## 1. The Focal Question: What are Biological Individuals?



The biological world contains an incredibly diverse variety of
individuals. At the ground level of common sense, there are
alligators, ants, beetles, marmots, moles, mushrooms, ostriches,
roses, trees, and whales. At this ground level, biological individuals
are physically-bounded, relatively well-integrated, autonomous agents,
the ones listed as being amongst those that can be readily detected
with the senses. Extending the reach of common sense through
magnification allows flagella-propelled protists, tRNA molecules,
prions, and bacteria of many kinds to be seen or inferred. At larger
or collective scales, there are herds of zebras, sweeping and
astonishing coral reefs, algae blooms, biofilms made up of many
different species, and even fungus complexes several hectares in area
and with masses greater than that of an elephant.



What we will call the *Focal Question*--what are
biological individuals?--can be paraphrased in a number of
ways:


* What constitutes being a biological individual?
* What makes something a biological individual?
* What is the nature of the category *biological
individual*?
* What is the best explicative definition of the term
"biological individual"?



In the rapidly expanding literature on biological individuals (cf.
Hull 1992 with Guay & Pradeu 2016a, 2016b, and Lidgard &
Nyhart 2017b), such questions take *biological individual* as a
general category that may subsume several kinds of biological
individual (e.g., evolutionary, developmental, genetic, metabolic; cf.
Okasha forthcoming).



The psychologist Hermann Ebbinghaus's famous quip that
"psychology has a long past, but only a short history"
(1908: 1, *Die Psychologie hat eine lange Vergangenheit, doch nur
eine kurze Geschichte*) might well be adapted to remind us that
answers to the Focal Question have a long past, one stretching back to
at least the late eighteenth-century with the emergence of the life
sciences. In their collection of essays *Biological
Individuality*, the historians Scott Lidgard and Lynne Nyhart
reviewed the literature of the past two hundred years to compile a
list of twenty three criteria used to define or characterize
"*individual* or its contained subset
*organism*", noting that while



> 
> 
> the terms are not equivalent, they have been used interchangeably in
> many publications, precluding a simple separation here. (2017a:
> 18)
> 
> 
> 



Addressing the Focal Question thus calls for sensitivity to this
tendency in the long past.



As Derek Skillings says, the "traditional target of accounts of
biological individuality is the organism" (2016: 880), a
tradition reinforced in some influential contemporary discussions that
simply identify biological individuals with organisms (Queller &
Strassmann 2009, Clarke 2013; see
 section 8
 below). The present review follows Lidgard and Nyhart and others
(Dupre & O'Malley 2009; Nicholson 2014; Pradeu 2016a,
2016b) in taking *biological individual* to name a
superordinate category whose nature and relation to the category
*organism* is complex and worthy of exploration. Some
commentators (e.g., Okasha forthcoming) may be skeptical that there is
any such superordinate category, suspecting instead that several
distinct categories, including organism, are typically lumped together
in unclear and misleading ways as 'biological
individuals'. By contrast, here we view answers to the Focal
Question as appropriate attempts to explore and clarify various
relationships between distinct sorts of biological individuals.



Philosophers of biology typically understand biological individuals to
be distinct from other kinds of entities in the biosciences, such as
properties, processes, and events; however, the development of a
process-focused ontology by John Dupre and colleagues has
challenged this (Dupre 2012, Nicholson 2018, Nicholson &
Dupre 2018, Meincke 2019; Kearney and Rieppel 2023; see Morgan
2022 for a critique). Biological individuals have three-dimensional
spatial boundaries, endure for some period of time, are composed of
physical matter, bear properties, and participate in processes and
events. Biological *processes* (such as photosynthesis) and
biological *events* (such as speciation) lack such a suite of
features. Although philosophers have explored the question of what
makes anything an individual of *any* kind (e.g., Strawson
1959; van Inwagen 1990; Chauvier 2016; French 2014, 2016; Lowe 2016;
Wiggins 2016), such questions are bracketed off here in order to
concentrate on *biological* individuals (cf. Love &
Brigandt 2017).



To provide a sense of the complexities that an answer to the Focal
Question must address, consider, below, two examples that take us from
the ground level of common sense with which this review began to the
intimate interplay between empirical data gathered by biologists and
the conceptual clarification provided by philosophers that is a
hallmark of thinking about biological individuals. The philosopher
Jack Wilson (1999: 23-25) introduced the first of these examples
into discussions of biological individuals, while the physiologist
Scott Turner (2000: ch.2) introduced the second; both were then drawn
upon in an early, sustained discussion of the nature of organisms that
takes up some of the complexities raised by such examples--a
discussion that pre-dates the consolidation of the contemporary
literature around the term "biological individuals" (R.A.
Wilson 2005: ch.3-4).


## 2. Some Complexities: A Humungous Fungus and Coral Reefs



In the early 1990s, a team of biologists reported in the journal
*Nature* that they had found high levels of genetic identity in
samples of a species of fungus (*Armillaris bulbosa*), which
had taken over a large geographic region in Michigan's Upper
Peninsula. They used this data to make a case for viewing these
samples as constituting parts of one gigantic biological individual
with an estimated biomass of more than ten tons and an estimated age
exceeding 1500 years. They concluded that "members of the fungal
kingdom should now be recognized as among the oldest and largest
organisms on earth" (Smith, Bruhn, & Anderson 1992: 431).
Some scientists have questioned whether this final claim about the
organismal status of the humungous fungus is warranted, and some have
argued it is mistaken to say the gigantic fungus constitutes a single
biological individual. Since then, other scientists have recognized
even larger funguses as biological individuals (Schmitt & Tatum
2008).



How does one judge such claims and disputes? Minimally, more empirical
information about the example is needed. Is the fungus a continuous
biological structure? Does it have a determinate growth pattern? Can
it reproduce? But this empirical information alone doesn't
settle the matter. One must also draw on antecedent concepts of
organism and biological individual. The empirical information, in
turn, also allows one to fine-tune, amend, or challenge those
antecedent concepts, better so than would common sense reflection
alone. For example, if the humungous fungus is not an organism but
some other sort of biological individual, which empirical
considerations motivate this distinction?



Consider a more elaborately described example (Turner 2000: ch.2; see
also Skillings 2016: 877-879). Coral reefs are spectacular and
beautiful parts of the living world, despite rapidly becoming a thing
of the past due to the climate changes associated with global warming.
At least at the ground level of common sense, they are often thought
of as consisting of two chief components. The first are accretions of
calcite deposits. The second are the small animals, polyps, which
produce and grow on the deposits. (Coral polyps belong to the same
Linnaean class as sea anemones, and to the same Linnaean phylum as
jellyfish.) The polyps are indisputably biological individuals. But
further, conservation biologists also often describe the coral reefs
themselves, consisting of the polyps and the deposits considered
together, as *living things* that can grow and die.



The reefs are at least biological individuals, typically being thought
of as ecosystems; formal methods already exist for modeling them as
such (e.g., Huneman 2014). And taking seriously their life, growth and
death leads to the question of whether they too might be organisms: to
a first approximation, metabolically-circumscribed entities that are
relatively well-integrated and function as a whole. The dependence
relations between the reefs and the polyps does not rule this out,
since such dependence is common in organisms. Human beings depend on
internal bacteria that outnumber our own cells by about ten to one,
and yet they are organisms (Ackerman 2012). Similarly, the polyps that
reefs depend on are themselves dependent on single-celled algae,
commonly referred to as *zooxanthellae*, for the glucose that
provides the energy necessary for polyp respiration, which in turn
drives the process of calcification. Moreover, it is the zooxanthellae
that supply the pigments that give living corals their spectacular
colors; when zooxanthellae are absent or diminished, this signals a
problem for the long-term survival of a coral reef. Neither are the
zooxanthellae free of dependence. By infecting the polyps they gain a
feeding den crucial to their survival.



Further reflection along these lines may suggest that an integrated
causal network of dependence relations is a mark of being an organism
or biological individual; "causal integration, cohesion,
collaboration, or agency of parts" is the criterion on Lidgard
and Nyhart's (2017a) list of criteria that they found most often
cited in the literature they reviewed. If that were so, then the coral
reef may come to be viewed as a better exemplar of either than are the
polyps and zooxanthellae, as the reef enjoys a kind or degree of
complex, functional integrity that polyps and zooxanthellae arguably
lack when considered singly (see also Combes 2001). Alternatively,
perhaps the reef should be thought of as some other kind of biological
individual, such as an ecosystem, that contains several distinct
organisms, the polyps and the zooxanthellae, as proper parts.



Again, knowing what to say about the striking claim that the
polyp-zooxanthellae-calcite deposit complex is an organism turns in
part on the empirical facts, but on more than just those. Polyps,
zooxanthellae and whole reef complexes do not wear placards that state
which is an example of an organism, and whether all three should be
viewed as biological individuals of some kind or other (and which
kind). The interplay between our conceptions and empirical
complexities both allows those conceptions to be unpacked and informs
how they might be regimented to better capture nuances of the
biological world inaccessible to commonsense reflection alone.



