Units and Levels of Selection (Stanford Encyclopedia of Philosophy)

1. Introduction

When we think of evolutionary theory and natural selection, we usually
think of organisms, say, a herd of deer, in which some deer are faster
than others at escaping their predators. These swifter deer will, all
things being equal, leave more offspring, and these offspring will
have a tendency to be swifter than other deer. Thus, we get a change
in the average swiftness of deer over evolutionary time. In a case
like this, the unit of selection, sometimes called the
“target” of selection, is the single organism, the
individual deer, and the property being selected, swiftness, also lies
at the organismic level, in that it is exhibited by the intact and
whole deer, and not by either parts of deer, such as cells, or groups
of deer, such as herds. But there are other levels of biological
organization that have been proposed to be units or targets of
selection—levels at which selection may act to increase a given
property at that level, and at which units increase or decrease as a
result of selection at that specific level of biological

But for over thirty years, some participants in the “units of
selection” debates have argued that more than one issue is at
stake. The notions of “replicator” and
“vehicle” were introduced, to stand for different roles in
the evolutionary process (Dawkins 1978, 1982a,b). In this case, the
individual deer would be called the “vehicles” and their
genes that make them tend to be swifter would be called the
“replicators.” The genic selection argument proceeded to
assert that the units of selection debates should not be about
vehicles, as it formerly had been, but about replicators. It was then
asserted that the “replicator” actually subsumes two
distinct functional roles, which can be broken up into
“replicator” and “interactor”:

Dawkins…has replicators interacting with their environment in
two ways—to produce copies of themselves and to influence their
own survival and the survival of their copies. (Hull 1980: 318)

The new view would call the individual deer the
“interactors.” It was then argued that the force of this
distinction between replicator and interactor had been
underappreciated, and if the units of selection controversies were
analyzed further, that the question about interactors should more
accurately be called the “levels of selection” debate to
distinguish it from the dispute about replicators, which should be
allowed to keep the “units of selection debate” title
(Brandon 1982; Mitchell 1987).

The purpose of this article is to delineate further the various
questions pursued under the rubric of “units and levels of
Four quite distinct questions will be isolated that have, in fact,
been asked in the context of considering, what is a unit of selection?
section 2,
these distinct questions are described.
Section 3
returns to the sites of several very confusing, occasionally heated
debates about “the” unit of selection. Several leading
positions on the issues are analyzed utilizing the taxonomy of
distinct questions.

This analysis is not meant to resolve any of the conflicts about which
research questions are most worth pursuing; moreover, there is no
attempt to decide which of the questions or combinations of questions
discussed ought to be considered “the” units of selection

2. Four Basic Questions

Four basic questions can be delineated as distinct and separable. As
will be demonstrated in
section 3,
these questions are often used in combination to represent the units
of selection problem. But let us begin by clarifying terms (see Lloyd
1992, 2001). (See the entry on
the biological notion of individual
for more on this topic.)

The term replicator, originally introduced in the 1970s but
since modified by philosophers in the 1980s, is used to refer to any
entity of which copies are made (Dawkins 1976, 1982a,b; Hull 1980; Brandon
1982). Replicators were originally described using two orthogonal
distinctions. A “germ-line” replicator, as distinct from a
“dead-end” replicator, is “the potential ancestor of
an indefinitely long line of descendant replicators” (Dawkins
1982a: 46). For instance, DNA in a chicken’s egg is a germ-line
replicator, whereas that in a chicken’s wing is a dead-end
replicator. Note that DNA are, but chickens are not, replicators,
since the latter do not replicate themselves as wholes. An
“active” replicator is “a replicator that has some
causal influence on its own probability of being propagated,”
whereas a “passive” replicator is never transcribed and
has no phenotypic expression whatsoever (Dawkins 1982a: 47). There is
special interest in active germ-line replicators,
“since adaptations ‘for’ their preservation are
expected to fill the world and to characterize living organisms”
(Dawkins 1982a: 47).

The original terminology of “replicator” was introduced
along with the term “vehicle”, which is defined as

any relatively discrete entity…which houses replicators, and
which can be regarded as a machine programmed to preserve and
propagate the replicators that ride inside it. (Dawkins 1982b: 295)

On this view, most replicators’ phenotypic effects are
represented in vehicles, which are themselves the proximate targets of
natural selection (Dawkins 1982a: 62).

In the introduction of the term “interactor”, it was
observed that the previous theory has replicators interacting with
their environments in two distinct ways: they produce copies of
themselves, and they influence their own survival and the survival of
their copies through the production of secondary products that
ultimately have phenotypic expression (Hull 1980). The term
“interactor” was suggested for the entities that function
in this second process. An interactor denotes that entity which
interacts, as a cohesive whole, directly with its environment in such
a way that replication is differential—in other words, an entity
on which selection acts directly (Hull 1980: 318). The process of
evolution by natural selection is

a process in which the differential extinction and proliferation of
interactors cause the differential perpetuation of the replicators
that produced them. (Hull 1980: 318; see Brandon 1982: 317–318)

One challenge to the term, “interactor,” was that
“interacting is not conspicuous during the process of
elimination that results in natural selection” (Mayr 1997:
2093). It’s difficult to imagine why anyone would say this,
given the original description of the interactor as “an entity
that directly interacts … in such a way that replication is
”. Perhaps more interestingly, the
“target of selection” language is rejected because
selection is seen as more of an elimination process; thus, it would be
misleading to call the “leftovers” of the elimination
process the “targets” of selection. The term
“selecton”, was proposed, which is defined as

a discrete entity and a cohesive whole, an individual or a social
group, the survival and successful reproduction of which is favored by
selection owing to its possession of certain properties. (Mayr 1997:

This seems remarkably similar to an interactor, with the difference
that no differential reproduction, and thus no evolution, is

At the birth of the “interactor” concept, the concept of
“evolvers” was also introduced, which are the entities
that evolve as a result of selection on interactors: these are usually
called lineages (Hull 1980). So far, no one has directly
claimed that evolvers are units of selection. They can be seen,
however, to be playing a role in considering the question of who owns
an adaptation and who benefits from evolution by selection, which we
will consider in sections

2.1 The Interactor Question

In its traditional guise, the interactor question is, what units are
being actively selected in a process of natural selection? As such,
this question is involved in the oldest forms of the units of
selection debates (Darwin 1859 [1964], Haldane 1932, Wright 1945). In
an early review on “units of selection”, the purpose of
the article was claimed as: “to contrast the levels of
selection, especially as regards their efficiency as causers of
evolutionary change” (Lewontin 1970: 7). Similarly, others
assumed that a unit of selection is something that “responds to
selective forces as a unit—whether or not this corresponds to a
spatially localized deme, family, or population” (Slobodkin
& Rapoport 1974: 184).

Questions about interactors focus on the description of the selection
process itself, that is, on the interaction between an entity, that
entity’s traits and environment, and on how this interaction
produces evolution; they do not focus on the outcome of this process
(see Wade 1977; Vrba & Gould 1986). The interaction between some
interactor at a certain level and its environment is assumed to be
mediated by “traits” that affect the interactor’s
expected survival and reproductive success. Here, the interactor is
possibly at any level of biological organization, including a group, a
kin-group, an organism, a gamete, a chromosome, or a gene. Some
portion of the expected fitness of the interactor is directly
correlated with the value of the trait in question. The expected
fitness of the interactor is commonly expressed in terms of genotypic
fitness parameters, that is, in terms of the fitness of combinations
of replicators. Hence, interactor success is most often reflected in
and counted through, replicator success, either through simple
summation of the fitnesses of their traits, or some more complicated
relation. Several methods are available for expressing the correlation
between interactor trait and (genotypic or genic) fitness, including
partial regression, variances, and

In fact, much of the interactor debate has been played out through the
construction of mathematical genetic models—with the exception
of work on group selection and on female-biased sex ratios (Wade 1980,
1985, 2016; D.S. Wilson & Colwell 1981; see especially Griesemer
& Wade 1988). The point of building such models is to determine
what kinds of selection, operating at which levels, may be effective
in producing evolutionary change.

