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Patterns and consequences of age-linked change in local relatedness in animal societies

Nature Ecology & Evolution volume 6, pages 1766–1776 (2022)Cite this article

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Abstract

The ultimate payoff of behaviours depends not only on their direct impact on an individual, but also on the impact on their relatives. Local relatedness—the average relatedness of an individual to their social environment—therefore has profound effects on social and life history evolution. Recent work has begun to show that local relatedness has the potential to change systematically over an individual’s lifetime, a process called kinship dynamics. However, it is unclear how general these kinship dynamics are, whether they are predictable in real systems and their effects on behaviour and life history evolution. In this study, we combine modelling with data from real systems to explore the extent and impact of kinship dynamics. We use data from seven group-living mammals with diverse social and mating systems to demonstrate not only that kinship dynamics occur in animal systems, but also that the direction and magnitude of kinship dynamics can be accurately predicted using a simple model. We use a theoretical model to demonstrate that kinship dynamics can profoundly affect lifetime patterns of behaviour and can drive sex differences in helping and harming behaviour across the lifespan in social species. Taken together, this work demonstrates that kinship dynamics are likely to be a fundamental dimension of social evolution, especially when considering age-linked changes and sex differences in behaviour and life history.

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Fig. 1: Predicted male and female kinship dynamics under three demographic scenarios.
Fig. 2: Predicted (left-hand panels, orange outline) and observed (right-hand panels, black outline) kinship dynamics for males (green) and females (purple) in seven species of group-living mammal.
Fig. 3: Selection on group directed behaviours given kinship dynamics under three dispersal scenarios.

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Data availability

Data to reproduce these analyses are available at https://doi.org/10.17605/OSF.IO/PZFEX. Anonymized data to derive kinship dynamics are included for banded mongooses, chimpanzees, killer whales and spotted hyena. Data sharing agreements mean that for the remaining species, anonymized data to reproduce the analysis need to be requested from the corresponding author, all other forms of data request should be addressed to the manager of the system in question.

Code availability

Code to reproduce these analyses are available at https://doi.org/10.17605/OSF.IO/PZFEX. The repository includes a Mathematica file to run and reproduce the mathematical model; R code to implement the kinship dynamics simulation model and R code to analyse both the simulation and observed kinship dynamics data. A simplified version of the simulation model can be explored at samellisq.shinyapps.io/kinship_dynamics_shinyapp_basic/ or downloaded from github.com/samellisq/kinship_dynamics_shinyapp. In addition, an R package, comparekin, created as part of this study, can be accessed at https://www.github.com/samellisq/comparekin.

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Acknowledgements

This project was conceived and funded as part of a Natural Environment Research Council (NERC) standard grant (no. NE S010327/1) awarded to D.P.C., S.E., R.A.J., D.W.F. and M.A.C., which also supported M.N.W. S.E. also acknowledges funding from a Leverhulme Early Career Research Fellowship. We thank members of the Centre for Research in Animal Behaviour at the University of Exeter for useful discussion and comments. We also thank K. Holekamp, E. Strauss and M. Sawdy for their engagement and support of this project. This study constitutes an international collaboration combining theoretical work and long-term empirical data from seven research projects on free-ranging mammals. These decade-long field research projects were supported by funds from: National Environment Research Council (NERC) (Banded Mongoose Research Project), Max Planck Society, European Research Council (ERC) and Swiss National Foundation (Taï Chimpanzee Project), DEFRA and NERC (Woodchester Park Badger Project), NERC (Center for Whale Research), ERC, NCRR and Office Invoirien des Parcs et Réserves of NIH (Caribbean Primate Research Center), Leibniz-IZW, DFG, DAAD, Werner Dessauer Stiftung and Messerli Stiftung (Ngorongoro Hyena Project), National Science Federation, National Institutes of Health, Duke University, Princeton University and University of Notre Dame (Amboseli Baboon Project). We also thank the local authorities for permission to conduct long-term field research in: Uganda (Uganda Wildlife Authority and Uganda National Council for Science and Technology to the Banded Mongoose Research Project), Ivory Coast (MESRSCI, Ministère des Eaux et Forêts and OIPR to the Taï Chimpanzee Project), Canada and the United States (FOC, DFO to the Center for Whale Research), Tanzania (TAWIRI, COSTECH and Ngorongoro Conservation Area Authority to the Ngorongoro Hyena Project), Kenya (KWS, NACOSTI and National Environment Management Authority to Amboseli Baboon Project). Detailed acknowledgements associated with each project are listed in Supplementary Text 2.

