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The stability of traits conception of the hologenome: An evolutionary account of holobiont individuality

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Abstract

Bourrat and Griffiths (Hist Philos Life Sci 40(2):33, 2018) have recently argued that most of the evidence presented by holobiont defenders to support the thesis that holobionts are evolutionary individuals is not to the point and is not even adequate to discriminate multispecies evolutionary individuals from other multispecies assemblages that would not be considered evolutionary individuals by most holobiont defenders. They further argue that an adequate criterion to distinguish the two categories is fitness alignment, presenting the notion of fitness boundedness as a criterion that allows divorcing true multispecies evolutionary individuals from other multispecies assemblages and provides an adequate criterion to single out genuine evolutionary multispecies assemblages. A consequence of their criterion is that holobionts, as conventionally defined by hologenome defenders, are not evolutionary individuals except in very rare cases, and for very specific host-symbiont associations. This paper is a critical response to Bourrat and Griffiths’ arguments and a defence of the arguments presented by holobiont defenders. Drawing upon the case of the hologenomic basis of the evolution of sanguivory in vampire bats (Nat Ecol Evol 2:659–668, 2018), I argue that Bourrat and Griffiths overlook some aspects of the biological nature of the microbiome that justifies the thesis that holobionts are evolutionarily different to other multispecies assemblages. I argue that the hologenome theory of evolution should not define the hologenome as a collection of genomes, but as the sum of the host genome plus some traits of the microbiome which together constitute an evolutionary individual, a conception I refer to as the stability of traits conception of the hologenome. Based on that conception I argue that the evidence presented by holobiont defenders is to the point, and supports the thesis that holobionts are evolutionary individuals. In this sense, the paper offers an account of the holobiont that aims to foster a dialogue between hologenome advocates and hologenome critics.

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Notes

  1. Following Dupré and O’Malley (2009), I will use the term “macrobe” or “microorganism” to refer to the mono-zygotically-descended multicellular host that composes the holobiont.

  2. Not necessarily pair associations. See e.g. Margulis and Sagan (2001).

  3. There is a previous use in a public lecture by Jefferson (1994), and in a paper about corals by Rohwer and colleagues (2002: 8, Fig. 5). However, Jefferson did not keep developing the theory, and Rohwer et al. only introduced the concept in a figure. Furthermore, contrary to what happened with the case of Reshef and colleagues, in neither of these cases was the term used immediately afterwards to open a debate about the concept of biological individuality.

  4. Sometimes also called the “hologenome concept of evolution” (Rosenberg and Zilber-Rosenberg 2013, 2016).

  5. In fact, it is likely that HTE would not be as controversial if the concept of holobiont kept its original meaning, as it was first formulated by Margulis (Díaz 2015).

  6. Most of these theses have been developed and clarified after HTE was first formulated, so the reader might not interpret this paragraph as meaning that all those theses were already clearly expressed in Zilber-Rosenberg and Rosenberg (2008). These theses correspond to different conceptual developments on the study of biological individuality and its application to the study of hologenomes (e.g. Dupré and O’Malley 2009; Dupré 2010, 2012, 2017; Pradeu 2016; DiFrisco 2017; Lidgard and Nyhart 2017).

  7. Strictly speaking, it is not accurate to identify evolutionary individuals with units of selection, since there can be units that might be argued to evolve—e.g. by neutral evolution, or by processes of sorting– despite not being naturally selected (e.g. Vrba and Gould 1986; Maynard-Smith 1987, 1991). In a strict sense, being a unit of selection is only necessary for cumulative evolution that leads to adaptations, but not for evolution per se (Suárez and Triviño 2020). Nonetheless, as the two notions are commonly used interchangeably, I will use them interchangeably in this paper as well.

  8. To clarify, by “trait” I do not mean “phenotypic trait”, but its the genetic basis (may be e.g. a gene, or a collection of genes in epistatic interaction, etc.). Also, I do not necessarily reduce genes to the DNA content of the genome, but I rather refer to what Lu and Bourrat (2017) have characterized as the “evolutionary gene” (see also Griffiths and Stotz 2013). My reasons for calling them “traits”, though, rest on the fact that the studies on the influence of the microbiome on animal evolution I build on refer to this genetic content as “trait”, plus the fact that if I used the concept of “gene”, I suspect it would be mostly taken to imply solely DNA.

  9. Similar claims can be found in late nineteenth and early twentieth century history of biology, always directed against those biologists that emphasized the integrative nature of symbiosis. Maybe the most interesting case is Pound (1893), reviewed in Suárez (2018: 80–82).

  10. Notice that their observation is not that the concept of interactor is irrelevant in evolutionary theory (cf. Okasha 2006; Godfrey-Smith 2009), but that as the concept is defined by HTE advocates, it is of little utility for deciding whether a multispecies system is an evolutionary individual. I think Bourrat and Griffiths’ point to that end is fair, although as I will argue later, they have missed some consequences of the interactor claims as they are formulated by HTE advocates that suggest that there is an evolutionary fact of the matter in arguing that holobionts are evolutionary individuals (Sects. 3, 4).

  11. This criterion may be interpreted as a formulation of the conditions for being an interactor for multispecies assemblages. Thanks to Pierrick Bourrat for clarifying this point to me.

