Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Cooperative interactions within the family enhance the capacity for evolutionary change in body size

Abstract

Classical models of evolution seldom predict the rate at which populations evolve in the wild. One explanation is that the social environment affects how traits change in response to natural selection. Here we determine how social interactions between parents and offspring, and among larvae, influence the response to experimental selection on adult size. Our experiments focus on burying beetles (Nicrophorus vespilloides), whose larvae develop within a carrion nest. Some broods exclusively self-feed on the carrion, while others are also fed by their parents. We found that populations responded to selection for larger adults, but only when parents cared for their offspring. We also found that populations responded to selection for smaller adults, but only by removing parents and causing larval interactions to exert more influence on eventual adult size. Comparative analyses revealed a similar pattern: evolutionary increases in species size within the genus Nicrophorus are associated with the obligate provision of care. Combining our results with previous studies, we suggest that cooperative social environments enhance the response to selection, whereas excessive conflict can prevent a response to further directional selection.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: The realized heritability of body size as a function of the different selection regimes and social environments.
Figure 2: The effect of the social environment on the response to selection, in each of the experimental treatments.
Figure 3: Adult pronotum width of burying beetle species mapped on an existing molecular phylogeny.

Similar content being viewed by others

References

  1. Carroll, S. P. et al. Applying evolutionary biology to address global challenges. Science 346, 1245993 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  2. Falconer, D. S. & Mackay, T. F. Introduction to Quantitative Genetics (Longman Group, 1996).

    Google Scholar 

  3. Merilä, J., Sheldon, B. & Kruuk, L. Explaining stasis: microevolutionary studies in natural populations. Genetica 112, 199–222 (2001).

    Article  PubMed  Google Scholar 

  4. McAdam, A. & Boutin, S. Maternal effects and the response to selection in red squirrels. Proc. R. Soc. B. 271, 75–79 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  5. Lande, R. & Kirkpatrick, M. Selection response in traits with maternal inheritance. Genet. Res. 55, 189–197 (1990).

    Article  CAS  PubMed  Google Scholar 

  6. Moore, A. J., Brodie, E. D. III & Wolf, J. B. Interacting phenotypes and the evolutionary process: I. Direct and indirect genetic effects of social interactions. Evolution 51, 1352–1362 (1997).

    Article  PubMed  Google Scholar 

  7. Wolf, J. B., Brodie, E. D. III & Moore, A. J. Interacting phenotypes and the evolutionary process. II. Selection resulting from social interactions. Am. Nat. 153, 254–266 (1999).

    Article  PubMed  Google Scholar 

  8. McGlothlin, J. W., Moore, A. J., Wolf, J. B. & Brodie, E.D. III Interacting phenotypes and the evolutionary process. III. Social evolution. Evolution 64, 2558–2574 (2010).

    Article  PubMed  Google Scholar 

  9. Drown, D. M. & Wade, M. J. Runaway coevolution: adaptation to heritable and nonheritable environments. Evolution 68, 3039–3046 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  10. West, S. A., Griffin, A. S., Gardner, A. & Diggle, S. P. Social evolution theory for microorganisms. Nat. Rev. Microbiol. 4, 597–607 (2006).

    Article  CAS  PubMed  Google Scholar 

  11. Bourke, A. F. Principles of Social Evolution (Oxford Univ. Press, 2011).

    Book  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  13. Wade, M. J., Bijma, P., Ellen, E. D. & Muir, W. Group selection and social evolution in domesticated animals. Evol. Appl. 3, 453–465 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  14. Kirkpatrick, M. & Lande, R. The evolution of maternal characters. Evolution 43, 485–503 (1989).

    Article  PubMed  Google Scholar 

  15. Hadfield, J. in The Evolution of Parental Care (eds Royle, N. J., Smiseth, P. T. & Kölliker, M. ) 267–284 (Oxford Univ. Press, 2012).

    Book  Google Scholar 

  16. Bijma, P. The quantitative genetics of indirect genetic effects: a selective review of modeling issues. Heredity 112, 61–69 (2014).