It has been widely held, for instance, that the conditions under which
group selection can effect evolutionary change are quite stringent and
rare. Typically, group selection was seen to require small group size,
low migration rate, and extinction of entire
Some modelers, however, disagree that these stringent conditions are
necessary, and show that in the evolution of altruism by group
selection, very small groups may not be necessary (Matessi &
Jayakar 1976: 384; contra Maynard Smith 1964). Others also
argue that small effective deme size is not a necessary prerequisite
to the operation of group selection (Wade & McCauley 1980: 811).
Similarly, another shows that strong extinction pressure on demes is
not necessary (Boorman 1978: 1909). And finally, there was an early
group selection model that violates all three of the
“necessary” condition usually cited (Uyenoyama 1979; see
Wade 2016).

That different researchers reach such disparate conclusions about the
efficacy of group selection is partly because they are using different
models with different parameter values. Several assumptions, routinely
used in group selection models, were highlighted, that biased the
results of these models against the efficacy of group selection (Wade
1978). For example, many group selection models use a specific
mechanism of migration; it is assumed that the migrating individuals
mix completely, forming a “migrant pool” from which
migrants are assigned to populations randomly. All populations are
assumed to contribute migrants to a common pool from which colonists
are drawn at random. Under this approach, which is used in all models
of group selection prior to 1978, small sample size is needed to get a
large genetic variance between populations (Wade 1978: 110; see
discussion in Okasha 2003, 2006).

If, in contrast, migration occurs by means of large populations,
higher heritability of traits and a more representative sampling of
the parent population will result. Each propagate is made up of
individuals derived from a single population, and there is no mixing
of colonists from the different populations during propagule
formation. On the basis of further analysis, much more
between-population genetic variance can be maintained with the
propagule model (Slatkin and Wade 1978: 3531). Thus, by using
propagule pools as the assumption about colonization, one can greatly
expand the set of parameter values for which group selection can be
effective (Slatkin and Wade 1978, cf. Craig 1982).

Another aspect of this debate that has received a great deal of
consideration concerns the mathematical tools necessary for
identifying when a particular level of biological organization meets
the criteria for being an
Overall, while many of the suggested techniques have had strengths,
no one approach to this aspect of the interactor question has been
generally accepted and indeed it remains the subject of debate in
biological circles (Okasha 2004b,c). Detailed work on two of the major
techniques, the Price equation and contextual analysis, has indicated
that neither approach is universally applicable, on the grounds that
neither provides a proper causal decomposition in all varieties of
selection (Okasha 2006). Specifically, it appears that while
contextual analysis may be superior in most cases of multi-level
selection, the Price equation may be more useful in certain cases of
genic selection (Okasha 2006).

It is important to note that, even in the midst of deciding among the
various methods for representing selection processes, these choices
have consequences for the empirical adequacy of the selection models.
This is true even if the models are denied to have a causal
interpretation, as is done by those promoting a
“statisticalist” interpretation of selection theory
(Walsh, Lewens, & Ariew 2002). On this view, evolution is seen as
a purely statistical phenomenon, and population genetics studies
statistical relations estimated by census, and not causal
relationships. The claim is that the “deeply
uninteresting” units of selection problem has been dissolved,
whereas in fact, it has simply been restricted to the interactor
question (while ignoring the other three “units” questions
entirely); the problem of how to deliver an empirically adequate
selection model is not directly addressed (2002: 470–471).
Instead, an unspecified method is assumed that “identifies
classes [that] … adequately predict and explain changes in the
structure of the population” (Walsh, Lewens, & Ariew 2002:
471), with no acknowledgment that this involves making a commitment to
one or another of the above methods of determining an interactor,
whether under a causal interpretation or not. Thus, the interactor
problem has not been escaped, whether or not it is interpreted
causally (see Otsuka 2016).

Note that the “interactor question” does not involve
attributing adaptations or benefits to the interactors, or indeed, to
any candidate unit of selection. Interaction at a particular level
involves only the presence of a trait at that level with a special
relation to genic or genotypic expected success that is not reducible
to interactions at a lower level. A claim about interaction indicates
only that there is an evolutionarily significant event occurring at
the level in question; it says nothing about the existence of
adaptations at that level. As we shall see, the most common error made
in interpreting many of the interactor-based approaches is that the
presence of an interactor at a level is taken to imply that the
interactor is also a manifestor of an adaptation at that level.

2.2 The Replicator Question

The focus of discussions about replicators concerns just which organic
entities actually meet the definition of replicator. Answering this
question obviously turns on what one takes the definition of
replicator to be. In this connection the revision of the original
meaning of “replicator” turned out to be central. The
revised meaning refined and restricted the meaning of
“replicator,” which was defined as “an entity that
passes on its structure directly in replication” (Hull 1980:
318). The terms replicator and interactor will be
used in this latter sense in the rest of this entry.

The revised definition of replicator corresponds more closely than the
original one to a long-standing debate in genetics about how large or
small a fragment of a genome ought to count as a replicating
unit—something that is copied, and which can be treated
separately in evolutionary theory (see especially Lewontin 1970; Hull
1980). This debate revolves critically around the issue of linkage
disequilibrium and led some biologists to advocate the usage of
parameters referring to the entire genome rather than to allele and
genotypic frequencies in genetical models (Lewontin
The basic point is that with much linkage disequilibrium, individual
genes cannot be considered as replicators because they do not behave
as separate units during reproduction. Although this debate remains
pertinent to the choice of state space of genetical model, it has been
eclipsed by concerns about interactors in evolutionary genetics.

This is not to suggest that the replicator question has been solved.
Work on the replicator question is part of a rich and continuing
research program; it is simply no longer a large part of the units
debates. That this parting of ways took place is largely due to the
fact that evolutionists working on the units problems tacitly adopted
the original suggestion that the replicator, whatever it turned out to
be, be called the “gene” (Dawkins 1982b, pp. 84-86; see
section 3.3).
This move neatly removes the replicator question from consideration.
Exactly why this move should have met with near universal acceptance
is to some extent historical, however the fact that the intellectual
tools (largely mathematical models) of the participants in the units
debates were better suited to dealing with aspects of that debate
other than the replicator question which requires mainly bio-chemical
investigation, surely contributed to this outcome.

There is a very important class of exceptions to this general
abandonment of the replicator question. Developmental Systems Theory
was formulated as a radical alternative to the interactor/replicator
dichotomy (Oyama 1985; Griffiths & Gray 1994, 1997; Oyama,
Griffiths, & Gray 2001). Here the evolving unit is understood to
be the developing system as a whole, privileging neither the
replicator nor the interactor.

There has also been a profound reconception of the evolution by
selection process, which has rejected the role of replicator as
misconceived. In its place the role of “reproducer” is
proposed, which focuses on the material transference of genetic and
other matter from generation to generation (Griesemer 2000a,b; see
Forsdyke 2010; see
section 3.5).
On this approach, thinking in terms of reproducers incorporates
development into heredity and the evolutionary process. It also allows
for both epigenetic and genetic inheritance to be dealt with within
the same framework. The reproducer plays a central role, along with a
hierarchy of interactors, in work on the units of evolutionary
transition (see
Evolutionary Transition;
Griesemer 2000c). This topic concerns the major transitions of life
from one level of complexity to the next, for example, the transition
from unicellularity to multicellularity. More recently, another notion
was introduced of a “reproducer” that is more broadly
inclusive, in that it relaxes the material overlap requirement and
focuses on an understanding of “who came from whom, and roughly
where one begins and another ends” (Godfrey Smith 2009: 86).

These two definitions of “reproducer” disagree about
retroviral reproduction, and what counts as a salient material bond
between generations. On one side is the claim that there is no
material overlap in the case of retroviral reproduction, and that the
key is formal or informational relations (Godfrey-Smith 2009). On the
other side, is a view that sees material overlap due to RNA strand
hybridization guiding and channeling flows of information (Griesemer
2014, 2016). There is also the introduction of a notion of reproducer
that involves only the copying of a property, with no substance
overlapping involved (Nanay 2011). Like the second view of reproducer,
it appeals to the case of retroviruses having no material overlap (cf.
Griesemer 2014, 2016).