This interplay has recently involved philosophers and biologists
attending more squarely to the *microbial* world
(O'Malley, Simpson, & Roger 2013; O'Malley 2014),
recognizing the various tight integrative and collaborative relations
between what prima facie are distinct biological individuals
(Dupre & O'Malley 2009, Ereshefsky & Pedroso
2015), and trying to make sense of the diversity one finds in the
processes of reproduction, metabolism, and development (Godfrey-Smith
2016b, Griesemer 2016). The next section provides an introductory
survey of this interplay via discussion of three subsidiary
questions.


## 3. Conceptual Space, Distinctions, and Beyond Organisms



Responses to the Focal Question have advanced discussion of at least
three closely related subsidiary questions:


1. *Beyond Organisms:* In what ways does the traditional focus
on organisms hinder us in thinking about biological individuals?
2. *Distinctions:* What are the most useful distinctions
between various kinds of biological individuals?
3. *Conceptual Space:* What is the most informative way to
articulate the conceptual space surrounding the concept of biological
individuals?



The first of these questions anchors our discussion in the short
history of thinking about biological individuals while acknowledging
the long past of the Focal Question.


### 3.1 Beyond Organisms: Microbialism, Eliminativism, and Holobionts



Scientists themselves--following common sense--have been
drawn first and foremost to organisms when beginning their theorizing
about biological individuals. For example, consider John Maynard Smith
and Eors Szathmary's *The Major Transitions of
Life* (1995), a wide-ranging book on the origins and evolution of
life that has stimulated much work on the evolution of individuality
(Buss 1987) and the Darwinian dynamics (Michod 1999) that governs
emerging kinds of biological entities (see Herron 2021 for recent
discussion and
 section 9
 below). The book opens with a simple point about the living world and
a characterization of the book's chief theme:



> 
> 
> Living organisms are highly complex, and are composed of parts that
> function to ensure the survival and reproduction of the whole. This
> book is about how and why this complexity has increased in the course
> of evolution. The increase has been neither universal nor inevitable.
> (Maynard Smith & Szathmary 1995: 3)
> 
> 
> 



Here organisms or biological individuals are viewed as exemplars of
complex living things composed of many parts, and their complexity is
taken to have increased--albeit unevenly and
contingently--through evolution by natural selection.



Likewise, an early collection of essays on evolutionary developmental
biology ("evo-devo") by Gerd Muller and Stuart Newman
(2003) focuses on how *organismal form* originated and on the
evolutionary, developmental, and ecological processes shaping it over
generations. The essays in that volume concentrate on the
relationships between basic body plans of organisms over phylogenetic
time, rather than the evolution of individuality as such, and do not
take up The Focal Question about biological individuals at all. But
like that of Maynard Smith and Szathmary, the project of
exploring these relationships is naturally expressed in terms of the
concept of an organism.



This should occasion no surprise, since, as
 section 1
 indicated, organisms have historically been regarded as prominent
examples of biological individuals and *organism* and
*biological individual* have often been used interchangeably.
But the short quotation drawn from Maynard Smith and Szathmary
also helps to explain why simply equating biological individuals with
organisms would be a mistake. The parts that compose organisms in all
their complexity are, often enough, themselves biological individuals.
Even if some of those parts are also organisms (e.g., the microbes
that live on and in macrobes), many are not. Precisely the same is
true of the populations and lineages that individual organisms in turn
constitute. These may occasionally be organisms (e.g., eusocial insect
colonies as "superorganisms"), but typically populations
and lineages are biological individuals that are *not*
organisms. If either this internal compositional complexity to
organisms or their formation into populations and lineages are
*necessary* features of organisms (which many philosophers and
biologists at least tend to think they are; see Lidgard & Nyhart
2017a: 18-23), then this would prove a stronger conclusion:
given that there are organisms, there *must be* some biological
individuals that are not organisms.



So one way in which the traditional focus on organisms can hinder us
in thinking about biological individuals is if, by equating the two,
there is too little attention focused on biological individuals that
are not organisms. But hindrance here could take a different form, as
some have argued. One might think that a focus on organisms,
particularly those identified at the ground level of common sense,
commits not just this kind of error of omission, but also proves
*positively misleading* about what biological individuals are.
Consider two positions that challenge the privileging of organisms in
discussions of The Focal Question:


* *Microbialism*: Understanding the living world requires
focusing on *collaborations* between macrobes and a variety of
microbes (e.g., viruses, prions, plasmids, symbionts), taking
seriously the idea that the biological individuals identified at the
ground level of common sense constitute a small part of that world
(Dupre & O'Malley 2007, 2009).
* *Eliminativism:* Far from being *paradigmatic*
biological individuals, organisms may be marginal or unusual special
cases of biological individuals and should be eliminated from our
ontology (Haber 2013, Okasha 2011).



Microbialism has been part and parcel of Dupre and
O'Malley's plaint against the *macrobist bias* in
the philosophy of biology and the positive case they have made for the
significance of the microbial world for reconceptualizing biological
individuals (O'Malley 2014, 2015; O'Malley, Simpson, &
Roger 2013; Dupre 2010). One direction that this has been taken
is Dupre's (2012) *promiscuous individualism* (for
the relationship between this view and processualism, see Morgan 2022:
616-617).



Promiscuous individualism is not simply the view that there are many
legitimate ways to classify the world into biological individuals. It
is also the corresponding ontological view that such legitimation is
provided by there being multiple biological individuals there to
classify. To illustrate this view, consider lichens, which are
typically regarded as what have been called *corporate
organisms* (R.A. Wilson 2005: 80-84), in this case made up
of a fungus and either a cyanobacterium or some other
photosynthesizing agent, such as green algae. Challenging the view
that there is just one biological individual (the lichen) or two (the
fungus and the cyanobacterium), an advocate of promiscuous
individualism can readily make the case that there are three
biological individuals (the lichen, the fungus, and the
cyanobacterium), pointing to the different purposes and goals one
might have in opting for any of the numerical counts here.



Given that it is a population of millions of cyanobacteria inhabiting
any given fungus that jointly compose a lichen, and that there are
multiple ways to draw the boundary between individual fungi of a given
species (Molter 2017; cf. Rayner 1997), note how rampant promiscuity
can run here. Dupre himself holds that populations, including
multispecies populations such as those found in microbial biofilms,
can themselves be both biological individuals and organisms (2012: 89,
175-176, 194, 203). He also says that "[w]hether a group
of microbes is a closely connected ecological community or an organism
may be a matter of biological judgment" (2012: 153). Promiscuous
individualism thus implies that there are many, many different numbers
of individuals present in this paradigm case. It seems even to suggest
that whether there are *any* biological individuals at all is
"a matter of biological judgment", rather than something
determined by the biological facts.



The emphasis on collaborations between living things in Microbialism
can undermine the focus on organisms without entering (at least
directly) into these deep metaphysical waters. That emphasis can also
motivate Eliminativism. One way it can do so is by embracing the idea
that it is not organisms but *holobionts* that are really
paradigmatic biological individuals. Introduced by Lynn Margulis
(1990) to refer to cases where there was intergenerational, inherited
symbiosis, such as that of the eukaryotic cell and of
*Buchnera*-aphid symbiosis), "holobiont" made its
way into discussions of coral reefs and a wider range of examples
early in the twenty-first century by loosening Margulis's
concept (see Suarez 2020 for discussion). In the literature on
biological individuals, a holobiont is, at least roughly, "the
multicellular eukaryote plus its colonies of symbionts" (Gilbert
& Tauber 2016: 842).



This concept has been attractive to some scientists (e.g.,
Zilber-Rosenberg & Rosenberg 2008; Bordenstein & Theis 2015;
Bosch & Miller 2016) but critiqued by others (Moran and Sloan 2015
and Douglas & Werren 2016) while also sparking ongoing
philosophical work (Theis et al. 2016, Booth 2014, Doolittle &
Booth 2017). For example, a special issue of the journal *Biology
& Philosophy* on biological individuality (volume 31, issue 6)
contains papers that focus on the significance of the holobiont for
immunology (Chiu & Eberl 2016; Gilbert & Tauber 2016) and for
the evolution of individuality and its major transitions (Queller
& Strassmann 2016, Skillings 2016; cf. Bourrat & Griffiths
2018). In an interesting recent paper, Lloyd and Wade (2019) argue
that the critics of the holobiont concept typically rely on
gene-centric and conflict-focused research on multispecies
interactions, suggesting that one can pursue a different set of
research questions within *community* genetics that pave the
way for an articulation of the co-evolutionary roles for holobionts.
As part of their case, they introduce the distinction between
*euholobionts* - "genuinely genetically integrated,
coadapted communities of obligately mutualistic organisms" which
are evolutionary and physiological individuals - and
*demiholobionts*, such as the squid-vibrio complex, that are
forms of mutualism with asymmetrical fitness and so adaptational
relationships (Lloyd and Wade 2019: 152). They argue that by viewing
these cases as "lying on a continuum of fitness interactions and
partner fidelities" (p.166), together with their advertised
multilevel research strategy, we arrive at a model of mutualism and
holobionts that better matches reality.



