Holobionts and the ecology of organisms: Multi-species communities or integrated individuals?

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Abstract

It is now widely accepted that microorganisms play many important roles in the lives of plants and animals. Every macroorganism has been shaped in some way by microorganisms. The recognition of the ubiquity and importance of microorganisms has led some to argue for a revolution in how we understand biological individuality and the primary units of natural selection. The term “holobiont” was introduced as a name for the biological unit made up by a host and all of its associated microorganisms, and much of this new debate about biological individuality has focused on whether holobionts are integrated individuals or communities. In this paper, I show how parts of the holobiont can span both characterizations. I argue that most holobionts share more affinities with communities than they do with organisms, and that, except for maybe in rare cases, holobionts do not meet the criteria for being organisms, evolutionary individuals, or units of selection.

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  • 22 August 2018

    In the original publication, the acknowledgment was published incorrectly. The correct version is given below.

Notes

  1. 1.

    O’Malley has since moved away from this view, recently stating that natural selection probably does not act at the collective level in multilineal systems, of which holobionts are one kind (O’Malley forthcoming).

  2. 2.

    See Clarke (2011) for a thorough survey of accounts of organismality and individuality.

  3. 3.

    I thank Thomas Pradeu for emphazing this point, as well as pointing out the gap in my treatment of physiological individuality in a previous draft.

  4. 4.

    I thank Thomas Pradeu for emphasizing this point.

  5. 5.

    See Sterelny (2006) for a similar argument regarding the individuation of ecosystems.

  6. 6.

    See Huss (2014) for an extended discussion and warning about reifying categories such as metagenome, microbiome and enterotype.

  7. 7.

    One reviewer suggested that many of the claims about holobionts as units of selection found in the quotations presented in the section entitled “Controversy about the Status of Holobionts” be interpreted as claims about holobionts being interactors. I disagree that this is the correct interpretation of the presented views. At the very least, it is unclear exactly what the quoted authors mean when they say holobionts are a unit of selection.

  8. 8.

    Bouchard (2013) presents a similar view, arguing that “superindividuality” can emerge in persistent, functionally-integrated, multispecies communities.

  9. 9.

    Queller and Strassmann (this issue) argue that it is extremely unlikely that any holobionts qualify as organisms.

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Acknowledgments

This paper found its impetus in conversations with Austin Booth and many of the ideas were worked out in discussion with him. I also thank Peter Godfrey-Smith, Jessie McCormack, Maureen O’Malley, Thomas Pradeu, the participants of the 2015 Philosophy of Biology at Dolphin Beach workshop, and three anonymous reviewers for their help and useful comments.

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Correspondence to Derek Skillings.

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Skillings, D. Holobionts and the ecology of organisms: Multi-species communities or integrated individuals?. Biol Philos 31, 875–892 (2016). https://doi.org/10.1007/s10539-016-9544-0

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Keywords

  • Holobiont
  • Symbiosis
  • Individuality
  • Organism
  • Bacteria
  • Microbe