2.3 The Beneficiary Question

Who benefits from a process of evolution by selection? There are two
predominant interpretations of this question: Who benefits ultimately
in the long term, from the evolution by selection process? And who
gets the benefit of possessing adaptations as a result of a selection
process? Take the first of these, the issue of the ultimate

There are two obvious answers to this question—two different
ways of characterizing the long-term survivors and beneficiaries of
the evolution by selection process. One might say that the species or
lineages (the previous “evolvers”) are the ultimate
beneficiaries of the evolutionary process. Alternatively, one might
say that the lineages characterized on the genic level, that is, the
surviving alleles, are the relevant long-term beneficiaries. I have
not located any authors holding the first view, but, for Richard
Dawkins, the latter interpretation is the primary fact about
evolution. To arrive at this conclusion, he adds the requirement of
agency to the notion of beneficiary (see Hampe & Morgan 1988). A
beneficiary, by definition, does not simply passively accrue credit in
the long term; it must function as the initiator of a causal pathway
(Dawkins 1982a,b). Under this
definition, the replicator is causally responsible for all of the
various effects that arise further down the biochemical or phenotypic
pathway, irrespective of which entities might reap the long-term
rewards (Sapienza 2010).

A second and quite distinct version of the beneficiary question
involves the notion of adaptation. The evolution by selection process
may be said to “benefit” a particular level of entity
under selection, through producing adaptations at that level (Williams
1966, Maynard Smith 1976, Eldredge 1985, Vrba 1984). On this approach,
the level of entity actively selected (the interactor) benefits from
evolution by selection at that level through its acquisition of

It is crucial to distinguish the question concerning the level at
which adaptations evolve from the question about the identity of the
ultimate beneficiaries of that selection process. One can think that
organisms have adaptations without thinking that organisms are the
“ultimate beneficiaries” of the selection
This sense of “beneficiary” that concerns adaptations
will be treated as a separate issue, discussed in the next

2.4 The Manifestor of Adaptation Question

At what level do adaptations occur? Or, “When a population
evolves by natural selection, what, if anything, is the entity that
does the adapting?” (Sober 1984: 204).

As mentioned previously, the presence of adaptations at a given level
of entity is sometimes taken to be a requirement for something to be a
unit of
Significantly, group selection for “group advantage”
should be distinguished from group selection per se (Wright
1980). In fact, the combination of the interactor question with the
question of what entity had adaptations had created a great deal of
confusion in the units of selection debates in general.

Some, if not most, of this confusion is a result of a very important
but neglected duality in the meaning of “adaptation” (in
spite of useful discussions in Brandon 1978, Burian 1983, Krimbas
1984, Sober 1984). Sometimes “adaptation” is taken to
signify any trait at all that is a direct result of a selection
process at that level. In this view, any trait that arises directly
from a selection process is claimed to be, by definition, an
adaptation (e.g., Sober 1984; Brandon 1985, 1990; Arnold &
Fristrup 1982). Sometimes, on the other hand, the term
“adaptation” is reserved for traits that are “good
for” their owners, that is, those that provide a “better
fit” with the environment, and that intuitively satisfy some
notion of “good
These two meanings of adaptation, the selection-product and
engineering definitions respectively, are distinct, and in
some cases, incompatible.

Consider the peppered moth case: natural selection is acting on the
color of the moths over time, and the population evolves, but no
“engineering” adaptation emerges. Rather, the proportion
of dark moths simply increases over time, relative to the industrial
environmental conditions, a clear case of evolution by natural
selection, on which a good fit to the environment is reinforced. Note
that the dark moths lie within the range of variation of the ancestral
population, they are simply more frequent now, due to their superior
fit with the environment. The dark moths are a
“selection-product” adaptation. Contrast the moth case to
the case of Darwin’s finches, in which different species evolved
distinct beak shapes specially adapted to their diet of particular
seeds and foods (Grant & Grant 1989; Grant 1999). Natural
selection here occurred against constantly changing genetic and
phenotypic backgrounds in which accumulated selection processes had
changed the shapes of the beaks, thus producing
“engineering” adaptations when natural selection occurred.
The finches now possess evolved traits that especially
“fit” them to their environmental demands; their newly
shaped beaks are new mechanisms beyond the original range of variation
in the ancestral population (Lloyd 2015).

Some evolutionary biologists have strongly advocated an engineering
definition of adaptation (e.g., Williams 1966). The basic idea is that
it is possible to have evolutionary change result from direct
selection favoring a trait without having to consider that changed
trait as an adaptation. Consider, for example, Waddington’s
(1956) genetic assimilation experiments. How should we interpret the
results of Waddington’s experiments in which latent genetic
variability was made to express itself phenotypically because of an
environmental pressure (Williams 1966: 70–81; see the lucid
discussion in Sober 1984: 199–201)? The question is whether the
bithorax condition (resulting from direct artificial selection on that
trait) should be seen as an adaptive trait, and the engineering
adaptationist’s answer is that it should not. Instead, the
bithorax condition is seen as “a disruption…of
development,” a failure of the organism to respond (Williams
1966: 75–78). Hence, this analysis drives a wedge between the
notion of a trait that is a direct product of a selection process and
a trait that fits the stronger engineering definition of an adaptation
(see Gould & Lewontin 1979; Sober 1984: 201; cf. Dobzhansky

In sum, when asking whether a given level of entity possesses
adaptations, it is necessary to state not only the level of selection
in question but also which notion of adaptation—either
selection-product or engineering—is being
used. This distinction between the two meanings of adaptation also
turns out to be pivotal in the debates about the efficacy of higher
levels of selection, as we will see in sections

2.5 Summary

In this section, four distinct questions have been described that
appear under the rubric of “the units of selection”
problem, What is the interactor? What is the replicator? What is the
beneficiary? And what entity manifests any adaptations resulting from
evolution by selection? There is a serious ambiguity in the meaning of
“adaptation”; which meaning is in play has had deep
consequences for both the group selection debates and the species
selection debates (Lloyd 2001). Commenting on this analysis, John
Maynard Smith wrote in Evolution:

[Lloyd 2001] argues, correctly I believe, that much of the confusion
has arisen because the same terms have been used with different
meanings by different authors … [but] I fear that the
confusions she mentions will not easily be ended. (Maynard Smith 2001:

section 3,
this taxonomy of questions is used to sort out some of the most
influential positions in five debates: group selection
species selection
genic selection
genic pluralism
as well as units of evolutionary transition

3. An Anatomy of the Debates

3.1 Group Selection

The near-deathblow in the nineteen sixties to group panselectionism
was, oddly enough, about benefit (Williams 1966). The interest was in
cases in which there was selection among groups and the groups as a
whole benefited from organism-level traits (including
behaviors) that seemed disadvantageous to the organism (Wynne Edwards
1962; Williams 1966; Maynard Smith 1964). The argument was that the
presence of a benefit to the group was not sufficient to establish the
presence of group selection. This was demonstrated by showing that a
group benefit was not necessarily a group adaptation (Williams 1966).
Hence, here the term “benefit” was being used to signify
the manifestation of an adaptation at the group level. The assumption
was that a genuine group selection process results in the evolution of
a group-level trait—a real adaptation—that serves a design
purpose for the group. The mere existence however, of traits that
benefit the group is not enough to show that they are adaptations; in
order to be an adaptation, under this view, the trait must be an
engineering adaptation that evolved by natural selection. The
argument was that group benefits do not, in general, exist
because they benefit the group; that is, they do not have the
appropriate causal history (Williams 1966; see Brandon 1981, 1985: 81;
Sober 1984: 262 ff.; Sober & Wilson 1998).

Implicit in this discussion is the assumption that being a unit of
selection at the group level requires two things: (1) having the group
as an interactor, and (2) having a group-level engineering-type
adaptation. That is, the approach taken combines two different
questions, the interactor question and the manifestor-of-adaptation
question, and calls this combined set the unit of selection
question. These requirements for “group selection” make
perfect sense given that the prime target was a view of group
selection that incorporated this same two-pronged definition of a unit
of selection (see Borrello 2010 for a philosophically-oriented history
of Wynne-Edwards and his views on group selection).