  12. It is important to bear in mind that natural selection, to produce cumulative effects and, thus adaptation requires the existence of a population of entities where: (i) different entities exhibit different phenotypic variants, (ii) different variants have different fitness, and (iii) those variants are transmitted (Okasha 2006; Godfrey-Smith 2009). If one of the criteria (i)–(iii) is missing, then the entities might be argued to evolve, but not to evolve by natural selection. Notice that no mention is made to the nature of the entities (i.e. how they must be individuated), nor to the mechanisms by which the variants are transmitted, or the level at which transmission occurs.

  13. A very similar idea applied to the notion of “shared history” among symbiont species was already suggested in the nineteenth century by Schneider (1897). See Suárez (2018: 82–84) for a review of Schneider’s ideas. Additionally, the account bears some similarity with Bouchard’s ideas about fitness and natural selection, although it also constitutes an elaboration of these ideas (Bouchard 2013, 2014).

  14. Pierrick Bourrat has told me that this would at most prove that microbiome traits are transgenerationally recurrent, but not necessarily that evolution by natural selection is happening at the holobiont level, since for that you also need some form of parent–offspring relationship (or I would be conflating reproduction of with reproduction by, see Ariew and Lewontin 2004). Although I agree with him that mere recurrence would not be enough, but a causal basis for this recurrence is also required, I am not sure that the case I am building on is one of “mere recurrence”. First, the hypothesis is that these traits only re-occur on a very restricted population of bats, which even if it does not restrict the recurrence to parent-offspring, it substantially restricts the individuals where this recurrence is possible. Second, because I suspect (although this is open to empirical research) that the reason for this recurrence is causal: it is highly related to the biological nature of vampire bats. It would be necessary to study further the exact causal basis of that recurrence, but the case study strongly suggests that there must be a selective basis behind it.

  15. I will only discuss the case of the microbiome for it is generally accepted among scientists working on bat biology that the vampire bat genome, alone, is clearly insufficient to keep vampire bats alive on the basis of a blood-sucking diet (Mendoza et al. 2018).

  16. Of course, one may argue that the lineages that bear the traits would still keep them if their new niche is another species of vampire bat, for the family Phyllostomidae Desmoodontinae includes three species. That is true but notice that this does not invalidate the claim that the microbiome traits have their fitness interests aligned to a very reduced set of host genomes.

  17. Notice that the model I present here is strictly speaking only an argument to consider holobionts as evolutionary individuals from a multilevel selection 1 or interactor perspective (Okasha 2006; Lloyd 2017b). However, it differs from other similar approaches (e.g. Roughgarden et al. 2018; Roughgarden 2019) because it emphasises the possibility that the microbiome traits that get their frequencies increased do so in virtue of being shared among different bacterial lineages, rather that in virtue of being increased within the bacterial lineage where they originally appeared. This thus opens the possibility for a new way of conceiving the possible role of the holobiont from a multilevel selection 2 perspective, i.e. as a reproducer.

  18. The strength of hologenomic selection will of course depend on the strength of selection at the level of the lineages that compose the host microbiome, as well as on the possibility of the specific traits undergoing hologenomic selection to get transferred horizontally to different lineages in the microbiome. This fact can may hologenomic selection inefficient in most cases. However, whether it is inefficient or not is open to empirical investigation and cannot be solved merely on a conceptual basis.

  19. Importantly, nothing of what I have said entails that the traits in the microbiome are coevolving with the host genome. This may be the case, and that situation would create more pressure for these traits to become motile elements. However, it is not necessarily so. An evolutionary individual is a unit whose elements have their fitness interests aligned, but not necessarily a unit whose elements are coevolving. See Brucker and Bordenstein (2013, 2014) for an excellent argument to that end.

  20. One reviewer argues that this form of independence seems to entail a form of emergence that rejects reductive physicalism, and that would require separate defence. I defend that view in Suárez and Triviño (2020).

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Acknowledgments

Different versions of this paper have been presented in the IAS-Research Seminar (University of the Basque Country, 2017), the European Philosophy of Science Association 17 (University of Exeter, 2017), the IX Conference of the Spanish Society for Logic, Methodology and Philosophy of Science (UNED, Madrid, 2018), the International Society for History Philosophy and Social Studies of Biology 2019 (University of Oslo, 2019), and the Congress of Logic, Methodology and Philosophy of Science and Technology 2019 (University of Prague, 2019). I acknowledge all the participants for their comments and feedback. Special thanks to John Dupré, for his constant feedback and encouragement, and Staffan Müller-Wille and Samir Okasha for having discussed these ideas with me in the wider context of my doctoral thesis. Also, thanks to Thomas Bonnin, Seth Bordenstein, Pierrick Bourrat, Mark Canciani, Roger Deulofeu, Ford Doolittle, Scott Gilbert, Cipran Jeler, William Jones, Ehud Lamm, Lisa Lloyd, Lisandra Z. Mendoza, Álvaro Moreno, Maureen O’Malley, Eugene Rosenberg, Elliot Sober, Adrian Stencel, Vanessa Triviño, Davide Vecchi, Sophie Veigl, Ken Waters, and Ilana Zilber-Rosenberg for having read and discussed previous versions of this paper with me.

Funding

Funding was provided by Spanish Ministry of Education (Grant No. FFU16/02570), Ministerio de Economía y Competitividad (Grant No. FFI2016-76799-P), and The Royal Institute of Philosophy.

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Suárez, J. The stability of traits conception of the hologenome: An evolutionary account of holobiont individuality. HPLS 42, 11 (2020). https://doi.org/10.1007/s40656-020-00305-2

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