Download Colonies Are Individuals: Revisiting the Superorganism Revival

Colonies Are Individuals:
Revisiting the Superorganism Revival
Matt Haber
Abstract
Superorganism accounts of colonies typically follow either a similarity or selection
approach. Similarity approaches appeal to the ways in which some colonies are like
organisms. These fall prey to problems of precision, lack of specificity, and tend to
obscure relevant ways in which colonies are dissimilar to organisms. Selection approaches make appeal to how colonies may participate in natural selection, much like
other individuals. Unfortunately, selection approaches link definitions of superorganisms tightly to particular accounts of selection (and, typically, fitness), leaving these
accounts more brittle than need be, while often pushing other evolutionary, developmental and ecological processes into the background. Rather than adopting either of
these approaches, I recommend adopting an account of colonies as individuals and a
rank-free approach to biological hierarchy. This preserves much of what is desirable in
selection approaches by requiring appeal to biological theory, yet allows space for evolutionary, developmental, ecological and other theoretical frameworks. It also avoids
the pernicious imprecision so often found in appeals to similarity, instead placing such
appeals firmly in an evolutionary context.
Contents
1 Introduction
2
2 Superorganism Approaches
2.1 Similarity Approaches . . . . . . . . . . . . .
2.1.1 Problems With Similarity Approaches
2.2 Selection Approaches . . . . . . . . . . . . . .
2.2.1 Reviving the Superorganism . . . . . .
2.2.2 Problems With Selection Approaches .
.
.
.
.
.
4
4
5
9
9
11
3 Colonies Are Individuals
3.1 The Individuality Thesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.2 Colonies Are Individuals . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
13
14
16
1
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
3.3
3.4
Colonies as Organisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Getting Rid of Organisms . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4 Conclusion
1
17
18
20
Introduction
The most general organismal character
of the ant-colony is its individuality.
Like the cell or the person, it behaves
as a unitary whole, maintaining its
identity in space, resisting dissolution
and, as a general rule, any fusion with
other colonies of the same or alien
species.
Wheeler, 1911 (310)
Social colonies present a challenge to the theory of evolution by natural selection. Namely,
these colonies are constituted, in varying degrees, by individuals that do not reproduce
(and, in many cases, have no capacity for reproduction). How might this be explained by a
theory of natural selection? Though Darwin addresses this ‘special difficulty’ in The Origin of Species (1859, chapter 7, Instinct), the question persists and remains illuminating
to ponder (Herbers 2009). More recently, Wynne-Edwards (1962) proposed a theory of
group selection to explain the presence of eusocial colonies, though this went into disfavor
following accounts of altruism and colony formation based on the individual as the unit
of selection (Williams 1966), or in terms of inclusive fitness (Hamilton 1964a,b) and kin
selection (Maynard Smith 1964; Michod 1982). Group-level theories of selection fell further into disrepute as a ‘gene’s-eye view’ perspective rose to ascendancy (Dawkins 1976,
1982).
Contemporary use of the term superorganism to describe eusocial insect colonies is typically
traced back to Wheeler (1911, 1928),1 falling out of favor along with group selection—
though E. O. Wilson (1971, 1975, 1985) provides a notable exception (Wilson and Sober
1989). Today, accounts of group and multi-level selection are back in vogue (e.g., Damuth
and Heisler 1988; Sober and Wilson 1998; Okasha 2006; Godfrey-Smith 2009), and the
superorganism concept has been revived. This is in no small part thanks to David Sloan
Wilson and Elliott Sober’s “Reviving the Superorganism” (1989). Rightfully regarded as
1
Though Huneman and Wolfe attribute usage to Clements (Huneman and Wolfe 2010). My brief account
here displays a bias borne of the focus on selection.
2
a modern classic, it accomplished just what is laid out in the title. This revival, however,
is due for revisiting.
Wilson and Sober distance themselves from traditional approaches to the superorganism,
strongly criticizing metaphorical treatments of the concept. Instead, Wilson and Sober
defend superorganisms as real biological individuals. Their argument, described below,
relies on a concept of assessing when an individual is a fitness-bearing individual, and
what it means to be a unit of selection.
Wilson and Sober represent one approach to defining superorganisms—a selection approach. Hamilton et al. (2009) describe this as one of two primary approaches typically
adopted in the evolutionary literature, contrasting it with a similarity approach. Similarity
approaches are, primarily, arguments by analogy of colonies to organisms. Though it is
useful to distinguish between these two approaches, they are not cleanly distinct from one
another. Superorganism arguments by analogy are not simply metaphorical treatments of
colonies; typically they centrally include some appeal to participation in evolutionary processes. Selection approaches, meanwhile, include elements of similarity arguments. They
are, in some sense, highly specified arguments by analogy, focused on functional organization and selection.
Regardless, both approaches are unsatisfactory. Defining superorganisms by way of analogy
threatens to obscure important features of colonies, either through a lack of precision
(i.e., leaning on too thin a concept of organism) or by too narrowly restricting the object
to which similarities are being drawn. These suggest a category error in drawing the
relevant comparison classes, and are symptomatic of the Problem of the Paradigm, i.e.,
the presumption either that organisms are paradigmatic individuals, or of a paradigmatic
organism to which all others must be judged against.
Defining a superorganism concept from accounts of fitness and selection provides the right
level of specification to avoid many of the traps associated with the similarity approach,
but at a cost. The end product is too brittle a notion, tied too closely to specific accounts
of selection, where a more general concept is needed—one approaching the generality of
the evolutionary framework within which these accounts of selection and fitness are offered.
At the same time, a narrow focus on how fitness and selection shape colonies threatens to
push other biological factors (e.g., developmental, ecological, phylogenetic, etc.) into the
background.
Below I revisit the superorganism revival, drawing on and endorsing the characterization
of colonies as individuals found in Hamilton et al. (2009). This approach has several advantages, among them the avoidance of the concerns described above, a sharpened focus on
the biology of colonies (as opposed to similarities to organisms), and the central role given
to participation in a wide spectrum of biological processes. However, the individuality approach is less wedded to any particular characterization of these processes, providing room
3
for competing accounts, e.g., substituting differential persistence in place of fitness (n.b.
Bouchard 2008). Regardless of whether these competing accounts are ultimately adopted,
rejected, or perhaps just tolerated, space ought to be carved out for their consideration,
i.e., rather than just rejecting them out of hand or by definition, such views need to be
tested and adequately assessed. This is similar in spirit to adopting a bottom-up approach,
(e.g., Dupré and O’Malley 2009) or diachronic perspective (e.g., Griesemer 2000; Okasha
2006). Ultimately, then, the individuality approach provides the foundation for a more
general defense of colonies as genuine units of selection, and solidifies the contribution of
Wilson and Sober (1989), even while moving away from the superorganism.
2
Superorganism Approaches
2.1
Similarity Approaches
Contemporary similarity approaches to superorganisms are a bit more careful than the
loose metaphorical treatments they might be made out to be. This is not to say they
are lacking in problems. The argumentative strategy is to explicitly argue from analogy
of colonies to organisms, specifying those analogies in terms of biological theory. Moritz
and Fuchs (1998, p.8), for example, frame their argument as critically assessing what they
describe as the “tempting view” of considering honeybee colonies as “superorganisms in
analogy to a complex higher organism being composed of numerous single cells.” They go
on to specify that appeal as:
. . . something special about the tightness of bee colonies which closely resembles
at least more primitive multicellular organisms, and thus seems to call for a term
such as superorganism.