This combined requirement of engineering group-level adaptation in
addition to the existence of an interactor at the group level is a
very popular version of the necessary conditions for being a unit of
selection within the group selection debates. For example, it was
claimed that the group selection issue hinges on “whether
entities more inclusive than organisms exhibit adaptations”
(Hull 1980: 325). Another view states that the unit of selection is
determined by “Who or what is best understood as the possessor
and beneficiary of the trait” (Cassidy 1978: 582). Similarly,
paleontological approaches required adaptations for an entity to count
as a unit of selection (Eldredge 1985: 108; Vrba 1983, 1984).

The engineering notion of adaptation was also tied into the version of
the units of selection question in other contexts (Maynard Smith
1976). In an argument separating group and kin selection, it was
concluded that group selection is favored by small group size, low
migration rates, and rapid extinction of groups infected with a
selfish allele and that

the ultimate test of the group selection hypothesis will be whether
populations having these characteristics tend to show
“self-sacrificing” or “prudent” behavior more
commonly than those which do not. (Maynard Smith 1976: 282)

This means that the presence of group selection or the effectiveness
of group selection is to be measured by the existence of nonadaptive
behavior on the part of individual organisms along with the presence
of a corresponding group-level adaptation. Therefore, this approach to
kin and group selection does require a group-level adaptation from
groups to count as units of selection. As with the previous view, it
is significant that the engineering notion of adaptation is
assumed rather than the weaker selection-product notion;

[A]n explanation in terms of group advantage should always be
explicit, and always calls for some justification in terms of the
frequency of group extinction. (Maynard Smith 1976: 278; cf. Wade
1978; Wright 1980)

More recently, geneticists have attempted to make precise the notion
of a group adaptation though the “Formal Darwinism
Project” (Grafen 2008), in which the general concept of
adaptation can be applied to groups (Gardner & Grafen 2009).
However, it is unclear how their notion of adaptation developed within
the formal Darwinism project relates to the previously discussed
engineering notion of adaptation. Philosophers have offered a
different analysis of group adaptation, one based on an earlier
analysis of selection and adaptation (Okasha & Paternotte 2012;
Grafen 2008). The key distinction, in the original view, is between a
trait that is a trait that merely benefits the group, i.e.,
“fortuitous group benefit,” and one that is a genuine
group adaptation, a feature evolved because it benefited the
group, i.e., “for the right reason” (Okasha &
Paternotte 2012: 1137). Contextual analysis, as well as the Price
equation, can provide a formal definition of group adaptation, but
both need to be supplemented by causal reasoning (Okasha &
Paternoster 2012).

In contrast to the preceding approach, we can separate the interactor
and manifestor-of-adaptation questions in our group selection models
(Wright 1980; see Lewontin 1978; Gould & Lewontin 1979). This is
done by distinguishing between what is called “intergroup
selection,” that is, interdemic selection in the shifting
balance process, and “group selection for group advantage”
(Wright 1980: 840; see Wright 1929, 1931). The term
“altruist” originally denoted, in genetics, a phenotype
“that contributes to group advantage at the expense of
disadvantage to itself” (1980: 840; Haldane 1932). This earlier
debate is connected to the main group selection debate in the 1960s,
in which the group selectionists asserted the evolutionary importance
of “group selection for group advantage” (Wright 1980).
The argument is that the primary kin selection model is “very
different” from “group selection for the uniform advantage
of a group”(1980: 841; like Arnold & Fristrup 1982; Damuth
& Heisler 1988; Heisler & Damuth 1987). There are excellent
summaries of the empirical and theoretical discoveries enabled by
“intergroup” selection models (Goodnight & Stevens
1997; Wade 2016).

Those supporting a genic selection view in the 1970s were taken to
task for mistakenly thinking that because they have successfully
criticized group selection for group advantage, they can conclude that
“natural selection is practically wholly genic”(Wright
1980: 841).

[N]one of them discussed group selection for organismic advantage to
individuals, the dynamic factor in the shifting balance process,
although this process, based on irreversible local peak-shifts is not
fragile at all, in contrast with the fairly obvious fragility of group
selection for group advantage, which they considered worthy of
extensive discussion before rejection. (Wright 1980: 841)

This is a fair criticism of the genic selectionist view. The problem
is that these authors failed to distinguish between two questions: the
interactor question and the manifestor-of-adaptation question. The
form of group selection that involves interdemic group selection
models involves groups only as interactors, not as manifestors of
group-level adaptations. More recently, modelers following Sewall
Wright’s interest in structured populations have created a new
set of genetical models that are also called “group
selection” models and in which the questions of group
adaptations and group benefit play little or no

For a period spanning two decades, however, the genic selectionists
did not acknowledge that the position they attacked, namely group
selection as engineering adaptation, is significantly different from
other available approaches to group selection, such as those that
primarily treat groups as interactors. Ultimately, however, genic
selectionists did recognize the significance of the distinction
between the interactor question and the manifestor-of-an-adaptation
question. In 1985, for example, we have progress towards mutual

If some populations of species are doing better than others at
persistence and reproduction, and if such differences are caused in
part by genetic differences, this selection at the population level
must play a role in the evolution of the species,

while concluding that group selection “is unimportant for the
origin and maintenance of adaptation” (Williams 1985:

And in 1987, we have an extraordinary concession:

There has been some semantic confusion about the phrase “group
selection,” for which I may be partly responsible. For me, the
debate about levels of selection was initiated by Wynne-Edwards’
book. He argued that there are group-level adaptations…which
inform individuals of the size of the population so that they can
adjust their breeding for the good of the population. He was clear
that such adaptations could evolve only if populations were
units of selection…. Perhaps unfortunately, he referred to the
process as “group selection.” As a consequence, for me and
for many others who engaged in this debate, the phrase cane to imply
that groups were sufficiently isolated from one another reproductively
to act as units of evolution, and not merely that selection acted on

The importance of this debate lay in the fact that group-adaptationist
thinking was at that time widespread among biologists. It was
therefore important to establish that there is no reason to expect
groups to evolve traits ensuring their own survival unless they are
sufficiently isolated for like to beget like…. When Wilson
(1975) introduced his trait-group model, I was for a long time
bewildered by his wish to treat it as a case of group selection and
doubly so by the fact that his original model…had interesting
results only when the members of the group were genetically related, a
process I had been calling kin selection for ten years. I think that
these semantic difficulties are now largely over. (Maynard Smith 1987:

Even the originator of the replicator/vehicle distinction also seems
to have rediscovered the evolutionary efficacy of higher-level
selection processes in an article on artificial life. In this article,
the primary concern is with modeling the course of selection
processes, and a species-level selection interpretation is offered for
an aggregate species-level trait (Dawkins 1989a). Still, Dawkins seems
not to have recognized the connection between this evolutionary
dynamic and the controversies surrounding group selection because in
his second edition of The Selfish Gene (Dawkins 1989b) he had
yet to accept the distinction made so clearly by group selectionists
in 1980 (Wright 1980). This was in spite of the fact that by 1987, the
importance of distinguishing between evolution by selection processes
and any engineering adaptations produced by these processes had been
acknowledged by the workers he claimed to be following most closely
(Williams 1985, 1992; Maynard Smith 1987). More recently, a related
debate has fired up between genic selection and group selection in the
journals, about the definitions of group and kin selection (E.O.
Wilson 2008; see below). But this debate is bound for nowhere without
tight enough definitions of these kinds of selection (Shavit &
Millstein 2008). The adoption of Wade’s strict definitions would
help, following the prescriptions of early group selectionists (Shavit
& Millstein 2008).

