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‘The importance of symbiosis in philosophy of biology: an analysis of the current debate on biological individuality and its historical roots’

Abstract

Symbiosis plays a fundamental role in contemporary biology, as well as in recent thinking in philosophy of biology. The discovery of the importance and universality of symbiotic associations has brought new light to old debates in the field, including issues about the concept of biological individuality. An important aspect of these debates has been the formulation of the hologenome concept of evolution, the notion that holobionts are units of natural selection in evolution. This review examines the philosophical assumptions that underlie recent proposal of the hologenome concept of evolution, and traces those debates back in time to their historical origins, to the moment when the connection between the topics of symbiosis and biological individuality first caught the attention of biologists. The review is divided in two parts. The first part explores the historical origins of the connection between the notion of symbiosis and the concept of biological individuality, and emphasizes the role of A. de Bary, R. Pound, A. Schneider and C. Merezhkowsky in framing the debate. The second part examines the hologenome concept of evolution and explores four parallelisms between contemporary debates and the debates presented in the first part of the essay, arguing that the different debates raised by the hologenome concept were already present in the literature. I suggest that the novelty of the hologenome concept of evolution lies in the wider appreciation of the importance of symbiosis for maintaining life on Earth as we know it. Finally, I conclude by suggesting the importance of exploring the connections among contemporary biology, philosophy of biology and history of biology in order to gain a better understanding of contemporary biology.

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Fig. 1

Notes

  1. Many authors still argue that the definition of symbiosis are not clear at present, e.g. Wilkinson (2001), Douglas (2010: 4), Martin and Schwab (2013).

  2. The review is not about the problem of biological individuality and how different biologists and philosophers have conceived the topic; rather, this review is about the relation between symbiosis and certain dimensions of the problem of biological individuality –the boundaries and composition of the biological individual and the units of selection. However, the reader must at least take into account that three different notions of biological individual will be considered, especially in part 2: biological individuals as functionally integrated units, biological individuals as units of selection and biological individuals as bounded units (with clear physical boundaries, such as a membrane). Readers interested in the philosophical problem of biological individuality might refer to Wilson and Barker (2013), Bouchard and Huneman (2013), Pradeu (2016a), DiFrisco (2017) and Lidgard & Nyhart (2017: 17-63).

  3. There are alternative ways to spell his name (e.g. Merezhkovski, Mérejkovski, Mereschkovsky). I use the spelling that appears in Sapp et al. (2002).

  4. My historical focus is selective and not exhaustive, since I aim to compare four parallelisms between the historical development of the concept of symbiosis and the recent developments of the concept of holobiosis. The reconstructed history I will present will reflect this interest. For the readers who are interested in seeing different historical reconstructions see Sapp (1994), Paracer & Ahmadjian (2000: 231-238), Wilkinson (2001), Peacock (2011), Martin and Schwab (2012), Egerton (2015), Carrapiço (2015), Gontier (2015, 2016a), Zook (2015).

  5. Frank N. Egerton, however, in his review paper on the history of symbiosis studies dedicates the first section to studies of symbiotic phenomena that appeared before the concept of “symbiosis” was introduced (2015: 81–90). He goes as far as to Herodotus, Aristotle and Theophrastus. Despite the interest of their research, as far as this review is about the philosophical implications of the concept and its relation to other philosophical concepts, I have chosen to begin with de Bary’s account.

  6. Parasitism was known while before van Beneden, but parasites (including those that we might call nowadays microorganisms, Pasteur’s germs) were basically considered as pursuing their own interests, thus necessarily damaging the other in a context of struggle for life (e.g. Spencer 1899; cf. Sapp 1994: 25–28). Precisely, what is innovative about van Beneden’s work was that he was the first in: (1) identifying the existence of an important number of associations among organisms that are not parasitic, a discovery that of course had historical precedents; (2) classifying the different types of biological associations in virtue of their effects in a systematic way, which is also conceptually different from previous views on the economy of nature (Egerton 2015: 84).

  7. It is important to note that lichenologists originally rejected Schwendener’s dual hypothesis (e.g. Crombie 1886), denying in some cases the evidence, among other reasons because its acknowledgment would threaten “the hard-won autonomy of lichenists themselves” (Sapp 1994: 4), in so far as lichens would stop being an independent biological individual. Interestingly, lichenologists did not lose their autonomy and it was precisely the study of lichens as dual individuals that began challenging traditional ways of understanding biological individuals more generally. This is the first moment, to my knowledge, that the problem of symbiosis and the philosophical problem of biological individuality get engaged in a way that questions the traditional conception of what counts as a biological individual.

  8. One of the reasons why symbiosis became identified with mutualism during this period is related to the influence of the political ideas of the time, especially the anarchist ideas of Kropoptkin (1902). Readers interested in the influence of political ideas on symbiosis thinking can refer to Sapp (1994: 18-25) and Gontier (2016a).

  9. Although he did not call them Rhizobium, but “tubercles,” stating “For all that I have read and seen, I am satisfied that the parasites [in Leguminosae] are bacteria, and I see no reason for separating them from the rest of Schizomycetes as Schneider does. I even doubt the necessity of creating a separate genus for them, as Frank did in 1890, under the name of ‘Rhizobium’” (Pound 1893: 517).

  10. See Oldroyd (2013) to realize that some of Frank’s observations were indeed true and Pound, while having a fair point about the lack of proper evidence for some of Frank’s statements, could have not been more mistaken.

