Genetic relatedness and its causal role in the evolution of insect societies

Abstract

The role of genetic relatedness in social evolution has recently come under critical attention. These arguments are here critically analyzed, both theoretically and empirically. It is argued that when the conceptual structure of the theory of natural selection is carefully taken into account, genetic relatedness can be seen to play an indispensable role in the evolution of both facultative and advanced eusociality. Although reviewing the empirical evidence concerning the evolution of eusociality reveals that relatedness does not play a role in the initial appearance of helper phenotypes, this follows simply from the fact that natural selection – of which relatedness is a necessary component – does not play a causal role in the origin of any traits. Further, separating two logically distinct elements of causal explanation – necessity and sufficiency – explains why the debate lingers on: although relatedness plays a necessary role in the evolution of helping and advanced eusociality, relatedness alone is not sufficient for their appearance. Therefore, if the relatedness variable in a given data set is held at a uniformly high value, then it indeed may turn out that other factors occupy a more prominent role. However, this does not change the fact that high relatedness functions as a necessary background condition for the evolution of advanced eusociality.

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Notes

  1. 1.

    Note that the value of ‘eusociality’ as a term describing insect sociality has been heavily criticized by Boomsma and Gawne (2017), who make a strong case for more precise terminology and specification of the traits whose evolution is being analyzed. Thus, while the articles under analysis here do not necessarily make such distinctions, we separate, whenever possible, between facultative eusociality (societies with reproductive division of labor that is behavioral and at least partly reversible, and thus conceptually similar to various forms of cooperative breeding) and obligate or advanced eusociality (‘organismal’ societies with physically separated castes and irreversible reproductive division of labor).

  2. 2.

    This claim, almost verbatim, is also made by Wilson and Hölldobler (2005, p. 13367) and Wilson and Wilson (2007, p. 340).

  3. 3.

    As above, we note (cf. Boomsma 2009, 2013; Boomsma and Gawne 2017) here that the analysis of Hughes et al. (2008) does not assess the role of life-time full-sibling relatedness, that seems to be limited to the advanced eusocial taxa, and thus does not account for the possibility of remating by the mother, or the possibility of the replacement of the reproductive individual, which would cause deviations from maximal life-time relatedness.

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Acknowledgements

We would like to thank Dr Neil Bell, Prof. Kristian Donner, Dr Luke Holman, Dr Gunther Jansen, Dr Jani Raerinne, Dr Isaac Salazar Ciudad, Dr Tobias Uller and an anonymous referee of the Journal of Biosciences for helpful comments and criticism on various versions of this article. This work has been financially supported by the Academy of Finland (grants #140990, #135970, #251337 and #284666) (HH), the Ella & Georg Ehrnrooth foundation (HH and TKP), the Emil Aaltonen Foundation (TKP), the Finnish Academy of Science and Letters (TKP), Kone Foundation (HH and TKP) and the Waldemar von Frenckell Foundation (TKP).

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Correspondence to Tuomas K Pernu.

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Corresponding editor: NG Prasad

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Pernu, T.K., Helanterä, H. Genetic relatedness and its causal role in the evolution of insect societies. J Biosci 44, 107 (2019). https://doi.org/10.1007/s12038-019-9894-2

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Keywords

  • Behavioral ecology
  • causal explanation
  • causal necessity
  • causal sufficiency
  • causation
  • group selection
  • inclusive fitness
  • kin selection
  • levels of selection
  • models
  • natural selection
  • necessary conditions
  • sociobiology