There has been an even more recent challenge to the received
understanding of kin selection, favoring a group selection
interpretation, which has been rebutted by those defending a strict
separation between kin and group selection (Nowak, Tarnita, &
Wilson 2010; Hölldobler & Wilson 2009; rebutted by Gardner,
West. & Wild 2011; Abbot et al. 2011). This view, has in turn,
been rebutted by others (van Veelen et al. 2012; Allen, Nowak, &
Wilson 2013; E.O. Wilson & Nowak 2014). Philosophers have offered
a very useful analysis of these debates about kin and group selection
(Birch & Okasha 2015). The basic prediction of kin selection
theory is that social behavior, especially social behavior that
benefits others, should correlate with genetic relatedness. This is
commonly expressed through Hamilton’s rule, (rb>c), where
r is relatedness, b is the benefit that behavior
offers the conspecific, and c is the cost to the actor (see
Hamilton 1975 for an expansion to multilevel selection). The critics
claiming that kin selection is a form of group selection, assert that
Hamilton’s rule “almost never holds” (Nowak et al. 2010:
That is, it almost never states the true conditions under which a
social behavior will evolve by selection. Their opponents claim the
opposite: that it is incorrect to claim that Hamilton’s rule
requires restrictive assumptions, or that it almost never holds. On
the contrary, they claim, it holds a great deal of the time (Gardner,
West, & Wild 2011).

On a philosophical analysis, there are really three distinct versions
of Hamilton’s rule, and thus three distinct versions of kin
selection theory under discussion. One involves many substantial
assumptions, including

weak selection, additive gene action, (i.e., no dominance or
epistasis), and the additivity of fitness payoffs (i.e., a relatively
simple payoff structure). (Birch & Okasha 2015: 23)

When these assumptions are weakened, we get more variants of
Hamilton’s rule. Particularly important are the payoff
parameters c and b. Sometimes these denote the
values of a particular model, called HRS (Hamilton’s Rule,
special), but other times, they denote averaging effects or partial
regression coefficients, in the case of HRG (Hamilton’s Rule,
general). A third approach, HRA (Hamilton’s Rule, approximate),
which uses first-order approximates of regression coefficients, is the
approach most commonly used in contemporary kin selection theory. The
special version is very restrictive, while the general version allows
a wide variety of cases. According to the philosophical analysis of
the cases, Nowak et al. are using the special version of
Hamilton’s rule when they say it “almost never
holds,” whereas Gardner, West, and Wild are using the
regression-based, general version of the rule, which allows a great
deal of leeway in application. In other words, they are talking past
each other (Birch & Okasha 2015). Significantly,

Neither [Nowak et al. nor Gardner, West, & Wild ] is referring to
HRA, even though this approximate version of the rule is the version
most commonly used by kin selection theorists. (Birch & Okasha
2015: 24)

On the same philosophical analysis, it is also argued that kin
selection and multilevel selection represented using the Price
equation are formally equivalent, and that preferences for kin
selection models may not be justified as they are usually (Birch &
Okasha 2015; cf. West et al. 2008). Some
biologists, for example, have argued that kin selection is more easily
applicable than group selection, and that kin selection can be applied
whenever there is group selection (West, Griffin, & Gardner 2007,
2008). Moreover, they deny that kin selection is a form of group
selection, despite formal similarities and derivations (West, Griffin,
& Gardner 2007: 424). Problems about using multilevel selection
models may stem from the group beneficiary problem arising from the
early group selection context wherein group selection was assumed to
involve both group benefit and group engineering adaptation (Birch
& Okasha 2015).

[A]lthough kin and multilevel selection are equivalent as statistical
decompositions of evolutionary change, there are situations in which
one approach provides a more accurate representation of the causal
structure of social interaction. (Birch & Okasha 2015: 30; see
also Okasha & Paternotte 2012 vs. Gardner & Grafen 2009 on
group adaptations)

Geneticists have offered an effective critique of the “Formal
Darwinism Project” to units of selection and adaptation, arguing
that the latter’s preferences for the level of individual
organism is arbitrary, as is their bias against multilevel selection
(Shelton & Michod 2014a).

In an analysis of the contextual analysis and Price equation methods
of representing hierarchical selection models, it was argued that
contextual analysis is superior overall, except in cases of meiotic
drive (Okasha 2006). However, it was recently argued that contextual
analysis can even handle cases of meiotic drive, thus making it the
superior approach to multilevel selection (Earnshaw 2015). In a
separate and helpful analysis, the relationship between kin and
multilevel models was spelled out using causal graphs (Okasha 2015).
Just because the two models can produce the same changes in gene
frequencies, it does not follow that they represent the same causal
structure, which is illustrated using causal graph theory and examples
from biology, such as group adaptation and meiotic drive (Okasha 2015;
Genic Selection: The Pluralists).
This goes very much against the claims of equivalence of the two
model types, kin and group selection (West, Griffin, & Gardner
2007, 2008; West & Gardner 2013), in which these technical
equivalences are taken to signify total equivalence of the
evolutionary systems (see also Frank 2013; Queller 1992; Dugatkin
& Reeve 1994; Sober & Wilson 1998). Take, for instance, the
claim: “There is no theoretical or empirical example of group
selection that cannot be explained with kin selection” (West,
Griffin, & Gardner 2008: 375),

It is good to keep in mind that there are dissenters from this claim
of the equivalence between group and kin selection models (e.g.,
Lloyd, Lewontin, & Feldman 2008; van Veelen 2009; van Veelen et
al. 2012; Hölldobler & Wilson 2009; Traulsen 2010; Nowak,
Tarnita, & Wilson 2010, 2011; E.O. Wilson 2012). Those who claim
full equivalence discuss the evolution of cooperation and altruism,
arguing that only kin selection allows an easy solution to these
evolutionary problems (West, Griffin, & Gardner 2008). From the
more robust group selectionist point of view, the so-called free rider
problems with kin and group selection—such as those that are
contemplated by evolutionists puzzling over the evolution of
altruism—are pseudo-problems based on misconceptions (Wade 2016;
see also Bowles & Gintis 2011; Planer 2015; Sterelny 2012).

One approach notes that kin selection (either in its inclusive fitness
form or the direct fitness approach) and multilevel selection
“differ primarily in the types of questions being
addressed” (Goodnight 2013: 1546). Whereas kin selection aims at identifying
character states that maximize fitness, multilevel selection methods
have the goal of looking at the effects of selection on trait changes.
While the two have formal similarities, the kin selection models arose
out of game theory and evolutionary stable strategies (ESS) and are
used to identify the optimal solution, but they cannot be used to
examine the process by which the population will achieve that
optimum or equilibrium. In contrast, the multilevel selection methods,
such as contextual analysis, which arise out of the quantitative
genetics traditions, are used to describe the processes acting on the
population in its current
Thus, the two methods are not the same, nor are they competing

Rather they should be considered complementary approaches that when
used together give a clearer picture of social evolution than either
one can when used in isolation. (Goodnight 2013: 1547; cf. Maynard Smith
1976; Dawkins 1982b; West, Griffin, & Garnder 2007, 2008; Gardner
& Grafen 2009)

In the laboratory, the hierarchical genetic approach of multilevel
selection has been used to demonstrate that populations respond
rapidly to experimentally imposed group selection, and that indirect
genetic effects are primarily responsible for the surprising strength
and effectiveness of group selection experiments, contra the
full equivalence claims (Goodnight 2013; Goodnight & Stevens 1997; cf. West, Griffin,
& Gardner 2007, 2008). Field studies using contextual analysis
have shown that multilevel selection is far more common in nature than
previously expected (Goodnight 2013; e.g., Stevens, Goodnight, & Kalisz 1995;Tsuji 1995; Aspi et al. 2003; Weinig et al. 2007; Eldakar et al. 2010;
Wade 2016). There is much less emphasis on the evolution of altruism
within the hierarchical genetic approach, as selection is observed as
it is occurring, and this includes group selection going in the same
direction as organismic selection, not just in opposition to it,
contra early genic selectionist recommendations (Maynard
Smith 1976). This sort of group selection of interactors is not based
on group level engineering adaptations, although some still persist in
confusing group selection itself with the combination of the two
features, group selection and group engineering adaptation (e.g.,
Ramsey & Brandon 2011).

