Introduction: The significance of the problem of biological individuality

The problem of biological individuality has been central for philosophers of biology, both recently (Wilson 2005; Okasha 2006; Clarke 2011; Pradeu 2012; Bouchard and Huneman 2013; Clarke 2013; Godfrey-Smith 2013; Wilson and Barker 2013) and less recently (Hull 1978, 1980, 1992; Wilson 1999). It has also been widely discussed by biologists (e.g., Medawar 1957; Ghiselin 1974; Buss 1987; Maynard Smith and Szathmáry 1995; Michod 1999; Gould and Lloyd 1999; Pepper and Herron 2008; Queller and Strassmann 2009; West and Kiers 2009; Folse and Roughgarden 2010; Minelli 2013; Herron et al. 2013; West et al. 2015). In general, asking what a biological individual is means asking what constitutes a countable, relatively well-delineated, and cohesive unit in the living world (Hull 1992; Wilson and Barker 2013; Chauvier 2016), but of course each component of this definition needs to be explained and justified.

The exploration of the problem of biological individuality in the last two decades has led to several productive results. In particular, a quasi-consensus has emerged on some important claims. Such claims include question-dependence, rejection of anthropocentrism, the need for a hierarchical approach to individuality, and the idea that individuality comes in degrees (See Table 1).

Table 1 Consensual claims for philosophers and biologists working on biological individuality
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This consensus, incidentally, is not always acknowledged. This has sometimes led to the repetition of certain already well-established claims. It is no longer useful to argue that our conception of individuality depends on the question and scientific context under consideration, that the level of the organism is not the only one at which biological individuality can be realized, or that biological individuality is a continuous rather than a discrete property. The careful examination of the literature on biological individuality also shows that other claims—e.g., that philosophers of biology interested in biological individuality have tended to be ignorant of “real” biological examples—are simply misplaced, as illustrated by the scientifically rich contributions of those like David Hull.

However, the consensus on some major claims should not hide the fact that there are many disagreements among the participants in the debate over biological individuality. In what follows, I will examine recent challenges to philosophical accounts about biological individuality and I will explain how the papers gathered in this special issue of Biology and Philosophy posit themselves with regard to those challenges.

Recent challenges

Several objections have recently been levelled at established philosophical accounts of biological individuality (see Box 1). First, many consider those accounts exceedingly monistic. Should we favour monism or pluralism when thinking about biological individuality? The debate has at least two aspects. The first concerns the question of individuality criteria. Many different, non-overlapping, individuality criteria co-exist in the scientific and philosophical literature (Santelices 1999; Clarke 2011; Godfrey-Smith 2013). These include genetic homogeneity, germ/soma separation, the possession of a developmental bottleneck, policing mechanisms, etc. Some philosophers are monists—either in the sense that they defend one particular criterion, or insofar as they try to find a fundamental and unifying mechanism underlying several (or even all) criteria (Clarke 2013). Other philosophers are pluralists, i.e., consider there must be different criteria of individuality, reflecting different scientific questions and contexts (Wilson 1999, 2005; Pradeu 2012; Wilson and Barker 2013; Godfrey-Smith 2014; Sterner 2015; Love and Brigandt 2017). The second aspect of the debate about monism focuses on the scientific disciplines used to establish our concept of a biological individual. In their reflections about biological individuality, philosophers of biology have tended to focus on a single biological field—generally evolution (Hull 1978, 1980, 1992; Okasha 2006; Godfrey-Smith 2009; Clarke 2013). In so doing, they have left aside many biological fields where the problem of biological individuality has also played a central role, including physiology, developmental biology, immunology, ecology, the cognitive sciences, among others (Dupré and O’Malley 2009; Pradeu 2010; Minelli 2011; Godfrey-Smith 2013; Huneman 2014). The two aspects of the debate are related, at least in the sense that taking into account more biological fields is likely to increase the number of possible individuality criteria.

Box 1 Recent objections to philosophical accounts of biological individuality
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The second objection is that philosophers have unduly privileged a theoretical approach to biological individuality—at the expense of more practical and experimental considerations (Kovaka 2015; Chen 2016; Love and Brigandt 2017). The influence of Hull—and, less directly, of Quine—helps explain this situation: in several texts (e.g., Hull 1992), Hull explained that the only way to distance ourselves from intuition-based approaches to individuality was to construct a theory-based perspective (which also explains why he sees the heavily theoretical field of evolutionary biology as the best pathway to defining biological individuality). A greater attention to practices might suggest, for instance, that, in everyday life, biologists “individuate” entities in a flexible and pragmatic way, without any strong ontological commitment (Love and Brigandt 2017). Of course, it remains to be determined whether such pragmatically isolated entities should be considered “individuals” or not, and on which grounds (Chauvier 2016; Guay and Pradeu 2016a).

The third objection is that the majority of philosophers of biology have neglected the studies of the concept of biological individuality made by historians of science (Lidgard and Nyhart 2017). Many of the issues raised today about biological individuality have already been raised, in a different context, in the past. For example, the idea of nested biological individuality was examined by Leibniz in response to work by Swammerdam, Leeuwenhoek and others (Duchesneau 2010); the concept of the multicellular organism as a society of cells was analysed by Claude Bernard (1974); finally, the question of part–whole relations, complex life cycles and alternation of generations fascinated nineteenth-century biologists (Nyhart and Lidgard 2011, 2017). It would be fruitful and inspirational to examine in detail those proposals and compare them with contemporary ones. It is also worthwhile noting that historians interested in biological individuality explore various biological domainsFootnote 1—instead of focusing on the domain of evolutionary biology only. Philosophers could perhaps be inspired by this comprehensive approach to the problem of biological individuality.

The fourth objection is that these investigations into biological individuality have often been done in relative isolation from other domains which have produced interesting work on individuality (Guay and Pradeu 2016a). These domains include physics (French 2014, 2016), the social sciences (Paternotte 2016), and metaphysics (Dorato and Morganti 2011; Morganti 2013; French 2014; Chauvier 2016; Lowe 2016). Importantly, several individuality criteria are common to different sciences, but do not play exactly the same role in each science. It could, thus, be useful to compare these different situations to build a better-informed conception of individuality in biology and philosophy of biology.

Metaphysics can also be helpful. It is well known that individuality has been a central question in metaphysics for several centuries (Strawson 1959; Chauvier 2016; Lowe 2016). Metaphysicians have produced precise analyses of individuality and cognate concepts or views—for instance identity, persistence, four-dimensionalism, sortalism, among many others. These contributions could certainly help philosophers of biology produce a more precise conception of a biological individual (Guay and Pradeu 2016b; Haber 2016a). From this point of view, recent innovative work at the interface of philosophy of biology and metaphysics might call attention to several benefits philosophers of biology could get from a stronger attention to metaphysical considerations (Ferner 2016; Wiggins 2016a, b).

The fifth objection concerns conceptual uncertainties. There is considerable confusion over the definition of the notion of a “biological individual”, and of related terms such as “organism”, “whole” and “parts”, “unity”, “cohesion”, among others (Santelices 1999; Clarke 2011). In the philosophy of biology literature, we find very few attempts to offer precise definitions of those terms, even though they constitute the backbone of the debate over what a biological individual is.

To these five objections, we can add another, more traditional, one. It asks: To which biological entities can the notion of biological individuality be applied? A concept of biological individuality that would be applicable to only a small fraction of the living world—for instance to animals only—would not be satisfying from a biological point of view (unless of course we have strong biological reasons to make such a distinction). As stated, the need to avoid biases towards vertebrates or even metazoans was emphasized in early philosophical discussions about biological individuality (Hull 1978, 1992; Wilson 1999). But philosophers of biology have recently begun discussing certain neglected cases, some of which might prove challenging for traditional criteria of individuality. This includes studies of fungi (Booth 2014a; Molter forthcoming), stem cells as compared to non-stem cells (Fagan 2016), living things with highly complex life cycles including some plants (Godfrey-Smith 2016a; Griesemer 2016) and some eukaryotic microbes (O’Malley 2016), and even perhaps viruses (Forterre 2016).

The challenges above are examined at length in several recent publications. The move from theory-centrism (Objection #2) to a stronger attention to practices and experimental contexts is made in many parts of current philosophy of science (e.g., Waters 2008; Ankeny et al. 2011; Love 2015), and this move is gaining prominence in the debate about biological individuality (Chen 2016; Fagan 2016; Love and Brigandt 2017). The combination of historical and philosophical approaches (in response to Objection #3) is the main topic of a forthcoming volume edited by Scott Lidgard and Lynn Nyhart (Lidgard and Nyhart 2017). Based on an analysis of past and present-day examples, Lidgard and Nyhart propose to divide the problem of biological individuality into four sub-problems: individuation (thresholds, boundaries, inside/outside, autonomy); hierarchy (levels of organization in complex systems); horizontality (interactions among parts in making a whole); and temporality (change through time, particularly in part-whole relations). These four categories are useful to locate and compare many contemporary positions within the debate over biological individuality. In parallel, there is an on-going attempt to collate biology with other domains (which constitutes a response to Objection #4), particularly physics and metaphysics (French 2011, 2014, 2016; Ferner 2016; Guay and Pradeu 2016b; Mygal et al. 2016).

This special issue of Biology and Philosophy mainly addresses Objections #1 and #5. The next section explains how the contributions gathered here can be seen as replies to these objections.

Attempts to build a more diversified and more precise conception of biological individuality

Many of the papers gathered in this special issue are interested in the monism–pluralism debate. Should we adopt several individuality criteria, or should we favour one criterion—and if so which one and with which arguments? Should we ground our concept of individuality in several biological domains or in one given domain—and, here again, if we opt for the monistic choice, on what basis should we do so?

Philosophical debates about biological individuality have focused almost exclusively on an evolutionary approach (Hull 1978, 1980, 1992; Okasha 2006; Godfrey-Smith 2009; Clarke 2013). One organising thought that informs this special issue is that a major aim for philosophers of biology should be to account for the numerous biological fields that explore the question of biological individuality. Indeed, the incorporation, confrontation, and combination of different biological perspectives probably constitutes the most generative way of building a unified and biologically informed conception of biological individuality (see Fig. 1).

Fig. 1
figure 1

The concept of a biological individual will be enriched by a confrontation and combination of the perspectives offered by different biological domains. Only six domains are mentioned here, but many others can contribute to debates about biological individuality

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Three papers of this special issue explore the field of immunology, in which the notion of individuality has been intensively explored in the last decades (Loeb 1930, 1945; Medawar 1957; Burnet 1960; Tauber 1991; Pradeu 2012). Lynn Chiu and Gérard Eberl (2016) (a world-leading scientist in the field of gut immunology) examine host-microbe associations in light of the recently proposed “equilibrium model of immunity” (Eberl 2016). Scott Gilbert and Alfred Tauber (2016) suggest that recent work on symbiosis and so-called “holobionts” (conceived as functionally integrated and cohesive units constituted of a host and the microbes that live within and on it) casts doubt on traditional views on biological individuality, and could potentially re-orient the whole field of immunology. Thomas Pradeu (2016) uses immunology to offer a refined conception of the delineation and persistence of physiological individuals, based on the argument that the immune system constitutes, in any living thing, a mechanism of inclusion and exclusion.

Peter Godfrey-Smith (2016b) examines the relation between biological individuality and the cognitive sciences, in light of work on “minimal cognition” and the emergence of early nervous systems (Keijzer et al. 2013). Developmental biology plays a central role in the contribution of Gilbert and Tauber (2016), who have long argued for a coming together of the study of development and immunology (Tauber 1991; Gilbert 2002). Furthermore, Pradeu  (2016) shows that, over more than two centuries, physiology has produced very important analyses of biological individuality, which should be combined with evolution-based approaches.

Finally, several contributors pay attention to what the field of ecology has to say about biological individuality, including David Queller and Joan Strassmann (2016), Derek Skillings (2016), and, in an “ecological-developmental” perspective, Gilbert and Tauber  (2016) as well as Chiu and Eberl (2016).