Author information

Author notes

  1. These authors contributed equally: Michael A. Cant, Daniel W. Franks, Michael N. Weiss.

Authors and Affiliations

  1. Centre for Research in Animal Behaviour, University of Exeter, Exeter, UK

    Samuel Ellis, Michael N. Weiss, Lauren J. N. Brent & Darren P. Croft

  2. Department of Zoology, University of Cambridge, Cambridge, UK

    Rufus A. Johnstone

  3. Centre for Ecology and Conservation, University of Exeter, Penryn Campus, Penryn, UK

    Michael A. Cant, Magali Meniri & Faye J. Thompson

  4. Departmen t of Biology, University of York, York, UK

    Daniel W. Franks

  5. Center for Whale Research, Friday Harbor, WA, USA

    Michael N. Weiss, Kenneth C. Balcomb & David K. Ellifrit

  6. Department of Biology, Duke University, Durham, NC, USA

    Susan C. Alberts

  7. Department of Evolutionary Anthropology, Duke University, Durham, NC, USA

    Susan C. Alberts

  8. National Wildlife Management Centre, Animal and Plant Health Agency, Sand Hutton, York, UK

    Claire H. Benton & Richard J. Delahay

  9. Institut des Sciences Cognitives, CNRS, Lyon, France

    Catherine Crockford

  10. Department of Human Behavior, Ecology and Culture, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany

    Catherine Crockford & Roman M. Wittig

  11. Taï Chimpanzee Project, Centre Suisse de Recherches Scientifique, Abidjan, Côte d’Ivoire

    Catherine Crockford & Roman M. Wittig

  12. Department of Primatology, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany

    Catherine Crockford & Linda Vigilant

  13. Department of Evolutionary Ecology, Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany

    Eve Davidian & Oliver P. Höner

  14. Ngorongoro Hyena Project, Ngorongoro Conservation Area, Arusha, Tanzania

    Eve Davidian & Oliver P. Höner

  15. Environment and Sustainability Institute, University of Exeter, Penryn Campus, Penryn, UK

    Robbie A. McDonald

  16. Department of Biosciences, Swansea University, Swansea, UK

    Hazel J. Nichols

  17. German Centre for Integrative Biodiversity Research, Leipzig, Germany

    Roman M. Wittig

Authors
  1. Samuel Ellis
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  2. Rufus A. Johnstone
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  3. Michael A. Cant
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  4. Daniel W. Franks
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  5. Michael N. Weiss
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  6. Susan C. Alberts
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  7. Kenneth C. Balcomb
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  8. Claire H. Benton
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  9. Lauren J. N. Brent
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  10. Catherine Crockford
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  11. Eve Davidian
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  12. Richard J. Delahay
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  13. David K. Ellifrit
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  14. Oliver P. Höner
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  15. Magali Meniri
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  16. Robbie A. McDonald
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  17. Hazel J. Nichols
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  18. Faye J. Thompson
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  19. Linda Vigilant
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  20. Roman M. Wittig
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  21. Darren P. Croft
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Contributions

S.E., R.A.J., M.A.C., D.W.F., M.N.W. and D.P.C. conceived and designed the study programme. S.E. designed and implemented the analysis, made the figures and wrote the first draft of the manuscript with input from R.A.J., M.A.C., D.W.F., M.N.W. and D.P.C. R.A.J. designed and implemented the analytical model with M.A.C. and with input from S.E., D.W.F., M.N.W. and D.P.C. Data from long-term research projects were contributed, collected and managed by: M.A.C., M.M., H.J.N., F.J.T (banded mongoose data); C.C., L.V., R.M.W. (chimpanzee data); C.H.B., R.J.D., R.A.M. (European badger data); K.C.B., D.K.E., M.N.W. (killer whale data); L.J.N.B. (rhesus macaque data); E.D., O.P.H. (spotted hyena data) and S.C.A. (yellow baboon data). All authors contributed to later drafts of the manuscript and approved it for publication.

Corresponding author

Correspondence to Samuel Ellis.

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Nature Ecology & Evolution thanks Mark Dyble and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary information

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Supplementary Text 1–4, Tables 1–8, Figs. 1–6 and References.

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Ellis, S., Johnstone, R.A., Cant, M.A. et al. Patterns and consequences of age-linked change in local relatedness in animal societies. Nat Ecol Evol 6, 1766–1776 (2022). https://doi.org/10.1038/s41559-022-01872-2

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