. Science 318, 1155-1158.
Hart, A. G. & Ratnieks, F. L. W. (2001). Task partitioning, division of labour and nest compartmentalisation collectively isolate hazardous waste in the leafcutting ant Atta cephalotes. Behavioral Ecology and Sociobiology 49, 387-392.
Hewlett, S. E., Delahunt Smoleniec, J. D., Wareham, D. M., Pyne, T. M. & Barron, A. B. (2018). Biogenic amine modulation of honey bee sociability and nestmate affiliation. PLoS One 13, e0205686.
Hol, T., Van den Berg, C. L., Van Ree, J. M. & Spruijt, B. M. (1999). Isolation during the play period in infancy decreases adult social interactions in rats. Behavioural Brain Research 100, 91-97.
Holbrook, T., Clark, R. M., Jeanson, R., Bertram, S. M., Kukuk, P. F. & Fewell, J. H. (2009). Emergence and consequences of division of labor in associations of normally solitary sweat bees. Ethology 115, 301-310.
Ioannou, C. C. (2021). Grouping and predation. In Encyclopedia of Evolutionary Psychological Science (eds T. K. Shackelford and V. A. Weekes-Shackelford), pp. 3574-3580. Springer International Publishing, Cham.
Ioannou, C. C., Ramnarine, I. W. & Torney, C. J. (2017). High-predation habitats affect the social dynamics of collective exploration in a shoaling fish. Science Advances 3, e1602682.
Ioannou, C. C., Rocque, F., Herbert-Read, J. E., Duffield, C. & Firth, J. A. (2019). Predators attacking virtual prey reveal the costs and benefits of leadership. Proceedings of the National Academy of Sciences 116, 8925-8930.
Irving, E. & Brown, C. (2013). Examining the link between personality and laterality in a feral guppy Poecilia reticulata population. Journal of Fish Biology 83, 311-325.
Jacoby, D. M. P., Fear, L. N., Sims, D. W. & Croft, D. P. (2014). Shark personalities? Repeatability of social network traits in a widely distributed predatory fish. Behavioral Ecology and Sociobiology 68, 1995-2003.
Jägers, P., Wagner, L., Schütz, R., Mucke, M., Senen, B., Limmon, G. V., Herlitze, S. & Hellinger, J. (2021). Social signaling via bioluminescent blinks determines nearest neighbor distance in schools of flashlight fish Anomalops katoptron. Scientific Reports 11, 6431.
Jakovcevic, A., Mustaca, A. & Bentosela, M. (2012). Do more sociable dogs gaze longer to the human face than less sociable ones? Behavioural Processes 90, 217-222.
Jawaid, A. & Mansuy, I. M. (2019). Inter-and transgenerational inheritance of behavioral phenotypes. Current Opinion in Behavioral Sciences 25, 96-101.
Jeanson, R. (2012). Long-term dynamics in proximity networks in ants. Animal Behaviour 83, 915-923.
Jeanson, R., Kukuk, P. F. & Fewell, J. H. (2005). Emergence of division of labour in halictine bees: contributions of social interactions and behavioural variance. Animal Behaviour 70, 1183-1193.
Jeanson, R. & Weidenmüller, A. (2014). Interindividual variability in social insects - proximate causes and ultimate consequences. Biological Reviews 89, 671-687.
Jolles, J. W., Boogert, N. J., Sridhar, V. H., Couzin, I. D. & Manica, A. (2017). Consistent individual differences drive collective behavior and group functioning of schooling fish. Current Biology 27, 2862-2868.
Kappeler, P. M., Cremer, S. & Nunn, C. L. (2015). Sociality and health: impacts of sociality on disease susceptibility and transmission in animal and human societies. Philosophical Transactions of the Royal Society B: Biological Sciences 370, 20140116.
Kappeler, P. M. & van Schaik, C. P. (2002). Evolution of primate social systems. International Journal of Primatology 23, 707-740.
Kim, S.-Y. & Velando, A. (2016). Unsociable juvenile male three-spined sticklebacks grow more attractive. Behavioral Ecology and Sociobiology 70, 975-980.
Kis, A., Bence, M., Lakatos, G., Pergel, E., Turcsán, B., Pluijmakers, J., Vas, J., Elek, Z., Brúder, I., Földi, L., Sasvári-Székely, M., Miklósi, Á., Rónai, Z. & Kubinyi, E. (2014). Oxytocin receptor gene polymorphisms are associated with human directed social behavior in dogs (Canis familiaris). PLoS One 9, e83993.
