Article

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

  • Nature Ecology & Evolution 1, Article number: 0178 (2017)
  • doi:10.1038/s41559-017-0178
  • Download Citation
Received:
Accepted:
Published online:

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.

  • Subscribe to Nature Ecology & Evolution for full access:

    $99

    Subscribe

Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.

References

  1. 1.

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

  2. 2.

    & Introduction to Quantitative Genetics (Longman Group, 1996).

  3. 3.

    , & Explaining stasis: microevolutionary studies in natural populations. Genetica 112, 199–222 (2001).

  4. 4.

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

  5. 5.

    & Selection response in traits with maternal inheritance. Genet. Res. 55, 189–197 (1990).

  6. 6.

    , & Interacting phenotypes and the evolutionary process: I. Direct and indirect genetic effects of social interactions. Evolution 51, 1352–1362 (1997).

  7. 7.

    , & Interacting phenotypes and the evolutionary process. II. Selection resulting from social interactions. Am. Nat. 153, 254–266 (1999).

  8. 8.

    , , & Interacting phenotypes and the evolutionary process. III. Social evolution. Evolution 64, 2558–2574 (2010).

  9. 9.

    & Runaway coevolution: adaptation to heritable and nonheritable environments. Evolution 68, 3039–3046 (2014).

  10. 10.

    , , & Social evolution theory for microorganisms. Nat. Rev. Microbiol. 4, 597–607 (2006).

  11. 11.

    Principles of Social Evolution (Oxford Univ. Press, 2011).

  12. 12.

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

  13. 13.

    , , & Group selection and social evolution in domesticated animals. Evol. Appl. 3, 453–465 (2010).

  14. 14.

    & The evolution of maternal characters. Evolution 43, 485–503 (1989).

  15. 15.

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

  16. 16.

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

  17. 17.

    , , & The contribution of social effects to heritable variation in finishing traits of domestic pigs (Sus scrofa). Genetics 178, 1559–1570 (2008).

  18. 18.

    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).

  19. 19.

    , & Using experimental evolution to study adaptations for life within the family. Am. Nat. 185, 610–619 (2015).

  20. 20.

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

  21. 21.

    , & Parental care improves offspring survival and growth in burying beetles. Anim. Behav. 55, 97–107 (1998).

  22. 22.

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

  23. 23.

    , & Parental care masks a density-dependent shift from cooperation to competition among burying beetle larvae. Evolution 69, 1077–1084 (2015).

  24. 24.

    & 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).

  25. 25.

    , & Selection, inheritance, and the evolution of parent-offspring interactions. Am. Nat. 164, 13–24 (2004).

  26. 26.

    , , , & 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).

  27. 27.

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

  28. 28.

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

  29. 29.

    , & A catalog of the Nicrophorinae (Coleoptera: Silphidae) of the world. Zootaxa 65, 1–304 (2002).

  30. 30.

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

  31. 31.

    & Beyond sociality: the evolution of organismality. Phil. Trans. R. Soc. B 364, 3143–3155 (2009).

  32. 32.

    & Molecular phylogeny of the burying beetles (Coleoptera: Silphidae: Nicrophorinae). Mol. Phylogenet. Evol. 69, 552–565 (2013).

  33. 33.

    , & The reproductive biology of Ptomascopus morio, a brood parasite of Nicrophorus. J. Zool. 255, 543–560 (2001).

  34. 34.

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

  35. 35.

    asreml: asreml() fits the linear model (2009).

  36. 36.

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

  37. 37.

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

  38. 38.

    Why h2 does not always equal VA/VP? J. Evol. Biol. 21, 647–650 (2008).

  39. 39.

    & Genetics and Analysis of Quantitative Traits (Sinauer, 1998).

  40. 40.

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

  41. 41.

    , & lme4: linear mixed-effects models using S4 classes. R package version 0.999375-39 (R Foundation for Statistical Computing, 2011).

  42. 42.

    , & APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).

  43. 43.

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

  44. 44.

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

  45. 45.

    & 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).

  46. 46.

    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).

  47. 47.

    , & Cost and necessity of parental care in the burying beetle Nicrophorus quadripunctatus. Zool. Sci. 18, 975–979 (2001).

  48. 48.

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

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

Affiliations

  1. Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK.

    • Benjamin J. M. Jarrett
    • , Darren Rebar
    •  & Rebecca M. Kilner
  2. Department of Biology, The University of the South, Sewanee, Tennessee 37383, USA.

    • Matthew Schrader
  3. Centre for Ecology and Conservation, University of Exeter (Penryn Campus), Penryn TR10 9FE, UK.

    • Thomas M. Houslay

Authors

  1. Search for Benjamin J. M. Jarrett in:

  2. Search for Matthew Schrader in:

  3. Search for Darren Rebar in:

  4. Search for Thomas M. Houslay in:

  5. Search for Rebecca M. Kilner in:

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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Benjamin J. M. Jarrett.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    Supplementary Figures 1–3, Supplementary Tables 1–4

Excel files

  1. 1.

    Supplementary Data 1

    Data for the quantitative genetics of body size across two social environments.

  2. 2.

    Supplementary Data 2

    The body size data for the selection experiment.

  3. 3.

    Supplementary Data 3

    Data for the family level for the selection experiment.