  11. Pound’s seems to assume a concept of biological individuality similar to what Queller and Strassmann have recently called the “cooperation/conflict conception” of the biological individual (2009, 2016). For Pound, as it happens for the authors, symbiotic assemblages cannot be considered individuals in the proper sense, as the entities that engage in the symbiosis are in constant struggle with each other.

  12. It must be noted, although in passing, that Schneider does not require that the two organisms that engage in symbiosis belong to different species: he only requires that they are morphologically different. That’s why, from his perspective, the mother and the embryo/foetus, the sexual cells that merge to form a zygote or even tumours or cysts would count as cases of symbiosis. This is, I think, different from de Bary’s original purpose –probably that’s why Schneider says that he uses symbiosis “in its broader meaning, not in the sense of De Bary” (1897: 923, fn. 1)–, who seemed to understand symbiosis requiring different species.

  13. Schneider acknowledges the problems of this position, which can be criticized on the same basis as Pound had criticized Frank’s account of mycorrhiza –“[t]hat every tree has its root system covered with mycelia, proves nothing” (Pound 1893: 516). However, he justifies his decision by claiming “[f]rom a priori reasoning one is, however, forced to conclude that the first symbiotic activities began with the first contact of organisms” (1897: 933).

  14. See part II of the paper for seeing how these sorts of claims are presently unsustainable.

  15. Of course, extinction of the symbiotic association, but not necessarily of the partners that interact symbiotically. Remember that Schneider’s paper aims to study exclusively the phylogenetic evolution of symbiotic associations without reference to the organisms that interact.

  16. Those readers who are not familiar with the different types of biological individuals (physiological, anatomical, developmental, evolutionary, etc.) can check Gilbert et al. (2012), Godfrey-Smith (2013), Pradeu (2016a, b), DiFrisco (2017). In brief, however, it is important that she notes that not all criteria for classifying biological individuals necessarily led to coincidental classifications and sometimes different criteria overlap. For the overlapping nature of biological classification see Clarke (2010).

  17. It is widely acknowledged that chloroplasts are responsible for the green colour of plants.

  18. Maynard-Smith does not use “units of selection”, but “units of evolution”, where a unit of selection is whatever entity exhibit phenotypic variation that led to multiplication of the entity within the population (thus being selected for or against), and a unit of evolution is a unit of selection that, furthermore, exhibits heredity (Maynard-Smith 1987). In contrast with Maynard-Smith, I will use “unit of selection” as it is conventionally used, i.e. requiring heredity, variance and fitness/multiplication, and thus meaning what Maynard-Smith means by “unit of evolution” (see Lloyd 2017a, c: 293–297; Gontier 2010, for an analysis of the concept of “unit of selection”)

  19. Originally, they referred to it as the hologenome theory of evolution. Later on, they started calling it the hologenome concept of evolution (cf. Gissis et al. 2017: 303–384).

  20. A clear antecedent to the hologenome concept is found in Sapp (2003: 234-251, 2004), when he coins the concept of “symbiome”. He defines the symbiome as the entity “comprising chromosomal genes, organellar genes, viral genes, as well as other microbial symbionts, sometimes inside cells and always outside them, functioning across a continuum from parasitism to mutualism, depending on their nature and context (…). Since every plant and animal consists of complex ecological communities of microbes, the symbiome must function as a unit of selection.” (2004: 1047). Nonetheless, Sapp first presents the concept in a section dedicated to developmental symbiosis (Sapp 2003: 235–236), and there is no reason to believe that a developmental organism should be delineated by the same boundaries than a unit of selection (e.g. DiFrisco 2017). The concept of “symbiome”, however, is not as frequent in current literature as the concept of “holobiont” and it has been recently used with two different meanings: first, to refer to the whole set of symbionts that associate with a host, without including the host (e.g. Boucias et al. 2013; Rosas-Pérez et al. 2017); second, to refer exclusively to “the colocalized and coevolving taxa in a given consortium” (Tripp et al. 2017: 552). If we define the concept according to the second formulation, then one might argue either that symbiome = hologenome (if the hologenome is proven to evolve as a single unit) or that the symbiome corresponds to the part of the hologenome that actually evolves as a single unit (e.g. the set of vertically transmitted symbionts). This warrants further discussion, which is, however, outside the scope of this paper. For my present purposes I will restrict the discussion to the concept of the holobiont sui generis.

  21. “Such that replication is differential” does not specify which are the entities whose differential replication might be affected by belonging to an interactor. It is conceptually possible that the holobiont is an interactor that promotes a more efficient replication of the different individuals that compose the holobiont (host, microbes of the microbiome), but not of the hologenome.

  22. This position is taken to the extreme in Doolittle (2017).

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Acknowledgments

I would like to thank Staffan Müller-Wille, Sabina Leonelli, Caglar Karaca, John Dupré, José Díez, who read previous versions of this manuscript and made helpful comment. Benjamin Smart is especially acknowledged for all his help and detailed comments in the final version of the manuscript. Finally, I would like to thank two anonymous reviewers for their comments, which clearly helped in improving the content and structure of the paper. This work was economically supported by the Spanish Ministry of Education (FFU16/02570) and the Spanish Ministry of Economy and Competitiveness (FFI2016-76799-P).

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Suárez, J. ‘The importance of symbiosis in philosophy of biology: an analysis of the current debate on biological individuality and its historical roots’. Symbiosis 76, 77–96 (2018). https://doi.org/10.1007/s13199-018-0556-1

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Keywords

  • Symbiosis
  • History of biology
  • Philosophy of biology
  • Biological individuality
  • Hologenome
  • Holobiont
  • Units of selection