Knoll, A. T., Jiang, K. & Levitt, P. (2018). Quantitative trait locus mapping and analysis of heritable variation in affiliative social behavior and co-occurring traits. Genes, Brain and Behavior 17, e12431.
Kocher, S. D., Mallarino, R., Rubin, B. E. R., Yu, D. W., Hoekstra, H. E. & Pierce, N. E. (2018). The genetic basis of a social polymorphism in halictid bees. Nature Communications 9, 4338.
Kohn, G. M. (2017). Friends give benefits: autumn social familiarity preferences predict reproductive output. Animal Behaviour 132, 201-208.
Kondrakiewicz, K., Kostecki, M., Szadzińska, W. & Knapska, E. (2019). Ecological validity of social interaction tests in rats and mice. Genes, Brain and Behavior 18, e12525.
Kotob, M. H., Menanteau-Ledouble, S., Kumar, G., Abdelzaher, M. & El-Matbouli, M. (2016). The impact of co-infections on fish: a review. Veterinary Research 47, 98.
Krafft, B., Colin, C. & Peignot, P. (1994). Diving-for-food: a new model to assess social roles in a group of laboratory rats. Ethology 96, 11-23.
Krause, J., James, R., Franks, D. W. & Croft, D. P. (2015). Animal Social Networks. Oxford University Press, Oxford.
Krause, J. & Ruxton, G. D. (2002). Living in Groups. Oxford University Press, Oxford.
Krause, S., Wilson, A. D. M., Ramnarine, I. W., Herbert-Read, J. E., Clément, R. J. G. & Krause, J. (2017). Guppies occupy consistent positions in social networks: mechanisms and consequences. Behavioral Ecology 28, 429-438.
Lacasse, J. & Aubin-Horth, N. (2014). Population-dependent conflict between individual sociability and aggressiveness. Animal Behaviour 87, 53-57.
Landgraf, T., Bierbach, D., Nguyen, H., Muggelberg, N., Romanczuk, P. & Krause, J. (2016). RoboFish: increased acceptance of interactive robotic fish with realistic eyes and natural motion patterns by live Trinidadian guppies. Bioinspiration & Biomimetics 11, 15001.
Laskowski, K. L. & Bell, A. M. (2014). Strong personalities, not social niches, drive individual differences in social behaviours in sticklebacks. Animal Behaviour 90, 287-295.
Le Galliard, J.-F., Paquet, M. & Mugabo, M. (2015). An experimental test of density-dependent selection on temperament traits of activity, boldness and sociability. Journal of Evolutionary Biology 28, 1144-1155.
Lea, A. J., Blumstein, D. T., Wey, T. W. & Martin, J. G. A. (2010). Heritable victimization and the benefits of agonistic relationships. Proceedings of the National Academy of Sciences 107, 21587-21592.
MacGregor, H. E. A., Cottage, A. & Ioannou, C. C. (2021). Suppression of personality variation in boldness during foraging in three-spined sticklebacks. Behavioral Ecology and Sociobiology 75, 71.
MacGregor, H. E. A., Herbert-Read, J. E. & Ioannou, C. C. (2020). Information can explain the dynamics of group order in animal collective behaviour. Nature Communications 11, 2737.
McCrae, R. R. & John, O. P. (1992). An introduction to the five-factor model and its applications. Journal of Personality 60, 175-215.
McDonald, D. B. (2007). Predicting fate from early connectivity in a social network. Proceedings of the National Academy of Sciences 104, 10910-10914.
Mehlman, P. T., Higley, J. D., Faucher, I., Lilly, A. A., Taub, D. M., Vickers, J., Suomi, S. J. & Linnoila, M. (1995). Correlation of CSF 5-HIAA concentration with sociality and the timing of emigration in free-ranging primates. The American Journal of Psychiatry 152, 907-913.
Michelangeli, M., Chapple, D. G. & Wong, B. B. M. (2016). Are behavioural syndromes sex specific? Personality in a widespread lizard species. Behavioral Ecology and Sociobiology 70, 1911-1919.
Michelangeli, M., Cote, J., Chapple, D. G., Sih, A., Brodin, T., Fogarty, S., Bertram, M. G., Eades, J. & Wong, B. B. M. (2020). Sex-dependent personality in two invasive species of mosquitofish. Biological Invasions 22, 1353-1364.
Michelena, P., Jeanson, R., Deneubourg, J. L. & Sibbald, A. M. (2010). Personality and collective decision-making in foraging herbivores. Proceedings of the Royal Society B: Biological Sciences 277, 1093-1099.
Moiron, M., Laskowski, K. L. & Niemelä, P. T. (2020). Individual differences in behaviour explain variation in survival: a meta-analysis. Ecology Letters 23, 399-408.
Mommer, B. C. & Bell, A. M. (2014). Maternal experience with predation risk influences genome-wide embryonic gene expression in threespined sticklebacks (Gasterosteus aculeatus). PLoS One 9, e98564.
Montero, A. P., Williams, D. M., Martin, J. G. A. & Blumstein, D. T. (2020). More social female yellow-bellied marmots, Marmota flaviventer, have enhanced summer survival. Animal Behaviour 160, 113-119.
Montiglio, P.-O., Dammhahn, M., Dubuc Messier, G. & Réale, D. (2018). The pace-of-life syndrome revisited: the role of ecological conditions and natural history on the slow-fast continuum. Behavioral Ecology and Sociobiology 72, 116.
Montiglio, P.-O., Ferrari, C. & Reale, D. (2013). Social niche specialization under constraints: personality, social interactions and environmental heterogeneity. Philosophical Transactions of the Royal Society B: Biological Sciences 368, 20120343.
Munson, A., Michelangeli, M. & Sih, A. (2021). Stable social groups foster conformity and among-group differences. Animal Behaviour 174, 197-206.
Muscedere, M. L., Johnson, N., Gillis, B. C., Kamhi, J. F. & Traniello, J. F. A. (2012). Serotonin modulates worker responsiveness to trail pheromone in the ant Pheidole dentata. Journal of Comparative Physiology A 198, 219-227.
Nagy, M., Ákos, Z., Biro, D. & Vicsek, T. (2010). Hierarchical group dynamics in pigeon flocks. Nature 464, 890-893.
Nagy, M., Vásárhelyi, G., Pettit, B., Roberts-Mariani, I., Vicsek, T. & Biro, D. (2013). Context-dependent hierarchies in pigeons. Proceedings of the National Academy of Sciences 110, 13049-13054.
Nakamura, K., Anitha, A., Yamada, K., Tsujii, M., Iwayama, Y., Hattori, E., Toyota, T., Suda, S., Takei, N., Iwata, Y., Suzuki, K., Matsuzaki, H., Kawai, M., Sekine, Y., Tsuchiya, K. J., et al. (2008). Genetic and expression analyses reveal elevated expression of syntaxin 1A (STX1A) in high functioning autism. International Journal of Neuropsychopharmacology 11, 1073-1084.
Nuñez, C. M. V., Adelman, J. S. & Rubenstein, D. I. (2015). Sociality increases juvenile survival after a catastrophic event in the feral horse (Equus caballus). Behavioral Ecology 26, 138-147.
Nunn, M. A., Barton, T. R., Wanless, S., Hails, R. S., Harris, M. P. & Nuttall, P. A. (2006). Tick-borne Great Island Virus:(II) impact of age-related acquired immunity on transmission in a natural seabird host. Parasitology 132, 241-253.
Öst, M., Seltmann, M. W. & Jaatinen, K. (2015). Personality, body condition and breeding experience drive sociality in a facultatively social bird. Animal Behaviour 100, 166-173.
Otterstatter, M. C. & Thomson, J. D. (2007). Contact networks and transmission of an intestinal pathogen in bumble bee (Bombus impatiens) colonies. Oecologia 154, 411-421.
Persson, M. E., Roth, L. S. V., Johnsson, M., Wright, D. & Jensen, P. (2015). Human-directed social behaviour in dogs shows significant heritability. Genes, Brain and Behavior 14, 337-344.
Persson, M. E., Wright, D., Roth, L. S. V., Batakis, P. & Jensen, P. (2016). Genomic regions associated with interspecies communication in dogs contain genes related to human social disorders. Scientific Reports 6, 33439.
Petelle, M. B., Martin, J. G. A. & Blumstein, D. T. (2015). Heritability and genetic correlations of personality traits in a wild population of yellow-bellied marmots (Marmota flaviventris). Journal of Evolutionary Biology 28, 1840-1848.
Planas-Sitjà, I. & Deneubourg, J.-L. (2018). The role of personality variation, plasticity and social facilitation in cockroach aggregation. Biology Open 7, bio036582.
Planas-Sitjà, I., Deneubourg, J.-L., Gibon, C. & Sempo, G. (2015). Group personality during collective decision-making: a multi-level approach. Proceedings of the Royal Society of London B: Biological Sciences 282, 20142515.
Proboste, T., Corvalan, P., Clark, N., Beyer, H. L., Goldizen, A. W. & Seddon, J. M. (2019). Commensal bacterial sharing does not predict host social associations in kangaroos. Journal of Animal Ecology 88, 1696-1707.
Ramos, L., Hicks, C., Caminer, A. & McGregor, I. S. (2014). Inhaled vasopressin increases sociability and reduces body temperature and heart rate in rats. Psychoneuroendocrinology 46, 46-51.
Rands, S. A., Cowlishaw, G., Pettifor, R. A., Rowcliffe, J. M. & Johnstone, R. A. (2003). Spontaneous emergence of leaders and followers in foraging pairs. Nature 423, 432-434.
Raulo, A., Ruokolainen, L., Lane, A., Amato, K., Knight, R., Leigh, S., Stumpf, R., White, B., Nelson, K. E. & Baden, A. L. (2018). Social behaviour and gut microbiota in red-bellied lemurs (Eulemur rubriventer): in search of the role of immunity in the evolution of sociality. Journal of Animal Ecology 87, 388-399.
Réale, D., Garant, D., Humphries, M. M., Bergeron, P., Careau, V. & Montiglio, P.-O. (2010). Personality and the emergence of the pace-of-life syndrome concept at the population level. Philosophical Transactions of the Royal Society B: Biological Sciences 365, 4051-4063.
Réale, D., Reader, S. M., Sol, D., McDougall, P. T. & Dingemanse, N. J. (2007). Integrating animal temperament within ecology and evolution. Biological Reviews 82, 291-318.
Rémy, A., Le Galliard, J., Odden, M. & Andreassen, H. P. (2014). Concurrent effects of age class and food distribution on immigration success and population dynamics in a small mammal. Journal of Animal Ecology 83, 813-822.
Rödel, H. G., Zapka, M., Talke, S., Kornatz, T., Bruchner, B. & Hedler, C. (2015). Survival costs of fast exploration during juvenile life in a small mammal. Behavioral Ecology and Sociobiology 69, 205-217.
Rodríguez-Prieto, I., Martín, J. & Fernández-Juricic, E. (2010). Individual variation in behavioural plasticity: direct and indirect effects of boldness, exploration and sociability on habituation to predators in lizards. Proceedings of the Royal Society of London B: Biological Sciences 278, 266-273.
Ross, H. E. & Young, L. J. (2009). Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior. Frontiers in Neuroendocrinology 30, 534-547.
Royauté, R., Berdal, M. A., Garrison, C. R. & Dochtermann, N. A. (2018). Paceless life? A meta-analysis of the pace-of-life syndrome hypothesis. Behavioral Ecology and Sociobiology 72, 64.
Ryabushkina, Y. A., Reshetnikov, V. V. & Bondar, N. P. (2020). Maternal separation early in life alters the expression of genes Npas4 and Nr1d1 in adult female mice: correlation with social behavior. Behavioural Neurology 2020, 7830469.
Sabol, A. C., Lambert, C. T., Keane, B., Solomon, N. G. & Dantzer, B. (2020). How does individual variation in sociality influence fitness in prairie voles? Animal Behaviour 163, 39-49.
Sala, M., Braida, D., Donzelli, A., Martucci, R., Busnelli, M., Bulgheroni, E., Rubino, T., Parolaro, D., Nishimori, K. & Chini, B. (2013). Mice heterozygous for the oxytocin receptor gene (Oxtr+/−) show impaired social behaviour but not increased aggression or cognitive inflexibility: evidence of a selective haploinsufficiency gene effect. Journal of Neuroendocrinology 25, 107-118.
Sarkar, A., Harty, S., Johnson, K. V.-A., Moeller, A. H., Archie, E. A., Schell, L. D., Carmody, R. N., Clutton-Brock, T. H., Dunbar, R. I. M. & Burnet, P. W. J. (2020). Microbial transmission in animal social networks and the social microbiome. Nature Ecology & Evolution 4, 1020-1035.
Sherwin, E., Bordenstein, S. R., Quinn, J. L., Dinan, T. G. & Cryan, J. F. (2019). Microbiota and the social brain. Science 366, eaar2016.
Shou, J., Tran, A., Snyder, N., Bleem, E. & Kim, S. (2019). Distinct roles of GluA2-lacking AMPA receptor expression in dopamine D1 or D2 receptor neurons in animal behavior. Neuroscience 398, 102-112.
Sih, A., Bell, A. & Johnson, J. C. (2004). Behavioral syndromes: an ecological and evolutionary overview. Trends in Ecology & Evolution 19, 372-378.
Sih, A., Hanser, S. F. & McHugh, K. A. (2009). Social network theory: new insights and issues for behavioral ecologists. Behavioral Ecology and Sociobiology 63, 975-988.
Sih, A., Mathot, K. J., Moirón, M., Montiglio, P.-O., Wolf, M. & Dingemanse, N. J. (2015). Animal personality and state-behaviour feedbacks: a review and guide for empiricists. Trends in Ecology & Evolution 30, 50-60.
Sih, A. & Watters, J. V. (2005). The mix matters: behavioural types and group dynamics in water striders. Behaviour 142, 1417-1431.
Silk, J. B., Alberts, S. C. & Altmann, J. (2003). Social bonds of female baboons enhance infant survival. Science 302, 1231-1234.
Silk, M. J. & Fefferman, N. H. (2021). The role of social structure and dynamics in the maintenance of endemic disease. Behavioral Ecology and Sociobiology 75, 122.
Silk, M. J., Hodgson, D. J., Rozins, C., Croft, D. P., Delahay, R. J., Boots, M. & McDonald, R. A. (2019). Integrating social behaviour, demography and disease dynamics in network models: applications to disease management in declining wildlife populations. Philosophical Transactions of the Royal Society B: Biological Sciences 374, 20180211.
Skinner, M. & Miller, N. (2020). Aggregation and social interaction in garter snakes (Thamnophis sirtalis sirtalis). Behavioral Ecology and Sociobiology 74, 51.
Smith, B. R. & Blumstein, D. T. (2008). Fitness consequences of personality: a meta-analysis. Behavioral Ecology 19, 448-455.
Snijders, L., Blumstein, D. T., Stanley, C. R. & Franks, D. W. (2017). Animal social network theory can help wildlife conservation. Trends in Ecology & Evolution 32, 567-577.
Snijders, L., Kurvers, R. H. J. M., Krause, S., Ramnarine, I. W. & Krause, J. (2018). Individual- and population-level drivers of consistent foraging success across environments. Nature Ecology & Evolution 2, 1610-1618.
Snijders, L., Naguib, M. & van Oers, K. (2016). Dominance rank and boldness predict social attraction in great tits. Behavioral Ecology 28, 398-406.
Snyder-Mackler, N., Burger, J. R., Gaydosh, L., Belsky, D. W., Noppert, G. A., Campos, F. A., Bartolomucci, A., Yang, Y. C., Aiello, A. E., O'Rand, A., Harris, K. M., Shively, C. A., Alberts, S. C. & Tung, J. (2020). Social determinants of health and survival in humans and other animals. Science 368, eaax9553.
Sol, D. & Weis, J. S. (2019). Highlights and insights from ‘Biological Invasions and Animal Behaviour’. Aquatic Invasions 14, 551-565.
Staes, N., Koski, S. E., Helsen, P., Fransen, E., Eens, M. & Stevens, J. M. G. (2015). Chimpanzee sociability is associated with vasopressin (Avpr1a) but not oxytocin receptor gene (OXTR) variation. Hormones and Behavior 75, 84-90.
Staes, N., Weiss, A., Helsen, P., Korody, M., Eens, M. & Stevens, J. M. G. (2016). Bonobo personality traits are heritable and associated with vasopressin receptor gene 1a variation. Scientific Reports 6, 38193.
Stamps, J. & Groothuis, T. G. G. (2010). The development of animal personality: relevance, concepts and perspectives. Biological Reviews 85, 301-325.
Stamps, J. A. (2007). Growth-mortality tradeoffs and ‘personality traits’ in animals. Ecology Letters 10, 355-363.
Stroeymeyt, N., Grasse, A. V., Crespi, A., Mersch, D. P., Cremer, S. & Keller, L. (2018). Social network plasticity decreases disease transmission in a eusocial insect. Science 362, 941-945.
Szopa-Comley, A. W., Duffield, C., Ramnarine, I. W. & Ioannou, C. C. (2020). Predatory behaviour as a personality trait in a wild fish population. Animal Behaviour 170, 51-64.