    Article  CAS  PubMed  Google Scholar 

  17. Bergsma, R., Kanis, E., Knol, E. F. & Bijma, P. The contribution of social effects to heritable variation in finishing traits of domestic pigs (Sus scrofa). Genetics 178, 1559–1570 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Wilson A. J. et al. Indirect genetic effects and evolutionary constraint: an analysis of social dominance in red deer, Cervus elaphus. J. Evol. Biol. 24, 772–783 (2011).

    Article  CAS  PubMed  Google Scholar 

  19. Schrader, M., Jarrett, B. J. M. & Kilner, R. M. Using experimental evolution to study adaptations for life within the family. Am. Nat. 185, 610–619 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  20. Scott, M.P. The ecology and behavior of burying beetles. Annu. Rev. Entomol. 43, 595–618 (1998).

    Article  CAS  PubMed  Google Scholar 

  21. Eggert, A.-K., Reinking, M. & Müller, J. K. Parental care improves offspring survival and growth in burying beetles. Anim. Behav. 55, 97–107 (1998).

    Article  CAS  PubMed  Google Scholar 

  22. Otronen, M. The effect of body size on the outcome of fights in burying beetles (Nicrophorus). Ann. Zool. Fenn. 25, 191–201 (1988).

    Google Scholar 

  23. Schrader, M., Jarrett, B. J. M. & Kilner, R. M. Parental care masks a density-dependent shift from cooperation to competition among burying beetle larvae. Evolution 69, 1077–1084 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  24. Rauter, C. M. & Moore, A. J. Quantitative genetics of growth and development time in the burying beetle Nicrophorus pustulatus in the presence and absence of post-hatching parental care. Evolution 56, 96–110 (2002).

    PubMed  Google Scholar 

  25. Lock, J. E., Smiseth, P. T. & Moore, A. J. Selection, inheritance, and the evolution of parent-offspring interactions. Am. Nat. 164, 13–24 (2004).

    Article  PubMed  Google Scholar 

  26. Schrader, M., Crosby, R. M., Hesketh, A. R., Jarrett, B. J. M. & Kilner, R. M. A limit on the extent to which increased egg size can compensate for a poor postnatal environment, revealed experimentally in the burying beetle, Nicrophorus vespilloides. Ecol. Evol. 6, 329–336 (2016).

    Article  PubMed  Google Scholar 

  27. Bartlett, J. Filial cannibalism in burying beetles. Behav. Ecol. Sociobiol. 21, 179–183 (1987).

    Article  Google Scholar 

  28. Falconer, D. S. Maternal effects and selection response. Genetics Today 3, 763–774 (1965).

    Google Scholar 

  29. Sikes, D. S., Madge, R. B. & Newton, A. F. A catalog of the Nicrophorinae (Coleoptera: Silphidae) of the world. Zootaxa 65, 1–304 (2002).

    Article  Google Scholar 

  30. Trumbo, S. T. Monogamy to communal breeding: exploitation of a broad resource base by burying beetles (Nicrophorus). Ecol. Entomol. 17, 289–298 (1992).

    Article  Google Scholar 

  31. Queller, D. C. & Strassmann, J. E. Beyond sociality: the evolution of organismality. Phil. Trans. R. Soc. B 364, 3143–3155 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  32. Sikes, D. S. & Venables, C. Molecular phylogeny of the burying beetles (Coleoptera: Silphidae: Nicrophorinae). Mol. Phylogenet. Evol. 69, 552–565 (2013).

    Article  CAS  PubMed  Google Scholar 

  33. Trumbo, S. T., Kon, M. & Sikes, D. S. The reproductive biology of Ptomascopus morio, a brood parasite of Nicrophorus. J. Zool. 255, 543–560 (2001).

    Article  Google Scholar 

  34. Boncoraglio, G. & Kilner, R. M. Female burying beetles benefit from male desertion: sexual conflict and counter-adaptation over parental investment. PLoS ONE 7, e31713 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Butler, D. asreml: asreml() fits the linear model (2009).