Most recently, a new topic has arisen in the context of multilevel
selection, involving the evolution of “holobionts,” i.e.,
the combination of a eukaryotic organism with its microbiotic load
(Zilber-Rosenberg & Rosenberg 2008). It has become clear that each
“individual” human being is actually a community of
organisms co-evolved for mutual benefit (Gilbert, Sapp, & Tauber
2012). Our microbiota (the collection of bacteria, viruses, and fungi
living in our gut, mouth, and skin) is necessary for our survival and
development, and our species is also needed in turn for their
survival. Bacterial symbionts help induce and sustain the human immune
system, T-cells, and B-cells (Lee & Mazamanian 2010; Round,
O’Connell, & Mazamanian 2010), as well as providing
essential vitamins to the host human being. Gut bacteria are necessary
for cognitive development (Sampson & Mazamanian 2015), as well as
for the development of blood vessels in the gut; lipid metabolism,
detoxification of dangerous bacteria, viruses, and fungi; and the
regulation of colonic pH and intestinal permeability (Nicholson et al.

The holobiont—the combination of the host and its
microbiota—functions as a unique biological entity anatomically,
metabolically, immunologically, and developmentally (Gilbert,
Rosenberg, & Zilber-Rosenberg forthcoming; Gilbert 2011). Similarly, a
holobiont is seen as an “integrated community of species,
[which] becomes a unit of natural selection” (Gilbert, Sapp,
& Tauber 2012: 334). That is, in essence, theorists claim that the
holobiont can function as an interactor since it has features that
bind it together as a functional whole in such a way that it can
interact in a natural selection process. So what ties the different
species together to produce an interactor? According to pioneering
philosophical thought on holobionts and symbionts, it is the
community’s common evolutionary fate, its being a
“functioning whole,” that characterizes it as an
evolutionary interactor, “objects between which natural
selection selects” (Dupré 2012: 160; see also
Dupré & O’Malley 2013; Zilber-Rosenberg &
Rosenberg 2008). This community can also be described as a
“team” of consortia undergoing selection (Gilbert et al.
forthcoming). Others describe
them as “collaborators” or “polygenomic
consortia”, which has the advantage of encompassing both
competition and cooperation within the holobiont (Dupré &
O’Malley 2013: 314; Lloyd forthcoming; see also Huttegger & Smead 2011 on stag
hunt game-theoretic results regarding the range of collaboration).

Holobionts can also be reproducers, where the host usually reproduces
vertically and the microbiota reproduce either vertically,
horizontally, or both. This situation has provoked discussion among
philosophers (Godfrey-Smith 2009, 2011; Sterelny 2011; Griesemer 2014,
2016; Booth 2014; Lloyd
forthcoming). Holobionts’ microbiota can reproduce
outside the context of the original host organism, so some holobionts,
e.g., the Hawaiian bobtail squid and its luminescent bacteria, are not
“Darwinian populations” (Godfrey-Smith 2009, 2011), and
therefore not units of selection (see Booth 2014). This approach
contrasts with that of the original reproducer approach which would
include the squid-bacteria system and also retroviruses excluded under
the “Darwinian populations” account (Griesemer2000a,

As in [my book, Darwinian Populations and Natural Selection],
I hold that it is a mistake to see things that do not reproduce as
units of selection. (Godfrey-Smith 2011: 509; Booth 2014)

This exclusion rests on the merging of the interactor with the
reproducer requirements, and as such will not hold sway over those who
do not buy such a confounding of roles (e.g., Dupré &
O’Malley 2013). This is yet another case wherein distinguishing
the interactor question from the replicator/reproducer question can be
“more illuminating” (Sterelny 2011: 496; see Dupré
& O’Malley 2013; Gilbert, Sapp, & Tauber 2012; Lloyd forthcoming).

Finally, holobionts can also be manifestors of adaptations, as in the
case of the evolution of placental mammals in the acquisition by
horizontal gene transfer from a retrovirus of a crucial gene coding
for the protein syncytin (Lloyd forthcoming; Dupressoir, Lavialle, & Heidemann
2012). Syncytin allows fetuses to fuse to their mother’s
placenta, a role crucial to the evolution of placental mammals.
Moreover, it seems that several retrovirally derived enhancers played
critical roles in the formation of a key cell in the uterine wall,
also crucial for maintaining pregnancy, enhancing the
holobiont’s role as a manifestor of adaptation (Wagner et al.

There are several other significant entries into the group selection
discussions, including the book, Unto Others: The Evolution and
Psychology of Unselfish Behavior
(Sober & Wilson 1998). Here,
a case for group selection is developed based on the need to account
for the existence of biological altruism. Biological altruism is any
behaviour that benefits another organism at some cost to the actor.
Such behavior must always reduce the actor’s fitness but it may
(following the work on interdemic selection), increase the fitness of
certain groups within a structured population. There was a big benefit
to bringing the attention of the larger philosophical community to
group selection models, and explaining them in an accessible fashion.
It has thus brought this aspect of the units of selection controversy
out onto the main stage of philosophical thought.

The “Darwinian populations” view previously mentioned
provides a considerably different view of the necessary conditions for
group selection, one which rejects many of the currently accepted
cases of the phenomenon. For a given selection story to be
descriptively valid, a “Darwinian population” must exist
at the level of selection being described, which requires the presence
of both an interactor and a reproducer at that level, thus putting
together what others have pulled apart (Godfrey-Smith 2009: 112). A
Darwinian population is conceived as, at minimum,

a collection of causally connected individual things in which there is
variation in character, which leads to differences in reproductive
output (differences in how much or how quickly individuals reproduce),
and which is inherited to some extent. (2009: 39)

There are further differentiations between paradigmatic, minimal, and
marginal Darwinian populations based on a variety of criteria, such as
the fidelity of heritability, continuity (the degree to which small
shifts in phenotype correlate to small changes in fitness), and the
dependence of reproductive differences on intrinsic features of
individuals (Godfrey-Smith 2009: Chapter 3).

For example, under this view, the case of the evolution of altruism,
which is commonly attributed to group selection, should not be
considered as such, because of the lack of a true reproducer at the
group level; the group level description depicts at best a marginal
Darwinian population (Godfrey-Smith 2009: 119). Rather, the argument
is that a neighborhood selection model, in which individuals are
affected by the phenotypes of their neighbors but cannot be seen as
“collectives competing at a higher level,” is fully
capable of capturing the selective process involved, and represents a
Darwinian population, in which the individuals are seen both as the
interactors and the reproducers (2009: 118). This would seem to entail
that many group selection accounts (e.g., Sober & Wilson 1998), as
well as any models classified as Multi-level selection 1 (MLS1) models
(Heisler & Damuth 1987), cannot be properly considered as such.
This view grants that there are empirical examples in which a
group-level reproducer clearly exists (for example, Wade &
Griesemer 1998; Griesemer & Wade 2000; there is otherwise no
discussion of Wrightian approaches to group selection). The approach
using Darwinian populations and reproducers is claimed to present an
advantage over other available analyses of units of selection because
it can account for previously neglected examples such as epigenetic
inheritance systems (Godfrey-Smith 2009). The question remains as to
whether gaining an account to deal with these is worth rejecting an
entire class of accepted group selection models, and whether such a
loss is truly necessary to deal with epigenesis, given that we have an
epigenetic account with reproducers that allows for group selection
(see Griesemer 2000c).

3.2 Species Selection

Ambiguities about the definition of a unit of selection have also
snarled the debate about selection processes at the species level. One
response to the notion of species selection comes with a classic
confusion: “It is individual selection discriminating against
the individuals of the losing species that causes the
extinction” (Mayr 1997: 2093). The individual death of species
members is confused with extinction: “the actual selection takes
place at the level of competing individuals of the two species”
(Mayr 1997: 2093). Once we overcome such difficulties, and succeed in
conceiving of species as unified interactors, we are still faced with
two questions. The combining of the interactor question and the
manifestor-of-adaptation question (in the engineering sense) led to
the rejection of research aimed at considering the role of species as
interactors, simpliciter, in evolution. Once it is understood
that species-level interactors may or may not possess design-type
adaptations, it becomes possible to distinguish two research
questions: Do species function as interactors, playing an active and
significant role in evolution by selection? And does the evolution of
species-level interactors produce species-level engineering
adaptations and, if so, how often?