Like the concept of an organism that it putatively supplements or
supplants, that of the holobiont encompasses a huge diversity of
entities. These include macro-organisms and the microbial
endosymbionts living within their cells (such as *Chlamydia*
and other obligate parasites); those that live beyond their cells but
in close symbiotic relations (such as cyanobacteria); and the
multispecies microbiota that inhabit the human intestine (Booth 2014).
There are challenges in how to delineate individual holobionts that,
as we will see in the next section, may be met by embracing particular
physiological criteria for individuation (Pradeu 2012). Yet those
challenges have suggested to some that the take-away lesson from
reflection on holobionts is that emphasis should be placed not on
another kind of individual, a holobiont, but instead on the process of
*holobiosis* (Doolittle & Booth 2017). Others have recently
defended a cluster of contrasting views (Suarez and Stencel
2020; Suarez 2020). One is that biological individuals can be
thought of as ecosystems, an idea that draws upon a notion of
"weak individuals" defined in terms of levels of
interaction (Huneman 2021); another is that holobionts are both
biological individuals *and* ecological communities or
ecosystems, which draws on the proposal that biological individuality
needs to be given a *part-dependent* characterization that
recognizes the perspective-dependence of questions about the ontology
of holobionts (Suarez and Stencel 2020). And finally there is
the idea that the hologenome should be conceptualized in terms of
stability of traits, rather than fitness alignment (Suarez
2020). These ideas enrich discussions of the concept of holobionts,
and whether that concept will live up to its still-early promise of
revolutionizing thinking about biological individuals is likely to
remain a topic of lively discussion in the immediate future.


### 3.2 Distinctions: The Evolutionary and the Physiological



Consider now our second subsidiary question, Distinctions: what are
the most useful distinctions between the various kinds of biological
individuals that exist? The most commonly recognized distinction here
is that between *evolutionary* and *physiological* (or
*metabolic*) individuals (Pradeu 2016a, 2016b), with a
corresponding discussion of the roles of evolution and metabolism in
thinking about biological individuals (see Clarke 2020 and
O'Malley 2020 for opposing views).



Prominent in contemporary thinking about evolutionary individuals is
the work of Peter Godfrey-Smith on what he calls *Darwinian
individuals*. On the view of evolution and natural selection he
defends in *Darwinian Populations and Natural Selection*
(2009), what evolves are "Darwinian populations",
collections of things in which at least three conditions hold: there
is *variation* in the traits had by things in the collection,
those traits are *heritable* within the collection, and some
variants of the traits confer reproductive advantage on the things
that bear them. In such a Darwinian population, the members are
Darwinian individuals, which are both bearers and active reproducers
of heritable traits (see Godfrey-Smith 2013: 19-20).



Godfrey-Smith's approach to evolutionary individuals is intended
to contrast with the earlier replicator-based views developed by
Richard Dawkins and others. Replicator views have been central to
discussions of the levels and units of selection (Godfrey-Smith 2015;
Sober & Wilson 1994, 1998; Okasha 2006), and derivatively so to
views of biological individuals. Here genes are paradigmatic
replicators, being housed in *interactors*, such as organisms,
and it is the survival of these replicators that matters in evolution.
The replicator framework emphasizes the importance for natural
selection of high-fidelity copying across generations. By contrast,
what matters for natural selection in Godfrey-Smith's view is
the establishment of parent-offspring lineages that feature
heritability, as well as the variety of forms that reproduction can
take in the establishment and stabilization of those lineages.



This shift from replication to the process of reproduction in accounts
of biological individuals has a longer history, particularly amongst
those sensitive to the relationships between evolution and
development. For example, James Griesemer (2000) has argued that
biological reproduction involves fission and fusion requiring what he
calls *progeneration*, a process that creates new entities
through *material overlap*, and that that process is a crucial
feature of how living agents evolve.
 Section 6
 takes up this issue in more detail in discussing reproduction, life
cycles, and lineages.



Whichever way evolutionary individuals are conceptualized, they do not
exhaust the realm of biological individuals any more than do
organisms. The general point here is that although evolution is
foundational when thinking about interactors and Darwinian
individuals, it does not play this role for all kinds of biological
individual, as Godfrey-Smith himself recognizes. Indeed, Godfrey-Smith
(2013) strikingly (and controversially) proposes that even some
*organisms*, understood from a metabolic point of view, are not
Darwinian individuals at all. These are a subset of corporate
organisms, multi-species organisms formed through symbiotic
relationships between members of different species. Here Godfrey-Smith
posits the Hawaiian bobtail squid (*Euprymna scolopes)* and the
Vibrio bacteria they contain as an example (see also Nyholm &
McFall-Ngai 2004; Bouchard 2010). Since the squid-Vibrio corporate
organism does not itself form the right kinds of parent-offspring
lineages it is not a Darwinian individual, differing in this respect
with other often-discussed corporate organisms, such as
aphid-*Buchnera* complexes (Andersson 2000):



![a diagram: link to extended description below](fig1.svg)

Figure 1: Godfrey-Smith's
Different Biological Individuals.
  

(Copied from Figure 4 of Godfrey-Smith 2013.)
  

[An
 extended description of figure 1
 is in the supplement.]




Whatever one says about the intricacies of such examples, in addition
to individuals delineated by evolutionary criteria there are also what
Thomas Pradeu calls *physiological* individuals. These are
biological individuals individuated by appeal to criteria such as
having a metabolism and being governed by internal control mechanisms
of various kinds. For Pradeu, each physiological individual is
"a functionally integrated and cohesive metabolic whole, made of
interdependent and interconnected parts" (Pradeu 2016b: 807; see
also Godfrey-Smith 2009: 71).



As Pradeu notes (2016b: 799-802), there is a long tradition in
the physiological sciences of addressing the Focal Question by asking
what it is that makes for *unity of functioning* in biological
individuals:



> 
> 
> to ask how distinct and heterogeneous components interact and
> constitute a cohesive whole, functioning collectively as a regulated
> unit that persists through time. (2016b: 800)
> 
> 
> 



Although there is typically a nod paid to physiological individuals in
early influential discussions of biological individuals in the short
history of the topic (e.g., Sober 1991, Hull 1992, Dawkins 1989:
ch.13), the bulk of this literature has focused until very recently on
evolutionary individuals. Pradeu's reminder of the long past of
the Focal Question, and the prominence of physiological individuals in
it, is a welcome redress to the resulting skew of attention.



In addition to this general point, Pradeu has also defended the view
that an organism is a particular kind of physiological individual,
being



> 
> 
> a functionally integrated whole composed of heterogeneous components
> that are locally interconnected by strong biochemical interactions and
> controlled by constant systemic immune interactions of a constant
> average intensity. (Pradeu 2012: 244)
> 
> 
> 



Here Pradeu builds on a particular view of immunology developed in his
*The Limits of the Self* that moves beyond the theory
associated with Frank Burnet, the self-nonself theory. In its place,
Pradeu offers a general account of immunogenicity that applies across
a wide range of phlya, ignoring the exogenous or endogenous origin of
antigens in favor of a criterion that emphasizes immune-tolerance and
acceptance.



Pradeu takes the boundary established and maintained by the immune
system as *the* boundary of the organism. On Pradeu's
view, organisms are inherently heterogeneous, given the collaborative
nature of the microbial and macrobial worlds articulated in
Microbialism. To put it slightly differently, the true organisms
delineated by Pradeu's immunity criterion are holobionts
constituted by a macrobial organism and all and only those microbes at
least tolerated by its immune system. This criterion provides a way to
individuate organisms *as holobionts*, and the resulting view
constitutes one way to constructively respond to the challenges of
Microbialism and Eliminativism. Whether holobionts are best thought of
as organisms or evolutionary individuals at all (Skillings 2016), or
whether Pradeu's view in particular can resolve the putative
"tension in seeing symbionts as both organisms themselves and
also parts of larger organisms" (Godfrey-Smith 2016c: 782),
remain live issues.



So minimally there are evolutionary individuals and there are
physiological individuals, and organisms are typically thought of as
exemplars of (but not strictly identical to) both.
Godfrey-Smith's articulation of evolutionary individuals as
Darwinian individuals has structured much recent and ongoing
discussion, and Pradeu's emphasis on physiological individuals
and his appeal to immunology as a source for ideas about organisms and
biological individuals more generally has garnered recent attention.
These responses to Distinctions also facilitate rich responses to our
remaining subsidiary question, Conceptual Space: What is the most
informative way to articulate the conceptual space surrounding the
concept of biological individuals?


### 3.3 Conceptual Space and Pluralism



Recognizing the distinction between evolutionary and physiological
individuals commits one to a minimal form of pluralism about what
populates that conceptual space. But there are also more radical forms
that pluralism about biological individuals has taken in the
literature.
 Section 3.1
 indicated that the emphasis on the collaborative nature of the
interactions between biological individuals in Microbialism motivates
Dupre's promiscuous individualism, a position that
invites a very liberal form of pluralism that makes biological
individuality seem, at least partly, a function of our epistemic,
practical, and other proclivities, rather than of just the structure
of the biological world itself.



Here Dupre can be understood as following the general intuition
that if some kind K seems too diverse to characterize, it should be
split into diverse sub-kinds, with each of those characterized. In
early philosophical work (J. Wilson 1999, 2000) also drew on this
intuition, where *K* = biological individual, moving beyond
that broad concept to characterize *genetic*,
*functional*, *developmental, and evolutionary*
individuals, a position more recently dubbed "kind
pluralism" and defended by appeal to explanatory power and
projectability (DiFrisco 2019). Famously, the botanist John Harper
invoked pluralism, where *K* = plant, by introducing the more
particular kinds *ramet* and *genet* to replace talk of
individuals. A ramet is what might be readily identified as an
individual plant; a genet is a collection of ramets that propagate, as
is often the case, through the clonal growth of a particular ramet
(Harper 1977). How many plants there are, in many cases, depends on
whether ramets or genets are meant. For example, while each of the
trees in an aspen grove that forms clonally is a ramet, collectively
they typically form a single genet. A pluralist might prefer a
description cast in terms of ramets and genets over any attempt to
answer the question of how many plants or individuals, per se, there
are in this case.