Takahashi, L. K., Haglin, C. & Kalin, N. H. (1992). Prenatal stress potentiates stress-induced behavior and reduces the propensity to play in juvenile rats. Physiology & Behavior 51, 319-323.
Thorlacius, M. & Brodin, T. (2018). Investigating large-scale invasion patterns using-small scale invasion successions-phenotypic differentiation of the invasive round goby (Neogobius melanostomus) at invasion fronts. Limnology and Oceanography 63, 702-713.
Thys, B., Eens, M., Aerts, S., Delory, A., Iserbyt, A. & Pinxten, R. (2017). Exploration and sociability in a highly gregarious bird are repeatable across seasons and in the long term but are unrelated. Animal Behaviour 123, 339-348.
Torquet, N., Marti, F., Campart, C., Tolu, S., Nguyen, C., Oberto, V., Benallaoua, M., Naudé, J., Didienne, S., Debray, N., Jezequel, S., Le Gouestre, L., Hannesse, B., Mariani, J., Mourot, A., et al. (2018). Social interactions impact on the dopaminergic system and drive individuality. Nature Communications 9, 3081.
van Boxelaere, M., Clements, J., Callaerts, P., D'Hooge, R. & Callaerts-Vegh, Z. (2017). Unpredictable chronic mild stress differentially impairs social and contextual discrimination learning in two inbred mouse strains. PLoS One 12, e0188537.
VanderWaal, K. L., Atwill, E. R., Isbell, L. A. & McCowan, B. (2014). Linking social and pathogen transmission networks using microbial genetics in giraffe (Giraffa camelopardalis). Journal of Animal Ecology 83, 406-414.
Varma, V., Vasoya, H., Jain, A. & Binoy, V. V. (2020). ‘The bold are the sociable’: personality traits and laterality in an indigenous megafish, the Deccan mahseer (Tor khudree). Ichthyological Research 67, 483-492.
Vogel, D., Nicolis, S. C., Perez-Escudero, A., Nanjundiah, V., Sumpter, D. J. T. & Dussutour, A. (2015). Phenotypic variability in unicellular organisms: from calcium signalling to social behaviour. Proceedings of the Royal Society of London B: Biological Sciences 282, 20152322.
Vogt, G. (2015). Stochastic developmental variation, an epigenetic source of phenotypic diversity with far-reaching biological consequences. Journal of Biosciences 40, 159-204.
Vogt, G., Huber, M., Thiemann, M., van den Boogaart, G., Schmitz, O. J. & Schubart, C. D. (2008). Production of different phenotypes from the same genotype in the same environment by developmental variation. Journal of Experimental Biology 211, 510-523.
Ward, A. J. W., Thomas, P., Hart, P. J. B. & Krause, J. (2004). Correlates of boldness in three-spined sticklebacks (Gasterosteus aculeatus). Behavioral Ecology and Sociobiology 55, 561-568.
Webster, M. M. & Laland, K. N. (2015). Space-use and sociability are not related to public-information use in ninespine sticklebacks. Behavioral Ecology and Sociobiology 69, 895-907.
Westgate, M. J. & Lindenmayer, D. B. (2017). The difficulties of systematic reviews. Conservation Biology 31, 1002-1007.
Wey, T. W. & Blumstein, D. T. (2012). Social attributes and associated performance measures in marmots: bigger male bullies and weakly affiliating females have higher annual reproductive success. Behavioral Ecology and Sociobiology 66, 1075-1085.
Wey, T. W., Burger, J. R., Ebensperger, L. A. & Hayes, L. D. (2013). Reproductive correlates of social network variation in plurally breeding degus (Octodon degus). Animal Behaviour 85, 1407-1414.
Winandy, L., Di Gesu, L., Lemoine, M., Jacob, S., Martin, J., Ducamp, C., Huet, M., Legrand, D. & Cote, J. (2021). Maternal and personal information mediates the use of social cues about predation risk. Behavioral Ecology 32, 518-528.
Yang, W. J., Maldonado-Chaparro, A. A. & Blumstein, D. T. (2017). A cost of being amicable in a hibernating mammal. Behavioral Ecology 28, 11-19.
Yuen, C. H., Pillay, N., Heinrichs, M., Schoepf, I. & Schradin, C. (2015). Personality does not constrain social and behavioural flexibility in African striped mice. Behavioral Ecology and Sociobiology 69, 1237-1249.