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Network reaction norms: taking account of network position and plasticity in response to environmental change

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Abstract

Consistent inter-individual differences in behaviour are thought to be related to consistency in social network position. There is also evidence that network structures can show predictable temporal dynamics, suggesting that consistency in social network position across time does not preclude some form of plasticity in response to environmental variation. To better consider variation in network position and plasticity simultaneously, we investigate the extension of the behavioural reaction norm (BRN) to dynamic social networks. Our aim is to estimate both an individual’s position and plasticity within a network across an environmental gradient (i.e. to generate a network reaction norm (NRN)). We show that it is possible to account for the non-independence of network measures using covariance structures but that, in cases where the independent variables are group-level environmental measures, a standard multilevel model is sufficient. We therefore outline when a standard multilevel model is appropriate for NRNs and highlight the benefits and limitations to this approach. As an illustrative example, we used an NRN approach on 7 years of behavioural data on chacma baboons to quantify both the consistency with which individuals maintained social behaviour (node strength) and central positions (eigenvector centrality) within the social network. We found evidence for individual plasticity for node strength but little evidence for eigenvector centrality. Conversely, we found evidence of consistent individual differences in eigenvector centrality but not strength. These results suggest that individual node strengths are influenced by environmental changes, but the social structure of the group remains remarkably stable nevertheless. We suggest that expanding from measures of repeatability in social networks to network reaction norms will provide a more contextually nuanced way to investigate social phenotypes, leading to a better understanding of the development and maintenance of social structures in changing environments.

Significance statement

An individual’s position within a social network can have consequences for its fitness, resulting in great interest into how individuals develop and maintain particular network positions. Here, we extend the notion of behavioural reaction norms to include social network data. Given the non-independence of network data, however, the application of BRNs is not straightforward. Consequently, we have developed an alternative statistical extension that uses covariance structures to account for non-independence. Although we find that under one specific set of assumptions, it is possible to apply the standard BRN to network data. Applying this approach to data from a social group of chacma baboons, we found individual social behaviours shifted in response to environmental variables, yet the social structure of the group remained remarkably stable.

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Data availability

The data and code used for this analysis are provided at https://github.com/tbonne/NRN.

References

  • Amat JA, Masero JA (2004) Predation risk on incubating adults constrains the choice of thermally favourable nest sites in a plover. Anim Behav 67:293–300

    Article  Google Scholar 

  • Aplin LM, Farine DR, Morand-Ferron J, Cole EF, Cockburn A, Sheldon BC (2013) Individual personalities predict social behaviour in wild networks of great tits (Parus major). Ecol Lett 16:1365–1372

    Article  CAS  PubMed  Google Scholar 

  • Aplin LM, Firth JA, Farine DR, Voelkl B, Crates RA, Culina A, Garroway CJ, Hinde CA, Kidd LR, Psorakis I (2015) Consistent individual differences in the social phenotypes of wild great tits, Parus major. Anim Behav 108:117–127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barrett L, Gaynor D, Henzi SP (2002) A dynamic interaction between aggression and grooming reciprocity among female chacma baboons. Anim Behav 63:1047–1053

    Article  Google Scholar 

  • Barrett L, Henzi SP (1998) Epidemic deaths in a chacma baboon population. S Afr J Sci 94:441

    Google Scholar 

  • Barrett L, Henzi SP, Lycett JE (2006) Whose life is it anyway? Maternal investment, developmental trajectories, and life history strategies in baboons. In: Swedell L, Leigh SR (eds) Reproduction and fitness in baboons: behavioral, ecological, and life history perspectives. Springer, Cham, pp 199–224

    Chapter  Google Scholar 

  • Bierbach D, Laskowski KL, Wolf M (2017) Behavioural individuality in clonal fish arises despite near-identical rearing conditions. Nat Commun 8:15361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blaszczyk MB (2018) Consistency in social network position over changing environments in a seasonally breeding primate. Behav Ecol Sociobiol 72:11

    Article  Google Scholar 

  • Bonnell TR, Vilette C (2021) Constructing and analysing time-aggregated networks: the role of bootstrapping, permutation and simulation. Methods Ecol Evol 12:114–126

    Article  Google Scholar 

  • Brent LJ (2015) Friends of friends: are indirect connections in social networks important to animal behaviour? Anim Behav 103:211–222

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Bürkner P-C (2017) brms: an R package for Bayesian multilevel models using Stan. J Stat Softw 80:1–28

    Article  Google Scholar 

  • Caceres RS, Berger-Wolf T, Grossman R (2011) Temporal scale of processes in dynamic networks. In: 2011 IEEE 11th International Conference on Data Mining Workshops. IEEE, pp 925–932

  • Cantor M, Chaparro AAM, Beck K, Carter GG, He P, Hillemann F, Irby JK, Lang S, Ogino M, Papageorgiou D (2019) Animal social networks: revealing the causes and implications of social structure in ecology and evolution. EcoEvoRxiv Preprints. https://doi.org/10.32942/osf.io/m62gb

  • Croft DP, Krause J, Darden SK, Ramnarine IW, Faria JJ, James R (2009) Behavioural trait assortment in a social network: patterns and implications. Behav Ecol Sociobiol 63:1495–1503

    Article  Google Scholar 

  • Croft DP, Madden JR, Franks DW, James R (2011) Hypothesis testing in animal social networks. Trends Ecol Evol 26:502–507

    Article  PubMed  Google Scholar 

  • Dall SR, Bell AM, Bolnick DI, Ratnieks FL (2012) An evolutionary ecology of individual differences. Ecol Lett 15:1189–1198

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 

  • Dingemanse NJ, Wolf M (2013) Between-individual differences in behavioural plasticity within populations: causes and consequences. Anim Behav 85:1031–1039

    Article  Google Scholar 

  • Dutilleul PRL (2011) Spatio-temporal heterogeneity: concepts and analysis. Cambridge University Press, New York

    Google Scholar 

  • Farine DR (2017) A guide to null models for animal social network analysis. Methods Ecol Evol 8:1309–1320

    Article  PubMed  PubMed Central  Google Scholar 

  • Farine DR, Carter GG (2022) Permutation tests for hypothesis testing with animal social network data: problems and potential solutions. Methods Ecol Evol 13:144–156

    Article  PubMed  Google Scholar 

  • Firth JA, Sheldon BC, Brent LJ (2017) Indirectly connected: simple social differences can explain the causes and apparent consequences of complex social network positions. Proc R Soc B 284:20171939

    Article  PubMed  PubMed Central  Google Scholar 

  • Formica V, Wood C, Cook P, Brodie E III (2017) Consistency of animal social networks after disturbance. Behav Ecol 28:85–93

    Article  Google Scholar 

  • Hart JDA, Weiss MN, Brent LJN, Franks DW (2021) Common permutation methods in animal social network analysis do not control for non-independence. BioRxiv 2021.06.04.447124

  • Hart JDA, Weiss MN, Franks DW, Brent LJN (2022) BISoN: a Bayesian framework for inference of social networks. BioRxiv:2021.12.20.473541

  • Henzi SP, Forshaw N, Boner R, Barrett L, Lusseau D (2013) Scalar social dynamics in female vervet monkey cohorts. Phil Trans R Soc B 368:20120351

    Article  PubMed  PubMed Central  Google Scholar 

  • Henzi SP, Lusseau D, Weingrill T, van Schaik CP, Barrett L (2009) Cyclicity in the structure of female baboon social networks. Behav Ecol Sociobiol 63:1015–1021

    Article  Google Scholar 

  • Jacoby DM, Fear LN, Sims DW, Croft DP (2014) Shark personalities? Repeatability of social network traits in a widely distributed predatory fish. Behav Ecol Sociobiol 68:1995–2003

    Article  Google Scholar 

  • Jolles JW, King AJ, Killen SS (2020) The role of individual heterogeneity in collective animal behaviour. Trends Ecol Evol 35:278–291

    Article  PubMed  Google Scholar 

  • Krackhardt D (1988) Predicting with networks: nonparametric multiple regression analysis of dyadic data. Soc Networks 10:359–381

    Article  Google Scholar 

  • Krause S, Wilson AD, Ramnarine IW, Herbert-Read JE, Clement RJ, Krause J (2017) Guppies occupy consistent positions in social networks: mechanisms and consequences. Behav Ecol 28:429–438

    Google Scholar 

  • Leidner AK, Buchanan GM (2018) Satellite remote sensing for conservation action: case studies from aquatic and terrestrial ecosystems. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • McElreath R (2020) Statistical rethinking: a Bayesian course with examples in R and Stan. Chapman and Hall/CRC, London

    Book  Google Scholar 

  • McFarland R, Barrett L, Boner R, Freeman NJ, Henzi SP (2014) Behavioral flexibility of vervet monkeys in response to climatic and social variability. Am J Phys Anthropol 154:357–364

    Article  PubMed  Google Scholar 

  • Müller R, Pfeifroth U, Träger-Chatterjee C, Cremer R, Trentmann J, Hollmann R (2015) Surface Solar Radiation Data Set - Heliosat (SARAH) - Edition 1. Satell Appl Facility Clim Monit. https://doi.org/10.5676/EUM_SAF_CM/SARAH/V001