Pluralism about biological individuals has also been motivated by the
general idea that particular epistemic *practices*, rather than
or additional to high-level biological theory, should drive
one's ontological commitments (Kovaka 2015, Chen 2016, Love
2018; for interplay of theory and experimental practice in this
connection, see Fagan 2016). Just as practices of the individuation of
species might vary with the differential practices of (say)
ciliatologists and ornithologists, so too might the very individuative
criteria for being a (relevant) biological individual differ according
to the varying epistemic practices across the biological sciences. How
radical the resulting form of pluralism is will depend in part on how
fine-grained one's view of the relevant practices is and the
expanse of the range of those practices. For example, are all of the
practices in developmental biology clustered, or are distinctions to
be drawn between those relevant to the experimental investigation of
growth and those relevant to homology? Are we to include among
biological individuals, as Roberta Millstein (2018) does when
discussing the *land community*, very large systems studied in
ecology, which are made up of diverse organisms, other living things,
and non-living things such as soil (see also Eliot 2011)? Answers to
such questions will influence whether the plausibility of what Alan
Love calls *strong individuality pluralism*, the view that
"for a given situation, individuality can be modeled correctly
in more than one way" (2018: 187). Kaiser and Trappes (2021)
have recently argued from this kind of "practice turn"
perspective, to motivate questions about uniqueness and temporality
that further broaden the problem agenda of appeals to biological
individuality.


## 4. Structuring Conceptual Space Beyond Pluralism



So far some of the pluralistic directions that discussions of
Distinctions and Conceptual Space have taken in the literature have
been outlined, leading to a conceptual landscape populated by a
plethora of adjectivally-modified kinds of individuals: evolutionary,
physiological, developmental, functional, genetic, etc.. Although
simply equating biological individuals with organisms would be a
mistake, some biologists (e.g., Pepper & Herron 2008; cf. Jagers
op Akkerhuis 2010) have explored the idea that a more nuanced appeal
to organisms can provide some informative structure to this landscape.
Noting that



> 
> 
> amongst biologists, the question of what constitutes an individual is
> usually identical with the question of what constitutes an individual
> organism. (Pepper & Herron 2008: 622)
> 
> 
> 



Pepper and Herron pose the question of whether any given biological
individual is an organism, a part of an organism, or a group of
organisms. Consider then a framework that holds that biological
individuals include exactly:


* *organisms* (such as wasps and whales)
* some *parts* of organisms (such as placentas and plasmids)
and
* some *groups* of organisms (such as zebra lineages and
colonies of bacteria).



Figure 2 depicts this framework visually.




![a diagram: link to extended description below](fig2.svg)



Figure 2: A Framework for Structuring
Conceptual Space. [An
 extended description of figure 2
 is in the supplement.]




These three sub-categories of biological individual need not be
mutually exclusive when considering any particular individual. For
example, a given bacterium, such as an individual *Buchnera*
bacterium, may both be an organism itself and be part of a corporate
organism, such as the human whose gut it is integral to (Andersson
2000). Likewise, some groups, such as the colonies of eusocial insects
sometimes called "superorganisms", or highly integrated
multispecies communities, may be *true* organisms. This kind of
view may also capture what truth lies behind proposals to extend the
term *organism* both to some parts and some groups of organisms
(e.g., Queller 1997; Okasha 2011): parts of organisms (such as
symbiotic gut bacteria), as well as groups of organisms (such as
colonies of ants or bees), are really organisms as well.



Directly relevant to the Focal Question is that this framework invites
a more systematic treatment of the relationship between each of the
primary kinds of biological individuals--evolutionary and
physiological individuals--and other key features typically
appealed to in characterizing them, including growth, reproduction,
lineages, cohesion, metabolism, and control.
 Sections 6 and 7
 will elaborate the initial visual summary offered by
 Figure 2
 in ways that further fill out the conceptual space occupied by
biological individuals. But first
 Section 5
 attends to the right-hand side of Figure 2 by providing a brief
overview of the idea of groups as biological individuals.


## 5. Groups as Evolutionary Individuals: Superorganisms, Trait Groups, Species, Clades



As the discussion of evolutionary individuals in
 section 3
 indicated, responses to the question of whether natural selection has
created groups that are themselves biological individuals has been
important to the history of the Focal Question. Groups here might
range from temporary dyads of individuals, such as two crickets
sharing a ride on a leaf (Sober & Wilson 1998), through to
higher-level taxonomic groups whose members are largely separated in
space and time, such as planktotrophic mollusks (Jablonski 1986,
1987). One fundamental distinction that emerged with the revival of
group selection, largely through the work of David Sloan Wilson (1975,
1977, 1980, 1983) and Elliott Sober (D.S. Wilson & Sober 1989;
Sober & Wilson 1994, 1998), is between two sorts of groups:
superorganisms and trait groups.



The term *superorganism* was introduced by the entomologist
William Morton Wheeler in his 1920 essay "Termitodoxa, or
Biology and Society", although he had talked of ant colonies as
organisms as early as his 1911 essay "The Ant-Colony as an
Organism". Paradigm examples of superorganisms are colonies of
social insects, e.g., *Hymenoptera* such as ants, wasps, and
bees, together with the taxonomically distinct termites, which are
typically viewed as a special kind of biological individual arising
from the specific genetics and reproductive division of labor in those
colonies.



*Trait group* was introduced by D.S. Wilson, by contrast,
specifically to name a type of group that he thought was pervasive in
nature, one that could be a unit of selection just as individual
organisms were. The intuitive idea behind a trait group is that
populations can feature evolutionarily relevant structure wherein
organisms belonging to one part of the population are subject to
causal influences on fitness that do not extend to the population as a
whole. A population of such *structured demes* would then
function as a metapopulation, with natural selection operating between
the trait groups that make up that metapopulation. The individuals in
a trait group could thus be seen as evolutionary individuals, being
the agents for evolutionary change over time.



A common two-pronged response to this distinction (e.g., Sterelny
1996) has been to concede the reality of superorganismic group
selection (but underscore its rarity) and argue that instances of
trait group selection are better described as cases of genic or
individual selection *relativized to a particular environment,
where part of that environment is composed of other individual
organisms* (see also Okasha 2006, 2018). In effect, this is to
allow for superorganisms as a special kind of biological individual,
but to reject a more expansive conception of evolutionary individual
at the group level. On this view, eusocial insects may be evolutionary
(and even physiological) individuals, but trait groups are
neither.



A distinct pathway taken by appeals to group selection has focused on
species and clade selection, particularly in work by paleobiologists
and paleontologists (Grantham 1995; see also Doolittle 2017). Clades
are monophyletic groups of organisms or species, groups defined by an
ancestor and all and only its descendants. Steven Stanley and Stephen
Jay Gould have been two of the most prominent defenders of the idea
that there are large-scale patterns of evolutionary change that are
due to species or clade selection, and both have done so in part by
explicitly developing an extended analogy between individual organisms
and species (e.g., Stanley 1979: 189; Gould 2002: 703-744).
Amongst putative examples of clade selection are the evolution of
planktotrophic mollusks in the late Cretaceous, being selected for
greater geographic dispersal and so longevity (Jablonski 1986, 1987),
the evolution of larger body size in males, selected via population
density and geographic range (Brown & Maurer 1987, 1989), and the
evolution of flowering plants, selected via vector-mediated pollen
dispersal (Stanley 1981: 90-91).



There is a similar caution in discussions of species or clades as
evolutionary or physiological individuals as there is with trait
groups. One of the chief threads to the debate over species and clade
selection also parallels that over trait group selection: are species
or clades themselves really the agents of selection, the units that
are being selected, or do they simply tag along for the ride, with
selection operating exclusively on organisms and genes? Elisabeth Vrba
(1984, 1989; Vrba & Gould 1986), for example, has distinguished
between species *sorting* and species *selection*,
arguing that while a sorting of species may be the product of
evolution by natural selection (see Barker & Wilson 2010), this
outcome is typically brought about not by species selection but by
individual selection. On this view, species or clades may be a
*product* of natural selection, and so in some sense
evolutionary individuals, but they are not themselves agents in the
*process* of natural selection. Rather, they are epiphenomena
of that process, lacking the kind of agency that full-blown
evolutionary individuals have.



