Abstract
We assess the arguments for recognising functionally integrated multispecies consortia as genuine biological individuals, including cases of so-called ‘holobionts’. We provide two examples in which the same core biochemical processes that sustain life are distributed across a consortium of individuals of different species. Although the same chemistry features in both examples, proponents of the holobiont as unit of evolution would recognize one of the two cases as a multispecies individual whilst they would consider the other as a compelling case of ecological dependence between separate individuals. Some widely used arguments in support of the ‘holobiont’ concept apply equally to both cases, suggesting that those arguments have misidentified what is at stake when seeking to identify a new level of biological individuality. One important aspect of biological individuality is evolutionary individuality. In line with other work on the evolution of individuality, we show that our cases can be distinguished by focusing on the fitness alignment between the partners of the consortia. We conclude that much of the evidence currently presented for the ubiquity and importance of multi-species individuals is simply not to the point, at least unless the issue of biological individuality is firmly divorced from the question of evolutionary individuality.
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Notes
Following Rosenberg and Zilber-Rosenberg (2013, 4), by “symbiosis” we mean mutualistic relationship between two or more partners. The examples we use in this article will involve partners that live in close proximity.
Note that there exists a literature which understands ecosystems as individuals (for reviews see Huneman 2014a, b; Van Baalen and Huneman 2014). As recognized by Huneman (2014a), this notion of individual is different from the notion of individuality typically used in evolutionary biology, the latter of which is the focus of our analysis. For that reason, we will not discuss the view of ecosystems as individuals, although we recognize that some connections between the literature on holobionts and ecosystems as individuals exist.
For an overview of this cycle see Sievert et al. (2007).
For O’Malley’s more recent views on the topic of biological individuality, see O’Malley (2016).
While the adjective gnotobiotic is often used to refer to germ-free animals, it is a more inclusive term that refers to situations where we know all the microorganisms on or in an organism, including cases where there are none at all (see Rooks and Garrett 2016, Box 2).
As pointed out by the Staffan Müller-Wille, one difference between the two systems might be in the specificity of associations between the partners. As mentioned earlier, this question remains an empirical one.
Although see the recent arguments against this view by Clarke (2016).
For a discussion on the mechanisms by which partners of a multispecies unit might align their fitness see O’Malley (2016).
For an extended discussion of how Developmental Systems Theorists can bridge this missing step in the argument, see Griffiths and Stotz (2018).
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Acknowledgements
We are thankful to Maxime Ardré, Brett Calcott, Guilhem Doulcier, Andrew Holmes, Arnaud Pocheville, Steven Quistad, Paul Rainey, Karola Stotz and Elena Walsh for their comments on a previous version of the manuscript. We are particularly thankful to Andrew Holmes and Arnaud Pocheville for discussions on this topic. This research was supported under Australian Research Council’s Discovery Projects funding scheme (Project DP0878650).
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Bourrat, P., Griffiths, P.E. Multispecies individuals. HPLS 40, 33 (2018). https://doi.org/10.1007/s40656-018-0194-1
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DOI: https://doi.org/10.1007/s40656-018-0194-1