If that was the extent of it, then a simple criticism of overreaching metaphor would be
sufficient. But Moritz and Fuchs proceed to assess that ‘close resemblance’ in terms of
biological structure, evolutionary mechanisms and organizational principles. The result is
a sophisticated similarity approach that, like selection approaches, places evolutionary processes and theory front and center, e.g., arguing that: “colonies can be envisaged as vehicles
for genes similar to individual [organisms], provided that sufficient genetic homogeneity is
maintained through the genetic bottlenecks of reproduction” (1998, p. 16). Beekeeper
breeding schemes are cited as evidence to this effect, where queens are selected based on
colony-level traits, as opposed to characters possessed by the queens. This is reminiscent
of arguments found in selection approaches (e.g., Wilson and Sober 1989).2
2
Strassmann and Queller (2007) provide another example of a sophisticated similarity approach, evaluating the organismality of colonies. Ultimately, though, they are concerned with defending the utility of
kin selection as providing an explanatory means of sociality, cooperation, and conflict in insect colonies.
4
2.1.1
Problems With Similarity Approaches
This is not to say that even these careful similarity approaches are without reproach.
Relying on similarity is to rely on a notoriously difficult relation to meaningfully capture
(Goodman 1972). Even when a relevant similarity does hold, too narrow a focus on that
relation can distract from dissimilar characters that colonies may have from organisms
(Mitchell and Page 1992; Hamilton et al. 2009). The similarity approach, then, can just
as easily hide relevant facts as highlight them, even when the theory grounding those
similarity claims is explicitly stipulated.
To help see how the similarity approach might be misleading, consider two different questions that might follow from treating eusocial colonies as superorganisms:
(1) What kind of individual is a colony?
(2) How are colonies like organisms?
These questions may be conflated if organisms are taken to be paradigmatic biological
individuals. Yet this would be a mistake. In the first case, the focus is on the biology of
colonies. No implicit presumption about the similarity of colonies and organisms should
be read into the question. Nothing about the status of colonies as individuals turns on
how organisms are individuals. Similarities between the two may be discovered and prove
enlightening, but are not definitional. The second question, on the other hand, is far
narrower, focusing strictly on the similarity of colonies to organisms. It represents one
way the first question may be addressed or fleshed out, but is certainly not a privileged or
exclusive strategy. Conflating these questions is to mistake a possible line of inquiry for
the larger set of questions being addressed. Treating these questions as variants threatens
to cut off interesting avenues of inquiry and obscure important research projects. It should
be resisted even if it comes at the cost of giving up on the utility of superorganism.
Goodman (1972) provides the standard complaint against similarity, though his is a broader
philosophical point and not particular to biology. His dissatisfaction is wide-ranging, observing that similarity arguments carry no explanatory power, and that since any two
things have at least some property in common, raw claims of similarity are hardly interesting or insightful. Sterelny and Griffiths (1999), among others, turn Goodman’s complaint
to biology, and Hamilton et al. (2009) more precisely to colonies. One of Goodman’s complaints about similarity arguments is the lack of specification of relevant theory, without
which similarity is an empty guide. But a demand for grounding similarity claims in some
specified framework is no mark against scientific explanation or conceptualization, despite
Goodman’s concerns. It may simply be a mark of good scientific practice or reasoning.
One way that specification may be accomplished is by locating arguments within or explicitly appealing to theory. Moritz and Fuchs (1998) clearly accomplish this. Still, similarity
arguments for superorganisms are problematic, and it is worth looking at how they fail
5
even in cases where relevant similarity is carefully stipulated.
Three concerns may be raised against even this sophisticated strain of similarity arguments:
(1) Imprecision, namely, the notion of organism on its own is too thin to support the work
being asked of it. Finer specification of organism can do the work, but at the risk of raising
the second concern: (2) Narrowness, i.e., a too fine specification of properties possessed
by (some kind of) organisms will exclude some groups by obscuring other properties that
may confer organismality on a group. These first two concerns are symptomatic of the
third concern: (3) the Problem of the Paradigm, i.e., presuming either that organisms
are paradigmatic individuals, or that there is a paradigmatic organism. Appreciation
of the richness of variation of individuality and organismality recommend rejecting this
presumption.
Consider imprecision. Even when grounded in relevant theory, a simple appeal to the
similarity of colonies to organisms is not well specified. The concept of organism is too
ambiguous to do the work being asked of it; the comparison class is simply too amorphous. Namely, what kind of organisms are colonies supposed to be similar to? This is no
pedantic question, but tracks genuine controversy over what organisms are. Pepper and
Herron (2008) survey organism concepts, identifying twelve variants. These range from
unitary individuals (Santelices 1999) to clonal and modular organisms (be they physically
contiguous or not) (Janzen 1977; Tuomi and Vuorisalo 1989a,b). To these we can add
extended organisms that persist rather than reproduce (Turner 2000; Bouchard 2008), and
microbial organisms (Dupré and O’Malley 2009).3 This variation of organismality suggests the similarity approach may be misguided, or even question-begging. Namely, what
if colonies are not similar to organisms, but simply are organisms? Indeed, Pepper and
Herron treat them just this way, defining them as “a group that possesses the properties
of an organism” (2008, p. 623), and, as shall be seen, Martens (2010) explores a similar
line of argument.
Debates over organism are complicated by the fact that physical contiguity can fail to track
unique genotypes, which can fail to track fitness and adaptation (Janzen 1977; Tuomi and
Vuorisalo 1989a,b; Pepper and Herron 2008; Folse III and Roughgarden 2010) and that
lineage-generating entities may fail to be metabolic wholes (Dupré and O’Malley 2009).
Consider, for example, disputes over what constitutes the world’s largest organism. Excitement over the discovery of the individual Armillaria bulbosa fungi in northern Michigan,
spanning over 15 hectares and weighing in excess of 10,000 kgs (Smith et al. 1992), was met
with skepticism that this ought to count as an organism: “. . . although clone 1’s reputation
as a champion genotype may yet be secure, its status as a champion organism depends
upon one’s interpretation of the rules” (Brasier 1992, p. 383). Furthermore, though terms
like ‘unitary individual’ may suggest a categorical approach, quite the opposite is the case,
3
Whether any of the variants described by Pepper and Herron (2008) adequately capture microbial
entities is, to my mind, an open question.
6
with organism accounts typically aiming to capture the continuously variable status of
organismality (n.b., Santelices 1999).
So it is anything but clear just what colonies are supposed to be similar to, let alone in
what respect, in order to qualify as superorganisms. Furthermore, given the diversity of
organismality, the appeal of the similarity approach cited by Moritz and Fuchs appears,
at least, to grow ever more dilute. What is insightful about Moritz and Fuch’s account
are the biological claims about colonies; that these data may be similar to facts about
organisms more generally is a separate claim in need of explanation, not an explanation
or defining body of facts in themselves. Losing sight of that is to miss a fruitful line of
research and explanation concerning the origin and evolution of individuality. Hence the
diachronic perspective: these similarities arose; one set is not explanatory of the other.