The much-discussed claim that species are individuals (Ghiselin 1974;
Hull 1976, 1978), which developed as part of a response to the
perceived failure of essentialism about species (Sober 1980; Okasha
2002; Barker 2013), might be viewed in this same light. The
species-as-individuals thesis reflects the way in which species were
treated within systematics and evolutionary biology not as kinds but
instead as spatiotemporally restricted *lineages*, with
individual organisms as their physical parts (Ereshefsky 1992a; R.A.
Wilson 1999b). The species-as-individuals thesis was originally
presented and seen as making a radical break with previous views of
the ontological status of species, as it implied that biologists and
philosophers alike had misidentified the basic ontological category to
which species belonged. But over time, both as its proponents have
clarified what the thesis implied (e.g., gravitating to talk of
historical entities rather than individuals) and as more sophisticated
options for defenders of the view that species are kinds were
developed (e.g., Boyd 1999, Griffiths 1999, R.A. Wilson 1999a), this
radical edge to the thesis has diminished. A now widely accepted
insight clarified in the process is that in the case of many species,
organisms belong to them (as parts or members) by virtue of their
interactions and their extrinsic rather than intrinsic properties
(Barker 2010; cf. Devitt 2008). Whether this combats (or instead
exemplifies) what the historian James Elwick has recently called
"resilient essentialisms" (Elwick 2017; cf. Hull 1965)
remains contentious.



Finally here, Mariscal and Doolittle (2020) have recently suggested
that all of life, i.e., the Last Universal Common Ancestor and all of
its descendants, is a biological individual in the sense in which
Ghiselin and Hull argued that species were (see Reydon 2021 for some
scepticism about both claims). They take life to be "a
monophyletic clade that originated with a last universal common
ancestor, and includes all of its descendants" (2020: abstract).
Complementing this is their adaption of Ereshefsky's (1992b)
eliminative pluralism about living things as a kind, arguing for
eliminativism about living things as a natural kind (cf. Barker
2019).


## 6. From Physiological to Evolutionary Individuals: Life, Reproduction, and Agency



Section 3
 indicated that John Maynard Smith and Eors Szathmary drew
explicitly on the concept of *living organisms* in
characterizing the chief theme of their influential work on the major
transitions in the history of life. However, reflection on organisms
as living agents generally has been backgrounded in work concentrating
on evolutionary individuals. This is perhaps for the obvious reason
that many evolutionary individuals--including genes, lineages,
and clades--are not themselves living things. Yet physiological
individuals are paradigms of living agents and a more complete sense
of the conceptual space that biological individuals occupy calls for
some discussion of life, including the roles that an appeal to life
cycles and agency play in characterizing physiological
individuals.


### 6.1 Physiological Individuals as Living Agents



One approach here would be to attempt to define life, or living agent,
or to provide necessary and sufficient conditions for these (Maynard
Smith & Szathmary 1995: 17-18; Cleland 2012). A
recurrent property referenced in such definitions is that of
*having a metabolism*, which involves both an *anabolic*
dimension in the breakdown of chemical molecules to produce energy and
a *catabolic* dimension in intracellular synthesis of those
compounds (Pradeu 2016b: 801). But there are other properties that
living agents have, some presupposed by that of having a metabolism,
others existing independently. These include what might be thought of
as *structural* properties--such as having heterogeneous
and specialized parts, including a variety of internal mechanisms, and
containing diverse organic molecules, including nucleic acids and
proteins--as well as *functional* or
*dispositional* properties--such as the capacity for
growth or development, reproduction, and self-repair.



Cells, organs, and perhaps bodily systems, such as the respiratory
system or the digestive system, are physiological individuals that
have most if not all of these properties that characterize living
agents. As physiological individuals, organisms also share these
properties, but are distinguished by one or more further
characteristics, such as possessing an immune system (as Pradeu
emphasizes) or having a *life cycle*, one that is typically
demarcated through reproduction, which is the focus of
 section 6.2
 below.



Conceiving of physiological individuals as living agents, and
supposing that all organisms are living agents but that there may be
both parts and groups of organisms that are not, allows us to extend
the visual summary introduced in
 Figure 2.
 Figure 3 depicts organisms as living agents but also contains
regions for organs such as hearts and other constituent parts of
organisms as living agents, as well as groups that may be living
agents but not organisms (e.g., perhaps a coral reef).




![a diagram: link to extended description below](fig3.svg)



Figure 3: Living Things as Biological
Individuals. [An
 extended description of figure 3
 is in the supplement.]



### 6.2 Reproduction, Life Cycles, and Lineages



One feature of organismic, physiological individuals that partially
distinguishes them amongst living things is that they have *life
cycles* that allow them to form reproductive lineages of a certain
kind. The importance of life cycles for evolutionary change has been
recognized both in the replicator-based view of evolutionary
individuals (Dawkins 1989: ch.13) and in reproductively-centered
accounts of Darwinian individuals (Godfrey-Smith 2009, 2016a). And the
close relationship between being an individual organism and having a
life cycle is widely accepted, being manifested in an extreme form by
Griffiths and Gray's (1994) identification of biological
individuals with their life cycles within developmental systems
theory.



Put most generally, a life cycle is an intergenerationally replicable
series of events or stages through which a living thing passes (Bonner
1993). These events or stages constitute a *cycle* in that they
begin and end with the same event, such as the formation of a
fertilized egg in sexually reproducing individuals, or the creation of
a fissioned cell in clonally reproducing individuals.
*Development* is the global name for the processes that
causally mediate between these events or stages in a life cycle, with
*reproduction* marking the transition to the creation of a new
individual, the offspring of one or more parents. Although Richard
Dawkins's suspicion



> 
> 
> that the essential, defining feature of an individual organism
> *is* that it is a unit that begins and ends with a
> single-celled bottleneck (1989: 264)
> 
> 
> 



has proven hyperbolic, the more cautious view that the "two
phenomena, bottlenecked life cycles and discrete organisms, go hand in
hand" (1989: 264) expresses a view that has been widely
endorsed.



It has long been recognized that some biological individuals, such as
flukes, have life cycles that take them literally through one or more
hosts, and that many insects undergo significant metamorphic changes
in bodily form through their life cycle. But such sophistications to
life cycles are only the tip of the iceberg here. While the stages
themselves often form standard sequences within particular species,
there can be tremendous variation across species and phyla in what a
given individual's life cycle consists in, as others have
emphasized (Buss 1987), including in recent discussions of complex
life cycles (Godfrey-Smith 2016b, 2016d; Griesemer 2016; Herron 2016;
O'Malley 2016; cf. Gerber 2018).



In the life cycles that are most immediately familiar, processes that
mark the end of one life cycle and the beginning of another of the
same kind of individual--processes such as material
bottlenecking, sexual reproduction, and
multiplication--temporally coalesce. In the life cycles of other
individuals, such as ferns and scyphozoan jellyfish, these processes
are sometimes dispersed, function differently, or are absent
(Godfrey-Smith 2016a, 2016b). Such cases call for a corresponding
sophistication of accounts of reproduction and, as James Griesemer
says, these complexities in life cycles may



> 
> 
> complicate relations between processes of development and reproduction
> to such an extent that even the meaning of 'organism'
> begins to break down. (Griesemer 2016: 804)
> 
> 
> 



Maureen O'Malley (2016) has drawn attention to other cases that
pose more radical challenges to the standard ways of thinking of life
cycles themselves. An example is the asexually reproducing
multicellular protist *Volvox carteri* (green algae), whose
"sexual phase of the life cycle is nonreproductive because there
is no multiplication" (O'Malley 2016: 838). This kind of
sexual recombination occurring between members of asexually
reproducing generations takes on a striking form in ciliates, such as
*Tetrahymena*, whose micronucleus provides germ-line isolation.
Whether O'Malley's concept of *multigenerational
individuals* can be squared with extensions of standard views of
reproduction and life cycles remains subject to further
exploration.



Although there is a relationship between having a life cycle and
reproducing, simply reproducing is *not* the distinctive
feature here, as a number of authors have recognized (Griesemer 2014,
Godfrey-Smith 2013, O'Malley 2016, R.A. Wilson 2005: 59-62).
Organisms and perhaps other biological individuals typically reproduce
through material overlap (Griesemer 2000), or via bottlenecks
requiring material minimalization and mark the transition between
generations (Godfrey-Smith 2009: ch.5). These kinds of constraints on
biological reproduction go hand in hand with growth and development as
part of the intergenerational life cycle of biological individuals.
Intergenerational life cycles, in turn, make it possible for
biological individuals to form reproductive *lineages* of
living things. Reproduction structures not only such lineages, but
also the lineages of *non-living* biological individuals,
whether they be smaller than the individuals they are parts of (such
as genes), or groups (such as populations) that feature centrally in
discussions of evolutionary individuals.



Despite the fact that reproduction has sometimes been conceptualized
as part of an individual's life cycle, the general role of
reproduction in intergenerational life cycles requires more careful
articulation. For there are many species in which only a small
minority of individuals actually get to reproduce, with reproductive
skew being a widespread feature. All of these biological individuals,
however much or little they reproduce, still possess a life cycle.
Note that even the *capacity* to reproduce is not a universal
feature of life cycles. This is not only because the capacity itself
may not be replicated, but also because there are biological
individuals *designed* by natural selection to be
non-reproductive, with sterile castes in eusocial insects being
perhaps the best-known example.



In such species, a few individuals (e.g., queens) do most if not all
of the direct reproductive labor, and many others are rendered
reproductively sterile throughout all or much of their life (e.g.,
worker castes). So there are reasons to include neither reproduction
nor the capacity to reproduce as part of the generic life cycle of
biological individuals. What is true, however, is that all organisms
have life cycles that allow them to form reproductive lineages. They
do so sometimes through the reproductive activity of members of the
lineage to which they belong, even if not every member of that lineage
reproduces or even can reproduce. Like viruses, individual members of
sterile castes of insects rely on the reproductive machinery *of
others* in order for descendant members of those castes to be
reproduced in future generations.