For the early history of the species selection debate, these questions
were lumped together; asking whether species could be units of
selection meant asking whether they fulfilled both the
interactor and manifestor-of-adaptation roles. For example, early
species selection advocates used a genic selectionist treatment of the
evolution of altruism as a touchstone in the definition of species
selection (e.g., Vrba 1984). The relevant argument is that kin
selection could cause the spread of altruistic genes but that it
should not be called group selection (Maynard Smith 1976). Again, this
was because the groups were not considered to possess design-type
adaptations themselves. Some species selectionists agreed that the
spread of altruism should not be considered a case of group selection
because “there is no group adaptation involved; altruism is not
emergent at the group level” (Vrba 1984: 319; Maynard Smith
gives different reasons for his rejection). This amounts to assuming
that there must be group benefit in the sense of a design-type
group-level adaptation in order to say that group selection can occur.
This species selection view was that evolution by selection is not
happening at a given level unless there is a benefit or engineering
adaptation at that level. The early species selection position
explicitly equates units of selection with the existence of an
interactor plus adaptation at that level (Vrba 1983: 388);
furthermore, it seems that the stronger, engineering definition of
adaptation had been adopted.

It was generally accepted among early species selectionists that
species selection does not happen unless there are species-level
adaptations (Eldredge 1985: 196, 134). Certain cases are rejected as
higher-level selection processes overall because

frequencies of the properties of lower-level individuals which are
part of a high-level individual simply do not make convincing
higher-level adaptations. (Eldredge 1985: 133)

Most of those defending species selection early on defined a unit of
selection as requiring an emergent, adaptive property (Vrba 1983,
1984; Vrba and Eldredge 1984; Vrba and Gould 1986). This amounts to
asking a combination of the interactor and manifestor of adaptation
questions. But the relevant question is not “whether some
particle-level causal processes or other
bear the causal
responsibility,” but rather “whether particle-level
selection bears the causal responsibility” (Okasha
2006: 107). An emergent character requirement conflates these two
questions. Such a character may be the result of a selection process
at the group/species level, but it should not be treated as a
pre-condition of such a process.

But consider the lineage-wide trait of variability. Treating species
as interactors has a long tradition (Dobzhansky 1956, Thoday 1953,
Lewontin 1958). If species are conceived as interactors (and not
necessarily manifestors-of-adaptations), then the notion of species
selection is not vulnerable to the original antigroup-selection
objections from the early genic selectionists (Williams
The old idea was that lineages with certain properties of being able
to respond to environmental stresses would be selected for, and thus
that the trait of variability itself would be selected for and would
spread in the population of populations. In other words, lineages were
treated as interactors. The earlier researchers spoke loosely of
adaptations where adaptations were treated in the weak sense as
equivalent simply to the outcome of selection processes (at any
level). They were explicitly not concerned with the effect of
species selection on organismic level traits but with the effect on
species-level characters such as speciation rates, lineage-level
survival, and extinction rates of species. Some argued, including the
present author, that this sort of case represents a perfectly good
form of species selection, using so-called “emergent
fitnesses,” even though some balk at the thought that
variability would then be considered, under a weak definition, a
species-level adaptation (Lloyd & Gould 1993; Lloyd 1988 [1994]).
Paleontologists used this approach to species selection in their
research on fossil gastropods (Jablonski 2008, 1987; Jablonski & Hunt 2006), and the approach has also been used in
the leading text on speciation (Coyne & Orr 2004).

Early species selectionists also eventually recognized the advantages
of keeping the interactor question separate from a requirement for an
engineering-type adaptation, dropping the former requirement that, in
order for species to be units of selection, they must possess
species-level adaptations (Vrba 1989). Ultimately, the current
widely-accepted definition of species selection is in conformity with
a simple interactor interpretation of a unit of selection (Vrba 1989;
see Damuth & Heisler 1988; Lloyd 1988 [1994]; Jablonski 2008).

It is easy to see how the two-pronged definition of a unit of
selection—as interactor and manifestor-of-adaptation—held
sway for so long in the species selection debates. After all, it had
dominated much of the group selection debates for so long. Some of the
confusion and conflict over higher-level units of selection arose
because of an historical contingency—the early group
selectionist’s implicit definition of a unit of selection and
the responses it provoked (Wynne Edwards 1962 ; Borrello 2010).

3.3 Genic Selection: The Originators

One may understandably think that the early genic selectionists were
interested in the replicator question because of the claims that the
unit of selection ought to be the replicator. This would be a mistake.
Rather, the primary interest is in a specific ontological issue about
benefit (Dawkins 1976, 1982a,b). This amounts to asking a special version of the beneficiary
question, and the answer to that question dictates the answers to the
other three questions flying under the rubric of the “units of

Briefly, the argument is that because replicators are the only
entities that “survive” the evolutionary process, they
must be the beneficiaries (Dawkins 1982a,b). What happens in the
process of evolution by natural selection happens for their
, for their benefit. Hence, interactors interact for the
replicators’ benefit, and adaptations belong to the replicators.
Replicators are the only entities with real agency as initiators of
causal chains that lead to the phenotypes; hence, they accrue the
credit and are the real units of selection.

This version of the units of selection question amounts to a
combination of the beneficiary question plus the
manifestor-of-adaptation question. There is little evidence that they
are answering the predominant interactor question; rather, the
argument is that people who focus on interactors are laboring under a
misunderstanding of evolutionary theory (Dawkins 1976, 1982a,b). One reason for
thinking this might be that the opponents are taken to be those who
hold a combination of the interactor plus manifestor-of-adaptations
definition of a unit of selection (e.g., Wynne-Edwards).
Unfortunately, leading genic selectionists ignore those who are
pursuing the interactor question alone; these researchers are not
vulnerable to the criticisms posed against the combined
interactor-adaptation view (Dawkins 1982a,b; Williams 1966). Some
insist that the early genic selectionists have misunderstood
evolutionary selection, an argument that is based upon interpreting
the units of selection controversy as a debate about interactors
(Gould 1977; Istvan 2013); however, because the early genic
selectionists’ say that the debate concerns the units of the
ultimate beneficiary, they are arguing past one another (Istvan 2013).
Section 3.4, Genic Selection: The Pluralists,
addresses those who interpret themselves as arguing against the
interactor question itself.

In the next few paragraphs, two aspects of Dawkins’ specific
version of the units of selection problem shall be characterized. I
will attempt to clarify the key issues of interest to Dawkins and to
relate these to the issues of interest to others.

There are two mistakes that Dawkins is not making. First, he
does not deny that interactors are involved in the evolutionary
process. He emphasizes that it is not necessary, under his view, to
believe that replicators are directly “visible” to
selection forces (1982b: 176). Dawkins has recognized from the
beginning that his question is completely distinct from the interactor
question. He remarks, in fact, that the debate about group versus
organismic selection is “a factual dispute about the level at
which selection is most effective in nature,” whereas his own
point is “about what we ought to mean when we talk about a unit
of selection” (1982a: 46). He also states that genes or other
replicators do not “literally face the cutting edge of natural
selection. It is their phenotypic effects that are the proximal
subjects of selection” (1982a: 47). We shall return to this
issue in
section 3.4, Genic Selection: The Pluralists.

Second, Dawkins does not specify how large a chunk of the genome he
will allow as a replicator; there is no commitment to the notion that
single exons are the only possible replicators. He argues that if
Lewontin, Franklin, Slatkin and others are right, his view will not be
affected (see
If linkage disequilibrium is very strong, then the “effective
replicator will be a very large chunk of DNA” (Dawkins 1982b:
89; Sapienza 2010). We can conclude from this that Dawkins is not
interested in the replicator question at all; his claim here is that
his framework can accommodate any of its possible answers.

On what basis, then, does Dawkins reject the question about
interactors? I think the answer lies in the particular question in
which he is most interested, namely, What is “the nature of the
entity for whose benefit adaptations may be said to

On the face of it, it is certainly conceivable that one might identify
the beneficiary of the adaptations as—in some cases,
anyway—the individual organism or group that exhibits the
phenotypic trait taken to be the adaptation. In fact, some writers
seem to have done just that in the discussion of group selection (see
But the original genic selectionist rejects this move, introducing an
additional qualification to be fulfilled by a unit of
selection; it must be “the unit that actually survives or fails
to survive” (Dawkins 1982a: 60). Because organisms, groups, and
even genomes do not actually survive the evolution-by-selection
process, the answer to the survival question must be the replicator.
(Strictly speaking, this is false; it is copies of the replicators
that survive. Replicators must therefore be taken in some sense of
information and not as biological entities (see Hampe & Morgan
1988; cf. Griesemer 2005).