This is a powerful and insightful perspective with implications for, among other things,
major evolutionary transitions.4
Even if similarity arguments instead appeal to a narrower view of organism that rejects
modular, clonal or persistent organisms, problems will persist with arguments by analogy.
(I also admit difficulty seeing the intuitive justification of a narrower view when the very
topic at stake concerns expanding something like organism to include colonies!) This is
true for any narrow specification of organism. That is, solving the problem of imprecision
introduces a problem of narrowness (Mitchell and Page 1992; Hamilton et al. 2009).
Narrowness is particularly a problem when offering a definition of superorganism in terms
of similarity with organisms. Even if you pick and choose among various kinds of organisms
(or organism concepts), that still may be too narrow an approach. After all, if colonies
represent a unique grouping, the key features of that grouping may simply be absent from
other organism groupings. That is, colony may simply be a kind of organism (see, e.g.,
Martens 2010), and defining it as simply analogous to other organisms is to both ignore the
unique biology of colonies and to beg the question of definition, i.e., the approach required
is to expand the concept of organism to include colonies. The resources to define colonies
in terms of other kinds of organisms are simply lacking.
John Dupré’s “The polygenomic organism” (2010) addresses a similar kind of mistake that
may be made. Most every vertebrate satisfies most every concept of organism. But this
is a feature of the fact that organism concepts are coincident about vertebrates. Though
this may give us confidence in asserting that all vertebrates are organisms, it does not
provide much guidance in assessing these various organisms concepts. The way(s) in which
vertebrates act as unitary entities provides limited guidance for a more general account
of organismality. Taking vertebrates as paradigmatic organisms, or, worse, evaluating or
defining organismality in terms of similarity to vertebraticity would be to miss important
4
Strassmann and Queller (2007, 2010) properly recognize the priority of explanation of similarity, and
frame their response, in part, in the context of work on major evolution transitions.
7
ways things may be organisms. It would be to impose too narrow a view. Such is the same
with defining colonies in terms of similarities to organisms.
Narrowness and imprecision are symptomatic of the Problem of the Paradigm. Here, this
problem may be one of two variants:
• Taking the organism to be the paradigmatic individual; or
• Presuming a paradigmatic organism.
These are instances of a more general mistake described by Sober (1980). Sober recalibrates
Ernst Mayr’s famous characterization of population thinking, contrasting it against an
Aristotelian natural state space, rather than against typological or essentialist thinking (see
Mayr 1959; Winsor 2006). Sober argues that it is not essentialist or typological thinking
that is primarily at odds with population thinking, but the presumption of some stable
natural state to which populations tend. This latter tendency promotes the view that
variation is deviation, be it over space or time. Instead, Sober argues, this natural state
space approach should go the way of absolute space in physics. There is no natural state
to which things tend towards, there is just variation. That variation, too, will vary.
How does this relate to similarity approaches to superorganism? Though not explicitly
about rejecting the adoption of a paradigmatic approach, we can apply Sober’s rejection
of a natural state space here. If organismality is a character of individuals subject to
(or arising from) selection, then it would be a mistake to treat some form (or range) of
organismality as the form to which others may approach or deviate. This is all the more
pressing in consideration of eusociality, for which we have strong evidence of multiple origins
and reversions (e.g., among wasps and bees (Michener 1974; Danforth et al. 2006; Danforth
2007; see also Godfrey-Smith 2009)). In other words, colonies, and superorganisms, are
just the sorts of things to which we ought to apply Sober’s lesson about about population
thinking.
The first variant of the problem of the paradigm is to adopt the view that organisms are
paradigmatic biological individuals, as opposed to simply those that we are most familiar
with. But if individuality is an evolved level of organization (or organizations), then we
should not expect any particular form of individuality to be paradigmatic. There is no
better reason to define colony-individuals (i.e., superorganisms) in terms of organisms, as
to define organisms in terms of similarity to colonies. Familiarity may provide grounds for
insight, but not for definition.
The second version of the problem of the paradigm is to presume that there is a paradigmatic form of organismality. Of course there isn’t, as was discussed above with regard to
the problem of imprecision, and has become increasingly evident since at least Buss’ survey
of individuality (1987).
Furthermore, debates over the concept of organism are likely to be as entrenched as de8
bates over species concepts. This further undercuts the argument by analogy to organisms,
suggesting it is not merely a conceptual confusion but a genuine reflection of the variation of organismality. (Or, at best, a deeply unsettled matter in the field.) Pepper and
Herron (2008) recommend the phrase organism syndrome to better reflect the continuous,
as opposed to categorical, nature of organismality. Though I have some quarrels on the
details of their application, I enjoy the phrase and appreciate its capacity for capturing the
relevant diversity here.5 A cautionary note to add, however, is to not confuse variation of
organismality for degree of organismality. The two are separate modes we might consider,
though both are relevant to questions about colonies as units of selection.
2.2
2.2.1
Selection Approaches
Reviving the Superorganism
Famously, Wilson and Sober resist the appeal to similarity in their “Reviving the Superorganism” (1989). They adopt another approach in making their case for superorganisms,
arguing on grounds of consistency that some colonies ought to be treated as units of selection. This represents a second way that question (1) above may be addressed. Namely, a
second approach to answering What kind of individual is a colony? is to consider the question Under what conditions are colonies units of selection? This is to consider individuality
in terms of selection.
“Reviving the Superorganism” is rightfully regarded as a modern classic, accomplishing
just what is laid out in the title. In it they lay out three primary theses: (1) that there is
room in contemporary evolutionary biology for the concept of the superorganism; (2) that
consideration of superorganisms support accounts of natural selection at the level of groups;
and (3) that group selection theory should not be viewed as an exclusive alternative to
other theories about the level of selection, but as a complementary competing conceptual
framework. “Reviving the Superorganism” found a receptive audience. It tapped into
latent discontent with the gene’s eye view perspective, while offering an alternative to
that view without directly invalidating it. It is among the most cited articles in the
Journal of Theoretical Biology, often as a justification for studies of the evolution of eusocial
colonies.
The second and third of these theses turn, in large part, on the first. To make their case
for the coherency of superorganisms, they appeal to a concept of fitness, and how fitnessbearing entities participate in evolutionary processes (notably, as units of selection).
5
This is not intended as an endorsement of Pepper and Herron’s notion of organism syndrome. Though
couched in terms of continuous variability and rejection of categorical approaches, their use of paradigm
organism is in need of further analysis.
9
Wilson and Sober argue that groups like colonies are fitness bearing in the right way to be
units of selection. The explicit appeal to selection is clearly on display in a central move
of their argument. Evolutionary theory may be framed as selection of individuals with the
greatest average fitness. Absent a presumption about what individuals are, any individual
becomes a candidate for selection. However, Wilson and Sober identify a contradiction
in arguments offered in favor of individual selection, but against group selection (p. 342,
citations suppressed):
[I]ndividuals can be regarded as groups of alleles. When the A-allele is more fit
than its alternative, averaged over all the individuals within which the alleles
occur, this is not regarded as an argument against individual selection. On
the contrary, such differences are required for traits to be heritable, and form
the very foundation of Darwin’s theory. How then can the greater fitness of
A-individuals, averaged over all groups within which the individuals occur, be
used as an argument against group selection?