This is an example of what Godfrey-Smith (2009: ch.5) calls
*scaffolded reproducers*, "entities which get reproduced
as part of the reproduction of some larger unit" and whose
"reproduction is dependent on an elaborate scaffolding of some
kind that is external to them" (2009: 88). These contrast with
what he calls *simple reproducers*, a paradigm of which is a
bacterial cell, being "the lowest-level entities that can
reproduce largely 'under their own steam'" (2009:
88). Both simple and scaffolded reproducers can be parts of what
Godfrey-Smith calls *collective reproducers*, which are



> 
> 
> reproducing entities with parts that themselves have the capacity to
> reproduce ... largely through their own [the parts']
> resources rather than through the coordinated activity of the whole.
> (2009: 87)
> 
> 
> 



Both groups and multicellular organisms exemplify collective
reproduction, and Godfrey-Smith's discussion of the continuous
dimensional space that characterizes collective reproducers, and
Darwinian individuals more generally, has been influential, and is
summarily depicted in
 Figure 4
 below.



![a diagram: link to extended description below](fig4.svg)

Figure 4: Godfrey-Smith's
Dimensional Space for Collective Reproduction. (From Figure 5.1 in
Godfrey-Smith 2009.) [An
 extended description of figure 4
 is in the supplement.]



### 6.3 Autonomous Agency



That all physiological individuals have some kind of autonomous agency
is widely recognized and is the intuitive basis for the early
systematic formal theorization of biological autonomy undertaken on
*autopoetic systems* by Maturana and Varela (1980) and more
recently by Moreno and Mossio (2015). Although such views are
typically cast in terms of biological *systems* rather than
individuals, they view the kind of unity of purpose that characterizes
both physiological and evolutionary individuals as arising from more
general principles governing biological organization, and that
organization is important to biological individuality.



Physiological individuals such as organisms, however, are not simply
biological systems but living agents that *have a life of their
own*. They are able to exercise some sort of special degree of
control over their whole selves and subsequently are relatively free
with respect to other things, including other agents and environments.
This might be expressed in terms of both the individual's
relative autonomy from its external environment and its control over
the activity of its components or internal parts (R.A. Wilson 2005:
62-65). Organisms in particular have a distinctive kind of
agency because of the integrity with which such autonomy and control
imbues them. For Moreno and Mossio (2015: ch.6), developmental
functions and constraints play an especially important role in
establishing this kind of *organismic* autonomy.



The idea of biological individuals having a *locus of control*
in ways that neither non-living things nor obligately-dependent living
things (such as organs) have is key here. Pradeu's (2012) view
of immunological control as marking the boundary of the biological
individual is one way of specifying this idea, as is
Godfrey-Smith's continuous dimension of *integration*,
which summarizes features such as



> 
> 
> the extent of division of labor, the mutual dependence (loss of
> autonomy) of parts, and the maintenance of a boundary between a
> collective and what is outside of it. (2009: 93)
> 
> 
> 



The high level of functional integration or cohesion possessed by
*parts* of individuals imbues the *whole* organisms they
constitute with both capacities to act and largely shared fates to
which those capacities contribute (Collier 2004; Okasha 2011: 59;
Sober 1991: 291). In some sense, this is why any organism has a life
*to lead*, rather than simply being alive.



This appeal to autonomous agency has a long history in thinking about
what is distinctive about the biological world, particularly when the
focus has been on physiological individuals. For example, in the first
volume of his *Principles of Biology* (1866), Herbert Spencer
argued at length that the capacity of a biological individual to



> 
> 
> continuously adjust its *internal* relations to
> *external* relations, so as to maintain the equilibrium of its
> functions (1866: 207, our emphasis)
> 
> 
> 



is one of the key features that sets it apart as biological. Likewise
when Julian Huxley later proposed three conditions of what he called
*minimal organismality*, one of these concerned integration of
*internal* functions and a second concerned independence from
*external* forces (Huxley 1912: 28). Like Spencer, Huxley saw
these internal and external matters as causally linked within
individuals, and as together achieving equilibria in distinctive ways.
Huxley thought this was due especially to the parts of biological
individuals being both more heterogeneous and functionally integrated
with each other than is seen in the non-biological context external to
such individuals. Two contemporary cousins of this idea in the
literature focused on evolutionary individuals will be the focus of
 section 8
 below.



Denis Walsh has articulated a general organism-centred perspective on
evolution and the biological sciences that emphasizes teleological
agency (Walsh 2015). Walsh dubs this perspective as
"methodological vitalism" (Walsh 2018) and the
"agential perspective" (Walsh and Rupik 2023) and has
argued that it constitutes an alternative to the view of evolution
associated with the Modern Synthesis (see Buskell and Currie 2017 for
discussion). Walsh and colleagues give important roles to autonomy in
the conception of organismal agency, with Fulda recently arguing that
the notion of autonomous agency can be used to provide a general
criterion for biological individuality (Fulda 2023), one in which
paradigm cases of biological individuality, like multicellular
organisms, display strong autonomous agency, while what he calls
"problematic cases" (Fulda 2023, section 4.4) display weak
agential dependence.



An interesting, relatively recent question is why the use of
*cognitive metaphors* in describing biological agency is
widespread, if not ubiquitous (R.A. Wilson 2005: ch.4). Explorations
of this question have involved some interesting integrative thinking
across the philosophy of biology, cognitive science, and the
philosophy of economics (Godfrey-Smith 2009: 142-145; Dennett
2011; Nicholson 2018; Okasha 2018). Four responses to this question
give some idea of the diverse literatures relevant to answering
it.



One early hypothesis (R.A. Wilson: 2005: 74-79) is that the
function of these metaphors is to *crystallize agency*,
bringing about a focus on the causal agency of biological individuals
by assimilating them to our paradigm of agents, human agents. This
crystallization thesis forms part of Wilson's tripartite view of
organismic living agents (R.A. Wilson 2005: ch.3) that draws on the
homeostatic property cluster view of natural kinds (Boyd 1999, R.A.
Wilson, Barker, & Brigandt 2007). A second view is that the
cognitive metaphor applies when behaviors and processes are
goal-directed, behavior is flexible, and there is exhibition of
adaptation, and the metaphor earns it keep through the parallels
between rational choice theory and evolutionary theorizing (Okasha
2018). Okasha is concerned to articulate the scope and limits of the
cognitive metaphor in evolutionary biology, taking organisms as his
paradigm agents. A third view is that the use of psychological
predication of the activities of cells, neurons, and bodily systems is
not metaphorical but should be taken *literally* (Figdor 2018).
Figdor's literalism is a response to what she views as an
anthropocentric perspective that assumes that human cognition is the
standard against which other uses of psychological ascriptions should
be judged. Finally, a fourth view is that appeals to the nature of
subjectivity and point of view are key here (Godfrey-Smith 2019; see
also Godfrey-Smith 2016c). Godfrey-Smith takes understanding the
evolution of subjectivity to be central to advancing responses to
"explanatory gap" arguments in the philosophy of mind,
implying the graduated nature of cognition itself.


## 7. Locating Biological Individuals in Conceptual Space



The discussion in
 section 6
 has drawn out more about the conceptual space that physiological
individuals occupy and their relationship to evolutionary individuals.
This section offers a more complete and integrative overview of that
conceptual space. Before populating the running summary diagram with
examples of various kinds of biological individuals, we first simply
add Darwinian or evolutionary individuals to
 Figure 3
 and label the resulting nine regions in it to arrive at
 Figure 5:




![a diagram: link to extended description below](fig5.svg)



Figure 5: Adding Darwinian Individuals.
[An
 extended description of figure 5
 is in the supplement.]




As simple as this modification to
 Figure 3
 is, it allows for much more fine-grained answers to the Focal
Question, both in terms of the relationship between the subsidiary
categories living agents, organisms, and Darwinian individuals, and in
terms of where particular individuals are located in the resulting
conceptual space. It may turn out that some of these regions are
unoccupied by actual biological individuals, or that some of the
adjacent regions collapse into one another. But the following proceeds
by indicating how the preceding discussion suggests all nine regions
are exemplified by distinct kinds of biological individual, moving
from less contentious to more contentious examples.



First, consider the lower half of
 Figure 5
 and regions 1, 2 and 3. While organisms are both Darwinian
individuals and living agents, there are two different types of
Darwinian individuals that are not living agents: some parts of
organisms, such as genes (region 2) and, perhaps more controversially,
groups such as colonies of eusocial insects (region 3). For example,
honey bee colonies appear to be Darwinian individuals even though they
are not literally living agents. Each individual bee within a colony
is alive, but as suggested by the discussion of living agency in
 section 6,
 it is only by invoking the cognitive metaphor that the whole colony
itself can be said to be a living agent.



Second, consider the outermost regions to the left and right of
 Figure 5,
 regions 4 and 5. There are both some parts and some groups of
organisms that are neither organisms nor Darwinian individuals nor
living agents. Most parts of the cellular machinery possessed by
organisms, such as lysosomes (region 4) or ribosomes, are biological
individuals that, like genes, are not living agents, but unlike them,
are not Darwinian individuals. Groups with this same status include
higher taxa, such as species and clades discussed in
 section 4.
 Clades (region 5) are neither organisms nor living agents. And even
the most optimistic of clade selectionists will probably agree that a
relatively inclusive and diverse taxon such *Bryophyta*,
consisting of about 10,000 moss species, is not itself a Darwinian
individual. Yet if the common assumption that monophyletic clades are
a type of biological individual is accepted, *Bryophyta* will
nonetheless count as a biological individual (De Luna, Newton, &
Mishler 2003
 Other Internet Resources).
 *Bryophyta* thus belongs in the far right of
 Figure 5.



Third, consider the upper half of
 Figure 5
 and regions 6 and 7. There are correspondingly two different types of
living agents that are not Darwinian individuals: some parts of
organisms such as hearts (region 6) and (again, perhaps more
controversially), groups of organisms such as coral reefs (region 7).
As physiological individuals, hearts are alive but they do not
reproduce or relate to reproducers in the manner that Darwinian
individuals do. As suggested at the end of
 section 6.1,
 a coral reef may also be an example of this kind of biological
individual at the group level. Coral reefs don't feature the
type of reproduction-involving life cycles characteristic of
organisms, and some of the same facts about reproduction likely
disqualify them from being Darwinian individuals. Yet perhaps the
reefs (in addition to their constituent individuals) have a better
chance than eusocial insect colonies of counting as living agents.



Finally, what of the two remaining regions of
 Figure 5,
 regions 8 and 9? These contain, respectively, biological individuals
that are parts of organisms and are both Darwinian individuals and
living agents, and organisms that are living agents but not Darwinian
individuals. Some viruses are at least plausible candidate examples of
the former category (region 8), since they have the internal
complexity and unity of function possessed by physiological
individuals but employ a scaffolded form of reproduction that relies
on the replicative machinery of their host. And perhaps corporate
organisms that are typified by tightly integrated multispecies
complexes exemplify the latter (region 9). Consider again the Hawaiian
bobtail squid plus its colony of *Vibrio fischeri* bacteria
that Godfrey-Smith (2013) discusses as such an example (see
 Figure 1
 above). Those who view this entity as an organism do so because of
the intricate integration between squid and bacteria (Nyholm &
McFall-Ngai 2004; Bouchard 2010). As such, it seems to be a living
agent or physiological individual. But lacking a reproductive life
cycle, it is not a Darwinian individual. One might well argue, by
contrast, that this feature of the squid-*Vibrio* complex also
disqualifies *it* as an organism, making it no different in
kind from coral reefs. Resolving this issue will turn partly on how
exactly different sorts of reproduction are distinguished, and which
sorts are required for evolution by natural selection, topics that
have recently become more intensely debated (e.g., Godfrey-Smith 2015,
2016b; Griesemer 2014, 2016; O'Malley 2016).



Figure 6
 completes this running visual summary of conceptual space that
biological individuals occupy, with the addition of a table that
associates the regions with the examples discussed above.







Regions with their examples| region | example |
| --- | --- |
| 1 | Fruit fly |
| 2 | Gene |
| 3 | Eusocial insect colony |
| 4 | Lysosome |
| 5 | Clades (such as Bryophyta) |
| 6 | Heart |
| 7 | Coral reef |
| 8 | Virus |
| 9 | Squid+*Vibrio* bacteria |





![same as figure 5 but with the adjacent list explaining the numbers](fig5.svg)





Figure 6: Biological Individuals in
Conceptual Space. [An
 extended description of figure 6
 is in the supplement.]



## 8. Regulating Evolutionary Individuals



It was noted at the outset that *organism* and *biological
individual* have been simply equated by several influential
contemporary authors (Queller & Strassmann 2009; Clarke 2012).
This section explores their views of the regulation of evolutionary
individuals.



David Queller and Joan Strassmann have provided one agenda for the
empirical study of what they call "the evolution of
organismality" (Queller & Strassmann 2009, 2016; Strassmann
& Queller 2010). They begin from the claim that the definitive
feature of organisms is the combination of high cooperation and low
conflict between their parts (see also Folse & Roughgarden 2010 on
organisms). Queller and Strassmann note both that these things are
matters of degree and that one can vary independently of the other.
They use these parameters to define a two-dimensional space that
represents a variety of biological individuals, as
 Figures 7A and 7B
 illustrate.




![first of two diagrams: link to both in extended description below](fig7a.svg)

7a: Groups of cells




![second of two diagrams: link to both in extended description below](fig7b.svg)

7b: Groups of multi-cellular
individuals




Figure 7: Varying Degrees of Conflict
and Cooperation (From Fig. 1 & 2, Queller & Strassmann 2009).
[An
 extended description of figure 7 (A and B)
 is in the supplement.]




To capture these ideas, it is useful to think of the feature that
Queller and Strassmann believe is definitive of biological individuals
as the *internal ratio*: it is the ratio of the level of
cooperation between internal parts of individuals to that of the
conflict between them. The higher this ratio is, the higher the degree
of individuality. Figure 7A indicates that, relative to other groups
of cells, a mouse will have a relatively large internal ratio, while a
yeast floc will have a relatively small internal ratio.



Since the internal ratio considers only the level of internal control
within a biological individual, focusing on it alone neglects the
other aspect of autonomous agency that arose in
 section 6.3:
 freedom from external influence. This external dimension to
individuality can also be thought of as involving a ratio between
cooperation and conflict--not between the parts of the individual
but between that individual and other individuals that it interacts
with. Just as an individual in Figure 7B with a relatively large
internal ratio has a higher level of individuality, according to
Queller and Strassmann, so too would an individual with a low
*external ratio*, i.e., one in which external cooperation was
low and external conflict was high. To extend Queller and
Strassmann's idea along these lines, the measure of the level of
individuality would be a type of *meta ratio*: the ratio
between the internal and external ratios.



This extension of Queller and Strassmann's view of individuality
may prove useful in fleshing out more details of what Godfrey-Smith
(borrowing a term of Huxley's) calls the *movement of
individuality* (2013: 33). This refers to the ways in which new
kinds of individual evolve slowly, over geological time scales, from
recurring collaborations between different types of Darwinian
individuals whose graded nature might be thought puzzling (Molter
2022). Such partnerships sometimes lead to new examples of paradigm
individuals, but other times falter or stall at the mere collaboration
stage with no new individuals at all. Closure of a pathway to a higher
degree of individuality could be brought about by either a drop in the
internal ratio (reduced individuality because of internal matters) or
a rise in the external ratio (reduced individuality because of
external matters). An extension of Queller and Strassman's idea
of organismality being a matter of degree has been deployed recently
to tentatively explore the idea of multispecies life cycles in a
sketch of some possible pathways from multispecies group
configurations to multispecies organisms (Andersson, Isaksson, and
Libby 2022).



In effect, Queller and Strassmann have proposed a view of evolutionary
individuals that is exclusively focused on the regulation of the parts
of an evolutionary individual as a means to avoiding subversion from
within. In a series of papers, Ellen Clarke has developed a more
integrative view of evolutionary individuals that develops this
regulative dimension to biological individuality (Clarke 2010, 2012,
2013, 2016a, 2016b). In work focused on plant individuality, Clarke
emphasizes the *mechanisms* that constrain either sources of
heritable variation, such as niche construction, bottlenecks, and
polyploidy, or fitness differences, such as investment in root
connections and the synchronization of flowering (2012: 351, 356).
Clarke then argues that something is an evolutionary individual if and
only if it possesses what she calls *policing* and
*demarcating* mechanisms (2013: 427).



A policing mechanism "is any mechanism that inhibits the
capacity of an object to undergo within-object selection"
(Clarke 2013: 421), typically by decreasing the genetic variation
between *parts* of an object. This decreases the chance that
the object's parts will undergo selection that disrupts the
integration of those parts. There is a sense in which demarcating
mechanisms operate in just the opposite way. Rather than working to
constrain or limit selective processes amongst an individual's
parts, a demarcating mechanism "increases or maintains the
capacity of an object to undergo between-object selection"
(2013: 424), doing so by promoting the variation (between objects)
that fuels selection.



For Clarke, it is *what* these two sorts of mechanisms do that
is important, not *how* the mechanisms do this in various ways
(Clarke 2013: 429). In other words, it is only the *functions*
of the mechanisms that Clarke thinks are definitive, not the various
*material* ways those functions are realized. As Clarke
stresses, this implies the multiple realizability of evolutionary
individuals. This "thoroughgoing functionalism about
individuality" (Sterner 2015: 610) abstracts away from specific
realizations of the functional roles of policing and demarcation. In
this respect, Clarke's view contrasts with many other views of
evolutionary individuals that emphasize the importance of particular
ways in which these mechanisms are realized. For example, Dawkins,
Maynard-Smith, and Bonner imply that certain material
bottlenecks--narrowings between generations exemplified by our
own single-celled, zygotic bottleneck--are essential ways for
policing to be realized in evolutionary individuals (Clarke 2013:
418-419), while Ratcliffe and Kirk instead make material
germ-soma separation essential (Clarke 2013: 420).



Clarke's functionalism thus leads her to reject "the
bottleneck condition" as strictly necessary for evolutionary
individuality, a condition that Marc Ereshefsky and Makmiller Pedroso
also reject as part of their defense of the view that multispecies
*biofilms* are evolutionary individuals (Ereshefsky &
Pedroso 2013, 2015). Clarke's functionalism thus in principle
facilitates the search for alternative mechanisms--perhaps such
as lateral gene transfer in the case of biofilms--that serve that
function in contexts where the usual material bottlenecks are not
present.



This makes all the more interesting Clarke's own disagreement
with those who have defended the idea that biofilms are evolutionary
individuals (Clarke 2016a), wherein she argues that many of the
important claims that underpin ascriptions of multicellularity to
biofilms--such as that they are physiologically unified systems
or contain cells that interact synergistically--are either not
verifiable (e.g., they have higher-level adaptions) or are false
(e.g., they display heritable variation in fitness). While
Clarke's functionalism means that she remains open to the
suggestion that there may be some non-genetic form of heritability in
biofilms (Doolittle 2013), she takes the relevant empirical evidence
here to be indecisive (Clarke 2016a: 202).


## 9. The Evolution of Biological Individuality



Finally, the evolution of biological individuality continues to be a
lively topic (Okasha 2011; Calcott & Sterelny 2011; Bourrat 2015;
Clarke 2016b; O'Malley & Powell 2016; Queller &
Strassmann 2016; Herron 2017, 2021; Sterner 2017). The starting point
here is the idea that the history of life is the history of the
construction of more complicated biological individuals from simpler
individuals, with natural selection, operating at one or more levels,
facilitating the transitions between these individuals (Buss 1987;
Maynard Smith and Szathmary 1995). Underlying these ideas is
the assumption that many or all biological individuals are
hierarchically organized: earlier individuals provide the material
basis for later individuals. For example, prokaryotes, which are
single-celled organisms without a nucleus, form the material basis for
single-celled eukaryotes, which do have a nucleus; in turn,
single-celled eukaryotes serve as the material basis for multicellular
eukaryotes (Herron, Conlin, and Ratcliff 2022).



The evolution of biological individuals from prokaryotes to
single-celled eukaryotes around 2 billion years ago, and from those to
multicellular eukaryotes in the last 600-800 million years, are
established facts. In addition, there appear to be no counter-examples
to this evolutionary trend. Yet speculation and controversy surround
almost everything else that has been said about these evolutionary
transitions. Consider five such issues on which there is a sort of
default position in the literature that remains subject to ongoing
philosophical and empirical interrogation.



First, it has been common to think, especially in work from and
influenced by Richard Michod (e.g., Michod 2005), that at the heart of
an evolutionary transition is some kind of fitness transfer or
decoupling, with the fitness of new, "collective"
evolutionary individuals increasing relative to that of the
"particles" from which they evolve until the two are
decoupled. Work by Matthew Herron and colleagues on nascent life
cycles (Ratcliff et al. 2017) and the evolution of multicellularity
(Herron, Conlin, and Ratcliff 2022) that speculates on the
intermediate processes driving evolutionary transitions are anchored
within this framework. This conception of evolutionary transitions and
the modelling frameworks in which it operates has been challenged by
Pierre Bourrat and colleagues (Black, Bourrat, and Rainey 2020;
Bourrat 2019; Bourrat et al. 2022), who look instead to trait-based
tradeoff breaking as an alternative indicator of evolutionary
transitions in individuality. Here ecological scaffolding and
population structure play critical roles in mediating the extended
process of a major evolutionary transition that is
"Darwin-like", becoming moreso with the endogenization of
the processes so scaffolded (Bourrat forthcoming, 2023).



Second, it is typically assumed that the evolution of individuality
itself is the evolution of complexity. There are, however, questions
both about how complexity itself should be measured or conceived and
about what empirical evidence there is for viewing the complexity of
individuals as increasing over evolutionary time (McShea 1991). Are
the number of cell types that an individual has considered (Bonner
1988), the types of hierarchical organization it manifests (Maynard
Smith 1988), or some more taxa-specific criterion, such as the
information required to specify the diversity of limb-pair types
(Cisne 1974)? Fossils constitute a principal source for the criteria
that have been proposed here. Yet different kinds of organisms leave
fossils with distinct kinds of features, and some kinds of organisms
are more likely to leave fossils than are others.



One natural suggestion is that there may well be different kinds of
hierarchies for the evolution of individuality, since kinds of
individuals can differ from one another in more than one way. Daniel
McShea (2001a, 2001b; McShea & Changizi 2003) has proposed a
structural hierarchy that is based on two components, the number of
levels of nestedness and the degree to which the highest individual in
the nesting is individuated or developed. McShea provides an
overarching framework in which eukaryotic cells can be viewed as
evolving from differentiated aggregations of prokaryotic cells that
have intermediate parts; multicellular eukaryotes as evolving from
differentiated aggregations of single-celled eukaryotes; and colonial
eukaryotes as evolving from differentiated aggregations of
multicellular eukaryotes.



By contrast, Maynard Smith and Szathmary (1995) focus on
differences in how genetic information is transmitted across
generations, proposing eight major transitions in the history of life.
These start with the transition from replicating molecules to
compartmentalized populations of such molecules, and end with the
transition from primate societies to human societies. While Maynard
Smith and Szathmary are interested in individuality and
complexity, their eight transitions do not form a continuous,
non-overlapping hierarchy. Their discussion is focused primarily on
exploring the processes governing each of the particular transitions
they propose in terms of changes in replicative control.
O'Malley and Powell (2016) have recently argued that not only
does this perspective omit critical events--such as the
acquisition of mitochondria and plastids, in what those authors prefer
to think of as turns rather than transitions in the evolution of
living things--but also that what is needed is a



> 
> 
> supplementary perspective that is less hierarchical, less focused on
> multicellular events, less replication oriented, and in particular,
> more metabolic. (O'Malley and Powell 2016: 175)
> 
> 
> 



Third, there is the question of just what processes and events should
be included as evolutionary transitions, major or otherwise. Some have
argued, for example, that the origin of oxygen-generating
photosynthesis should be added to the major transitions (e.g.,
O'Malley and Powell 2016; see Szathmary and Fernando 2011
for a longer list of additions). Pushing back against the trend to
propose a more expansive list of major evolutionary transitions,
whether mediated by the loosening of existing criteria or by general
pluralistic tendencies that we've seen emerge in the literature
on biological individuals in various ways, Herron (2021) has recently
argued for a narrowing of the definition of a major transition by
requiring that it lead to the creation of a new population of
evolutionary individuals, drawing on an analogy with what happened in
2006 with the exclusion of Pluto from the category
"planet" as a motivating intuition pump. On this view,
neither the origins of the genetic code nor the origin of language,
both major transitions according to Maynard Smith and Szathmary
(1995), belong on the list of major evolutionary transitions,
independent of their overall evolutionary significance.



Fourth, it is common to view the trend from prokaryotes to
multicellular eukaryotes as resulting from some type of directional
bias, one that makes the trend a tendency supported by underlying
mechanisms and constraints. Perhaps the tendency is underwritten by
thermodynamic, energetic considerations, by facts about the generative
entrenchment of developmental systems (Griffiths & Gray 2001), or
by evolutionary advantages of increases in size (McShea 1998). But in
supposing that there is some type of directional bias, each of these
hypotheses might be thought committed to the sort of Panglossianism
about adaptation that Gould and Lewontin (1979) are famous for
critiquing, or (more subtly) to a view of evolutionary change as
progressive or inevitable in some way. Gould has used his discussion
of the Burgess Shale (Gould 1989) to challenge such views of
evolution, arguing that the disparity of the fossils in that shale
indicates that living things are significantly *less* different
from one another than they once were. Gould argues that the range of
biological individuals now on the planet is largely the result of
highly contingent extinction events, and there should be wariness of
immediately assuming that observed trends or patterns are adaptive (or
other) tendencies.



Fifth, many authors have recognized that whatever trends or tendencies
there are in the evolution of individuals, there have also been
changes over evolutionary time in the social relations between
individuals (e.g., Frank 1998), and in the sorts of shared resources
that are available to the biological individuals that Douglas Erwin
has discussed drawing on the economic concepts of *public
goods* and *club goods* (Erwin 2015, McInerney & Erwin
2017). Yet how sociality should be integrated into a view of the
evolution of biological individuals remains under-theorized (for
recent exceptions, see Birch 2017, Okasha 2018, and Lloyd and Wade
2019). And however limited fossil evidence for individual structures
and ecological niches may be, such evidence for the kinds and extent
of sociality is significantly more sparse. Much of the work to be done
here seems distinctly philosophical in that it concerns how sociality
is conceptualized. Should one accept the simple aggregation of
individuals as a basic form of sociality? Does sociality essentially
involve some form of cooperation, and if not, what is the relationship
between "prosocial" sociality and antagonistic forms of
sociality (e.g., competition or predation)? Although the
"evolution of sociality" has been taken up by animal
biologists (especially by primatologists) and evolutionary
anthropologists (where it is often viewed game-theoretically), this
has served to reinforce a view of sociality that seems somewhat
narrow, e.g., the view is not clearly applicable to structurally
simpler individuals. Perhaps the idea that sociality is not a
relatively recent addition to multicellular life needs to be taken
seriously. Instead, sociality may be a more sweeping feature of many
if not all biological individuals, with the evolution of individuality
understood in tandem with the idea of changing, shared, public and
club goods. This would make for a more dynamic and cyclical view of
the history of life than has been assumed in past thinking about
biological individuals.