    Article  Google Scholar 

  • Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956

    PubMed  Google Scholar 

  • Newman M (2018) Networks. Oxford University Press, Oxford

    Book  Google Scholar 

  • O’Brien PP, Webber QM, Vander Wal E (2018) Consistent individual differences and population plasticity in network-derived sociality: an experimental manipulation of density in a gregarious ungulate. PLoS ONE 13:e0193425

    Article  PubMed  PubMed Central  Google Scholar 

  • Pearl J, Mackenzie D (2018) The book of why: the new science of cause and effect. Basic Books, New York

    Google Scholar 

  • Romano V, Duboscq J, Sarabian C, Thomas E, Sueur C, MacIntosh AJ (2016) Modeling infection transmission in primate networks to predict centrality-based risk. Am J Primatol 78:767–779

    Article  PubMed  Google Scholar 

  • Ross CT, McElreath R, Redhead D (2022) Modelling human and non-human animal network data in R using STRAND. BioRxiv:2022.05.13.491798

  • Schradin C (2013) Intraspecific variation in social organization by genetic variation, developmental plasticity, social flexibility or entirely extrinsic factors. Phil Trans R Soc B 368:20120346

    Article  PubMed  PubMed Central  Google Scholar 

  • Sevi A, Annicchiarico G, Albenzio M, Taibi L, Muscio A, Dell’Aquila S (2001) Effects of solar radiation and feeding time on behavior, immune response and production of lactating ewes under high ambient temperature. J Dairy Sci 84:629–640

    Article  CAS  PubMed  Google Scholar 

  • Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378

    Article  PubMed  Google Scholar 

  • Sueur C, Romano V, Sosa S, Puga-Gonzalez I (2019) Mechanisms of network evolution: a focus on socioecological factors, intermediary mechanisms, and selection pressures. Primates 60:167–181

    Article  PubMed  Google Scholar 

  • Tucker CB, Rogers AR, Schütz KE (2008) Effect of solar radiation on dairy cattle behaviour, use of shade and body temperature in a pasture-based system. Appl Anim Behav Sci 109:141–154

    Article  Google Scholar 

  • Turner W, Rondinini C, Pettorelli N, Mora B, Leidner AK, Szantoi Z, Buchanan G, Dech S, Dwyer J, Herold M (2015) Free and open-access satellite data are key to biodiversity conservation. Biol Conserv 182:173–176

    Article  Google Scholar 

  • van de Pol M, Wright J (2009) A simple method for distinguishing within-versus between-subject effects using mixed models. Anim Behav 77:753

    Article  Google Scholar 

  • Weiss MN, Franks DW, Brent LJ, Ellis S, Silk MJ, Croft DP (2021) Common datastream permutations of animal social network data are not appropriate for hypothesis testing using regression models. Methods Ecol Evol 12:255–265

    Article  PubMed  Google Scholar 

  • Westneat DF, Hatch MI, Wetzel DP, Ensminger AL (2011) Individual variation in parental care reaction norms: integration of personality and plasticity. Am Nat 178:652–667

    Article  PubMed  Google Scholar 

  • Westneat DF, Wright J, Dingemanse NJ (2015) The biology hidden inside residual within-individual phenotypic variation. Biol Rev 90:729–743

    Article  PubMed  Google Scholar 

  • Wice EW, Saltz JB (2021) Selection on heritable social network positions is context-dependent in Drosophila melanogaster. Nat Commun 12:3357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson AD, Krause S, Dingemanse NJ, Krause J (2013) Network position: a key component in the characterization of social personality types. Behav Ecol Sociobiol 67:163–173

    Article  Google Scholar 

  • Wolf M, Weissing FJ (2012) Animal personalities: consequences for ecology and evolution. Trends Ecol Evol 27:452–461

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank Cape Nature for providing permission for the baboon research and a host of students and assistants who contributed to the long-term data set. We would also like to thank the anonymous reviewers whose efforts greatly improved this manuscript.

Funding

This work was supported by the Leakey Foundation (USA), National Research Foundation (South Africa), and Natural Science and Engineering Research Council of Canada (NSERC) Discovery Grants to SPH and LB. LB is also supported by NSERC’s Canada Research Chairs Program (Tier 1). TB is supported by the Canada Research Chairs program (LB).

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Correspondence to Tyler R. Bonnell.

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Communicated by D. Paul Croft

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Bonnell, T.R., Vilette, C., Henzi, S.P. et al. Network reaction norms: taking account of network position and plasticity in response to environmental change. Behav Ecol Sociobiol 77, 35 (2023). https://doi.org/10.1007/s00265-023-03300-2

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