So in the same way that evolutionary theory may treat an individual organism as a group of
alleles, Wilson and Sober argue that evolutionary theory provides the conceptual resources
to treat groups as collections of individuals (whatever those individuals may be).6 If those
individuals are fitness-bearing, and if between-group selection overwhelms within-group
selection, then those groups may be treated as units of selection. Yet, argue Wilson and
Sober, advocates of individual (organism) level selection fail to adopt group-selection.
Resolving this contradiction requires imposing consistency on how individuals at different
levels are treated in evolutionary theory. The first option is to use levels-of-selection theory,
and apply the same standards to genes, organisms, colonies, communities, etc. On this
approach, individuals, regardless of level, which satisfy the criteria of selection may be
considered units of selection. The other option identified by Wilson and Sober is to simply
describe all evolutionary change at a single level, typically allelic or genetic (e.g., Williams
1966; Dawkins 1976, 1982).
Wilson and Sober (p. 345) proceed to make the case for superorganisms:
[N]atural selection sometimes is sufficiently concentrated at higher levels to
produce single-species groups and multi-species communities that approach individual organisms in their degree of functional organization.
Eusocial insect colonies, cellular slime molds and phoretic associations are all offered as
examples. For each, the case is made that the conditions for natural selection are met.
Notice the appeal to similarity, though the appeal is not so pernicious as above. The focus
is on degree of functional organization, with no specification of what form that organization
6
Okasha (2006) pursues this strategy further, drawing on the distinction between MLS1 and MLS2
(Damuth and Heisler 1988), and offering a generalized account of selection using the Price equation.
10
must take. It’s entirely possible that very different kinds of functional organizations may
produce similar degrees of organization (in terms of bearing fitness). This diversity would
be expected were functional organization of groups an evolved character.
Primarily, though, Wilson and Sober’s defense of the superorganism rests on their specific
account of fitness and selection. Their focus is on how groups may exhibit a “degree
of functional organization” comparable to the parts of organisms. Nothing is asserted
about what may constitute functional organization in those groups, aside from an effect on
allocation of fitness. Any similarity arguments here are highly specified and concerned with
participation in evolutionary processes, not concerning the details of how that participation
may be expressed.
Wilson and Sober argue that superorganisms are real things, namely, biological entities that
participate in evolutionary processes and may be described as units of selection by virtue
of that participation. More specifically, superorganisms satisfy a precise set of conditions
(p. 342):
1. Subdivision of population into a number of groups;
2. Group fitness;
3. Variation in group fitness due to heritable underlying genetic differences;
4. No differences in the fitness of individuals within groups.
The details of conditions that must be met to be a unit of selection vary among commentators, and we could contrast Wilson and Sober’s with other accounts. Reeve and Hölldobler
(2007) adopt a similar approach, arguing that colonies are superorganisms when withingroup competition is nearly nonexistent and between group competition is high. Folse III
and Roughgarden (2010) use a broader account that encompasses much of what is specified
by Wilson and Sober, distinguishing between cases where fitness may be aligned between
or exported to members of a group (see Damuth and Heisler (1988) and Okasha (2006) for
a more general discussion of this distinction). Godfrey-Smith (2009), too, offers a different
account of conditions that identify when some group is acting as a unit of selection, emphasizing bottlenecks and other conditions on which groups constitute Darwinian Populations.
Though the details vary, these approaches are explicitly about selection.
2.2.2
Problems With Selection Approaches
Selection approaches have the advantage of grounding definitions of superorganism explicitly in an account of fitness and selection. As we shall see, this is also a drawback, and
suggests that the specification of similarity of functional organization is not a full approach
itself, but a subsequent step to a more general approach.
11
Wilson and Sober define a superorganism as “a collection of single creatures that together
possess the functional organization implicit in the formal definition of organism” (1989,
p. 339). This definition runs at odds with their more robust treatment of superorganisms
(and colonies in particular) as individuals capable of being selected. That is, a stronger
claim appears to be lurking in this definition than in the passage above, that natural
selection may produce groups that “approach individual organisms in their degree of functional organization” (1989, p. 345, emphasis added). The stronger claim is that there is
some functional organization implicit in the formal definition of organism that determines
how organism-like some collection is—a claim that runs directly into the Problem of the
Paradigm. The contrast is comparable to the questions at the beginning of §2.1.1. The
first question, What kind of individual is a colony? asks after the biology of colonies; the
second question, How are colonies like organisms? in contrast, runs into the problem of
the paradigm. Defining a superorganism in terms of some implicit functional organization
found in the definition of organism reveals an ambiguity implicit in the selection approach
to superorganisms. As described above, it is anything but obvious what the formal definition of organism is, much less what functional organization is implicit in that definition.
This imprecision is reflected in how Wilson and Sober’s definition is being read, e.g., Pepper and Herron (2008) attribute the definition of superorganism as “a group that possesses
the properties of an organism” to Wilson and Sober (p. 623).7 That even Wilson and
Sober are apt to slip here is a testament to how closely aligned selection arguments are to
similarity arguments. (Indeed, I consider the former to just be a highly specified form of
the latter.)
However, even if we leave aside concerns over whether a selection approach collapses into a
similarity argument, problems remain. The reliance on a narrow view of what fitness is and
what it means to participate in evolutionary processes ties a definition of superorganism,
and, by extension, an account of selection in which colonies may act as units of selection,
directly to a particular account of selection and fitness. But superorganism accounts ought
to be more general than this, and be able to persist in other accounts of selection, in case
their home account proves problematic. In other words, Wilson and Sober’s superorganism
is too brittle, where it needs to be robust.
Hamilton et al. (2009) put this well, arguing that while selection approaches have the
advantage of prioritizing evolutionary processes over poorly specified similarities, these approaches lack the resources to directly address colony-level reproduction and development,
and may push other colony-level processes into the background (see also Oyama et al.
2001). In particular, Hamilton et al. argue that development gets short shrift, though a
similar complaint may be made regarding ecological (and possibly other) processes (see
Martens 2010).
Recent examples of what may be missed by too tight an adherence to particular selection
7
For what it’s worth, I do not think this captures Wilson and Sober’s definition.
12
approaches are evident in Hou et al. (2010) and Yang (2007). Hou et al. test the view
that eusocial colonies should be considered individuals by applying predictions to that end
using metabolic scaling theory (West et al. 1997). This requires a consideration of colonylevel physiological and life history traits, which distinguish eusocial colonies from simple
groups of individuals. Here and elsewhere (Gillooly et al. 2010), these findings are used as
evidence for colony-level selection, and support for research programs focused on colony
reproduction, development, growth and survival. Notice, though, that consideration of
fitness and colony-level selection follow from, rather then lead to, consideration of other
colony-level biological features.
Yang (2007) recommends using superorganisms as model organisms for EvoDevo studies.
One motivation is to expand our understanding of development, which Yang argues has
been “conditioned by the assumption that the individual organism is the canonical unit
of analysis” (p. 400). This concern echoes the problem of the paradigm described above.
Instead, Yang argues, using “colonial organisms” as model organisms in EvoDevo research
will raise “critical conceptual and empirical questions about what kinds of processes fundamentally characterize developmental systems and their evolution” (p. 399). This embodies
the careful consideration of colony-level reproduction in terms of development that Hamilton et al. (2009) call for (see Griesemer 2000).
The remedy, as will be seen, is to recast the units of selection question about colonies in
the context of the individuality thesis. This places the focus on biological questions about
colonies, regardless of their similarity (or not) to organisms.