  36. R Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2016).

  37. Visscher, P. M. A note on the asymptotic distribution of likelihood ratio tests to test variance components. Twin Res. Hum. Genet. 9, 490–495 (2006).

    Article  PubMed  Google Scholar 

  38. Wilson, A. J. Why h 2 does not always equal VA/VP? J. Evol. Biol. 21, 647–650 (2008).

    Article  CAS  PubMed  Google Scholar 

  39. Lynch, M. & Walsh, B. Genetics and Analysis of Quantitative Traits (Sinauer, 1998).

    Google Scholar 

  40. Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. 57, 289–300 (1995).

    Google Scholar 

  41. Bates, D., Maechler, M. & Bolker, B. lme4: linear mixed-effects models using S4 classes. R package version 0.999375-39 (R Foundation for Statistical Computing, 2011).

  42. Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).

    Article  PubMed  Google Scholar 

  43. Kembel, S. W. et al. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26, 1463–1464 (2010).

    Article  PubMed  Google Scholar 

  44. Orme, D. caper: comparative analyses of phylogenetics and evolution in r. R package version 0.5.2 (R Foundation for Statistical Computing, 2013).

  45. Anduaga, S. & Huerta, C. Effect of parental care on the duration of larval development and offspring survival in Nicrophorus mexicanus Matthews (Coleoptera: Silphidae). Coleopt. Bull. 55, 264–270 (2001).

    Article  Google Scholar 

  46. Capodeanu-Nägler, A. et al. From facultative to obligatory parental care: interspecific variation in offspring dependency on post-hatching care in burying beetles. Sci. Rep. 6, 29323 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  47. Satou, A., Nisimura, T. & Numata, H. Cost and necessity of parental care in the burying beetle Nicrophorus quadripunctatus. Zool. Sci. 18, 975–979 (2001).

    Article  Google Scholar 

  48. Pukowski, E. Oekologische Untersuchungen an Necrophorus. Morph. Okol. Tiere 24, 518–586 (1933).

    Article  Google Scholar 

Download references

Acknowledgements

This project was funded by a European Research Council grant (310785_Baldwinian_Beetles), and a Royal Society Wolfson Research Merit Award, both to R.M.K. We are very grateful to S.-J. Sun and D. Howard for providing unpublished information about other burying beetle species, and to C. Creighton for discussion. We thank S. Herce Castañón for help with MATLAB; M. Barclay and R. Booth from the Natural History Museum, London for their help with the beetle collections; and K. MacLeod and P. Lawrence for commenting on earlier drafts. A. Backhouse, S. Aspinall and C. Swannack maintained the beetles while A. Attisano, E. Briolat, A. Duarte and O. de Gasperin helped in the laboratory.

Author information

Authors and Affiliations

Authors

Contributions

B.J.M.J. and R.M.K. codesigned the selection experiment. B.J.M.J. and M.S. carried the experiment out, and collected and analysed the associated data. B.J.M.J. and T.M.H. codesigned the quantitative genetic experiment and analysed the data together. D.R. helped carry out the quantitative genetic experiment. R.M.K. conceived the project and oversaw the analyses. B.J.M.J. and R.M.K. cowrote the manuscript, with contributions from M.S., T.M.H. and D.R.

Corresponding author

Correspondence to Benjamin J. M. Jarrett.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Figures 1–3, Supplementary Tables 1–4 (PDF 491 kb)

Supplementary Data 1

Data for the quantitative genetics of body size across two social environments. (XLSX 261 kb)

Supplementary Data 2

The body size data for the selection experiment. (XLSX 2413 kb)

Supplementary Data 3

Data for the family level for the selection experiment. (XLSX 457 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jarrett, B., Schrader, M., Rebar, D. et al. Cooperative interactions within the family enhance the capacity for evolutionary change in body size. Nat Ecol Evol 1, 0178 (2017). https://doi.org/10.1038/s41559-017-0178

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41559-017-0178

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing