emergentist slogan, according to which “the (higher-level) whole is more than the sum of its (simultaneous, lower-level) parts.”

Yet, recent developments have shown that there actually exists a bona fide (fam-
ily of) concept(s) of emergence that is free of both these assumptions and which is
referred to as “transformational emergence” (Humphreys, 2016; Guay & Sartenaer,
2016; Guay & Sartenaer, 2018).<fnref n="12" /> In contrast with traditional emergence, transfor-
mational emergence is *diachronic*, the putative emergent being typically instanti-
ated later than its emergence basis, and *not hierarchical*, both the emergent and the
basis belonging to the same level. What matters for us here is that, as its name sug-
gests, transformational emergence is not driven by organization*, but rather by
transformation. In a nutshell, the uniqueness or distinctiveness of emergents doesn’t
come about because unchanging entities are organized* in a very idiosyncratic way.
Rather, it comes about because these entities themselves are *transformed* in a very
idiosyncratic way.

Let us illustrate the contrast that is at stake here by considering the case of a putatively emergent organism.<fnref n="13" /> In the traditional perspective, an organism at time *t* emerges from a basis made of cells at *t*, for the organism is considered both dependent on and autonomous from these cells. For instance, in the ontologically modest declination of organicism, one could argue that the organism at *t* is constituted by its cells at *t* and that the former is able to downwardly constraint the behavior of these cells at *t*. In this first perspective, that the organism is able to do so proceeds from the fact that the organism is an organization* of its constitutive cells.

Things are different in the transformational perspective. It is indeed rather con-
sidered there that an emergent organism at *t* both depends on, and is autonomous
from, a basis made of cells at a previous time *t*'. For example, it could be contented
that the organism at *t* is causally or nomologically dependent on the cells at *t*' and
that the former exercises at *t* causal powers that are different from any combination
of the causal powers that the cells had at *t*'. In this second speculative scenario, that
the organism has new causal powers at *t* proceeds from the fact that the cells that
make it up at *t* are ontologically different from the cells at *t*', for the latter have been
properly transformed. As it appears, the organism at *t* is nothing “over and above” a
sum of cells at *t* – it actually is a mere organization, and not an organization*, of
these cells at *t* – though it is ontologically distinct from any sum of cells at *t*'. Under
the form of a slogan: with transformational emergence, “the whole just is the sum
of the parts that have been transformed.” It is noteworthy that, in such a view, the

<footnote n="12">¹²Of course, these developments have some historical precedents, among which Humphreys (1997)'s own "fusion emergence." Epistemological variants of transformational emergence have also been proposed, for instance, by Bedau (1997) or Rueger (2000). Despite the fact that "transformational emergence" is a label that is sometimes used interchangeably with the one of "diachronic emergence," I will stick here to the convention that consists in considering transformational emergence as a subspecies of diachronic emergence, which has the peculiarity of being flat and ontological.</footnote>

<footnote n="13">¹³Just to be clear: I do not offer here the slightest argument to support the claim that organisms are in fact emergent (synchronously or transformationally).</footnote>
<table><caption>**Table 6.2** Varieties of organicism along both dimensions X and Y, together with the type of emergence they are committed to. “S” and “D” subscripts stand for “synchronic” and “diachronic,” to the effect that the corresponding causal determination is to be considered downward and flat, respectively</caption><thead><tr><th>X</th><th>Organicism</th><th>Determination (Y)</th><th>Emergence</th><th>Physicalism</th></tr></thead><tbody><tr><td rowspan="3">Org.*</td><td>Thin</td><td>Logical</td><td>Weak</td><td>Yes</td></tr><tr><td>Modest</td><td>Non-causal</td><td>Modest</td><td>Yes?</td></tr><tr><td>Meaty</td><td>Causal</td><td>Strong<sub>S</sub></td><td>No</td></tr><tr><td>Transf.</td><td>Transf.</td><td>Causal</td><td>Strong<sub>D</sub></td><td>Yes</td></tr></tbody></table>

organism and the sum of the transformed cells are one and the same thing, to the effect that the emergence at stake is “flat” or nonhierarchical.

Now, should organisms be transformationally emergent entities, their determinative effectiveness would be of a causal nature. As a result, the emergence at play could be considered as “strong,” according to the terminological convention adopted above. Yet, it is important to emphasize that such a strong emergence would not be inconsistent with physicalism, to the extent that, in a diachronic and flat scenario, the newly acquired causal powers are unambiguously physical (for the physical level is the only level there is)<fnref n="14" />. Accordingly, and in contrast with the corresponding synchronic scenario, the very idea of transformationally emergent organisms – though strong – doesn’t encounter the risk of any detrimental acquaintance with putatively disreputable forms of vitalism.

Table 6.2 summarizes the upshot of this discussion. “Transformational organism” just is the view according to which [O<sup>o</sup>] and [O<sup>em</sup>] come out as true when X is fixed on transformation rather than on organization*.

At this stage of the discussion, answering the main question of this chapter requires a last step, which is to be taken in the next, last section. It only remains to be shown that transformation is a legitimate scientific process, which indeed leads to transformational emergents being (causally) determinative in their own right.

## 6.4 Transformational Organicism and the Autonomy of Biology

This last section, at the term of which I’ll finally be able to answer the question I started with, is structured in two moments. First, I’ll show that transformational emergentism is a conceptually viable view – both in general and, in particular, in its organicist declination – to the extent that there is at least one proper construal of transformation that does the job of securing the irreducible determinative

<footnote n="14">¹⁴ For more detail on that point, see Sartenaer (2018b). In a nutshell, transformational emergence is immune to Kim-style exclusion arguments and, as such, allows for consistently combining in a same package causal irreducibility and the causal closure of the physical world.</footnote>
effectiveness of transformational emergents and, in so doing, grounding the autonomy of the science that study them. In and of itself, this first endeavor is sufficient to answer my main question, whose nature is essentially conceptual. Second and as a bonus, I will briefly explore the idea that there could well be transformational emergents at stake in organismic biology, consistently with claims made by organicists themselves.

### 6.4.1 Transformational Organicism Is Conceptually Sound

In order to support the claim that transformational organicism is a conceptually viable view, I offer here what essentially amounts to an argument by analogy.

Let us suppose that “condensalism” is a view that is conceptually analogous to organicism, the chauvinist claim of uniqueness being merely shifted from organisms to condensed materials. Coherently with the previous discussion, a possible twofold definition of condensalism would thus be as follows:

> [C<sup>o</sup>] – X makes (some) condensed matter emerge<sup>Y</sup> from a physical basis, that is, it makes (some) condensed matter what it is – a determinative<sup>Y</sup> entity in its own right. That (some) condensed matter is such makes condensed matter physics an autonomous science.

And:

> [C<sup>em</sup>] – There is some restricted class of entities in nature, namely, (some) condensed matter, that has X.

In what follows, I argue that there is a suitable, scientifically kosher transformation X that makes both [C<sup>o</sup>] and [C<sup>em</sup>] true, with Y being then fixed on transformational or strong<sub>D</sub> emergence, or, equivalently, “flat” causal determination. On this basis, I then simply exploit the hypothesized conceptual analogy to support the truth of the following claim:

> [O<sup>o</sup>] – Transformation makes organisms transformationally emergent from a physical basis, that is, it makes organisms what they are – (causally) determinative entities in their own right. That organisms are such makes biology an autonomous science.

At this stage, my main objective will be met: organization<sup>*</sup>, and organization a fortiori, will have been shown not to be necessary for organicism. As an extra, I'll also propose some further considerations in the next section that will provide some preliminary reasons to also take as true the further, empirical claim:

> [O<sup>em</sup>] – There is some restricted class of entities in nature, namely, organisms, that are the product of a transformation.

This being said, I now turn to providing support for the truth of [C<sup>o</sup>] and [C<sup>em</sup>], with X being fixed on transformation. For this purpose, I here exploit the results of some previous works, in which the emergentist position of a prominent figure in
contemporary physics, namely, the 1999 Nobel Prize winner Robert Laughlin, has been philosophically reconstructed in a transformational perspective (Guay & Martenaer, 2016; Guay & Martenaer, 2018). In a nutshell, what has been shown there is that the organicist's general methodology, as described in Sect. 2.2, can also be found at play in the debate that pertains to the putative reducibility of condensed matter physics to particle physics. More particularly, it is possible to argue that the physics of some worldly phenomena supports the following argumentative schema: there is transformational emergence in condensed matter physics (empirical claim). Therefore, condensed matter is determinative (qua condensed matter; ontological claim). Therefore, condensed matter physics is autonomous from particle physics (epistemological claim).

It is not the place here to extensively develop the way in which such an argumen-
tative structure can be uphold (the interested reader is kindly asked to look into the
relevant papers for more detail). I content myself with highlighting its most rele-
vant steps:

* There is a well-documented phenomenon in physics, called the quantum Hall effect, that occurs when some piece of conductor, in which an electric current flows, is placed in a strong, orthogonal magnetic field at very low temperature. The effect in question manifests itself through the existence of plateaus of constant Hall resistance (associated with the transverse current induced), which occur for certain values of the applied magnetic field. These plateaus can be ordered according to a certain filling factor, which can take either integer values only – we then speak of the “integer quantum Hall effect” [IQHE] – or fractional values, the effect is then referred to as the “fractional quantum Hall effect” [FQHE].

* The FQHE is generally associated with the coming into being of a new type of (quasi)particle called “anyon” (Laughlin, 1999, 863; Laughlin doesn’t use that term, which comes from Wilczek). Anyons have a striking peculiarity: they obey fractional statistics, making them neither bosons nor fermions. As it appears, anyons are to be counted among the elementary particles of nature, on the model of photons (which are bosons) and electrons (which are fermions).

* The FQHE can be seen as the result of a transformation of a state of a physical system that involves electrons, to a state of the same system with anyons. Such a transformation leads to anyons being transformationally emergent from electrons, in the sense that the former both (diachronically and nonhierarchically) depend on and are autonomous from the latter. In particular, although anyons are a product of a transformation of electrons, they have new determinative powers and obey new laws. These powers are new in a strong sense: they are forbidden to exist in the pre-transformation phase according to natural laws. This striking observation has a theoretical counterpart: the quantum electrodynamical model that best captures the pre-transformation state lacks the resources for “talking about” anyons (it can actually only describe bosons and fermions). In the words of Laughlin himself: “[The discoverers of the effect – his Nobel co-laureates
Tsui and Stormer – found something] which should have been impossible”
(Laughlin, 2005, 77).

* Accordingly, the science that study materials in which anyons arise is autono-
mous<sup>15</sup>. Rather than a “Theory of Everything” that will serve as the final and
unique basis for explaining all there is – including the behavior of anyons – sci-
ence is rather made of many irreducible “theories of things” (Laughlin & Pines,
2000, 30).

The upshot of this is condensalism is a viable view (though it can of course be mis-
taken as a true description of our world), so is therefore transformational organicism.

6.4.2 Is Transformational Organicism More than Just
Conceptually Sound?

I see two ways in which a transformational version of organicism can be claimed to
be more than just a conceptually consistent view. Without going as far as supporting
the idea that there actually are proper transformations at stake in the biological
world, together they at least provide hints that transformational organicism would
deserve philosophical scrutiny.

A first way to go in this respect is to make use of an a fortiori argument. In the
previous section, it has been claimed that there could be a proper transformation
leading to transformational emergence in physics, to the effect that [C<sup>em</sup>] was given
some plausibility. Should such a claim go through, it would indirectly support the
truth of [O<sup>em</sup>], for, a fortiori, if some relevant transformation does take place in the
physical world, one could expect it to also occur in the biological world. After all,
biological entities just are (or are also) physical entities. Without claiming of course
that something like the FQHE occurs within organisms, it would be unsurprising
that transformations of a similar nature occur among the very elementary constitu-
ents of organisms, for then “percolating up,” so to speak, to the organisms themselves.

This apart, another (certainly stronger) case can be made that trans-formational
organicism deserves further exploration. It essentially rests on the fact that organicists
themselves may have advocated – implicitly to be sure – something along the lines of
transformational emergence. As an example, I here consider Soto et al. (2008)’s
approach to emergence as it would be substantiated in developmental biology.

As I see it, the core of their approach can be captured through the three following
ingredients: diachrony, downward causation, and the breaking of the causal closure

<footnote n="15"><sup>15</sup>Obviously, as the considerations developed here make it clear, the idea of autonomy understood under the transformational perspective is slightly different from the one associated with traditional, synchronic emergence. In the transformational approach, the usual epistemic cutoffs have to be understood diachronically. For instance, non-derivability, unpredictability, or non-explainability has to hold between antecedent and posterior states, and not between higher- and lower-level states. For more details about the impact of such a way of construing autonomy onto the structure of science, see Sartenaer (2019).</footnote>
of the physical world. For any philosopher that is well-versed in the arcane of the emergence literature, this for sure appears as a quite odd combination. Indeed, if one takes these ingredients at face value, they together delineate a position that happens not to take the best of two worlds, as it were. In the pursuit of biology's autonomy, buying into diachrony alone could actually be enough – this is the main message of transformational emergence – to the extent that there is no need to endorse an extra, possibly controversial commitment to downward causation and the correlative breaking of the causal closure of the physical world. Similarly, biology's autonomy could very well be advocated on the basis of a commitment to the existence of downward causation and the correlative breaking of causal closure, without adding a nonconventional, diachronic twist to the picture.

In the face of what thus appears as an unnecessary metaphysical inflation, two interpretative options are available. First, what *really* matters to Soto et al.'s emergence is downward causation (and the correlative breaking of closure), diachrony being a rather peripheral, extra ingredient. If this is the case, then their account happens to collapse on O'Connor and Wong (2005)'s theory of emergence, which itself is to be taken as conceptually isomorphic to *synchronically* strong emergentism, its self-proclaimed diachronic nature notwithstanding (Wilson, 2015). The issue with this first option is blatant: as it was emphasized in Sect. 3.1, it “dangerously” looks like full-fledged vitalism.<fnref n="16" />

Hopefully, a second option is available. It consists in taking diachrony seriously while not sticking to the letter of the traditional way of framing downward causation (and its purported implications on closure). There are reasons to believe that this actually is Soto et al.'s implicit strategy. For one thing, they are adamant about the importance of taking time seriously – “Time is acting [...]. This action is real and has an ontological meaning” (Soto et al., 2008, 271). But furthermore, they also seem to adopt a conception of downward causation that is very different from what emergentists usually have in mind when appealing to the notion (most of the time critically). As they put it: “[B]asic properties are changing [...]. This is the meaning of downward causation” (*Ibid*., 272). That the very determinative effectiveness of emergents is to be understood through the changing of basic properties should ring a bell. This is indeed nothing else than the defining claim of transformational emergentism. Keeping in mind that the main motto of transformational emergence is indeed that novelty comes from the “parts” changing through time (rather than being organized*), the following kind of claim renders the association rather legitimate:

> By the time the tissue is formed, the 'parts' that we identify in them are no longer the parts that interacted in their formation. The cellular components now present did not pre-exist the tissue itself – they are interacting in a particular way that is reciprocal. When we artificially separate the components of the tissue, for instance the cells forming epithelium and its

<footnote n="16">¹⁶ It is noteworthy that such an association is not a source of great trouble for O'Connor and Wong, as they are explicitly willing to defend a version or property dualism at the service of a libertarian agenda. And what doesn't seem (apparently) *that* unreasonable when it comes to the obscurities of the mind turns out to be less legitimate when it comes to biological phenomena.</footnote>
subjacent stroma, cells cease to perform the functions they executed when together in their
proper three-dimensional arrangement (*Ibid*., 268).

Though it is not the time and place to initiate a new philosophical exploration, it is
noteworthy that the viability of the transformational emergence that is at stake here
rests on the assumption that (at least some) biological kinds should be functionally
individuated, to the effect that a given biological entity, say a cell, is to become a
new individual as soon as it begins or ceases to exercise its proper function in the
organism. Such an idea is certainly not heretical, especially with respect to organi-
cism, as the words of one of the founding fathers of the view indicate:

> If a large bomb is dropped upon a populous town we might apply the term ‘town-plasm’ to
> the debris which remained, but it would be a little absurd to say that towns were composed
> of such town-plasm, and that from a sufficient knowledge of such debris it would be pos-
> sible to gain an adequate knowledge of the organization of towns (Woodger, 1929, 294).

In such a (unnecessarily morbid) scenario, it is indeed contended that the very
process of a town’s explosion is not to be construed as the disruption of an organiza-
tion*, the unchanging parts – town-plasm – being once organized* and then not
anymore. Rather, the town’s explosion is a proper *transformation*: what was at some
point an individual (let’s say, the roof of a bank and the gates of a school) simply
stops being such once the explosion occurred.

6.4.3 A Possible Objection and the Way Forward

Before wrapping up, it is important to defuse a possible objection that might be
raised against the conceptual possibility of a genuine form of transformational
organicism<fnref n="17" />. In a nutshell, the objection goes as follows: as it has been shown in
Sects. 4.1 and 4.2, it might be the case that transformational emergence does occur
in nature, be it within some (possibly restricted classes of) physical or biological
systems. Accordingly, transformational emergence might serve as a possible tool
for arguing in favor of the autonomy of certain scientific fields within the physical
and the biological sciences, as well as, incidentally, within other areas of science
(e.g., the chemical, psychological, or sociological sciences). But, should that indeed
be the case – and here actually lies the objection – what appears as transformational
emergentism’s very high degree of *generality* is largely outbalanced by its concomi-
tant low degree of *specificity*. As such and with regard to what really matters here,
the previous discussion does not provide legitimate reasons why organisms (or
other biological systems for that matter) should be transformationally emergent in a
specific way and, accordingly, why the specific science that study them, namely,
biology, should be autonomous.

<footnote n="17">¹⁷ I would like to thank a reviewer of this chapter as well as the editor of the volume for having drawn my attention to this possible issue.</footnote>
I think this objection actually picks up on an important point. It reveals a possible blind spot in the reflection carried out so far, whose origin lies, I think, in the very conceptual, generic, and decontextualized methodology that has been adopted to drive home the chapter's main point. Indeed, when organicism is conventionally characterized through [O<sup>em</sup>], "X makes organisms emerge<sup>Y</sup> from a physical basis. That organisms emerge<sup>Y</sup> makes biology an autonomous science" – it reduces the inherent subtlety of the view to its core autonomist end, irrespective of the specificity of the *mean* to reach it. And with such a chosen focus, it is the very "chauvinist" flavor of some variants of organicism – intimately associated with the claim that organisms are somehow of a quite unique and remarkable nature – that is downplayed.

In the face of such an objection, I see two countermoves. First, in the spirit of *avoiding* – rather than defusing – the issue, one might be willing to bite the bullet. For all we know, not all organicists, past, present, and even future, need to be chauvinists about organisms and might actually find themselves happy with the idea that the autonomy of biology is not intrinsically tied to some empirical fact – be it organization* or transformational emergence – that should *only* obtain within organisms. But, in the spirit of reaching to as many strands of organicism as I could, I'd rather adopt a second, more interesting strategy.

Though this has not been frontally addressed so far, I actually believe that there are ways in which organicists' chauvinism might be safeguarded along the lines of the empirical thesis [O<sup>em</sup>] established in Sect. 2.2 ("there is some *restricted* class of entities in nature, namely, organisms, that are the product of a transformation"). Put differently, there actually is a story to tell about the possible specificity of transformational emergentism as applied to biology. Although exploring this line of thought in detail is certainly the topic of a completely different paper, it is worthwhile mentioning here two possible strategies in that regard, which both take inspiration from Dobzhansky's (1973) famous *dictum*: "Nothing in biology makes sense except in the light of evolution."

A first way to go would be through the following steps:

* (i) Natural selection, which is the driving force of evolution, has the ontological status of a law of nature (Reed, 1981).

* (ii) Natural selection is a fundamental, nonderivative law of nature (Rosenberg, 2006)<fnref n="18" />

* (iii) There is room in all the available metaphysical frameworks about laws of nature for the possibility that the set of fundamental laws changes through time (Sartenaer et al., 2021). In particular, there is room for thinking that (the law of) natural selection wasn't "preformed" before some instant in time, at which it actually "appeared" together with whatever constituted the first units of selection.

<footnote n="18">¹⁸ A claim that is often cast in terms of natural selection being a “force” that cannot be reduced to other forces (be they evolutionary or not). That Rosenberg actually embraces some form of reductionism, that he considers the law of natural selection as being (oddly) chemical in character, or that he doesn’t necessarily embrace some form of nomic realism isn’t what matters here. The point is that considering the law of natural selection as fundamental isn’t completely heretical.</footnote>
* (iv) That the set of fundamental laws actually at play at some instant in time can change is taken to be a coextensive with transformational emergence (Humphreys, 2016; Guay & Sartenaer, 2016).

* (v) The first units of selection – *and only them* – are transformationally emergent.

It is noteworthy that this argumentative schema is only claimed to have *programmatic* validity. Rather than properly legitimizing a chauvinist version of transformational organicism – which it clearly doesn’t – the proposed schema reduces to what merely constitutes a possible research agenda for the view.

Given that this first strategy is intimately associated with the ontological category of laws of nature, and given that such a category might plausibly be totally out of place in biology (Smart, 1959), one might be willing to envision an alternative approach that rather relies upon an ontological category that is better suited for biology, and to which the category of laws of nature may be taken to reduce, namely, *individuals* or *objects* (and their properties, in the spirit of, e.g., Machamer et al. (2000)). Such an alternative approach, which also has the validity of a research plan, goes as follows:

* (i) Biological evolution has been the occasion of several “major evolutionary transitions” (Szathmary & Maynard Smith, 1995).

* (ii) While some of these transitions were “organizational” or holistic, some were rather “transformational” (Jablonka & Lamb, 2006) – like the one from RNA to DNA – in the sense that they were diachronic and flat (or “rank-free”; Okasha, 2011).

* (iii) Such transitions were the occasion of the coming into being of new biological individuals (Godfrey-Smith, 2011; Clarke, 2013).

* (iv) The advents of such new individuals are to be construed as instances of transformational emergence.

Obviously, a lot should be said in order to provide (iv) with some plausibility, though it strikes me as perfectly congruent with Soto, Sonnenschein, and Miquel’s line of though as described in Sect. 4.2, where the ontological nature of emergence at stake is to be grounded in a change in objects rather than laws.

As it appears, in the face of the objection according to which transformational emergentism might fail to be specific to biology, and hence fall short of appropriately grounding some (chauvinist) variants of organicism, there exist some prospects – to be fully fleshed out to be sure – of rendering the view sufficient for vindicating the autonomy of biology.

## 6.5 Conclusion: The Good Fortune of Organicism

Contrary to the received wisdom, I showed in this chapter that organicism could actually fare well even if, for some reason, it finally turned out that organization* is an illegitimate notion. That organicism doesn’t really need organization in order to
remain chauvinist about organisms and autonomist about biology doesn't entail, to be sure, that organization is not a good way, or even the best way, to meet such standards. The claim made in this chapter is of a purely conceptual nature: there certainly is a possible world in which, although organisms are not organized*, organicism is a flourishing doctrine that happens to be true.

Though certainly not conventional, organicism without organization*, or transformational organicism, has some prima facie interesting features, which together concur to make it an option in the reductionism/antireductionism debate that deserves further exploration. To begin with, transformational organicism has no need to reify “levels of nature,” so it happens to be consistent with the currently rising deflationism about levels in the philosophy of biology (see Potochnik and McGill (2012) and Eronen (2015)). Incidentally, as it eschews any commitment to putative forms of downward determination, there is no risk for transformational organicism to be assimilated to dualistic forms of vitalism, nor to be undermined by Kim-style exclusion arguments, which notoriously cast doubts on the very viability of (even thinly) ontological forms of (synchronic) emergence (Kim, 2005).

As it appears, with such a backup plan, the prospects of organicism look very good indeed.

**Acknowledgments** I would like to thank Argyris Arnellos, Charbel El-hani, Giuseppe Longo, Carlos Sonnenschein, Ana Soto, Charles Wolfe, and more broadly, the audience of the Paris workshop: *Organisation as a Theoretical Principle for the Life Sciences*, for helpful comments and discussions on an earlier version of this chapter. I also thank the editor of this volume, Matteo Mossio, for his numerous advices, comments and suggestions, which considerably helped improve my thoughts on this topic. Finally, I gratefully acknowledge the financial support of the Alexander von Humboldt Foundation.

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Chapter 7

Organisms: Between a Kantian Approach and a Liberal Approach

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Check for
updates

Philippe Huneman

**Abstract** The concept of “organism” has been central to modern biology, with its definition and philosophical implications evolving since the nineteenth century. In contemporary biology, the divide between developmental and physiological approaches and evolutionary approaches has influenced the definition of organism. The convergence between molecular biology and evolutionary biology has led to the term “suborganismal biology,” while the return to the organism has been characterized by animal behavior studies and Evo-devo. The philosophical approach to the concept of individual is divided between a Kantian understanding of organism, which defines necessary and sufficient conditions for any X to be a “natural purpose,” and an evolutionary approach, which considers what a biological individual is and confers natural selection a key role in this definition. While the former aims to find necessary and sufficient conditions for an organism, the latter thinks in terms of conceptual spaces, being much more liberal in pointing out organisms in the world. The paper examines possible connections between these two approaches and assesses the prospects of a reconciliation between them.

The notion of organism stands between self-evidence and inscrutability: self-evidence, because someone outside of theoretical biology would easily agree that most of the living things are organisms or, in other words, that whatever life is, it comes under the form of “organisms;” and inscrutability, because when one wants to make sense of organisms, difficulties are innumerable: What do make them different from other complex systems? Should they be principally understood as products of evolution, as, according to Huxley’s phrase, “bundles of adaptation?” Are they just an instance of *an organization* or something specific that requires more than “organization” to be understood?

In current days, this difficulty appears even more pressing, for at least two reasons. Borrowing the usual distinction between functional biology and evolutionary biology that Ernst Mayr has drawn based on a difference between proximate and

<footnote>P. Huneman (✉)
Institut d'Histoire et de Philosophie des Sciences et des Techniques (IHPST, CNRS/Paris1
Sorbonne), Paris, France</footnote>
ultimate causation (Mayr, 1961), let's survey these reasons. In molecular biology, the pervasiveness of network thinking (e.g., Barabasi, 2018, Newman, 2010) challenges the idea that biological systems should be investigated mechanically or in a reductionist way (i.e., starting from the parts – cells or molecules – and their dispositions). Thus, it contributed to the rise of systems biology (Kitano, 2002, Green, 2013), an approach designed to address organisms as wholes irreducible to the effects of their parts, that is, as a set of instructions given by the genes. While the hope of elaborating the basic explanatory repertoire of biology at the suborganismal level of macromolecules vanishes, the notion of the organism itself, engaged by systems biology, requires a novel theoretical framework.

On the other hand, it has been repeatedly said that the Modern Synthesis in evolutionary biology tended to confer organisms an ancillary status because the basic evolutionary processes stand at the levels of genes and populations. Organisms were something to be explained, as Dawkins (1976) suggests by wondering why genes tend to coalesce into organisms instead of living by themselves; or they were an instance supposedly left aside by evolutionary biology, whereas developmental biology or Evo-devo rightly take organisms as a structuring concept: this omission of organisms was the target of the famous “spandrel paper” by Gould and Lewontin, whose major claim is the inability of the current evolutionary biology to soundly handle organisms. Walsh (2017) sees evolutionary theory as a “suborganismal” account (opposed to a potential organismal one). But for more than a decade, evolutionary theory has been undergoing major controversies about the necessity to revise or expand (Gould, 2002) the modern synthesis framework, and one important issue arising here concerns the status of organisms (Bateson, 2005, Huneman, 2010). Several dimensions of the claim of a return of the organism coexist:

* The idea that organisms contribute to causing their environment (named *niche construction*, Odling-Smee et al., 2003).

* The idea that some variation can be heritable and directed toward adaptation, for instance, based on *phenotypic plasticity* (West-Eberhard, 2003; Sultan, 2015, Walsh, 2015).

* The relevance of organismal development to evolution, while it has been separated from evolution on the ground of various concurring conceptual distinctions, such as development vs inheritance, somatic vs germinal lineages, or even lately those-called “central dogma of molecular biology”.

Evo-devo has been built around this call to reintegrate developing organisms in evolution (e.g., Raff, 1996; Gilbert et al., 1996), and the developmental systems theory (Griffiths & Gray, 1994; Oyama et al., 2001) is a general account intending to replace genes by developmental cycles as units of selection or evolution.

All these critiques were noticeably led by philosophers (e.g., Walsh, Stotz, Griffiths, Oyama) and biologists alike.

Granted, claims that organisms have been neglected from evolutionary biology seem unfair, to the extent that behavioral ecology is the science of the traits of organisms as adaptations and in general conceives of evolution at the level of organismal phenotypes – named “strategies” (see Grodwohl, 2019). However, what’s left out from
behavioral ecology is the sense of the integration of all the strategies within one organism – hence, the specific sense of the organization of the organism, which was precisely the target of Gould and Lewontin (1978) under the name of *Bauplan*, a term borrowed from the German tradition of transcendental morphology in the late nineteenth century.

From the viewpoint of either functional or evolutionary biology, this organismal organization should therefore be the object of a theorizing effort. This is not to say that such an effort does not exist. On the contrary, most of what labels itself “theoretical biology,” from Rashevsky on, thought intensively about what the organization of an organism is, using ideas forged by some inaugural figures of this tradition (Rashevsky, D’Arcy Thompson, Rosen, Ganti, to name a few). In this paper, I will consider that two threads of thought about organisms coexist in biology and will leave out this tradition of theoretical biology; the question of explicitly articulating these two trends to such tradition should be the object of another paper. One of these threads is mostly found in the circles of developmental biology or Evo-devo and philosophically owes a lot to Kant; the other is mostly elaborated by evolutionary biologists and I will argue that it is much more liberal than the former one. They give room to two general ways of thinking about how the two notions of biological *individual* and *organism* are connected. After having presented these two accounts of what organisms are – and their highly different methodologies – I will say a word about their respective conditions of validity.

# 7.1 Making Sense of Organisms: The Kantian View

## 7.1.1 Purposiveness

Among philosophers who addressed biology before the Darwinian turn, Immanuel Kant cannot be overlooked. His *Critique of Judgment* provides an “analytic of teleological judgment” that has often been interpreted as an inquiry into the conditions of possibility of biology.<fnref n="1" /> And his key claim that “organisms” (or organized being, *Organisierte Wesens*) are the “natural purposes” (*Naturzwecke*) directly connects with the idea that ‘organism’ became a crucial concept for biology at the times of Kant’s philosophy. Developmental biology or embryology developed after Caspar Wolff’s seminal *Theorie der Generation* (1764) into a science of the developing organisms whose key figures in the nineteenth century have been exposed to Kantian thinking, as had been made clear by several historians of biology (e.g., Lenoir, 1982; Richards, 2001; Sloan, 2002). Among these biologists, Blumenbach was in epistolary contact with Kant, and major names such as Pander or Von Baer belonged to the same tradition (Von Baer authored the *Entwicklungsgeschichte den Thieren* (1828), arguably the most important nineteenth-century biology book, as Darwin himself acknowledged).

<footnote n="1">¹For this claim, Lenoir (1982), Zumbach (1984), McLaughlin (2000), Huneman (2008), and Ginsborg (2004) against Zammito (2018) and Richards (2001).</footnote>
Comparative anatomy built itself on two key principles, the “principle of the conditions of existence” and the “principle of the connections,” leading to the “principle of unity of type.” The former was advocated by George Cuvier, whose *Leçons sur l'anatomie comparée* (1805) were a milestone in this science; the latter is developed by Geoffroy Saint-Hilaire, who was a young colleague of the former. Even though they are often contrasted as two divergent ways of making biology, the former focusing on *function* and the latter on *form* – and this is the influential reading by Russell (1911) that Amundson (2005) endorsed later on – both their principles target the structured organism.

The fact that Kant’s analytics of biology centers on the notion of organisms – which I will explicate quickly – therefore matches with the new role of organisms in the nineteenth-century biology.<fnref n="2" /> Thus, it sounds natural that those who vindicate a return of the organisms in evolutionary biology through the evolutionary theory of development (or Evo-devo) trace back their key concept to Kant’s view of organisms (e.g., Gilbert & Sarkar, 2000).

When Gould and Lewontin (1978) use the German term “Bauplan” to label what – in an organism – resists the adaptationism proper to the Modern Synthesis, in a paper that has been heavily quoted by Evo-devo people when arguing against the treatment of organisms by this Modern Synthesis, the connection between developmental thinking in evolution and a Kantian tradition in biology becomes obvious. It is thus natural that I sketchily expose this Kantian view now. Since this is not a piece of Kantian scholarship, I’ will be fast in reconstructing Kant’s reasoning, citing materials likely to back up my claims (including my work).

Let’s start with this key notion of purposiveness since Kant’s main object is the judgment that ascribes finality to natural systems. Such a judgment explains something by invoking a preexisting concept of this thing – a concept standing “at the root of the production of the object,” as Kant says. This is the most general concept of purposiveness. When Kant adds “natural purposiveness,” he means such things that are judged purposive but that are at the same time naturally produced, in contrast with artificial and technical items.

It is often reminded that Kant contrasts mechanisms and teleology – those are his two terms, and a section in the *Critique of Judgement*, the “Antinomy of the teleological judgment,” intends to articulate them. *Mechanism* is about explaining a whole from the parts, and *teleology* is therefore the opposite, explaining the parts from the whole. This latter characterization of purposiveness instantiates the most general definition I gave above (in terms of a kind of causality of a presupposed concept). Saying that I explain the part based on a knowledge of the whole is to say that the part needs the idea of the whole to be understood, and this constitutes the presupposition of a concept at the root of the item to be explained.

Regarding biology, this becomes clear when we turn to a classical example also considered by Kant: the eye. In the eye coexist lots of distinct parts – retina, cones, rods, crystalline, cornea, etc. Each of them follows its proper, distinct “laws”, as he

<footnote n="2">²A claim defended at length in Huneman (2008, forth).</footnote>
argued in the First Introduction to the *Critique of Judgement*. If they were arranged
differently, for instance, the retina slightly more to the left, then we would see noth-
ing. To explain why all the parts are where and as they are, one has to posit some-
thing: the notion of a seeing device, at the root of the production of this organ.
Otherwise, it seems that pure chance distributed all these elements in such a way;
whereas if the concept of vision is the ground for the construction of the eye, this
harmony between the proper laws of each organ becomes necessary. That is a teleo-
logical judgment.

This allows us to understand a decisive phrase Kant uses to explicate what is
purposiveness: it is the “lawlikeness of the contingent as such” (First Introduction
to the CJ). What is necessary cannot be otherwise, it follows the laws of nature.
Whatever X is contingent on could be otherwise – X is contingent upon the anteced-
ent state of the universe, in the sense that, had this state been different, X would be
different. But some systems are such that to understand them one needs to consider
that the contingency of their states (as contingent upon other antecedent states) can
be bracketed in favor of a sort of necessity of their features. The “concept” alluded
to by a teleological judgment is an instantiation of this necessity, a sort of rule for
behavior proper to such systems. This pattern holds for biology: even if contingent
on the laws of physics, as contingent, living entities have some lawlikeness of their
own when taken as living entities. For instance, it is merely physically contingent
that the development of a chick embryo ends up in a chicken or a monster, yet from
the viewpoint of a biologist, these two states are not at all on a par. We call this dif-
ference viability vs. teratology. Viability is a norm. While physics knows no norms,
biology does; for instance, besides the norms of development, any function in biol-
ogy states a norm – “functioning vs malfunction” is normative: a kidney that does
not eliminate toxins is abnormal even though (or rather: because) its function is to
eliminate toxins.<fnref n="3" /> These norms constitute a “lawlikeness for the contingent as such”;
and the “concept” assumed in any teleological judgment instantiates such a norm.

7.1.2 Regulative Principle?

Purposiveness, that is, normativity as a lawlikeness of the contingent as such, assumption of a concept at the root of production, and epistemic precedence of the whole over the parts: those are the main elements of Kant's idea of teleological judgment. And for this reason, an organism, an organized being, is a natural purpose: a purpose, because it has parts that are only understandable based on the whole, hence on the concept of the whole. Thus, from the viewpoint of science, a concept stands at the roots of their production, hence the contingency of the agreement of the parts shows, as such, a lawlikeness – and this lawlikeness is not in the things themselves; it is in the eye of the beholder. This latter point is the other major

<footnote n="3">³For the normative interpretation of Kant, see Ginsborg (2004, 2014) and Huneman (2014a, b, c).</footnote>
aspect of this view of organisms as natural purposes – namely, such lawlikeness stems from our project of understanding life as such: it is a “regulative” principle for our cognition. Kant writes: “This principle does not pertain to how such things are possible themselves through this kind of production (things considered themselves as phenomena) but pertains only to the way our understanding can judge them” (CJ § 77, 408). This regulative character makes perfect sense with the requirement that the “concept” at the root of their production is posited by the teleological judgment to the aim of guaranteeing this lawlikeness at the biological level, which will then constitute the object of inquiry for the biologist.

Three things must be written now:

(a) The “concept” of vision, used to allow an investigation of the eye, and more generally any of these concepts that take the role of norms in biological inquiry behave like *attractors*. What does it mean?

Suppose a complex system in phase space. If the system, when faced with a small range of initial conditions, lightly changes its final state, we have a classic case of predictable determinism. But if in the same situation the system hugely changes its dynamics and final state, it is unpredictable, since the error margin on measuring the initial conditions is mapped onto a very large margin of error regarding the final result. The range of final states now is too large to predict anything from the knowledge of an initial state.

But in addition to these two situations, we can consider a third pattern where, whatever the initial conditions, the system will always end up in the same final state. Such a state is called an *attractor*; an example turned into a metaphor is a valley at the bottom of a mountain: whatever place one lets a stone roll down from the top, it will end up at the same location – down in the valley.

The concept of vision somehow turns a pattern of the type “sensitivity to initial condition” into the pattern of the type “attractor.” Physical conditions of the embryogenesis of the chick can vary a lot, but then one can (most of the time) safely assume that the chick will develop an eye, since the whole development for the biologist is supposed to produce an eye. There are many different obstacles in embryogenesis but in the end the animal mostly sees. Embryologists have a concept to name the way the developmental process almost always reaches the adult type as a target, even when the initial genes are mutated: “canalization,” a term famously coined by Conrad Waddington. Canalization is a form of attractor thinking.

(b) The “concept” (supposed at the root of the purposive system) being a concept of the whole, one has to emphasize Kant’s shift between the concept pair “means-ends” (which involves references to utility and intentionality) and “whole-parts” in the very meaning of purposiveness (see Huneman, 2007, 2017). Arguably, Kant detached the notion of purposiveness from the notion of utility and intentionality – while it intends to remain scientific.<fnref n="4" />

<footnote n="4">⁴Notice that this idea of design is quite different from the English tradition: hence, Kant tends to detach organism design from natural theology.</footnote>
(c) Philosophically, Kant's analysis puts the difference between things that are likely to be explained by pure physics and things that can't – namely, physics and organisms, to say it bluntly – in epistemology rather than in ontology. Physical systems not organized should be explained starting from the parts; in organisms the direction of explanation is inverted, or at least, an “ideal” causation, from the whole to the part, is articulated to a real mechanical causation (i.e., from the parts to the whole). This difference is obviously epistemic, not metaphysical. It's about what is required for an explanation to be possible.

The concept at the root of the production of the purposive thing is part of the teleological judgment rather than “within” the thing. Many philosophers and scientists in the early nineteenth century, while interested in Kant’s account of the whole-parts relationship, will give up on this notion of regulative principle: Blumenbach to begin with, and then Kielmayer or Meckel. Historical epistemology is cleaved about that question: Lenoir, who initially considered what he called the “vital-materialists,” namely Kant, Blumenbach, and other German biologists, lumped all of them in a sort of Kantian tradition in which teleology constitutes a regulative framework to search for mechanisms (what he called “teleomechanists”). Larson (1979), Richards (2001), and later Zammito (2018) on the contrary argued that Kant was alone in his view of regulativeness and that biologists will consider that purposiveness as described by Kant (including this focus on whole-parts relationship) is objective; with Zammito, they often also see this disconnection with Kant as a source of the fruitfulness of the attitude. This stance is also a feature of current views of organisms, such as the ones defended by researchers in the wake of Varela, Rosen, or Maturana, who start with the notion of self-organization understood as autopoieisis – e.g. Moreno and Mossio (2015), Montévil and Mossio (2015), or Saborido et al. (2011): there is something objective in organims’ being purposive. Yet for Kant, the concept of purposiveness, because of its constitution – namely, positing, within the judgment, a concept at the source of the production of the object – is necessarily regulative, in the sense that it concerns the modalities of the judgment rather than the thing about which one judges.

### 7.1.3 Natural Purposes and Self-Organization

Up to now, I unpacked the notion of purposiveness; but organisms are “natural purposes.” What does natural stand for here? Purposes can be artificial – in this case, the “concept” at the root of the production of the thing is simply the idea that the maker, the craftsman, or the artist has when she makes the product. The antecedence of wholes over parts is clearly here taking place. But natural items are such that they have no makers; they seem to be produced by themselves. In this case, when a natural purpose is found, the parts are what exist, so they create themselves in accordance with an idea of the whole – which, says Kant, is merely a “principle of cognition” and not a “principle of production” (CJ §65). This idea of the whole is
not the principle of their *making* but the condition of our understanding of organs and traits as parts of an organism, i.e., as involved in the development and functioning of a living entity.

Kant precisely says:

> In such a product of nature each part, at the same time as it exists throughout all the others, is thought as existing with respect to [um...willen] the other parts and the whole, namely as instrument (organ). [1] That is nevertheless not enough (because it could be merely an instrument of art, and represented as possible only as a purpose in general); the part is thought of as an organ *producing* the other parts (and consequently each part as producing the others reciprocally). [2] (CJ §65).

Condition [1] for being a natural purpose characterizes a purpose in general, as I explicated it until now. It is not proper to organisms, and it is where arise functions and functionality (as playing a role in a whole). I call it (Huneman, 2014c, 2017) the *design* criterion, since it fits any system that is designed and/or has a design. And criterion [2] specifies what makes a *natural* purpose. Kant then develops his view of what a “part producing another part” means: “Thus, concerning a body that has to be judged as a natural purpose in itself and according to its internal possibility, it is required that the parts of it produce themselves [hervorbringen] together, one from the other, in their form as much as in their binding, reciprocally, and from this causation on, produce a whole.” I call this criterion [2] the *epigeneticism* criterion (see also Huneman (2017)). It distinguishes organisms from artifacts because their design, in the sense of an arrangement of the parts according to an idea of the whole, is not achieved by some external agent considering precisely such idea of the whole as a building plan – the process of building organisms is rather done by the parts themselves; hence, they produce themselves: as a consequence says Kant, “organized beings are self-organized beings” (ib.). This essential character of such systems accounts for the sort of triadic phenomenology of organized beings proposed by Kant just before (CJ §64), namely, its self-production as individuals, when the tree grows; as a set of parts, when it grows leaves; and as a species, when it disperses seeds that grow.

This original occurrence of the word self-organizing will be quoted later by Kauffman (1993), who sees Kant as a father of the theories of self-organization, even though we now have a galaxy of “self-X” terms, such as self-assembly, self-maintenance, self-building, etc., within which “self-organization” stands rather on the side of physics. Even though Kant would not acknowledge the formal apparatus of Kauffmann or Santa Fe style theories, he indeed held this strong thesis that living organization is self-organization. But his claim was rather tied to nascent embryology theory, namely, Wolff’s epigeneticism, than to the mathematics of nonlinear differential equations, fractals, and Boolean networks, as it is now (see Ruelle, 1989).

More generally, I don't refer (with my labels) to the current notion of “epigenetics” (namely, whatever touches on the regulation of gene expression) but only to the notion opposed to preformism, namely, the capacity of living systems to build themselves through all the interactions with their external environment, without a preexisting template, and based on the activity of their parts producing other parts
(for instance, we would now talk about cells). This criterion (2) provides us with a
grasp between a general account of organization and the specificity of biological
organization, which can't rely on an extant template – a difference being addressed
in the introduction of this volume.

## 7.2 Making Sense of Organisms? From Kant to the Modern Synthesis

For Kant, the design criterion (1) and the epigeneticism criterion (2) are two criteria
for ultimately capturing the instantiations of one concept: they are unified through
the unity of the concept of purposiveness as a transcendental presupposition, a con-
cept of which they are the two facets. Both refer to an “idea of the whole” as “prin-
ciple of cognition”; and it is the *same whole* in each case, and Kant analyzes at
length the justifications for this claim in his “transcendental deduction” of the con-
cept of purposiveness, undertaken in the Dialectics of the third *Critique*. But does
this have any relevance for anyone now interested in the concept of organism? I will
argue for the affirmative since, as indicated above, Kant’s views of organization in
general (criterion 1 above) and of *biological* organization (criterion 2 above) are
mentioned as a philosophical foundation for thinking of organisms by Evo-devo
people (e.g., Raff, 1996; Caroll, 2005), or theoretical biologists interested in self-
organization, or, indirectly, by critiques such as Gould and Lewontin in their span-
drels paper.

Thus, I will quickly consider what are these two criteria in the context of current
evolutionary biology and developmental biology.

### 7.2.1 *Design Criterion*

The design criterion consists in presupposing that organisms are wholes in which
parts fit the needs and demands of the persistence of these wholes. It is easy to see
that such a criterion suits well the practice of behavioral ecology, namely, the sub-
discipline of evolutionary biology that studies traits of organisms as adaptations or
equilibrium strategies. Clearly, “traits” are more general than parts, but we can con-
sider behavior as something of the organism, and then behavioral traits as parts of
this dimension of the organism.

Methodologically, behavioral ecology is generally adaptationist as made clear by
Reeve and Sherman (1993) or Krebs and Davies (1995), namely, it starts by assum-
ing that a trait results from natural selection, either by maximizing fitness, or inclu-
sive fitness, or (in the case where fitness payoffs depend upon the frequencies of
traits) by realizing an “evolutionary stable strategy,” which is a kind of equilibrium
in evolutionary contexts (Maynard-Smith, 1982).
Behavioral ecology asks questions such as the following: “Why do passerines or great tits lay four or five eggs by nest?”; “Why do gorillas of this region change mate every three years? ”; and “Why are the leaves of the cypress of this size?”. Behavioral ecologists center on traits, hence on phenotypes; they demand that traits are somehow *heritable*, which means that some alleles make a difference in the value of the trait. Such heritability is assumed; it may be very low but, in most cases, the precise genetic makeup involved in traits under focus is unknown. More than a hundred genes are involved in a phenotype as seemingly simple as the size of mammals, so one should not expect that traits such as foraging behavior, studied in behavioral ecology, rely on a knowable genetic circuitry.

In this approach, parts – traits – are assumed to fulfill environmental demands. One often uses here the method labeled “reverse engineering” – namely, assuming that a part is an adaptation, and trying to reconstitute the environmental demands it was designed to fulfill. For instance, the horn of the *Parasaurolophus* has been intensively studied, and many hypotheses about the environmental demands it addressed have been emitted until one reached a consensus on the idea that it was used as a communication tool in sea or river shores (Turner, 2000) (Fig. 7.1).

To this aim, the structure of the horn, and especially its hollowness, has been taken into account, to deduce what the effect of such a horn could be – emitting recognizable sounds has been declared a much more probable selected effect than fighting competitors with the head.

Assuming that in a given system the conditions for natural selection that population genetics can unravel are met, then the traits we see are adaptations, which means that they fulfill environmental demands. By examining them, we

<figure><img src="image_17.png" /><figcaption>**Fig. 7.1** *Parasaurolophus and its hollow horn*</figcaption></figure>
may reconstitute these environmental demands. Such reverse engineering is
thereby a legitimate method. This justifies that the design criterion is still nowa-
days legitimate since we’ve seen that reverse engineering is a clear instance of
this criterion.

But the process of adaptive evolution involves a process of allele frequency change. Population genetics models such a change. In this approach, evolution is due to forces that act on populations modeled as gene pools<fnref n="5" />; those forces are migration, mutation, natural selection, and random genetic drift (which is, to say it quickly, a sort of error sampling, whose intensity – by definition – decreases with population size<fnref n="6" />). Among them, natural selection is the only one that creates adaptation, hence its epistemic primacy for evolutionary biologists. But nothing guarantees that in a given population, natural selection will overcome the other forces: if it is a very small population, or if migration is too strong, natural selection will be superseded by other forces and evolution will not yield adaptation.<fnref n="7" />

More precisely, natural selection understood as the “survival of the fittest” means that it tends to increase fitness, understood as the expected number of offspring. This maximization generally produces an adjustment between organisms and the environment, since meeting environmental demands allows one to survive and reproduce optimally.<fnref n="8" /> The general idea is that being more adapted than others involves surviving more and reproducing more so that the organisms or the traits that maximize their fitness tend to be optimized regarding environmental demands. In a given environment, for instance, the leaves of the cypress will have a size that allows them to maximally photosynthesize, and produce more trees, and more seeds, than if it were having smaller leaves; otherwise, genetic variants with other leaf sizes would thrive against the resident trees and would invade the population. It is such a process, at the level of gene dynamics, which justifies the reverse engineering, hence grounds the design criterion.

However, things are more complicated. Is it really the case that natural selection
in principle optimizes and then creates the environmental fit with organisms? Or at
least that it tends to optimize<fnref n="9" />? Birch (2015) and Okasha (2018) have indeed shown
that there is no satisfying a priori proof that selection by itself and alone always
optimizes fitness or inclusive fitness and that equating selection with optimization
and adaptation can only be locally legitimate and often waits for empirical
corroboration.

<footnote n="5">⁵See Sober (1984) for a canonical formulation of this account.</footnote>

<footnote n="6">⁶On drift see Plutynski (2007), Abrams (2007).</footnote>

<footnote n="7">⁷Of course, this is the simplest case and I bypass here issues regarding social evolution and then kin selection and inclusive fitness, (Hamilton, 1964) as well as population structure or maternal effects. Suffices to say that natural selection tends to produce adaptation because maximizing fitness entails optimizing traits with regard to environmental demands.</footnote>

<footnote n="8">⁸Fitness is as we know a much-discussed and controversial concept; but this is not my point here.</footnote>

<footnote n="9">⁹As to the prospects of this optimization, see also Huneman (2014a, b, 2019b).</footnote>
To this extent, the design criterion cannot be seen as what should any organism
satisfy on the grounds of the fact that a population fulfills the classical conditions of
heritability, variation, and fitness that Lewontin (1970) famously formulated as con-
ditions for potential evolution by natural selection (or any other version of the char-
acterization of the conditions of evolution by natural selection).

7.2.2 *Epigeneticism Criterion*

Cell theory, which is, along with molecular biology and evolutionary theory, the
third major global theory of life underpinning modern biology (Gayon & Petit,
2019), provides us with a clear instance of this criterion (as explicated in Sect.
7.1.3): cells are producing cells, and this production leads to the organism. But this
is also happening in accordance with an “idea of the whole,” as Kant required.
Why? Early molecular biology, in the enthusiasm of the discovery of DNA and the
genetic code, would easily consider that this idea of the whole is the genotype and
therefore exists rather “in” the cell than within the epistemic activity of the
researcher. This is a kind of preformationism (as made clear by Müller and
Hallcrimson (2003)), but recent developmental biology has increasingly shown that
development is more complex than the unfolding of a program.

Granted, cells differentiate according to what Kant calls an “idea of the whole”; yet unlike what I just said, it’s not the genetic program that differentiates each cell since all carry the same genotype – in most metazoan and plants; on the contrary, differentiation is an epigenetic process involving the environment of each cell, the activation states of the genome in neighboring cells, and for each gene, the gene regulatory network that regulates its expression according to the states of all elements (other genes, transcripts, etc.; see Davidson, 1986; Oliveri et al., 2008).<fnref n="10" /> Thus, we seem to move away from the gene-based preformationism toward a more epigeneticist account of development in which cells produce cells in accordance with a general “idea of the whole” that is less located “in” the genotype than instantiated in a distributed way across genotypes, cell environments, and multiplicity of gene regulatory networks (GRN).

To make this kind of production clearer, remember, in developmental biology,
the classical French flag model (Fig. 7.2) (due to Wolpert, 1969). In this account,
cell differentiation as the response to a gradient of morphogenetic substance turns a
continuous proportion of morphogen into a discrete series of expression states (the
“flag”). It realizes an instance of this self-organization conceived of by Kant, to the
extent that the organism is created on the basis of cells that respond individually to
an overall state of the whole that they locally encounter, as represented by the state
of the gradient in a flag.

<footnote n="10">¹⁰Such process during embryogenesis also involves “programmed cell death” or apoptosis (Kerr et al., 1972), a major dimension of development that I studied in Huneman (2023).</footnote>
<figure><img src="image_18.png" /><figcaption>**Fig. 7.2** A representation of the French flag model of cell differentiation (Wolpert)</figcaption></figure>

In turn, the GRNs are also, and maybe even more, an instance of this epigeneticism criterion. Developmentalists nowadays think of them as explaining the French flag model among other things (Davidson et al., 2003). They determine the expression of a gene based on the states of hundreds or thousands of other genes or genetic elements in the cell. GRNs react to the state of the organism – which is, for the cell, its environment – and determine in response to the contribution of the focal cell (Fig. 7.3). This corresponds to the self-organizing logic of the epigeneticism criterion.

Moreover, GRNs are implied in both the development of the organism and its functioning, since their dynamics in each case determines what a gene – and then all genes – do, and therefore, what does a cell of such and such genotype within the organism, at each stage of the life cycle. Given that GRNs instantiate the epigeneticist criterion, the fact of their involvement in cell physiology can be interpreted as acknowledging the epigenetic character of organism functioning, which would clearly correspond to the Kantian view of organisms. In any case, we see here a neat intertwining between development and functioning: genetic regulatory networks are involved both in cell specification and pattern formation – and within the regular activity of the cell.
<figure><img src="image_19.png" /><figcaption>**Fig. 7.3** Gene regulatory networks in starfish and sea urchin</figcaption></figure>

While the two criteria for purposiveness were unified by Kant since there was one single “idea of the whole” involved in the teleological judgment and expressed in each of these criteria, my analysis emphasizes differences in the way these criteria can make sense of purposiveness today and possibly reassert the claim that organisms are natural purposes.

The design criterion and the epigeneticism criterion appear indeed not only distinct, as in Kant, but also wholly separated. Emphasizing the design criterion means focusing on the way the whole organism is designed, namely, the way that parts are contrived; these contrivances are the effect and the sign of natural selection. Contrived wholes are adapted, and adaptation results from natural selection, according to the Modern Synthesis. On the other hand, emphasizing the epigeneticism criterion means focusing on development as the proper epigenetic process, and then, more generally, on self-organization of the whole. When authors in the tradition of self-organization as an account of organisms refer to Kant's idea of self-organization, they commit to Kant's idea of parts that create other parts and themselves according to the an “idea of the whole”, even though of course they rely on a much richer empirical work, and sometimes they use types of mathematical tools unknown by Kant – Kauffman's Boolean networks or, on another side, Rosen's algebra.

But for Kant, the two criteria were unified as two aspects of the same “idea of the whole” which is involved in the notion of “natural purpose” as a transcendental principle for reflective judgment. This transcendental or criticist dimension of Kant’s thinking - visible in the notion of ‘regulative principle’ - is not adopted by the thinkers interested in self-organization, nor is it related to the modern avatar of the design criterion, namely, the various brands of adaptationism (reverse engineering, etc.; see Lewens (2004)). Hence, the two criteria are divided. They can’t be understood as the two criteria of “organisms” (themselves being instantiations of “natural purposiveness”).

Through these reflections, I put in a Kantian light the conflict between adaptationism and developmentalism as it is considered by supporters of Evo-devo, and
sometimes deemed unsurpassable (e.g., by Amundson, 2005). It is not the only possible reading of such analyses of the two criteria of purposiveness, but it helps put them in the context of current theoretical cleavages.

And as it is, it shows that there is a major issue with any attempt to now use the Kantian analysis of organisms – which is one of the major philosophical analyses of this concept – as a way to make sense of organisms in current biological thought. Maybe that leads to a final verdict of unsurpassable cleavage: focusing on the epigeneticism criterion leads to viewing self-organization while focusing on the design criterion sketches of the whole organism as a set of responses to environmental demands, and the two views of the “whole” that emerges on its side remain separated.

With these words, I turn to a wholly different approach, which is the way an ontological theorizing based on Darwinian principles intends to make sense of organisms understood as a major kind of “biological individuality.”

## 7.3 Evolutionary Individuals: A Liberal Approach Based on Conceptual Spaces

### 7.3.1 *Transitions in Individuality*

Biological individuality has been the object of many conceptualizing attempts from philosophers and biologists relying on the Modern Synthesis. I'm not trying to review these accounts or systematize them here since this would require a full paper or a book. But I think that the underlying idea grounding these sometimes conflicting accounts is the connection made by David Hull in his seminal paper "A matter of individuality" (1980) – namely, a connection between individuality and natural selection. In a nutshell, to be an individual is to be a target of selection. Since this latter notion is controversial and not well defined, approaches to the individuality/ selection connection are numerous. Yet all share the idea that to see what are individuals in the world, one has to identify what is the object of some selection. Some accounts intend to specify what exact concept of a unit of selection is required to single out individuals (e.g., Folse III & Roughgarden, 2010; Clarke, 2014; Bouchard, 2008), while others are more pluralist, allowing for several types of individuality according to the aspect of selection considered (e.g., Goodnight, 2013). Yet in Sect. 7.2, I will argue that these accounts yield views more liberal than the Kantian-based view of organisms because they don't commit to the idea that something could be either an individual or not an individual, but most of the cases of individuality are graded stages of individuality.

Granted, organisms are individuals; but of course other things can be biological individuals, and this intuition is backed by selection-based accounts of individuality: bacteria (which are unicellular and may not be organisms strictly speaking); genes, given that there exists a selection at the level of genes, for instance, in the case of segregation distorters (Burt & Trivers, 2006); possibly colonies of
hymenopteran insects; and perhaps species, if one follows Ghiselin and Hull who famously argued that species are not classes but individuals whose conspecific organisms are genuine parts (Hull, 1980, Ghiselin, 1974). The Darwinian approach intends to make sense of all individuals based on natural selection. But among them, multicellular organisms enjoy a paradigmatic status: first, they constitute most usually our favorite example of individuals, since they fit our intuition more than species or genes; second, they display spatial contiguity and often genetic homogeneity – in the case of most metazoans – which makes easy to talk of the self-containment and indivisibility implicit in the word “individual.” If, following Aristotle, “individuality” means the logical inseparability (a horse and a horseman can be separated into two concepts of particulars, but a horse cannot), the genetic homogeneity of something that was born a zygote and then developed based on clonal cell division makes it into something apparently logically indivisible.

Hence, “organisms” as understood by the Kantian approach that I exposed, namely, multicellular organisms, are a paradigmatic but not exclusive kind of biological individual. The question of “organisms” may therefore be summarized by the question raised by Dawkins (1976), namely, why does life on Earth comes mostly under the form of organisms rather than by a total mess of genes as the only individuals? The start of an answer is given by the program called “evolutionary transitions,” initiated by Buss (1988) and then Maynard-Smith and Szathmáry (1995) and Michod (1999). The main idea is that throughout evolution, distinct forms of individuality understood as entities that reproduce by themselves and thereby can be targets of selection came into existence. For instance, cells appeared on the basis of macromolecules possibly replicating because of them being autocatalytic and templates; cells that made up life on Earth from 3,5 By ago to 1 By ago evolved into multicellular organisms. And then some of them evolved into forms of individuality that can be composed of individuals and show the division of labor between reproduction and survival/development that is characteristic of multicellular organisms: namely, hymenopteran insects form colonies where a cast reproduces and a cast does defense, territoriality, and foraging without reproducing.

This research program, most generally understood, intends to capture the generic processes leading from groups to individuals made up of a collection of entities. The process of going from prokaryotes or unicellular eukaryotes to multicellularity is one crucial transition. But the same general rules should govern all processes, even though local differences are investigated. As to themselves, multicellular organisms *develop*; the development possibly (and most often) starts with a genetic bottleneck; those individuals contain differentiated cells with identical genomes, hence the need for epigenetic gene expression mechanisms; many recent clades feature sequestration of germ-line paralleling the division of labor in hymenopteran insects (Buss, 1988).

The main process involved in the evolution of forms of individuality is “multi-level selection” (MLS) (Michod, 1999, 2005). It means that selection operates in opposite ways at two levels: the one constituted of entities and the one constituted of groups of these entities – for instance, cells and groups of cells. Among cells, those that reproduce faster or more than the average have better evolutionary
success. But at the level of groups, having too many cells that work "for them-
selves" may distort the group, and then such a group eventually fares less well than
groups where cells are more coordinated. Hence, selfishness – in the sense of repro-
ducing more than others – wins *among cells*, but altruism, in the sense of reproduc-
ing less than others, or, more formally, having a lesser fitness, wins *among groups*.
This is multilevel selection, a concept considering selection as the result of combin-
ing intragroup competition and intergroup competition (Sober & Wilson, 1998).

The researchers interested in evolutionary transitions emphasize not only the fact
that multilevel selection may foster altruism (while at the intragroup level, altruism
always loses); but also that this process may ultimately lead to groups that are likely
to reproduce as a single entity. This is exactly what plausibly happened with multi-
cellular organisms. Briefly said, altruism among cells is maintained because of
group benefits, and in some cases, the group starts reproducing as one, and then
emerging policing devices ensure the persistence of this reproduction.

This process can be understood in several ways. Appealing to the useful distinc-
tion made by Damuth and Heisler (1988) between two kinds of MLS defined by two
kinds of group fitness, labeled MLS1 and MLS2, Okasha (2006) and Michod (1999)
argued that a transition is a transition between these two kinds of fitness. In MLS1,
fitness is defined by counting the total number of offspring of all the individuals of
a given group; in MLS2, it's defined by counting daughter groups of a group. This
intuitively fits the transition toward multicellularity: a fitness of a group of cells is
the amount of cells after one generation; but the fitness of a multicellular organism
is the number of daughter organisms, not the total number of cells at the next gen-
eration. The transition toward multicellularity is therefore a transition from one to
the other type of MLS, from MLS 1 to MLS2. And formally, what makes this pos-
sible is the decoupling between these two kinds of fitness, and it often happens
because the trade-off between fecundity and viability in cells becomes a convex
function when the group size increases (Michod, 2005).

This explanatory scheme is supposed to account for all kinds of transitions.
However, multicellular organisms constitute a paradigmatic transition. For this rea-
son, researchers such as Michod and his team extensively investigated a clade in
which unicellular and multicellular species coexist – namely, the order *Volvocales* (*or*
*Chlamydomonadales*), within which *Chlamydomonas* is a unicellular species,
Gonium is a colonial species undifferentiated, and Vovox is a colonial differnetiated
species (the transition took 35 My to occur). But the key role of multicellular organ-
isms for the question of individuality is not only due to the intuitive appeal they have
for us, and then our familiarity with metazoan. Within evolutionary theorizing, this
is also a salient feature. Take the hierarchy of individuality. What scholars are inter-
ested in evolutionary transition research is the generative process that accounts for
steps in individuality, as I said. But while individuality is hierarchical, through a
hierarchy based on compositionality (chromosomes -> cells-> multicellular organ-
isms -> colonies, as Michod (1999) shows), the nature of this hierarchy is complex.
Paleobiologist Niles Eldredge argued in the late 1980s that there are at least two
hierarchies, one genealogical and one ecological (Eldredge, 1985).
The genealogical hierarchy consists of levels of increasing complexity in repro-
duction: each level consists of entities that include entities of the previous level but
reproduce by themselves. They have a direct genealogical link. The ecological hier-
archy consists of levels of ecological interaction: chromosomes assemble through
meiosis; cells interact in microbial ecology; organisms interact within ecological
settings; and groups of organisms may compete and cooperate in competitive con-
texts. Interestingly, “organism” is the level that belongs to the two hierarchies: it is
a main agent in ecological interactions, and it is also a crucial step in genealogy.

For this reason, the multicellular organism is crucial for the notion of individual-
ity in Darwinian contexts even though, as Godfrey-Smith (2009) forcefully claimed,
not all organisms are Darwinian individuals – since some of them don’t reproduce
by themselves – and not all Darwinian individuals are organisms.

7.3.2 Conceptual Spaces: Being Liberal

These considerations indicate that such an approach to individuality may not pro-
vide a complete account of organisms, even though organisms are individuals. But
a closer look at the evolutionary transition programs reveals that this approach is
quite different in its spirit from the Kantian approach.

The parallel between bee colonies and organisms, grounded on the division of
reproductive labor, comes with a few lessons. Colonies are individuals, in the sense
that they can be seen as units of selection under some perspectives, for instance,
MLS; but they lack the self-contained character of organisms as well as their capac-
ity to reproduce for themselves. Everything happens as if the transition from MLS1
to MLS2, through which the groups have daughter groups that can be counted, did
not come to terms. In Huneman (2013), I proposed to distinguish two kinds of tran-
sition, depending on whether they come to an achievement (like multicellular organ-
isms) or not (like bee colonies). Pandas realize exemplarily complete transitions;
bee colonies realize component transitions.

But this is less a binary distinction than two poles of a continuum. There are
degrees in “component transition” and inversely some organisms may lack or lose
features of complete transition – e.g., cancer as disruption of organisms (see
Featherston & Durand, 2012), failure of policing devices in the case of immunity
disease, etc.

That gives us a flavor of the liberality proper to the Darwinian approach: systems
can be more or less individuals, to the extent that they can come from more or less
complete transitions. Organisms are a result of the former, but for the same reason,
“being an organism” will come by degrees.

However, this continuum of biological individuality has been even more
expanded. In a series of papers, Joan Strassmann and David Queller (Strassmann &
Queller, 2010; Queller & Strassmann, 2009) have suggested a view of individuality
that is less a gradient than a two-dimensional hyperspace (Fig. 7.4). They argue that
individuals require cooperation – in the sense of altruism, as indicated in the context
<figure><img src="image_20.png" /><figcaption>**Fig. 7.4** The space of biological individuality, according to Queller and Strassmann (2009)</figcaption></figure>

of multilevel selection – but also a loss of potentiality for conflict. They claim that these are two different things, even though both of them are defined in relation to natural selection, which characterizes this account as a Darwinian account of individuality. Therefore, systems should be situated within a general conceptual hyper-space of organismality – but I would say “individuality” – whose dimensions are the degree of cooperation and the degree of absence of conflict. In honey bees, for instance, there is lots of cooperation, as in corals, but the system of repressing possible alternative queens in bee colonies allows them to have far less conflict than in corals. This means that it is not always possible to say that a system is more an individual than another one – everything depends upon the dimension (decreasing conflict/degree of cooperation) that one favors.

For this reason, I consider the Darwinian approach as the most liberal: not only “being an individual” and then “being an organism” is not a question for which necessary and sufficient conditions (NSC) should be given; but even in the space of individuality, there is some liberality in the dimension supposed to be the most relevant. I call it the conceptual space approach and it philosophically differs from the Kantian approach consisting in building the concept of the organism, thereby setting criteria for being an organism.

Additionally, in this view, there is no requirement for genetic homogeneity or species homogeneity – associations between different species such as aphid and *Buchnera*, or in general host with symbionts, but also ant-plants or kinds of multicellular organisms made up of distinct species can form individual in evolutionary time.
I proposed that the component vs complete transition should be supplemented with another distinction due to Queller (1997) in order to make complete sense of the space of individuality. In effect, most of the transitions in individuality that I talked about are what Queller called “fraternal transitions”: the entities that tend to coalesce into a higher-level individual are genetically similar or close or highly related. But many of the individuals in the space of individuality are made up of genetically heterogeneous entities: think of the lichens made up of fungi and algae. And most deeply in evolutionary history, we have the ancestor of eukaryotic cells, supposed to be the result of encapsulation of an archaea into a bacterium (Margulis, 1970). A story similar to this story of the emergence of the nucleus of a eukaryotic cell has also been told (also by Margulis) about the mitochondria, which is the result of the integration within a eukaryote of a smaller prokaryote, through endosymbiosis. In these transitions, the result is an autonomous individual; the components lose their individuality, not only because they don’t reproduce by themselves but also because they lose many of their genes since the functions supported by these genes can be done through genes of the host individual, and reciprocally.

There is no definite criterion for being a biological individual, but mostly dimensions in an abstract space, and then the characterization of elements of this space according to Table 7.1. Given that transitions can be egalitarian or fraternal and then can be ranged across a gradient that goes from poorly component transition to complete transition, we have four extreme cases for transitions, summarized in Table 7.1. Importantly, given that most organisms are made of cells but also of many symbionts that constitute their microbiota, the egalitarian transitions are all over the place. As a result, an element in the space of individuality can be understood according to the following:

- How it scores on each of the two dimensions (lack of conflicts, cooperation).

- How much complete it is – and here, the measure of the “completeness” is given by the norm of the vector (OA) where point A is the putative individual with measures x and y on each axis of the space, and O is the origin (the norm U is computed in the ordinary scalar way, $U^2 = x^2 + y^2$): the largest is this norm, the more complete is the transition.

- To what extent it is egalitarian or fraternal.

<table><caption>**Table 7.1** Four types of transition (a quadripartition that structures the space of biological individuality)</caption><thead><tr><th colspan="3">The four kinds of transitions</th></tr><tr><th></th><th>Complete transition</th><th>Component transition</th></tr></thead><tbody><tr><th>Fruternal</th><td>Transition toward multicellular organisms</td><td>Colony of Melipona bees (high level of potential conflict makes them different from organisms; see Queller & Strassmann, 2009); Bacillus subtilis bacteria</td></tr><tr><th>Egulitarian</th><td>Transition toward eukaryotic cells (mitochondria as symbionts); Termite mounds by Macrotermes (Turner, 2000); Lichens</td><td>Some fig.pollinator wasp mutualisms</td></tr></tbody></table>
This conceptual space approach is clearly much more liberal than the Kantian approach; it requires one to be pluralist regarding the sense of individuality and therefore to give up the hope to capture what an organism is. Granted, organisms are in the space of individuality; one can require that they have a high degree of completeness in transition, but this leaves lots of room for many possibilities for organismal structures, features, and functions, as I will consider in the next section.

### 7.3.3 Ecosystems, Individuals, and Organisms

Additionally, taking into account egalitarian transitions raises a complex issue, namely, the individuality of ecosystems. Ecosystems are made up of many individuals of many species and include the overall abiotic element. They are generally not seen as units of selection, given that they don't display (obvious) heritability; thus, they would hardly respond to selection. To this extent, they could not pretend to be individuals in the Darwinian liberal view.

However, ecologists still often think that some ecosystems are more individual than others. The intuition behind this idea is that while some ecosystems are a loose assortment of species, whose unity is in the eye of the beholder, others are quite cohesive sets of entities likely to persist in time.<fnref n="11" /> As Evelyn Hutchinson – a key figure in modern ecology – tended to say, these communities or ecosystems show much stronger interactions within themselves than with others, and that’s why they are ontologically more robust.<fnref n="12" />

I gave a formal characterization of the individuality that such ecosystems feature, called “weak individuality.”¹³¹d But my only point here is to show that these ecosystem individuals may enter the space of individuality, even though they are not obviously part of them since concerning them selection cannot be appealed to. I suggest that we have here a local instance of ecological individuals that appears as a limit of evolutionary biological individuals when the degree of egalitarianism of the transition is extremely higher than the coefficient of “fraternality.”

But following the indications I gave while discussing “weak individuality” (Huneman, 2020), one can sketch another conceptual space, proper to ecological individuality. The axes then would be the relative strength of the major interactions

<footnote n="11">¹¹This view was held by the very influential treatise *Principles of Animal Ecology*, published in 1949 by prominent ecologists Clyde Allee, Thomas Park, Orlando Park, Alfred Emerson, and Karl Schmidt. They thought that a selection at the level of the group of species fosters the unity of an ecological community exactly as natural selection fosters the unity and individuality of organisms. This view faded away in the 1950s with the emergence of behavioral ecology, which mostly relies on natural selection, (for instance Lack, 1954) and then with the devastating critique of group selection by George Williams (1966).</footnote>

<footnote n="12">¹²See Hutchinson (1957). On the problematic ontological character of ecological communities, see Sterelny (2006).</footnote>

<footnote n="131">¹³¹dI developed a conception of weak individuality to make sense of these accounts of individuality (Huneman, 2014b, c, 2020).</footnote>
<figure><img src="image_21.png" /><figcaption>**Fig. 7.5** The space of ecosystemic individuality. Each axis represents a structuring interaction. The situation of a given ecosystem depends upon the relative strengths of the interactions. (After Huneman, 2020)</figcaption></figure>

that hold together an ecosystem: competition, mutualism, parasitism, predation, and
niche construction.

This “space of ecosystemality,” so to say, pertains to the same conceptual space
approach as the space of individuality. It is not wholly orthogonal to it, since eco-
logical interactions are the ground of the selective pressures, which in turn make up
the selective force, which drives the constitution of evolutionary individuals. In
Fig. 7.5, I present a version of this space of ecosystemality. My only concern here is
in showing that the conceptual space approach *generaliter* allows one to conceptu-
alize quite extensively issues related to individuality.

7.4 Confronting the Approaches

Is it possible to go further in confronting these two approaches?

To summarize, we have two distinct approaches toward organisms and individu-
als in general:

(a) In the wake of Kant's *Critique of Judgment*, the necessary and sufficient conditions (NCS) approach provides *the two criteria for organisms*: design and epigeneticism.

In a non-Kantian context, the issue is whether unification is possible. What could be the unification principle? Especially, what happened if only one criterion is fulfilled? As I
wrote, the transcendental perspective implied that the idea of “natural purpose” instantiated by organisms is unified. But outside this perspective, things change. Especially, the two criteria can be fulfilled independently; whereas in the Kantian view, once something satisfies the epigeneticism criterion, an “idea of the whole” is presupposed by the biologist as what guides the epigenetic process, and therefore this idea of the whole is also the design of the system. But independently of Kant, one may find things that satisfy the design criterion – design with no self-production (artifacts) – and things that satisfy only the epigeneticism criterion, especially many of the systems investigated by the so-called science of complex systems, starting with the iconic Bénard convection cells, which are not at all alive and don’t include functional parts.<fnref n="14" />

(b) On the other hand, we have a liberal attitude: the conceptual space approach (CSA). Here, *organisms inhabit a space of individuality*. The axes are defined by cooperation and by lack of conflict, and the transitions feature several degrees of completeness.

This approach meets its proper issues: first, *how to define “degrees” of individuality in the absence of total order*, assuming that the scalar norm is a too-rough measure? Another issue concerns the axes: are they the only ones? And what is the relation with the space of ecosystematicity addressed in Sect. 7.3.3? And finally, given that some modeling of organisms appeal to ecological concepts, by seeing processes in terms of predation and competition rather than execution of a genetic program (e.g., Costello et al., 2012), or sometimes reintroducing ecological concepts such as niche (Scadden, 2006), would it be possible to think of the organism as ecosystems first, before being something else (I investigated the plausibility of this proposition in Huneman (2020))?

One may be dissatisfied with having two accounts of organisms, distinct but with obvious overlaps. Granted, an option could consist in saying the following: organisms are one thing; they pertain to several biological investigations often lumped under the label “functional biology” (sensu Mayr); and they are integrated, develop, and feature adaptations, but may not necessarily be under natural selection. On the other hand, evolutionary biology handles entities that could be counted, so that the concept of fitness can be instantiated, since fitness is a mathematical construct based on a probability distribution over offspring numbers.

Thus, a reasonable pluralism could say that there are two concepts of organisms: the direct concept in functional biology and the evolutionary concept according to which organisms represent an important kind of individuals, and then individuals are thought of in evolutionary terms.

<footnote n="14">¹⁴Trying to recover from within the set of self-organizing system such as Bénard cells, candle flames or whirlpool, the subset of things that are alive and therefore that feature functions, and then would be in Kantian terms fulfilling the design criterion: this endeavor has been undertaken by Mossio, Moreno and Saborido in a set of papers and by Mossio and Moreno (2015) Their notion of “closure of constraints” would play the role of what unifies the two criteria, in the present perspective.</footnote>
This reasonably pluralist option is not dismissing the major claim I want to make in this paper, namely, the difference between an NSC approach and an approach via conceptual space (CSA), as I have exposed them. There is a principled distinction between these two approaches, and I tried to show their respective justifications. And the NSC and the CSA approach could be let as it is: they would coexist as two distinct approaches, each favored by one theoretical school, evolutionists being massively interested in the CSA. This strategy fits the view of Godfrey-Smith (2013), who tends to see organisms and individuals as two conceptual elements proper to two distinct explanatory projects, which can sometimes overlap. But the two approaches do not exactly match with, respectively, a developmentalist concept of the organism used in functional biology and an evolutionary-based concept of individual, according to the reasonable pluralism just sketched. Why? Because the Kantian concept is in itself divided between a developmentalist and an adaptationist understanding.<fnref n="15" />

Thus, how can we articulate the NCS approach of the organism and the CSA liberal evolutionary approach to individuality? I will sketch two strategies successively. I label the first one the threshold strategy and the second one the pragmatic strategy.

### 7.4.1 Threshold Strategy

According to the threshold strategy, one has to specify a boundary (in terms of a scalar norm) above which X in the space of individuality is a genuine organism. This gives way to articulate individuals and organisms, organisms being a proper subspace of the space of individuality (Fig. 7.5). But how to justify the values of the thresholds? That is the main issue with this otherwise attractive approach. It is hard to do it without some arbitrariness, for instance, by saying that this individual (quaking aspen) is an individual but this other one (ant colony? Dandelion field?) is not an organism. Or, if one wants to avoid being arbitrary, one should provide a concept of organism – which implies an obvious case of circularity, since the whole point here is about determining organisms within the space of individuality (and not extrinsically) in order to make it correspond to the NSC approach to the organism.

But even though we accept arbitrariness or circularity, there is a more pressing issue with this approach. Consider the epigeneticism criterion, which characterizes organisms as natural purpose (qua natural) according to the Kantian approach: “Thus, concerning a body that has to be judged as a natural purpose in itself and according to its internal possibility, it is required that the parts of it produce themselves [hervorbringen] together” (CJ § 65). We said that this criterion easily fits the development of multicellular organisms. However, in the CSA liberal approach, we

<footnote n="15">¹⁵ See Jaeger, (this volume), which suggests another route toward this problem.</footnote>
Organisms according to the NSC approach

<figure><img src="image_22.png" /></figure>

Individuals according to the CSA

**Fig. 7.6** The threshold strategy: organisms according to NCS approach correspond to a subspace in the CSA approach, delimited by a threshold

included products of the “egalitarian” transitions: here, there are heterospecific individuals; along evolution, different species coevolved and concurred in producing such individuals; and along development, a given individual accepts and recruits bacteria (see Nyholm and McFall-Ngai (2004) on the *Vibrio fischeri* bobtail squid with its luminescent bacteria). But this recruitment is not production, at least in the way cells produce new cells. Thus, even within a “zone” of the space of individuality supposed to fit “organisms,” the epigeneticism criterion fails, so the two approaches don’t match (Fig. 7.6).

An answer to the objection would consist in deflating the sense of “production” in the criterion. Hence, any kind of causation, for instance, counterfactual causation, would suffice – and since bacteria recruited in an organism, for instance, in the bobtail squid, are counterfactually cause of the form of the squid – in the sense that if the bacteria were different (its species being different from the set of species recruited by the squid), they wouldn’t end up in the squid –, this case fulfills the epigeneticism criterion.

Ecologists talk of “facilitation” when species A increasing in abundance makes another species B increase in abundance, for instance, by eating more of the predators of B (Bruno et al., 2003). Thus, if causation means something like facilitation, heterospecific individuals could fulfill the epigeneticism criterion. But the drawback is significant: one loses the distinction between the two criteria of organism in Kant’s sense since both of them are now about “causing” (in a nonproductive sense) the form of the parts! Therefore, the design criterion and epigeneticism criterion collapse, and the whole approach loses its benefits.
Thus, whether one accepts or rejects this conceptual alternative, namely, weakening the epigeneticism criterion, the threshold strategy raises massive issues.

## 7.4.2 Pragmatic Strategy

If now we turn to the pragmatic strategy, what are the prospects?

As a strategy, pragmatism means that individuals and organisms are two distinct concepts, whose extensions overlap, and this overlap is determined by the respective uses of these concepts in models and theories. So, “organism” is used in some disciplines and allows to ask questions such as “what is the mechanism of this life-sustaining function?”, but not in others: for instance, when there is a specific process of natural selection at play, one will count individuals, and in case of multilevel selection, models will include two kinds of individuals (e.g., cells/organisms or organisms/herds) rather than two kinds of organisms. Some philosophers came to contest the legitimacy of “organisms” in individuality biology, arguing that it is enough to talk about “individuals” (Haber, 2013; Bouchard, 2008); pragmatists will reject this option and keep the duality of concepts while accepting that in many contexts, “individuals” is the only useful and legitimate concept.

This strategy accounts for the differences between individuals and organisms; it makes sense of the fact that there is no point in inferring from “organisms” traits likely to define individuals in general, or that “organisms” cannot be a subclass of “individuals” since what matters is the context of use of these concepts rather than their purported rigid reference.

However, one major issue is the lack of complete separation between these two concepts: as I said, the evolutionary models account for some aspects of the design criterion (see also Huneman, 2017). Thus, the specificity of organisms with respect to biological entities is to some extent acknowledged within the concept if individuality, defined from the liberal viewpoint of evolution.

A pragmatist strategy assumes that the concepts are independent, in terms of their meaning. It happens that they coincide, in the sense that one concept picks out in some contexts the same thing as the other concept employed in other contexts – even though they are different. The strength of a pragmatist strategy is that the two concepts, as I tried to show, are very different, to the extent that one is defined in terms of NSC and the other comes from a liberal CSA approach.

But since there is an overlap in their signification, to the extent that the design criterion belongs to the organism concept but can be accounted for in the CSA in the context of a discourse about biological individuality, the pragmatist’s strategy may not be perfectly legitimate. One may discuss whether the conditions of applying a pragmatist strategy are met in general. Yet, if the two frameworks, NSC and NCA, are not independent, then they are competing when it comes to accounting for several classes of biological realities; and therefore, they cannot be handled through a pragmatist strategy.
## 7.5 Conclusion

In this paper, I have reviewed two approaches to the concept of organisms. In the former one, organisms are understood through a “necessary and sufficient conditions” approach, via two criteria inherited from the Kantian approach as an early investigation in the ontology of organization (itself embedded in the birth of descriptive embryology (Lenoir, 1982, Huneman, 2007; forth)), an investigation that the present volume continues. The latter derives from an ontology grounded on evolutionary models and ideas. I insisted on the difference in the logical structure of the two approaches. A conceptual space allows for much more liberality, while the NCS approach is precise in the sense that it supposedly picks up the “organisms” and nothing else. The conceptual space approach does not provide us with an idea of what are organisms and therefore cannot provide identity conditions or truth-makers of the sentence “X is an organism.” It is therefore much more deceptive from an ontological or metaphysical viewpoint. But it may fit some scientific practices, within which sharp boundaries between extensions of concepts and the rest are often hard to find, given the model-relativity of many of the propositions uttered by scientists. Its liberality may be appreciable in other cases; therefore, the distinction I found here between Kantian and evolutionary approaches, namely, a distinction between NCS and CSA, may be relevant for metaphilosophy and helps address other, unrelated, issues.

Clearly, organisms are at the crossroads of several hierarchies of individuals and ways to talk about individuals in biology; Eldredge's two hierarchies here are indicative of the multiplicity of takes on organisms and, therefore, of the sense in which “organism” can be seen as a crossroad concept. “Design” as a concept making sense of this organization proper to organisms is torn between a selectionist understanding in terms of bundles of adaptations and ultimately natural selection and functions in an etiological sense (Millikan, 1984, Neander, 1991) – and a concept of an organization that anchors organization in self-organizing processes rather than external selective pressures.

As a consequence, the plurality of conceptual schemes to make sense of organisms will probably cohabit in biology, and the duality between functional biology and evolutionary biology is not enough to distinguish these schemes – given that design is an idea proper to both approaches.

In the last step, I tried to propose some ways the two approaches – the NCS Kantian one and the evolutionary liberal one – can mutually relate. The result is a rather mild skepticism (to be aptly contrasted with Jaeger's chapter, in this volume). I don't think the concept of the organism, given its uses in biology, can be the place where a pacific coexistence between accounts can take place. The skepticism of this paper tends toward an acceptance of the conflictual and fractured essence of the concept of the organism in biology.
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# Chapter 8
## The Fourth Perspective: Evolution and Organismal Agency

Johannes Jaeger

**Abstract** This chapter examines the deep connections between biological organization, agency, and evolution by natural selection. Using Griesemer's account of the reproducer, I argue that the basic unit of evolution is not a genetic replicator, but a complex hierarchical life cycle. Understanding the self-maintaining and self-proliferating properties of evolvable reproducers requires an organizational account of ontogenesis and reproduction. This leads us to an extended and disambiguated set of minimal conditions for evolution by natural selection—including revised or new principles of heredity, variation, and ontogenesis. More importantly, the continuous maintenance of biological organization within and across generations implies that all evolvable systems are agents or contain agents among their parts. This means that we ought to take agency seriously—to better understand the concept and its role in explaining biological phenomena—if we aim to obtain an organicist theory of evolution in the original spirit of Darwin's struggle for existence. This kind of understanding must rely on an agential perspective on evolution, complementing and succeeding existing structural, functional, and processual approaches. I sketch a tentative outline of such an agential perspective and present a survey of methodological and conceptual challenges that will have to be overcome if we are to properly implement it.

### 8.1 Introduction

There are two fundamentally different ways to interpret Darwinian evolutionary theory. Charles Darwin's original framework grounds the process of evolution on the individual's struggle for existence (Darwin, 1859). It is a theory centered around the organism. The neo-Darwinian interpretation of the modern synthesis, in contrast, sees evolution grounded in the shift of allele frequencies in populations. It

<footnote>J. Jaeger (✉)
Department of Philosophy, University of Vienna, Vienna, Austria
Complexity Science Hub (CSH), Vienna, Austria</footnote>
completely brackets out the organism, focusing on the lower level of the gene and the higher level of the population instead (see, e.g., Walsh 2015; or Amundson, 2005, for a historical perspective). This reductionist approach provided much needed clarity for the study of evolutionary phenomena in the early twentieth century. But it hardly does justice to the complexity of causes underlying evolutionary change which—through Darwin’s struggle for existence—may involve nontrivial contributions of organismic behavior.

Many researchers in the field are aware of this limitation and are trying to move beyond it. The principal aim of evolutionary developmental biology (evo-devo), for example, can be construed as providing causal-mechanistic explanations for the evolution of the complex regulatory processes involved in development (Wagner et al., 2000; Calcott, 2009; Brigandt, 2015; DiFrisco & Jaeger, 2019; DiFrisco et al., 2020). The limits of reductionism have also come to the attention of philosophers of biology, and there is much interesting work on the subject (some of which will be discussed here). Unfortunately, progress toward an organismic evolutionary biology remains slow, in part because of the daunting intricacy of the matter, in part because of the lamentable and still widespread identification of “mechanism” with explanations at the molecular level (Nicholson, 2012), but also because many criticisms of reductionism in evolutionary biology remain wide of the mark, failing to properly engage the problem of organismic complexity in a philosophically grounded manner.

One particularly prominent example of this problem is a recent talk about understanding the “causal structure of evolution” by addressing the role of “constructive development” and “causal reciprocity” in the context of an “extended evolutionary synthesis” (e.g., Laland et al., 2015). *Constructive development*—defined as the ability of the organism to shape its own ontogenetic trajectory—implies some kind of agency, leading to open-ended exploratory evolution, in ways which are never clearly defined. *Causal reciprocity* emphasizes the mutual influence between ontogeny and phylogeny, or an evolving population and its environment. It is claimed to be widespread and to violate Ernst Mayr’s (1961) classical distinction between proximate and ultimate explanations in evolution. One problem is that such claims are hardly original. The constructive role of the organism in evolution goes straight back to Darwin himself (see, e.g., Amundson, 2005, or Walsh, 2015), and reciprocal causation is an integral part of many models in classic evolutionary genetics (Svensson, 2018; Buskell, 2019).

However, there is a more serious problem: such shallow theorizing does not even scratch the surface of the causal complexity underlying evolution. It is not wrong. It even goes in the right direction. But it does not go far enough. If we are serious about investigating the complex causes governing evolutionary change, we must tackle issues such as organismal agency and the fundamentally dialectic nature of evolutionary causation head on. We must call these problems by their name without avoiding the uncomfortably radical conclusions that might spring from their examination. This is what I am trying to do here.

Tackling the causal complexity underlying the evolutionary struggle for existence is no task for the faint-hearted. The causal structure of evolution is profoundly impenetrable. In fact, I believe that the whole undertaking is completely hopeless,
unless it is informed by an adequate ontology and epistemology, specifically devel-
oped for the task. Luckily, such a foundation is available in the form of William
Wimsatt’s *perspectival realism* (Wimsatt, 2007). It properly reckons with the lim-
ited nature of our cognitive abilities and the utterly byzantine character of reality. As
an added bonus, it takes a differentiated view on the role of reductionism as an
epistemic tool in biology and is antithetical to any quixotic quest for a grand synthe-
sis of evolutionary thought.

At the heart of Wimsatt’s ontology lies the recognition that the causal structure
of the world resembles a rich and dynamic tropical-rainforest ecosystem rather than
the eliminativist desert suggested by traditional ontological reductionism (Wimsatt,
1994, 2007). In this lush ontological forest, there are areas that exhibit cleanly sepa-
rated levels of organization, defined as “local maxima of regularity and predictabil-
ity in the phase space of alternative modes of the organization of matter” (Wimsatt,
2007, p. 209). Examples are the subatomic, atomic, and molecular levels studied by
physics and chemistry. In other areas of reality, however, this compositional hierar-
chy breaks down into more localized and less resolved causal structures, captured
by *perspectives*—defined as “intriguingly quasi-subjective (or at least observer,
technique or technology-relative) cuts on the phenomena characteristic of a system”
(Wimsatt, 2007, p. 222). Ultimately, even perspectives break down, resulting in
*causal thickets*, which are hard to disentangle since they lack any discernible regu-
larity or layering. The causal structure underlying the process of organismic evolu-
tion is a perfect example of such an impassable thicket.

Organizational levels and causal thickets require different epistemic strategies. In particular, reductionist methods can be useful, but remain fundamentally limited in the context of *the evolutionary causal thicket* (Wimsatt, 2007). What is needed to assess, complement, and contextualize them is a perspectival approach that aims to cut through the thicket in alternative ways. This refocuses our attention and our limited resources toward important aspects of evolution that are usually neglected in the standard reductionist account of evolutionary genetics.

At first glance, a multiplicity of limited and biased perspectives seems to consti-
tute an insurmountable obstacle for obtaining robust empirical knowledge. There is
no way to “step out of one’s own head” to gain a truly objective “view from nowhere”
(Giere, 2006; Wimsatt, 2007; Massimi, 2016). Upon closer examination, however,
an explicitly perspectival approach enriches scientific inquiry into complex causal
thickets in two important ways. First, the higher the diversity of perspectives, the
wider the range of questions we can ask, and the larger the variety of approaches we
can use to answer those questions. Second, comparative analyses of theoretical per-
spectives yield valuable insights into their respective applicability and limitations,
as well as the robustness and consistency of their claims (Giere, 2006; Griesemer,
2006; Wimsatt, 2007; Massimi, 2016). Put simply, more diverse approaches can
lead to broader and more trustworthy insights into complex and entangled processes
such as evolution. What we need are more varied and valid perspectives rather than
some kind of misguided theoretical synthesis, which is the remnant of an earlier—
and by now thoroughly outdated—positivist view of evolutionary biology
(Smocovitis, 1996; see also Walsh, 2015).
In this spirit, James Griesemer (2006) suggests a radical change of philosophical focus for evolutionary theory, from selecting the best among competing approaches and generalizing it toward a comparative analysis of the strengths, weaknesses, and complementarities of different local perspectives. These perspectives are not right or wrong, better or worse, per se, but succeed or fail to achieve their specific purpose. Griesemer (2006) distinguishes three kinds of evolutionary perspectives: structural, functional, and processual. To this, I will add a *fourth perspective* here, which emphasizes the agency of evolving organisms. A truly comprehensive science of evolution will have to include all four. Together, they yield more inclusive explanations of relevant evolutionary phenomena than each one of them on their own. In addition, a comparative approach allows us to reveal and assess the abstractions, idealizations, and simplifications that each approach is bound to make. Finally, the robustness of specific claims “can only be assessed if a scientific community pursues phenomena from a variety of perspectives… It is not enough merely to compete.” (Griesemer, 2006, p. 363). Is it really that surprising that a field centered on biological diversity would profit from a more diversified epistemic approach?

Furnished with these epistemological tools, we will now embark on a journey that explores the importance of organismic organization and organismic agency for the basic principles underlying evolution by natural selection. This journey starts with an introduction to the central concepts of organizational closure and organizational continuity in Sect. 8.2. I then briefly recall Lewontin’s (1970) minimal conditions for natural selection in Sect. 8.3. These conditions by themselves may be simple, but their mapping onto the physical world is incredibly complex. To unravel this complexity, we can take structural, functional, or processual perspectives, as described in Sect. 8.4. In Sect. 8.5, I will focus on Griesemer’s (2006) reproducer perspective, a processual view demonstrating that genetic replicators must be deeply embedded in a complex and hierarchical life cycle to be able to multiply themselves. Section 8.6 reviews why an organizational account of reproduction is necessary to understand such life cycles and, at the same time, implies organismal agency and self-determination. For this reason, agency itself becomes a fundamental aspect of systems that are evolvable by natural selection. This is why we need a fourth perspective on evolution. Section 8.7 presents a very preliminary exploration of what such an agential perspective would look like in terms of its mathematical and explanatory structure. I conclude with some general thoughts on what this implies, not only for evolutionary theory but also for scientific explanation in general.

## 8.2 Organizational Closure and Continuity

In this chapter, I focus on processual and agential perspectives on evolution, which revolve around the distinctive *organization* of living systems and how it is maintained—within and across generations—through *continuous regeneration* (Saborido et al., 2011; Mossio & Pontarotti, 2020; DiFrisco & Mossio, 2020; Pontarotti, this
volume). Biological organization, of course, is the unifying topic of this volume, and I refer the reader to its introduction for a general overview (Mossio, this volume; see also Moreno and Mossio (2015) and Toepfer, this volume). In this section, I will only briefly revisit those organizational concepts that are particularly relevant to my argument.

The organizational account is founded on the basic insight that the important difference between life and nonlife is not a difference of composition (what organisms are made of) but a difference in the way that system components relate to each other (how organisms are organized). The central defining feature of biological organization is *organizational closure*, a concept introduced by Jean Piaget (1967), which means that all essential parts of a living system mutually depend on each other, could therefore not exist without each other, and must maintain each other through their collective interactions. Organizational closure is complementary to thermodynamic openness; in fact, it can only occur in far-from-equilibrium systems. It leads to a causal circularity that is already reflected in La Mettrie's metaphor of the living body as “a spring that winds itself.” Organisms are closed to efficient causation (Rosen, 1991): their organization is maintained *from within*, even though matter and energy constantly flow through the system. It is in this sense that organisms are self-making and self-producing: they are *autopoietic systems* (Varela et al., 1974; Maturana, 1980).

Causal circularity and closure are necessary but not sufficient to account for the organization of autopoietic systems. Biological organization also requires a dialectic relationship between the physicochemical processes that materially compose an organism and the system-level constraints that act upon them (Montévil & Mossio, 2015; Mossio et al., 2016). *Processes* denote various kinds of transformations (such as chemical reactions or the physical rearrangement of cells and tissues) that involve the generation, constitution, alteration, consumption, and destruction of system components. *Constraints* act on processes but remain unaltered by them (at least at the time scale at which the constrained process occurs). Constraints can be external or internal to the system. They reduce the degrees of freedom of the process on which they act. Their effect is strongly context-dependent. Examples of organismic constraints are enzymes, or the vascular system in vertebrates, which catalyze their metabolic reactions and transport blood without themselves being altered at the time scale of the process they constrain.

Just like any other physicochemical component of a living system, its constraints need to be constantly replaced, repaired, and maintained. Enzymes, for example, decay and must be replenished through the processes involved in protein synthesis. This means that constraints can depend on each other. They are generated by processes on which other constraints are acting. In turn, they can generate other constraints by regulating the processes that produce them. The synthesis of enzymes, for example, depends on ribosomes whose synthesis, in turn, depends on enzymes. If each constitutive constraint in a living system is both dependent on and generative for at least one other constraint, then there is *closure of constraints*, which represents a specific kind of organizational closure (Montévil & Mossio, 2015; Mossio et al., 2016). It means that the constrained overall dynamics of the system determine
the conditions for the continued existence of the constraints. In this way, the pro-
cesses and constraints of a living system logically and materially entail each other.
One is required for the existence of the other.

This raises the question of how living processes and constraints co-emerge
through their dialectic dynamic interactions. Kauffman (2000) argues that living
organization must be powered by work-constraint cycles. Incorporating this into the
account of Montévil and Mossio (2015), we can say that the constrained release of
energy by the organized system provides the physical work required to maintain its
existing constraints and to constantly generate new ones. In this way, work-
constraint cycles can explain various kinds of self-organization far from equilib-
rium, but are not yet specific enough or sufficient to account for the emergence,
persistence, and propagation of organizational closure in living systems. For this,
we need the additional concept of organizational continuity (DiFrisco & Mossio,
2020; Mossio & Pontarotti, 2020; Pontarotti, this volume). It means that closure at
any particular time dynamically presupposes closure of constraints that have oper-
ated earlier (see Bickhard, 2000). Organizational continuity represents a specific
type of causal continuity. The key point here is that the particular organization of
constraints in an organism not only can but *must* continuously change for it to main-
tain organizational closure and to continue living (Montévil et al., 2016; see also
Nicholson, 2018). It must engage in a process of continuous regeneration (Saborido
et al., 2011). Hans Jonas (1966) calls this *needful freedom*—the capacity of living
matter to change its form—and the *thermodynamic predicament*, the irremissible
necessity for it to do so.

On this view, the organism can be seen as a continuously changing but persistently closed organization of constraints that “lifts itself” out of the thermodynamic background of all possible physicochemical processes (see, e.g., Hofmeyr & Cornish-Bowden, 2000; Kauffman, 2000). It does this through work-constraint cycles that recursively actualize a closure of constraints. What this means is that the organization of constraints at any point in time—the channeling of physicochemical processes in certain directions—arises from *within* the organism itself. Due to the condition of organizational continuity, it is a consequence of previous organismic constraints, of earlier organizational closure. For this reason, we cannot predict its temporal evolution from considerations of far-from-equilibrium thermodynamics (or other physical laws of nature) alone. It is in this sense that the organism has a degree of *autonomy* from its environment (Moreno & Etxeberria, 2005; Moreno & Mossio, 2015). The organism generates its own dynamics of unfolding closed constraints. These constraints determine not only the internal constitution of the system but also its interactions with the environment. Simply put, all organisms possess at least some minimal kind of agency—they “act on their own behalf” (Kauffman, 2000; Moreno & Mossio, 2015, esp. Chap. 4).

In this way, the organizational account grounds the teleological notions of bio-
logical function, as well as self-determination and agency on naturalistic principles
that lie perfectly within the scope of scientific explanation (see also Sect. 8.7).
Functional constraints in living systems are defined as those that contribute to orga-
nizational closure and continuity (Mossio et al., 2009a; Moreno & Mossio, 2015;
Mossio & Pontarotti, 2020). Self-determination arises from the recursive and reflex-
ive diachronic emergence of functional constraints from previous realizations of
organizational closure (Mossio & Bich, 2017). Agency is defined as the capacity to
internally generate causal effects (actions) that involve interactive functions—those
constraints subject to closure which mediate the organism's boundaries and
exchanges with its environment (Moreno & Etxeberria, 2005; Barandiaran &
Moreno, 2008; Barandiaran et al., 2009; Moreno & Mossio, 2015). Put more simply,
the organism selects and initiates the kind of interactions it has with its surround-
ings. This kind of agency is an observable property of an organism—its ability to
cope with a particular situation, to pursue its goals in response to opportunities or
obstacles present in its perceived environment (Walsh, 2015).

What is most important to point out here is that *all these teleological properties
are a direct and necessary consequence of the fundamental self-maintaining orga-
nization of living systems*. Anything that is alive can be legitimately described from
the perspective of organismic agency and goal-orientedness (Walsh, 2015).

But if such teleological aspects are fundamental—and unproblematic from the
point of naturalistic explanation—why do we constantly attempt to explain them
away? Why do we ignore them? Why do we not take them at face value, even
though they imply profound and radical challenges for our thinking about biological
systems and their evolution? What does this mean for what we consider a scientific
explanation? These are the kind of questions that will keep us busy throughout this
chapter.

8.3 Minimal Conditions for Darwinian Evolution by
Natural Selection

To better understand the close and intricate relationship between organismal organi-
zation, agency, and the process of evolution by natural elections, I must briefly
review the prerequisites for this type of evolution to occur. Ever since Darwin, biol-
ogists and philosophers of biology have sought to stipulate the most concise formu-
lation of necessary and sufficient conditions for evolution by natural selection
(reviewed in Godfrey-Smith, 2007, 2009). The shortest one I could find is Sober's
"Darwinian general principle": "if there is heritable variation in fitness, then there
will be evolution" (Sober, 1984, p. 28, original emphasis).

The most cited core requirements are those first published in Lewontin (1970)
and, slightly revised, in Lewontin (1978), which state that the process of evolution
by natural selection is based on three fundamental principles or propositions: (1) *the
principle of variation*, there is variation in physiological, ontogenetic, morphologi-
cal, and behavioral traits between individuals in a population; (2) *the principle of
heredity*, this variation is (at least in part) inherited such that offspring resemble
their parents; and (3) *the principle of differential fitness*, different phenotypic vari-
ants vary in their influence on the rate of survival and reproduction of their bearers
in different environments, leading to different numbers of offspring in either immediate or remote generations. While these principles hold, a population will undergo evolution by natural selection.

There are many more elaborate formulations of these conditions, and it has been pointed out that any simple enumeration of core requirements provides more of a *recipe for evolutionary change*, rather than a true summary that encapsulates all cases of evolution by natural selection (Godfrey-Smith, 2007). For the purposes of my argument, a recipe will suffice. It is absolutely not my intention to defend any kind of adaptationism stating that evolution occurs by natural selection only. Quite the contrary, my interest here is to explore a new perspective on what makes such evolution possible in the first place. In this spirit, I will continue my argument by reviewing three existing perspectives on evolution by natural selection before adding a new one to the canon.

## 8.4 Three Different Perspectives on the Evolutionary Causal Thicket

The minimal conditions for evolution by natural selection appear deceptively simple. However, the path to understanding how they map onto physical reality is complex and full of conceptual pitfalls. One particularly important aspect of this problem concerns the connection between population-level descriptions of evolution and the underlying causal structure of the process, which is ultimately rooted in Darwin's famous struggle of individual organisms for their survival (Walsh, 2015; see Sect. 8.1). It seems unlikely that population-level statistical averages (e.g., mean and relative fitness measures) and emergent properties (arising from interactions of individuals and their environment) will suffice to explain all aspects of these highly complex and heterogeneous underlying causal dynamics at the organismic level. But what kind of understanding *can* be gained at this underlying level? Considering the immensity, diversity, and complexity of individual-level causal interactions, is it possible to gain any foothold at all? This question remains not only unresolved but mostly also unasked in current evolutionary biology.

One way to unravel the evolutionary causal thicket is to distinguish different perspectives that can validly be adopted to tackle the central problems related to evolution by natural selection. As already mentioned, we can distinguish three kinds of perspectives on evolution by natural selection (Griesemer, 2006). Each of these perspectives focuses on a different set of questions and has different advantages and limitations. I will briefly review each of them (with examples) and show how they relate to one another.

1. *Structural perspectives* focus on what evolves. The most famous debate in this domain is concerned with the units of selection (Lewontin, 1970). Approaches within this perspective consider evolving lineages as organizational hierarchies of compositional levels (molecules, organelles, cells, tissues, organs, organisms,
populations, and species). They ask at which level (or levels) selection applies and attempts to identify the pertinent structural units on which it acts. Such units must meet the minimal conditions for evolution by natural selection through completing the circle of development, reproduction, and selection (Brandon, 1990). Evolutionary change is treated as change in unit structure. Structural approaches are indispensable for the investigation of multilevel selection. They are powerful tools for the formalization of selection and inheritance. Their main weaknesses are that they leave unexamined the evolutionary origin of the multi-level hierarchy they presuppose and that they have difficulties accommodating inter-level processes such as development (which maps changes at the genetic level to phenotypic ones; see Griesemer (2000a,b, 2006) for details).

2. *Functional perspectives* focus on *why* things evolve. A well-known example is the replicator-interactor perspective developed by Dawkins (1976, 1983) and refined by Hull (1980, 1981, 1988). Replicators are entities able to transmit their structure directly and (relatively) intact through a copying process that produces more entities like themselves. Interactors, in contrast, are entities that engage with their immediate environment in ways that lead to differential replication. The focus here is not on the exact structure of either replicators or interactors (even though the former are generally assumed to be genes, and the latter organisms), but on the functional roles they play in generating the minimal conditions for evolution by natural selection. Dawkins and Hull differ on this matter. While Hull acknowledges selection of interactors at multiple compositional levels, Dawkins only recognizes replicators as true units of selection, since they alone are stably and faithfully copied and transmitted through the germ-line from generation to generation (see Griesemer, 2005). Apart from being the cause of inheritance, replicators also determine the development of the interactor's phenotypic traits, and even the construction of environmental features such as beavers' dams and human megacities, as proposed by Dawkins' (1982) perspective of the "extended phenotype." The environment then acts as a filter on populations of interactors, allowing some to survive and reproduce better or worse than others, depending on what kind of (extended) phenotypes are encoded by their replicator genes. This leads to a clean separation of development and inheritance. These processes do not interact directly, even though they share replicators as their common cause. Its conceptual simplicity is the main advantage of this perspective. At the same time, its failure to accommodate causal interactions between the processes of development, selection, and inheritance is also its biggest shortcoming. It leaves the functional separation of these processes unexamined, presupposing an excessive form of genetic determinism instead, which leads to an extremely oversimplified replicator/gene-centered view of evolution. Another problematic aspect is that both replicators and interactors are defined in circular ways that implicitly depend on goal-oriented processes (i.e., replication and the interaction of the organism with its environment), which are simply taken for granted (see Griesemer, 2006, for details).
3. *Process perspectives* focus on *how* evolutionary change occurs. As their name indicates, these perspectives focus on processes as the basic units of evolution. One example of such a perspective is process structuralism, which aims to understand the lawlike behavior of developmental processes that generate biological form (Goodwin, 1982a,b; Webster & Goodwin, 1982, 1996). It describes these generative processes as morphogenetic fields, whose underlying causal structure determines their dynamic behavior and the kind of phenotypic transitions they can produce. A methodical exploration of these structures through dynamical modeling and simulation would result in a rational system of related forms and the transformations between them. This provides an ahistorical "space of the possible," which the historical process of evolution explores. In this sense, process structuralism provides an understanding of the structured variability that provides the substrate for natural selection to act on. This is something neither structural nor functional perspectives can provide. But there are two main drawbacks. First, the rules behind the processes that generate variability are assumed to be universal and time-invariant, an assumption that is no longer tenable (see Sect. 8.6). Second, process structuralism only deals with regular phenomena in evolution. However, the generic forms that are actually realized in evolution are probably only a tiny fraction of all possible forms, which means that contingency probably still plays a dominant role in evolutionary dynamics (Griffiths, 1996).

Developmental systems theory (DST) is another example of a process perspective, which addresses this problem of contingency (Oyama, 1986; Oyama et al., 2001). Its basic unit is a developmental system, a process which is organized through the interactions of a variety of developmental resources in ways that lead to the completion of the life cycle. The precise structure of these interactions is not the focus here, since it is assumed to be a contingent product of evolution by natural selection. Instead, DST emphasizes the distributed and decentralized nature of control in evolving developmental systems. On this view, the transformation of biological form requires not only genetic resources but also epigenetic and environmental factors that are treated as equally important. In other words, the entire developmental system, rather than the gene, is the replicator (Griffiths, 1994). The main weakness of the approach is, however, that the boundaries of a developmental system are extremely difficult to define. This makes it hard to represent different modes of inheritance or to delimit life cycles between parents and offspring (see Griesemer, 2000a, 2006, for more details).

Traditionally, all of these perspectives are seen as competing with each other. DST, for example, explicitly positions itself as an alternative and a replacement for process structuralism (Griffiths, 1996). However, the existence of generic forms and more or less plausible evolutionary transformations does not deny the importance of historical contingency. Both can be seen as complementary aspects of the evolution of form. Similarly, functional approaches—in their unbridled ambition to provide a complete and unified account of evolutionary change—often treat structural or process perspectives as superfluous. However, we have seen how these perspectives can
cooperate in a debate about the nature of the replicator. Griesemer (2006) expands on this topic by introducing his own process perspective, which sheds light on the nature of biological multiplication. This *reproducers perspective*—originally developed as a tool to investigate major transitions in evolution (Griesemer, 2000c)—powerfully illustrates how we can identify and transcend the limitations of specific approaches through an inclusive and comparative perspectival framework.

## 8.5 Reproducers, Evolvability, and the Completion of the Life Cycle

The reproducer perspective takes a closer look at the process of biological replication (Griesemer, 2006). In the previous section, we have seen that Dawkins' ultra-reductionist functional approach considers replicators as the only valid units of evolution. They alone are transmitted stably and faithfully through the kind of template-based copying process—exemplified by semiconservative DNA replication—that is presumed to form the basis for heritable variability. We have also noticed the circularity of their definition: replicators are essentially defined as structures able to replicate, which takes the seemingly goal-oriented process of replication itself for granted, leaving its underlying principles (and its origins) unexamined.

Can this circularity be avoided? To find an answer to this question, we have to examine the rules underlying the copying process. Specifically, to be a proper unit of evolution, an entity must adhere to the following three principles (Szathmáry & Maynard-Smith, 1993): (1) *the principle of multiplication*, entity A must give rise to more entities of type A; (2) *the principle of heredity*, entity A must produce entities of type A (not B); and (3) *the principle of variability*, the copying process is not perfect such that, every so often, entity A will give rise to an entity A' (which, in fact, may be identical to entity B). If we add different copying rates for different entities, we arrive back at Lewontin's minimal conditions for the process of evolution by natural selection as described in Sect. 8.2. What is new in this approach centered on the unit of evolution is an explicit focus on the notion of biological "multiplication."

What does it mean for an entity A to give rise to more entities of type A in an evolutionary context? And which conditions must be met for this process of biological multiplication to result in principles of heredity and variability that enable evolution by natural selection? There are several reasons to suspect that simple template-based replicators fail to meet these conditions. They are all connected to the problem of *evolvability*: the capacity of a system to generate (at least potentially) adaptive variability (Wagner & Altenberg, 1996).

The first of these reasons is that template-based copying by itself is too fragile and imprecise to support the kind of stability that is needed for the evolution of complex living systems. This argument is rooted in Eigen's paradox (Eigen & Schuster, 1977, 1979). In its original formulation, it states that the production of
complex enzymes requires a large and complex genome, while the replication of a large and complex genome requires complex enzymes (necessitating a complex and precisely regulated cellular environment). More specifically, the enzymes required for genome replication must be able to proofread, i.e., to correct errors in the copying process. Without proofreading, complex genomes would be too unstable to evolve: copying mistakes would rapidly accumulate over time, inducing an *error catastrophe* that causes the collapse of the organization of a living system. This sets a very narrow upper limit on the size and complexity of evolvable genomes. But even if most mutants would be viable and able to reproduce (as may be the case in viral evolution), the original genome would quickly be lost in a sea of different variants, leading to the inevitable dilution and disappearance of any evolutionary lineage.

How could this fundamental limitation on the evolvability of complex living systems be overcome? One way is through compartmentalization and the hierarchical organization of living systems. Szathmary and colleagues have formulated a *stochastic corrector model*, which shows how compartmentalized probabilistic replicators can overcome Eigen's error catastrophe by constantly being selected at the higher level of the compartment population (Szathmáry, 1986; Szathmáry & Demeter, 1987; Grey et al., 1995; Zintzaras et al., 2002). This indicates that multi-level composition may be required to render an evolutionary unit evolvable.

Alternatively, it has been proposed that autocatalytic processes could lead to stable self-maintenance without complex genomes or hierarchical organization. Based on this general idea, Eigen and Schuster (1979) developed their own minimal autocatalytic model, the *hypercycle*, as a proof of concept. Unfortunately, hypercycles were shown to be extremely vulnerable to “selfish” replicators within them. In the meantime, Stuart Kauffman (1971, 1986, 1993) was proposing more general and robust models for autocatalytic sets. Kauffman’s models consist of networks of chemical reactions that are capable of self-maintenance through catalytic closure: every reaction within the set is catalyzed by at least one product of the network itself. Even though this avoids error catastrophes, it is difficult for autocatalytic sets to generate the kind of variability that evolution requires. In stark contrast to the fragility of template-based replication, these sets are too rigid, since any reaction that does not contribute to the self-maintenance of the network is quickly outcompeted. Because of this, the system strongly converges to one particular optimal and invariant set of autocatalytic reactions (an attractor in the sense of being a strongly self-maintaining organization), which leaves very little heritable variability for selection to act upon (Fontana & Buss, 1996).

All of this suggests that Lewontin's minimal conditions on their own are not quite sufficient. They remain ambiguous. Evolution by natural selection not only needs heritable variability but also needs *the right amount of heritable variability in the right context*. Neither systems that are too stable nor systems that are too unstable can evolve. Stuart Kauffman famously illustrated this by his metaphor that evolvable systems must be poised “at the edge of chaos,” a dynamic regime including “islands of chaos” among a “percolating network or order” (Kauffman, 1993).
Whatever we make of this metaphor, it is certainly true that the principle of variability imposes more specific and stringent conditions on evolution than is evident at first sight and that some sort of self-organization within the context of a hierarchical organization is required for natural selection to occur.

Based on the argument so far, let us take a closer look at the self-organizing processes able to generate the kind of heritable variability required for evolution. There is another reason why biological multiplication must be more complex than a simple template-based copying process. Copying does not require any material continuity between generations. Copies must resemble their template in form (e.g., similar genetic sequences), but can be made of different material components (the bases that are incorporated into the newly synthesized strand of DNA come from outside the original double helix). In this case, there is a clear separation between copying cycles: we can precisely determine when one cycle ends and another one begins. In contrast, biological multiplication always involves some *material and temporal overlap* between parents and offspring and between reproducer and reproduced. Organisms arise from material components of other organisms, and they do this in a gradual manner.

This implies some kind of *development*, which for the purpose of my evolutionary argument can be defined in a broad and minimal sense as “acquiring the capacity to reproduce” (Griesemer, 2006). Unlike the common (and narrower) definition of development as “embryogenesis” or “morphogenesis,” this more general concept applies to unicellular and multicellular life-forms alike (see also Bich & Skillings, this volume, and Montévil & Soto, this volume). To come back to Eigen’s example: a mitotic cell must first replicate its genome before it can divide again. This qualifies as “development” sensu Griesemer. To avoid confusion, I will use the term *ontogenesis* to describe the totality of regulatory processes—metabolic, physiological, developmental, and behavioral—that are involved in acquiring the capacity to reproduce.

This brings us to a central point of the argument: it is the process of ontogenesis which must provide the error-correcting capabilities that are needed to produce the kind of heritable variability required for evolution by natural selection. Both template-based replicators and autocatalytic networks lack ontogenesis, which is why they are not properly evolvable. In Eigen’s example, a complex genome cannot be faithfully replicated unless it is embedded in the kind of complex and precisely regulated cellular environment which provides the necessary proofreading enzymes. Genome replication only ever happens if it is embedded within the more complex context of a cell cycle (even in those cases where the resulting cells do not separate completely). This illustrates the fundamentally dialectical relationship between ontogenesis and reproduction in evolution. They logically and materially entail each other. This relationship goes beyond mere causal reciprocity (see Sect. 8.1). Ontogenesis and reproduction do not only influence each other, *but cannot exist independently*—they *must* co-emerge for organisms to be evolvable. They dynamically presuppose each other (Bickhard, 2000). The resulting system is a true unit of evolution called a *reproducer* (Griesemer, 2006).
Reproducers are more complex than replicators, since they include ontogenesis and material overlap between generations. Ontogenesis and reproduction together form the life cycle of the reproducer. *This life cycle must be completed* for biological multiplication to continue from generation to generation. Variability cannot disrupt life cycle completion without disrupting evolution. In other words, freshly multiplied entities *a* must be *organized* in a way that enables them to mature into entities *A*, which have the capacity to reproduce. Otherwise, they are not evolvable. This constitutes a *principle of ontogenesis* (or *development*), which we must add to the principles of multiplication, heredity, and variability to define a proper unit of evolution (Griesemer, 2006).

One additional point requires our attention. In principle, ontogenesis could be based exclusively on some robust but spontaneous process of self-organization. However, this alone does not allow for natural selection to occur: in such systems, there is no true heredity of organization (beyond parents and offspring sharing the physical context that enables self-organization) and thus no selectable heritable variability. Moreover, it is quite probable that, even if they could evolve, purely self-organizing reproducers would easily be outcompeted by those possessing some kind of inherent hereditary processes, which lead to a much more efficient and stable propagation of organization across generations. Thus, heritable variability must be reliably regenerated and re-established through ontogenesis during each generation. For reproducers to meet the minimal conditions for evolution by natural selection, they require not only ontogenesis and material overlap between parents and offspring but also some kind of inter-generational *continuity of organization* that allows for heritable variability to be regenerated. The precise nature of this kind of organizational continuity will be the focus of Sect. 8.6.

In the reductionist framework of Dawkins, the source of organizational continuity is located entirely within the replicators themselves: it is the genes alone that are transmitted across generations, and genes alone determine the phenotypic traits of the interactor. This presupposes, however, that replicators are able to reproduce (complete a life cycle) all by themselves. Unfortunately, I have just shown that this is not the case: the simple template-based copying process on which replication is based fails to provide proper principles of heredity and variability for evolution by natural selection. To put it more simply: replicators can only evolve if they are embedded in the more complex dynamics of a reproducer process (Griesemer, 2006). The reproducer perspective therefore absorbs and replaces functional perspectives based on replicators as the fundamental units of evolution. The latter may still be useful to study the evolutionary role of genetic replication—but they can no longer serve as the foundation for a comprehensive theory of evolution. What the reproducer perspective offers is no extended synthesis, but rather evolutionary theory put back on its original Darwinian footing (see Walsh, 2015). A couple of examples will serve to illustrate this fundamental point.

The simplest reproducer systems that we currently know of are infective prions and virus particles. Because of their self-assembling structure, they are the closest we have to a “naked” replicator in nature. The mature, infectious forms of these entities self-aggregate from their macromolecular components according to simple
thermodynamic principles. Thus, at first glance, they appear to lack proper ontogen-
esis or organizational continuity as defined above. However, this appearance is mis-
leading. To generate their macromolecular components, prions and viruses rely on
the pathways for biosynthesis and the homeostatic maintenance of the cellular
milieu in a living host. These cellular processes are necessary to provide the sub-
strates and the appropriate conditions for self-aggregation to occur. Moreover, both
biosynthetic pathways and homeostatic mechanisms are central features of the
host's self-maintaining organization (Hofmeyr, 2017). They provide the organiza-
tional principles required for prions and viruses to acquire the capacity to repro-
duce. Therefore, prions and viruses are not evolvable at all, if considered as isolated
replicators apart from their hosts. In order to evolve, they *must* be embedded within
a reproducer—the complex ontogenetic processes that constitute their host's life
cycle (see Moreno & Mossio, 2015, Chap. 4, for a more detailed discussion).

As a second example, let us look at multicellular animals, which are vastly more
complex than prions and viruses. They are particularly interesting in our context,
because of their exceptionally well-defined separation between germ-line and soma.
As we have seen in Sect. 8.4, the strict separation of reproduction (germ-line) and
development (soma) is a central postulate of replicator-inheritor theory. But even in
this case, replicators must be embedded in the larger context of a reproducer process
in order to propagate and evolve. In fact, there are replicator processes at multiple
levels of organization. We have already seen that the replication of a genome only
ever occurs in the context of a cell cycle. At the tissue level, the maintenance and
proliferation of germ cells require a specific niche within the context of the larger
multicellular body. Finally, at the organismic level, animal reproduction relies (at
least to some extent) on the behavior of the organism and its complex and goal-
oriented interactions with the environment and other members of its species. I'll
revisit this important point in Sect. 8.6.

Let me emphasize the main point of the argument once again: replicators cannot
be the fundamental units of evolution unless they are embedded in a reproducer
system, which necessarily includes a process of ontogenesis that generates the kind
of heritable variability needed for evolution by natural selection. With this in mind,
we can now reexamine the nature of a replicator. The ontogenetic process underly-
ing replication must have the specific character of a *coding system* (Griesemer,
2006). To complete the replication cycle, ontogenesis must produce an interactor.
The traits of this interactor must somehow be *encoded* in the genome. For this to
work, the number of possible states in such a coding system must vastly outnumber
the actual states that occur in an evolving population. This kind of coding process is
what allows for a separation of genotype and phenotype. Without the cell to inter-
pret and replicate it, however, there is no sense in which the genome carries a code
(see Waddington, 1957). Therefore, replication must be seen as a highly specialized
and context-dependent ontogenetic process, embedded in a hierarchy of reproduc-
tive organizations. As stated in no uncertain terms by Griesemer (2006, p. 359):
“Far from being master molecules, genes are prisoners of development, locked in
the deepest recesses of a hierarchy of prisons” (see also DiFrisco & Jaeger, 2020).
## 8.6 Organization, Reproduction, Agency, and Minimal Evolution

The reproducer account blurs the distinction between structural, functional, and processual perspectives. It shifts our focus from replicators to the more general category of reproducers as the fundamental (processual) units of evolution. Considered from a functional point of view, the central question about biological multiplication shifts from a simple template-based copying process (replication) to the propagation of complex biological organization across generations (reproduction). What are the heritable organizational principles that enable the reproduced system to acquire the capacity to reproduce? What are the heritable organizational principles that govern its ontogenesis and the completion of its life cycle through reproduction? Griesemer (2006) argues that these principles have to be based on some kind of organized material propagules, not mere informational programs as in a replicator perspective. These propagules must not only account for ontogenesis to explain self-maintenance, self-production, and self-regeneration within a life cycle but must also form the basis for an organizational account of reproduction.

There are several such accounts in the literature. The ones I will focus on here extend the notions of organizational closure and organizational continuity (see Sect. 8.2) across generations, beyond the temporal boundaries of the individual organism (Christensen & Bickhard, 2002; Saborido et al., 2011; Mossio & Pontarotti, 2020; DiFrisco & Mossio, 2020; Pontarotti, this volume). One option, from a functional point of view, is to treat entire reproductive lineages as organized systems (Christensen & Bickhard, 2002). However, such higher-order organization remains difficult to delineate precisely. Instead, we can take a more focused approach and consider the reproducer-reproduced dyad as a continuously organized system (Saborido et al., 2011). The important point here is to distinguish the boundaries of self-maintaining organization from the boundaries of the individual (DiFrisco & Mossio, 2020).

On the one hand, reproducer and reproduced can be considered the same organized system since there is organizational continuity between the two: closure of constraints must be maintained throughout the process of reproduction. An egg cell, for example, is both the product of the organization of the reproducer and the source of the organization of the reproduced. It exerts its function within the context of a cross-generational organization (Saborido et al., 2011; Mossio & Pontarotti, 2020; Pontarotti, this volume). On the other hand, the reproduced system is not the same individual as the reproducer. In fact, reproducer and reproduced often continue to coexist, more or less independently of each other. In this context, they must be treated as different organized systems. But there is no contradiction here, just a simple distinction: what sets apart reproduction from ontogenesis is not a break in organizational continuity, but a difference in the number of organized systems that are present at a given moment (DiFrisco & Mossio, 2020). Discontinuities between generations are characterized by fission (e.g., nuclear or cellular division, budding, or birth), or fusion (e.g., gametic, in case of sexual reproduction) of organized
systems. A fertilized egg cell is the product of the functional organization of two different reproducer systems. It is dynamically presupposed by both of them (Bickhard, 2000).

On this view, the reproductive process is seen as the means of an organism to maintain its organization beyond the boundaries of its individual life cycle despite the discontinuities that characterize reproduction, and reproductive functions are those that contribute to inter-generational closure. But what exactly is meant by organizational continuity across generations? This concept clearly goes beyond mere material overlap through propagules (Griesemer, 2006), and it is more specific than the general notion of shared developmental resources (Griffiths, 1994). We have already seen in Sect. 8.2 that organizational continuity is a special case of causal continuity. Now that we have extended it to organizational closure across generations, it enables a new principle of heredity as *continuous self-maintenance of cross-generational functional organization* (Mossio & Pontarotti, 2020; Pontarotti, this volume). Remember that this does *not* imply that any specific physical structures or components of the system must persist unchanged through reproduction. Structure and material composition are in constant flux. What persists is the organization required to acquire the capacity to reproduce a specific kind of biological entity, a disposition for recurrent ontogenesis where similar functional constraints reoccur at the time scale of each generation (Mossio & Pontarotti, 2020; Pontarotti, this volume).

This organizational account of the reproducer affects several of the principles that underlie the minimal conditions for evolution by natural selection. Most important of all, it renders the replicator obsolete and replaces it with reproducers as the proper units of evolution. Furthermore, it suggests a new organizational principle of heredity: conservation of cross-generational functional organization, which requires organizational continuity. This kind of heredity enables and at the same time also depends on a new principle of ontogenesis: the capacity to reproduce must be reacquired during each generation in order to complete the life cycle (Griesemer, 2006). The flip-side of both principles of ontogenesis and heredity is a revised principle of variability (Montévil et al., 2016): variation can only occur under the general constraint of maintaining organizational closure within and across generations. Without this kind of cross-generational organizational continuity, life cannot go on and evolution cannot occur. In summary, we end up with the following set of tightly interlocked principles: a *new principle of ontogenesis, radically revised and refined principles of heredity and variation* (plus Lewontin's *unchanged original principle of differential fitness*). Together, they comprise an extended and disambiguated set of minimal conditions for an *organizational theory of evolution by natural selection, which has the organism (and its struggle for existence) back at its core*, as it was in Darwin's original theory (Walsh, 2015).

But this is not all. Behind this revision of the minimal conditions for evolution by natural selection lies an even more significant implication for evolutionary theory. It is rooted in the simple fact that organizational closure must be retained throughout ontogenesis and reproduction for a life cycle to be completed. And the life cycle must be completed for evolution to occur. In other words, *without organizational*
continuity and the functional conservation it enables, there is no reproducer, and thus no proper unit of evolution. Without organizational continuity, there are no evolvable systems.

If we accept this general conclusion, we must face another profound consequence: any proper unit of evolution, any evolvable system, must involve some kind of agency. It must be an autonomous agent with some degree of self-determination, since self-determination and autonomy are fundamental properties of organized systems (see Sect. 8.2). This is even true for the example of prions and viruses from Sect. 8.5: they require a host with organizational continuity (and thus agency) to reproduce and evolve. It may come as a surprise, but *evolution by natural selection is always the evolution of autonomous self-determining agents*, or occurs in higher-level organized systems—such as ecosystems, cultures, or economies—that involve autonomous self-determining agents. This basic insight has important implications for the theory of evolution. But what are these exactly? What does it mean to look at evolution from an *agential perspective*?

## 8.7 The Fourth Perspective: An Agential Theory of Evolution

Before I outline the possible shape of an agential theory of evolution, it is important to reiterate what agency is, and what it is not. Most importantly, *agency is the capacity of an organism to originate causal effects from within its own boundaries* (Barandiaran et al., 2009), particularly those that define its interactions with its external environment (see Sect. 8.2). These effects are observable as goal-oriented actions—selected from a more or less ample behavioral repertoire—which enable the organism to attain its ends by taking advantage of opportunities or avoiding obstacles in its experienced environment (Walsh, 2015). Biological organization and continuity provide the self-determination and autonomy necessary for true goal-oriented agency (cf. Sects. 8.2 and 8.6). Shadlen and Gold (2004) call this kind of relative autonomy “freedom from immediacy.” While the organism’s actions arise from its interactions with its environment, they are not directly imposed or determined by it.

This kind of *agential emergentism* (Walsh, 2015) stands in strong opposition to the more traditional approach to “agency” in evolution, which was first introduced by Ernst Mayr, and is still widely shared by biologists today. Mayr (1961) popularized the notion of *teleonomy* to denote preprogrammed behavioral routines that *appear* goal-seeking because they are adapted to their environment through evolution by natural selection. On this view, there are no causal effects (no actions) that are generated within the organism. Organisms have no intrinsic goals. There is only automated processing of external stimuli into responses adapted to a given environment. In other words, *there is no true organismic agency*. Adapted behaviors are explained entirely by factors in the external environment. The environment poses
problems that organisms solve through evolution by natural selection (Lewontin,
1978; Levins & Lewontin, 1985). While denying true agency to organisms, this
view can lead to the strange result that information-processing becomes interpreted
as cognitive ability in simple organisms without a nervous system (e.g., bacteria;
see Fulda, 2017, for an excellent critique). Such paradoxical consequences arise
because the conventional view does not take agency quite serious enough—as it
does not even include true agency in its ontology.

What happens to evolutionary theory if we do take agency at face value? Walsh (2015) provides a very thorough philosophical analysis of this question and concludes that a number of implications follow from agential emergentism. First, evolution must be treated as a fundamentally *ecological* or *relational phenomenon* arising from the purposive engagement of the organism with its experienced environment (Darwin's struggle for existence). Second, it is not possible to causally separate the processes of inheritance, reproduction, and development: “fragmented” evolutionary theory is an idealization. Third, there is no privileged control by replicator genes: genetic causation always has to be interpreted in its organismic context (see also DiFrisco & Jaeger, 2020). These insights do not fundamentally differ from claims made by other movements toward a more organismic evolutionary biology, such as the extended evolutionary synthesis (Laland et al., 2015). However, there is a central question that an agential theory of evolution raises, which remains largely unexplored by other approaches: *how does true organismic agency impact evolutionary change?* Timid first steps toward an exploration of this question have been made in studies of phenotypic plasticity (e.g., West-Eberhard, 2003; Moczek et al., 2011; Levis & Pfennig, 2016; Uller et al., 2019) and niche construction (e.g., Odling-Smee et al., 2003; Scott-Phillips et al., 2014; Uller & Helanterä, 2019). But so far, none of these efforts incorporate the dialectic multilevel dynamics underlying biological organization and the goal-oriented behavior of the organism. They remain anchored in a flattened and shallow cybernetic view of “agency” as mere information-processing and feedback-driven goal-seeking.

Why is that so? The problem is as simple as it is fundamental: because of the
widespread mechanistic distrust concerning the notion of purposiveness, we do not
possess the conceptual and mathematical tools required to appropriately incorporate
true organismic agency into models of evolutionary dynamics. This is why we'd
rather pretend the phenomenon does not exist, rather than taking it seriously. In fact,
there are three related epistemological and methodological issues that need to be
considered here.

The first issue concerns the general nature of our scientific theories, which pre-
dominantly fall under what Lee Smolin (2013) has called the Newtonian paradigm,
or “physics in a box,” and which Rosen (1991) identifies with mechanistic reduc-
tionism. Theories that adhere to this paradigm are *object theories*: they describe and
explain the dynamics of a set of objects in a predefined space of possibilities (the
bounded “box” or *configuration space* of the system). There is *transcendence*: the
behavior of the objects is determined entirely by principles (forces, laws, etc.) that
are outside and beyond themselves. There is an *explanatory asymmetry*: these prin-
ciples determine the properties of the objects, but the objects do not explain the
principles. The traditional teleonomic account of “agency” outlined above corresponds to an object theory. It must avoid invoking actions generated from within the organism at all cost; otherwise, it would no longer comply with the rules that define an object theory. This is why it fundamentally fails to capture the nature of true agency in the first place.

An *agential or agent theory* of evolution is a fundamentally different kind of theory (Walsh, 2015). It does not conform to the Newtonian paradigm. Organisms become both the subject and the object of evolution (Levins & Lewontin, 1985). There is *immanence*: agents themselves cause changes in their own state and organization, through interactions with their perceived environments (see also Fontana & Buss 1994, 1996). There is *explanatory reciprocity*: agents both generate and respond to the conditions of their existence. There is no predefined “box” or configuration space. There is no list of prestatable possibilities. Agents generate their own rules internally, which is what enables their autonomy and, ultimately, their open-ended evolution (Kauffman, 2000, 2014; Ruiz-Mirazo et al., 2004; Longo et al., 2012). Some things in evolution happen *because organisms make them happen* (Walsh, 2015). This is the central conclusion we have to draw once we accept autonomous reproducers as the fundamental units of evolution.

The second issue concerns what we accept as a scientific explanation. Aristotle distinguished four ways of answering the question “why.” His four causes—material, formal, efficient, and final—are not really causes in the modern sense, but rather aitia, denoting something (or someone) responsible for a given phenomenon. For simplicity, I will use the less technical (but also less precise) notion of (be)causes here. (Be)causes correspond to different categories of determinants that complement each other to yield a full understanding of a phenomenon. This does not imply that Aristotle had a non-factive notion of causation, even though our modern scientific notion of “cause” is much more restricted: it roughly corresponds to efficient (be)causes only. In addition, modern science implicitly takes the material (be)cause for granted, although it no longer considers it a proper cause.

This is illustrated by current accounts of mechanistic explanation (e.g., Nicholson, 2012; Craver & Tabery, 2019). Evo-devo, for instance, relies on dynamic mechanisms as explanations, which are formulated in terms of structures “that perform a function in virtue of [their] component parts, component operations, and their organization,” and whose “orchestrated functioning” is “manifested in patterns of change over time in properties of its parts and operations” (Bechtel & Abrahamsen, 2010, p. 323). Developmental evolution is characterized by plausible transformation sequences for such dynamic mechanisms (DiFrisco & Jaeger, 2019). Such explanations (called *lineage explanations*; Calcott, 2009) rely entirely on material and efficient (be)causes, that is, on changes in the components of the mechanism and the operations between them.

Robert Rosen, in “Life Itself” (1991), formalizes Aristotelian (be)causation, explicitly distinguishing between material and efficient causes in his relational characterization of organizational closure. Formal (be)causes can also be integrated into his account. Very roughly speaking, formal (be)cause relates to the *kind of causal organization* that implements closure—for instance, the specification of particular