In addition to all these biological domains, the contributors of this special issue explore, at length, studies on symbiosis. These studies do not constitute a “biological domain” as such; instead, they are located at the interface of many disciplines, including microbiology, evolutionary biology, ecology, developmental biology, immunology, among several others (McFall-Ngai 2008; McFall-Ngai et al. 2013). Symbiosis studies have flourished in the last ten years, and they have offered key insights for anyone interested in biological individuality. The fact that virtually every living thing is home to “foreign passengers”—some of which play important functional roles in the host—raises important issues regarding biological boundaries, individuality criteria based on genetic homogeneity, etc. (Gilbert 2002; Bosch and McFall-Ngai 2011; Gilbert and Epel 2015). Building on recent philosophical work on symbiosis (Pradeu and Carosella 2006; Bouchard 2009; Dupré and O’Malley 2009; Pradeu 2011; Godfrey-Smith 2013; Booth 2014b; O’Malley 2016), the contributors of this special issue examine symbiosis from different, yet complementary points of view. One major question concerns what we can call the “holobiont debate”, i.e. the question of the degree of unity and cohesion found in a holobiont. This question—particularly animated in some scientific circles (e.g., Zilber-Rosenberg and Rosenberg 2008; Bordenstein and Theis 2015; Bosch and Miller 2016; Douglas and Werren 2016; Theis et al. 2016)—is discussed in all the contributions of this special issue. Queller and Strassmann (2016) argue that complex holobionts are generally not organisms because, even when they show some cooperation, they still express levels of internal conflict that are too high to constitute organismic units. Skillings (2016) explores the holobiont debate from the point of view of the “founding” example of corals. He holds that most holobionts share more affinities with communities than they do with individual wholes, and that, in general, holobionts do not meet the criteria for being evolutionary individuals, units of selection, or organisms. In contrast, Gilbert and Tauber (2016) consider that holobionts are unified communities, acting as units from physiological, developmental, immunological, and evolutionary viewpoints. Pradeu  (2016) defends the view that, from an immunological point of view, a biological individual is made of all the components that are immunologically tolerated, which include many (but not all) microbes found in or on a host. Chiu and Eberl  (2016) assert that microorganisms are constitutive of host immunity as external scaffolds, varying in degrees of reliability, specificity, and exclusivity. In their view, even if holobionts are not internally integrated enough to qualify as organisms or units of selection, they are still individuals in a different and more general way: the holobiont must be seen as the host plus the microorganisms that scaffold its immunity. Haber (2016b) sees holobionts as nested individuals, with sometimes distinct, non-overlapping life cycles. Clarke (2016) interprets holobionts in light of reproductive synchrony (Frank 1997) and fitness alignment (Friesen 2012) between the symbiotic partners.

By offering this wide range of perspectives, we hope to offer the readers the opportunity to take a better-informed decision in favour of monism or pluralism. For pluralism-oriented people, a further choice is between a “promiscuous” pluralism (where the different perspectives coexist and remain largely autonomous) and a “combining” pluralism (where one major aim is to combine the different perspectives to produce a unified picture) (Guay and Pradeu 2016a).

In addition to examining neglected biological domains, several contributors attempt to clarify certain central concepts in this debate. Queller and Strassmann  (2016) think that the main debate should be about the notion of an organism—which they define as a unit in which all the subunits have evolved to be highly cooperative, with very little conflict (see also Queller and Strassmann 2009). Clarke (2013) defends the view that the notions of organism and biological individual are synonymous, and in her contribution to this special issue  (2016) she interprets evolutionary transitions as changes in the extent to which selection acts at one hierarchical level rather than another, a view she grounds in her definition of evolutionary individuality in terms of an object’s capacity to undergo selection at its own level. Pradeu  (2016) insists, on the contrary, on the differences between the notions of organism and biological individual; he suggests distinguishing at least two categories of a biological individual, namely the physiological individual (“unit of functioning”) and the evolutionary individual (“selective unit”). Godfrey-Smith  (2016) also distinguishes organism from evolutionary individual. Complementing previous work in which he defines evolutionary individuals as Darwinian individuals (that is, reproducing units: Godfrey-Smith 2009, 2013), he focuses on the organism, which he defines as a bounded and self-maintaining unit, engaged in traffic with its environment (see also Arnellos and Moreno 2015). Skillings (2016) also makes a difference between evolutionary individuals (which he defines, following Godfrey-Smith, as Darwinian individuals) and organisms (which he defines as bounded individuals that are functionally or metabolically integrated, i.e. systems with mutually dependent components that work together to maintain the system’s structure or developmental trajectory). Haber (2016b) offers a different perspective. He shows that, for the individuality thesis, individuals (be they organisms, species, etc.) must be understood recursively, meaning that biological individuals are “lineage-generating entities that are both constituted by and constitutive of other biological individuals”.

Our hope is that, in exploring new biological fields dealing with biological individuality, and by refining certain conceptual distinctions, this special issue will participate in the on-going project of building a conception of biological individuality that will be more unified, more inspired by historical and metaphysical considerations, and that will better reflect current biological perspectives and practices (Lidgard and Nyhart 2017).