An advantage of the selection approach to superorganisms is that it clearly frames the
conflict over accounts of selection; the cost is that there is then no account of selection
from which a superorganism concept might be derived except by definition. The question,
then, becomes what is gained from calling such colonies ‘superorganisms’, as opposed to,
say, colonies or individuals.
3
Colonies Are Individuals
I suggest following Hamilton et al. (2009) and treating colonies as individuals, rather than
superorganisms.8 It has the advantages of disentangling a defense of the colony as a unit
of selection from any particular account of selection, while still firmly embedding any such
treatment in biological theory. This generalizes the approach to colonies in a way that
spans across competing accounts of selection, including accounts that jettison fitness, e.g.,
replacing fitness for differential persistence (n.b. Bouchard 2008). The upside is a far more
robust notion of colonies as units of selection.
8
Alternatively, this suggestion might read that we treat superorganisms as a kind of biological individual.
The precise semantic lesson drawn strikes me as less important than the positive thesis described below.
13
The individuality approach adopted by Hamilton et al. preserves the core of the Wilson
and Sober approach, without tightly linking it to any particular account of selection. More
precisely, it leaves open as a research question how such individuals may participate in
evolutionary processes.
3.1
The Individuality Thesis
Michael Ghiselin and David Hull’s individuality thesis, famously, concerned the status
of species (Ghiselin 1966, 1974; Hull 1976, 1978). However, the individuality thesis may
be read as a much more general thesis than this, with the application to species as a
special case. Other applications are possible, e.g., to taxa more generally (Ereshefsky
1991; Baum 1998). However, though widely applied, the individuality thesis is also too
often misconstrued as both stronger and weaker than it actually is. My reading of the
individuality thesis is that it consists of three primary components:9
1. The Parity Thesis
• Species (and other taxa), like organisms, are individuals.
2. The History Thesis
• Biological individuals are defined by ancestry, not possession of intrinsic properties, traits or characters.
• Traits and characters play a diagnostic, not definitional, role in biological individuals.
3. The Part/Whole Thesis
• Biological individuals are concrete (spatio-temporally located) objects, composed of parts (as opposed to members);
• The relevant part/whole relations are biological, not logical.
Each of these has been challenged or misunderstood. Consider, briefly, the parity thesis, a
misreading of which might look like:
1a. The Parity Thesis
• Species are individuals like organisms.
This reading quickly runs into the problem of the paradigm. It encourages evaluating
species-individuality in terms of organism-individuality. Ghiselin and Hull were careful to
distinguish this misreading from the rendering above. Characteristically, Hull is well aware
9
Clearly this reading stands in need of argumentative support. Though the individuality thesis is surely
not in need of reviving, my own view is that it is in need of re-articulation.
14
of the dangers of accepting the view that organisms are paradigm individuals, offering
this cautious characterization (1976, p. 175, emphasis added): “From the point of view of
human perception, organisms are paradigm individuals.” Paradigm, here, is something like
familiar. Of course, much of the remainder of Hull’s argument is spent encouraging us to
try to step away from the point of view familiar to us, and to consider individuality on a
much larger scale of time and space.
The history thesis is intended to capture how taxa are ostensively defined. Though definition by ancestry is not necessarily ostensive, it is how Ghiselin and Hull describe the
assignment of taxa names (in addition to the references above, consider Ghiselin 1984,
1995, and Hull 1984). For the part/whole thesis it will be enough to stress that the relevant part/whole relations are biological, not logical. Of course, there are many logical
wholes that are not biological ones, and left unspecified is what biological relations parts
must stand to each other in order to be considered a biological whole. To address that is
to specify what Haber and Hamilton (2005) call Cohesion Generating Relations, or CGRs.
Haber and Hamilton use this notion to navigate through various debates over what constitutes a particular kind of biological individual, e.g., a species. To argue that some group of
individuals is a species, is to assert that those individuals cohere in some meaningful way
that tracks some particular concept of species. CGRs are a general description of whatever
relations confer cohesion on the parts of a biological whole, and must be specified in any
application of biological individuality. Though the nature of that cohesion will vary on
competing concepts of species (or colonies, or other biological individuals), those concepts
will have specifiable, theoretically motivated accounts of that cohesion.
So though the part/whole thesis clearly has a metaphysical component, a full account includes a biological component as well. Indeed, it is just this specification of CGRs that
generates so much of the controversy over species, e.g., competing species concepts may be
characterized as disagreement over what CGRs satisfy the criteria for grouping organisms
into a species (be it interbreeding relations, genealogical relations, etc.). Likewise, specification of CGRs also underlie colony and organism concepts (Pepper and Herron 2008;
Hamilton et al. 2009; Folse III and Roughgarden 2010; Strassmann and Queller 2010). Notice, though, that the individuality thesis is silent on what CGRs specify some group as an
organism, population, colony, species, etc. Certainly Ghiselin and Hull had views on this,
but these may be kept distinct from the individuality thesis, or treated as an application
of the thesis. Indeed, that’s part of what makes the individuality thesis so powerful—it
serves as a base theoretical framework that gets filled in by appeal to biological facts and
theory. It demands some specification of relevant biological theory. This feature is just
what Hamilton et al. (2009) exploit in their treatment of colonies as individuals.
15
3.2
Colonies Are Individuals
Let’s revisit the Hamilton et al. proposal to treat colonies as individuals in light of the
above discussion. They argue that (p. 577):
All by itself the [individuality] thesis carries no information about the features
of units of selection.
In other words, though the individuality thesis requires a specification of CGRs, it is neutral
with regard to what that specification need be. Specification of CGRs is a hypothesis
about the biology of the kind of individual under scrutiny. It is one reason that systematic
monographs should be read as taxonomic hypotheses.
So within a colony-individual framework what is a good guide for working out these features? We have seen that both the selection and similarity approaches fail to be robust
enough, or fall prey to the problem of the paradigm. Similarity approaches lack a precise
and appropriate target; specifying similarity in terms of functional organization and selection too narrowly focuses on particular accounts of fitness, and may push other biological
processes into the background.
What is needed, instead, is an appeal to appropriate CGRs. Whether colony-level individuals and organism-level individuals will have the same CGRs exhibited is both an empirical
and conceptual question. The conceptual matter concerns an analysis of the central components of selection; the empirical question regards whether different kinds of CGRs may
exhibit individuality. Let’s consider the empirical question first.
Since the publication of Wilson and Sober (1989) there has been a growing appreciation
for the diversity of organismality and individuality across life. In part this appreciation
is due to the success of Wilson and Sober! The relevance here is that individuality, like
other evolved characters, is highly variable across taxa. Just as any account of species
needs to account both for the similarity and variation of the parts of species, the same
holds for accounts of biological individuals, organisms or colonies. A general account of
colony-individuals must allow room to explain both similarities and differences from other
biological individuals. Colonies will be biological individuals by virtue of CGRs between
their parts. Some of these CGRs may also be exhibited by parts of organisms, others
may not. Whatever similarities or differences persist among colonies or (other) organisms
is an empirical question, the results of which will stand in need of explanation in various
biological frameworks (e.g., evolutionary, developmental, ecological, etc.) and serve as data
for other explanations and hypotheses.
Not all organism concepts are without controversy; nor species and colony concepts. Indeed, what will count as legitimate will depend, in part, on what criteria are used to
evaluate these concepts. Here biological theory is needed to fill in the details on which the
individuality thesis remains neutral. On this there is a great deal of dispute over what kind
16
of cohesion unifies parts into wholes that ought to be regarded as biological individuals, be
they organisms, colonies or species. Wilson and Sober (1989) advocate for a functional integration producing greater within-group than between-group fitness; Hamilton (1964a,b)
and Gadau and Laubichler (2006) rely on relatedness; sociality (Queller 2000), alignment
versus exportation of fitness interests (Damuth and Heisler 1988; Okasha 2006; Folse III
and Roughgarden 2010), and formation of Darwinian Populations (Godfrey-Smith 2009)
are other competing accounts informative of how to evaluate CGRs, and when parts, taken
together, ought to be counted as a whole.
Hamilton et al. (2009), like Yang (2007), make the case for considering colonies as individuals in terms of development and reproduction. For Hamilton et al. this is not presented
as an exclusive view of colonies. Instead, like Wilson and Sober, they present this as a competing conceptual framework in order to advocate the utility of applying the individuality
approach to colonies. This perspective permits Wilson and Sober’s treatment of colonies
as units of selection, just as much as it leaves room for Yang’s evo-devo perspective and
other biological accounts.
3.3
Colonies as Organisms
Recently, a new approach to colonies and superorganisms has emerged, describing them
simply as organisms (Martens 2010; Okasha 2011).10 Though superficially similar to the
similarity approaches to superorganisms above, these organismal approaches are not arguments by analogy, but instead treat colonies as real biological individuals that are best
considered as organisms. In many ways, these approaches are very much in line with the
individuality approach taken by Hamilton et al. (2009). It will be helpful to briefly consider these approaches, as they represent various ways forward in our conceptualization of
colonies.
Martens (2010) considers superorganisms to be real individuals, rejecting a metaphorical
treatment of colonies. Martens argues that superorganisms are just a kind of organism,
where organisms are groups exhibiting a division of labor of reproduction, and superorganisms are just organisms whose parts are other multicellular organisms. This distinguishes
them from other organisms, whose parts are cells.11 On Martens’ view, this distinction is
insignificant with regard to the problem of division of labor of reproduction. Though many
details need to be worked out and superorganisms may face unique challenges with regard
to policing relevant divisions of labor, this hardly makes them unique among organisms. Af10
Okasha (2011) identifies this approach as echoing themes found in Queller (2000). He might have
reached back even further and identified Wheeler (1911) as a predecessor.
11
We might extend Martens’ view to include microbes as well. Namely, microbial organisms are those
whose parts exhibit a division of labor of reproduction, where those parts are organelles and other subcellular
structures.
17
ter all, the same may be said for any kind of organism. This approach embodies the parity
thesis commitment of the individuality approach, despite its retention of the term superorganism, by rejecting arguments from analogy and placing an emphasis on how colonies,
as individuals, participate in a broad suite of biological processes. The central role given
to reproduction also helps avoid the narrow focus that dogged selection approaches, as
fleshing out the details of reproduction will require appeal to ecological and developmental
concerns (see, e.g., Griesemer 2000; Oyama et al. 2001; Godfrey-Smith 2009).
Okasha’s (2011) approach also allows room for social insect colonies to be considered superorganisms, but, like Martens’, considers this to simply be a kind of organism. Okasha
departs from Martens’ approach with a slightly more expansive concept of organism, nesting it in a rank-free perspective. Okasha’s innovation is to apply the rank-free approaches
of phylogenetic systematics to major evolutionary transitions, rejecting organism as a rank
of ecological hierarchy, arguing instead that all “all entities in that hierarchy, at all levels
of inclusiveness, are organisms, or at least approximate that status” (p. 59). On Okasha’s
account, ranks in an ecological hierarchy are intended to be exclusive sorts of kinds; an
entity may occupy exactly one rank, and may not be constituted by or be a part of other
entities of that same rank. By adopting a rank-free approach to the ecological hierarchy,
Okasha rejects the view that these criteria may be met by kinds like organism. Instead
we should view organisms much like we do other biological individuals—e.g., as capable of
standing in part-whole relations to each other. In this, Okasha is rejecting, to some extent,
the bright line many have sought to draw between organisms and individuals (e.g. Ghiselin
1974; Hull 1976; Wilson and Sober 1989). He agrees that individuality is much broader
than what has traditionally fallen under the rubric of organism, but rejects traditional
approaches to organism as too narrow.
3.4
Getting Rid of Organisms
Both Martens (2010) and Okasha (2011) are applications of the colonies as individuals
approach. Any disagreements between these approaches and that of Hamilton et al. (2009)
may be traced back to disagreements over how the individuality thesis ought to be applied
or interpreted. But this is fully to be expected, given that the individuality thesis, on its
own, simply does not have the resources to develop a full concept of what eusocial colonies
are. Instead, it simply provides a framework with guidelines on how that framework needs
to be filled in by appeal to biological theory and metaphysical commitments. Hamilton
et al. provide little guidance to that end.
Martens and Okasha extend the notion of organism. However, another approach is available: getting rid of organisms. This is analogous to Mishler’s “Getting rid of species”
(1999), in which he argues that the term species is not merely no longer useful, but downright misleading. Among other things, it encourages equating dissimilar units of cohesion,
18
leading to faulty reasoning about evolutionary hypotheses, e.g., incorrectly tracking relatedness among organisms across populations, and mis-identifying homologies (see Velasco
(2008, 2009) for further discussion of related matters). This is particularly problematic
in systematics, or, more specifically, in how the products of systematics get used by nonsystematists. If species and the distribution of homologies across species are those facts of
evolution in need of explanation, then mistakes conflating kinds of species will be amplified
as the targets of explanation are simply artifacts.
Mishler’s response is to advocate for a particular phylogenetic interpretation of lineages,
and a rejection of the rank species.12 Short of endorsing that, a lesson to be gained is
to simply jettison the term species for whatever it is that species is intended to capture,
e.g., terminal taxa, interbreeding groups, etc. In practice, one could argue, biologists
already do this; the problem is when those various groups are all labeled species and
treated equivalently. This solution has similarities to, though ultimately is distinct from,
Ereshefsky’s (1992) eliminative pluralism. Ereshefsky recommends designating kinds of
species (e.g., ‘phylospecies’ or ‘biospecies’), suggesting doing away with the term species
altogether.
What I am suggesting is something similar for organisms and colonies, thus endorsing the
term superorganism strikes me as moving in the wrong direction. Like Okasha (2011) this
is a rejection of the rank of organism, but goes one step further. Like Mishler (1999) does
with species, it is to recognize that organism is not simply not doing any work, but instead
obfuscating matters. Rather than worrying about whether a particular grouping, be it of
cells, multicellular individuals, or cellular parts, constitutes an organism or not, it is instead
to focus on individuals and features of those individuals. In place of asking whether an
individual is an organism, we instead ask whether that individual is a lineage generating individual. Even this, though, may be too strong. Some individuals do not generate lineages,
per se, but instead persist by way of containing lineage generating individuals (Bouchard
2008).13 This disagreement, though, clearly turns on an interpretation of biological theory, and which kinds of individuals participate in various evolutionary processes. Whether
these individuals are organisms, colonies or superorganisms is less interesting than whether
and how they evolve, are maintained, and may come to be.
12
This does not mean he rejects species grouping criteria, distinguishing, much as Okasha and others,
ranking from grouping.
13
Or it may be that these persistent individuals force us to expand our notion of what counts as a
lineage. I suspect it will be enough to note that these individuals are constituted by lineages, much as other
individuals are.
19
4
Conclusion
So where do we stand? In my introduction I stated that no revival was needed of the
superorganism concept—Wilson and Sober effectively accomplished that. Instead I recommended a refinement. Let’s take a look at how that might work:
In their consideration of the units of selection in modular organisms, Tuomi and Vuorisalo
(1989b, p. 228) characterize selection thusly:
Selection results when individual organisms, due to differences in their phenotypic properties, interact with the environment in such a way that their
reproduction is differential, and as a consequence of this phenotypic selection
genetic units may be differentially propagated to the succeeding generations.
Following the recommendations above, replace organism with individual, and allow for
persistence in addition to reproduction and we get:
Selection results when individuals, due to differences in their phenotypic properties, interact with the environment in such a way that their reproduction
or persistence is differential, and as a consequence of this phenotypic selection genetic units may differentially persist or be propagated to the succeeding
generations.
After all, the upshot of Wilson and Sober (1989) concerns the unit of selection; they are
ultimately arguing that the superorganism ought to be counted as a unit of selection, and
that this stands for a larger point about levels-of-selection more generally. But it is not by
virtue of some functional organization that colonies are sometimes units of selection, it is
the other way around: colonies are functionally organized because they are participating in
evolutionary processes in a particular way. The shape of that functional organization may
vary enormously, and we would be wise to offer an account of individuality that was as
neutral as possible with regard to that. Thus reconstruing Tuomi and Vuorisalo’s (1989b)
characterization of selection with concern for individuals and allowing for persistence provides a much wider base of what sorts of individuals we will discover function as units of
selection, and recognition of a richer diversity of how individuality is expressed, evolved
and maintained.
Like Okasha (2011), Hamilton et al. (2009) recognize the similarity of ‘the colony problem’
to that of higher taxonomic ranks, species and organisms, and suggest a similarly healthy
discussion of colony concepts is likely to ensue. This can be taken one step further, namely,
like taxonomic ranks, organism should also be recognized as being both a rank and a
grouping criterion. Though the former is intended to map onto the latter, the latter
includes more entities than the former typically categorizes—including, following Martens
and Okasha, colonies. And, just as distinguishing rank/group criteria in species and other
20
taxa helped clarify what was a biological from a bookkeeping problem (e.g., Raikow 1986;
O’Hara 1997; de Queiroz 1998; Baum 2009), the same will likely be true of organism.
Namely, a rank-free perspective may extend beyond just the Linnaean ranks, and to the
entirety of the biological hierarchy (Okasha 2011). This is surely preferable to adding
superorganism to the ranks.
Colonies are individuals. Whether they are superorganisms or not turns on (1) what an
organism is, and (2) what it means for an individual to be a unit of selection. Both
approaches to superorganisms are problematic for various reasons, and either distract from
the biology of colonies, or too narrowly focus on a single aspect of that biology. The
individuality approach avoids these problems, and provides a neutral framework from which
to build up a biological account of how colonies evolve, persist, and participate in a variety
of biological processes.
A common thread in the literature on superorganisms and group- and multi-level selection
theory is a demand for consistency across levels of the biological hierarchy. Wilson and
Sober (1989) appeal to this in making the case for groups as units of selection; Martens
(2010) appeals to this to make the case that superorganisms are simply organisms made up
of multicellular organisms, and Okasha (2011) appeals to this in order to reject organism
as a rank, while expanding it as a notion of biological individuality. I find the appeal here
compelling, though my application diverges from these. Just as colonies are best conceived
of as individuals, and not superorganisms, so too are other individuals.
References
Baum, D. A. (1998). Individuality and the existence of species through time. Systematic
Biology, 47(4):641–653.
Baum, D. A. (2009). Species as ranked taxa. Systematic Biology, 58(1):74–86.
Bouchard, F. (2008). Causal processes, fitness, and the differential persistence of lineages.
Philosophy of Science, 75(5):560–570.
Brasier, C. (1992). A champion thallus. Nature, 356(6368):382–383.
Buss, L. (1987). The Evolution of Individuality. Princeton University Press, Princeton,
NJ.
Damuth, J. and Heisler, I. L. (1988). Alternative formulations of multilevel selection.
Biology and Philosophy, 3:407–430.
Danforth, B. (2007). Bees. Current Biology, 17(5):R156–R161.
Danforth, B. N., Sipes, S., Fang, J., and Brady, S. G. (2006). The history of early bee
21
diversification based on five genes plus morphology. Proceedings of the National Academy
of Sciences, 103(41):15118–15123.
Darwin, C. (1964 [1859]). On the Origin of Species. Harvard University Press, Cambridge,
MA, 1st (facsimile) edition.
Dawkins, R. (1976). The Selfish Gene. Oxford University Press.
Dawkins, R. (1982). The Extended Phenotype. Oxford University Press.
de Queiroz, K. (1998). The general lineage concept of species, species criteria, and the
process of speciation. In Howard, D. J. and Berlocher, S. H., editors, Endless Forms:
Species and Speciation, chapter 5, pages 57–75. Oxford University Press.
Dupré, J. (2010). The polygenomic organism. The Sociological Review, 58:19–31.
Dupré, J. and O’Malley, M. A. (2009). Varieties of living things: Life at the intersection
of lineage and metabolism. Philosophy & Theory in Biology, 1:1–25.
Ereshefsky, M. (1991). Species, higher taxa, and the units of evolution. Philosophy of
Science, 58(1):84–101.
Ereshefsky, M. (1992). Eliminative pluralism. Philosophy of Science, 59(4):671–690.
Folse III, H. J. and Roughgarden, J. (2010). What is an individual organism? A multilevel
selection perspective. The Quarterly Review of Biology, 85(4):447–472.
Gadau, J. and Laubichler, M. D. (2006). Relatedness: Capturing cohesion in biological
systems. Biological Theory, 1(4):414–417.
Ghiselin, M. T. (1966). On psychologism in the logic of taxonomic controversies. Systematic
Zoology, 15(3):207–215.
Ghiselin, M. T. (1974). A radical solution to the species problem. Systematic Zoology,
23(4):536–544.
Ghiselin, M. T. (1984). “definition,” “character,” and other equivocal terms. Systematic
Zoology, 33(1):104–110.
Ghiselin, M. T. (1995). Ostensive definitions of the names of species and clades. Biology
and Philosophy, 10:219–222.
Gillooly, J. F., Hou, C., and Kaspari, M. (2010). Eusocial insects as superorganisms.
Communicative & Integrative Biology, 3(4):360–362.
Godfrey-Smith, P. (2009). Darwinian Populations and Natural Selection. Oxford University
Press, Oxford.
22
Goodman, N. (1972). Seven strictures on similarity. In Problems and Projects, chapter IX,
pages 437–446. The Bobbs-Merrill Company, Inc., Indianapolis, IN.
Griesemer, J. (2000). The units of evolutionary transition. Selection, 1(1-3):67–80.
Haber, M. H. and Hamilton, A. (2005). Coherence, consistency, and cohesion: Clade
selection in Okasha and beyond. Philosophy of Science, 72(5):1026–1040.
Hamilton, A., Smith, N. R., and Haber, M. H. (2009). Social insects and the individuality
thesis: Cohesion and the colony as a selectable individual. In Gadau, J. and Fewell, J.,
editors, Organization of Insect Societies, chapter 25, pages 572–589. Harvard University
Press.
Hamilton, W. D. (1964a). The genetical evolution of social behaviour. I. Journal of
Theoretical Biology, 7(1):1–16.
Hamilton, W. D. (1964b). The genetical evolution of social behaviour. II. Journal of
Theoretical Biology, 7(1):17–52.
Herbers, J. M. (2009). Darwin’s ‘one special difficulty’: celebrating Darwin 200. Biology
Letters, 5(2):214–217.
Hou, C., Kaspari, M., Vander Zanden, H. B., and Gillooly, J. F. (2010). Energetic basis
of colonial living in social insects. Proceedings of the National Academy of Sciences,
107(8):3634–3638.
Hull, D. L. (1976). Are species really individuals? Systematic Zoology, 25(2):174–191.
Hull, D. L. (1978). A matter of individuality. Philosophy of Science, 45(3):335–360.
Hull, D. L. (1984). Can Kripke alone save essentialism? A reply to Kitts. Systematic
Zoology, 33(1):110–112.
Huneman, P. and Wolfe, C. T. (2010). Introduction to special issue: The concept of
organism: Historical, philosophical scientific perspectives. History and Philosophy of the
Life Sciences, 32(2-3):147–154.
Janzen, D. H. (1977). What are dandelions and aphids?
111(979):586–589.
The American Naturalist,
Martens, J. (2010). Organisms in evolution. History and Philosophy of the Life Sciences,
32(2-3):373–400.
Maynard Smith, J. (1964). Group selection and kin selection. Nature, 201:1145–1147.
Mayr, E. (1959). Darwin and the evolutionary theory in biology. In Meggers, B. J., editor,
Evolution and Anthropology: A Centennial Appraisal, chapter 1, pages 1–10. Washington
DC: The Anthropological Society ofWashington.
23
Michener, C. D. (1974). The Social Behavior of the Bees: A Comparative Study. Belknap
Press, Cambridge.
Michod, R. E. (1982). The theory of kin selection. Annual Review of Ecology and Systematics, 13(1):23–55.
Mishler, B. D. (1999). Getting rid of species. In Wilson, R. A., editor, Species: New
Interdisciplinary Essays, pages 141–185, Cambridge, MA. MIT Press.
Mitchell, S. and Page, R. E. (1992). Idiosyncratic paradigms and the revival of the superorganism. Technical report, Report NR. 26/92 of the Research Group on Biological
Foundations of Human Culture, Bielefeld, Germany.
Moritz, R. F. and Fuchs, S. (1998). Organization of honeybee colonies: characteristics and
consequences of a superorganism concept. Apidologie, 29:7–21.
O’Hara, R. J. (1997). Population thinking and tree thinking in systematics. Zoologica
Scripta, 26(4):323–329.
Okasha, S. (2006). Evolution and the Levels of Selection. Oxford University Press, Oxford.
Okasha, S. (2011). Biological ontology and hierarchical organization: A defense of rank
freedom. In Calcott, B. and Sterelny, K., editors, The Major Transitions in Evolution
Revisited, Vienna Series in Theoretical Biology, chapter 3, pages 53–64. MIT Press.
Oyama, S., Griffiths, P. E., and Gray, R. D., editors (2001). Cycles of Contingency:
Developmental Systems and Evolution. MIT Press.
Pepper, J. W. and Herron, M. D. (2008). Does biology need an organism concept? Biological Reviews, 83(4):621–627.
Queller, D. C. (2000). Relatedness and the fraternal major transitions. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 355(1403):1647–
1655.
Raikow, R. J. (1986). Why are there so many kinds of passerine birds? Systematic Zoology,
35(2):255–259.
Reeve, H. K. and Hölldobler, B. (2007). The emergence of a superorganism through intergroup competition. Proceedings of the National Academy of Sciences, 104(23):9736–9740.
Santelices, B. (1999). How many kinds of individual are there?
Evolution, 14(4):152–155.
Trends in Ecology &
Smith, M. L., Bruhn, J. N., and Anderson, J. B. (1992). The fungus armillaria bulbosa is
among the largest and oldest living organisms. Nature, 356(6368):428–431.
24
Sober, E. (1980). Evolution, population thinking, and essentialism. Philosophy of Science,
47(3):350–383.
Sober, E. and Wilson, D. S. (1998). Unto Others: The Evolution and Psychology of Unselfish Behavior. Harvard University Press, Cambridge, MA.
Sterelny, K. and Griffiths, P. E. (1999). Sex and Death: An Introduction to Philosophy of
Biology. University of Chicago Press, Chicago, IL.
Strassmann, J. E. and Queller, D. C. (2007). Insect societies as divided organisms: The
complexities of purpose and cross-purpose. Proceedings of the National Academy of
Sciences, 104(Suppl 1):8619–8626.
Strassmann, J. E. and Queller, D. C. (2010). The social organism: Congresses, parties,
and committees. Evolution, 64(3):605–616.
Tuomi, J. and Vuorisalo, T. (1989a). Hierarchical selection in modular organisms. Trends
in Ecology & Evolution, 4(7):209–213.
Tuomi, J. and Vuorisalo, T. (1989b). What are the units of selection in modular organisms?
Oikos, 54(2):227–233.
Turner, J. S. (2000). The Extended Organism. Harvard University Press.
Velasco, J. D. (2008). Species concepts should not conflict with evolutionary history, but
often do. Studies in History and Philosophy of Science Part C: Studies in History and
Philosophy of Biological and Biomedical Sciences, 39(4):407–414.
Velasco, J. D. (2009). When monophyly is not enough: exclusivity as the key to defining
a phylogenetic species concept. Biology and Philosophy, 24(4):473–486.
West, G. B., Brown, J. H., and Enquist, B. J. (1997). A general model for the origin of
allometric scaling laws in biology. Science, 276(5309):122–126.
Wheeler, W. M. (1911). The ant-colony as an organism. Journal of Morphology, 22(2):307–
325.
Wheeler, W. M. (1928). The Social Insects. Harcourt, Brace & Co., New York.
Williams, G. C. (1966). Adaptation and Natural Selection. Princeton University Press,
Princeton.
Wilson, D. S. and Sober, E. (1989). Reviving the superorganism. Journal of Theoretical
Biology, 136(3):337–356.
Wilson, E. O. (1971). The Insect Societies. Belknap Press.
Wilson, E. O. (1975). Sociobiology. Harvard University Press.
25
Wilson, E. O. (1985). The sociogenesis of insect colonies. Science, 228(4707):1489–1495.
Winsor, M. P. (2006). The creation of the essentialism story: An exercise in metahistory.
History and Philosophy of the Life Sciences, 28(2):149–174.
Wynne-Edwards, V. C. (1962). Animal dispersion in relation to social behaviour. Olivery
and Boyd, Edinburgh.
Yang, A. S. (2007). Thinking outside the embryo: The superorganism as a model for
EvoDevo studies. Biological Theory, 2(4):398–408.
26