But there is still a problem. Although the conclusion is that
“there should be no controversy over replicators versus
vehicles. Replicator survival and vehicle selection are two aspects of
the same process” (1982a: 60), the genic selectionist does not
just leave the vehicle selection debate alone. Instead, the argument
is that we do not need the concept of discrete vehicles at all. This
is what we shall investigate in
section 3.4 Genic Selection: The Pluralists.

The important point for now is that, on Dawkins’ analysis, the
fact that replicators are the only survivors of the
evolution-by-selection process automatically answers also the question
of who owns the adaptations. Adaptations must be seen as being
designed for the good of the active-germ-line replicator for the
simple reason that replicators are the only entities around long
enough to enjoy them over the course of natural selection. The genic
selectionist acknowledges that the phenotype is “the all
important instrument of replicator preservation,” and that
genes’ phenotypic effects are organized into organisms (that
thereby might benefit from them in their lifetimes) (1982b: 114). But
because only the active germ-line replicators survive, they are the
true locus of adaptations (1982b: 113; emphasis added). The
other things that benefit over the short term (e.g., organisms with
adaptive traits) are merely the tools of the real survivors, the real
owners. Hence, Dawkins rejects the vehicle approach partly because he
identifies it with the manifestor of adaptation approach, which he has
answered by definition, in terms of the long-term beneficiary.

The second key aspect of genic selectionists’ views on
interactors is the desire to do away with them entirely. Dawkins is
aware that the vehicle concept is “fundamental to the
predominant orthodox approach to natural selection” (1982b:
116). Nevertheless, he rejects this approach in The Extended
, claiming, “the main purpose of this book is to
draw attention to the weaknesses of the whole vehicle concept”
(1982b: 115). But this “vehicle” approach is not
equivalent to “the interactor question”; it encompasses a
much more restricted approach.

In particular, when arguing against “the vehicle concept,”
Dawkins is only arguing against the desirability of seeing the
individual organism as the one and only possible vehicle. His target
is explicitly those who hold what he calls the “Central
Theorem,” which says that individual organisms should be
seen as maximizing their own inclusive fitness
(1982b: 5, 55).
These arguments are indeed damaging to the Central theorem, but they
are ineffective against other approaches that define units of
selection as interactors.

One way to interpret the Central Theorem is that it implies that the
individual organism is always the beneficiary of any selection
process. The genic selectionists seem to mean by
“beneficiary” both the manifestor of adaptation and that
which survives to reap the rewards of the evolutionary process.
Dawkins argues, rightly and persuasively, I think, that it does not
make sense always to consider the individual organism to be the
beneficiary of a selection process.

But it is crucial to see that Dawkins is not arguing against the
importance of the interactor question in general, but rather against a
particular definition of a unit of selection. The view being
criticized assumes that the individual organism is the interactor,
and the beneficiary, and the manifestor of
adaptation. Consider the main argument against the utility of
considering vehicles: the primary reason to abandon thinking about
vehicles is that it confuses people (1982b: 189). But look at the
examples; their point is that it is inappropriate always to ask how an
organism’s behavior benefits that organism’s inclusive
fitness. We should ask instead, “whose inclusive fitness the
behavior is benefiting” (1982b: 80). Dawkins states that his
purpose in the book is to show that “theoretical dangers attend
the assumption that adaptations are for the good of…the
individual organism” (1982b: 91).

So, Dawkins is quite clear about what he means by the “vehicle
selection approach”; it always assumes that the organism is the
beneficiary of its accrued inclusive fitness. Dawkins advances
powerful arguments against the assumption that the organism is always
the interactor cum beneficiary cum manifestor of adaptations. This
approach is clearly not equivalent to the approach to units of
selection characterized as the interactor approach. Unfortunately,
genic selectionists extend Dawkins’ conclusions to these other
approaches, which he has, in fact, not addressed. The genic
selectionists’ lack of consideration of the interactor
definition of a unit of selection leads to two grave problems with
this view.

One problem is the tendency to interpret all group selectionist claims
as being about beneficiaries and manifestors of adaptations as well as
interactors. This is a serious misreading of authors who are pursuing
the interactor question alone.

Consider, for example, this argument that groups should not be
considered units of selection:

To the extent that active germ-line replicators benefit from the
survival of the group of individuals in which they sit, over and above
the [effects of individual traits and altruism], we may expect to see
adaptations for the preservation of the group. But all these
adaptations will exist, fundamentally, through differential replicator
survival. The basic beneficiary of any adaptation is the active
germ-line replicator (Dawkins 1982b: 85).

Notice that this argument begins by admitting that groups can function
as interactors, and even that group selection may effectively produce
group-level adaptations. The argument that groups should not be
considered real units of selection amounts to the claim that the
groups are not the ultimate beneficiaries. To counteract the intuition
that the groups do, of course, benefit, in some sense, from the
adaptations, the terms “fundamentally” and
“basic” are used, thus signaling what the author considers
the most important level. Even if a group-level trait is affecting a
change in gene frequencies, “it is still genes that are regarded
as the replicators which actually survive (or fail to survive) as a
consequence of the (vehicle) selection process” (Dawkins 1982b:
115). Thus, the replicator is the unit of selection, because it is the
beneficiary, and the real owner of all adaptations that exist.

Saying all this does not, however, address the fact that other
researchers investigating group selection are asking the interactor
question and sometimes also the manifestor of adaptation question,
rather than Dawkins’ special version of the (ultimate)
beneficiary question. He gives no additional reason to reject these
other questions as legitimate; he simply reasserts the superiority of
his own preferred unit of selection. In sum, Dawkins has identified
three criteria as necessary for something to be a unit of selection:
it must be a replicator; it must be the most basic beneficiary of the
selection process; and it is automatically the ultimate manifestor of
adaptation through being the beneficiary.

Finally, further work in the philosophy of biology brings the level of
the unit of selection down even further than the original genic
selectionists do (Rosenberg 2006). Higher level selection is reducible
to more fundamental
Taking a reductionist stance, which is taken to be necessary to avoid
an “untenable dualism” in biology between physicalism and
antireductionism, the argument is that the principle of natural
selection (PNS) should be properly viewed as a basic law of physical
science (specifically chemistry), which can operate at the level of
atoms and molecules (Rosenberg 2006: 189–191). Different
molecular environments would favor different chemical types, and those
that “more closely approximate an environmentally optimal
combination of stability and replication,” are thus the
“fittest” and would predominate (2006: 190). This could
then be applied at each step of the way from simple molecules to
compounds, organelles, cells, tissues, and so on, such that

the result at each level of chemical aggregation is the instantiation
of another PNS, grounded in, or at least in principle derivable from,
the molecular interactions that follow the PNS in the environment
operating at one or more lower levels of aggregation. (Rosenberg 2006:

This approach addresses antireductionist arguments regarding group
level properties. The claim is that this new envisioning of the PNS as
a purely physical law allows us to better understand the lower level
origins of apparently higher level causes, thus revealing that
“the appearance of ‘downward causation’ is just
that: mere appearance.” (Rosenberg 2006: 197) For example, the
claim is that group level selection explanations, such as are commonly
given for altruism, do not require an antireductionist stance, since
physical laws, such as that second law of thermodynamics, can allow
for local unfavorable changes (in this case, local decreases in
entropy) as long as compensation is made elsewhere. With regard to the
physical PNS,

groups of biological individuals may experience fitness increases at
the expense of fitness decreases among their individual members for
periods of time that will depend on the size and composition of the
group and the fitness effects of their traits. What the PNS will not
permit is long-term fitness changes at the level of groups without
long-term fitness changes in the same direction among some or all of
the individuals composing them. (Rosenberg 2006: 198)

In other words, this is supposed to show that there is no need to
think in terms of irreducible group level interactors. Again, note
that this analysis merges characteristics of interactors and

In the next section, we will consider some relatively more recent work
in which genic selectionism is defended through a pluralist approach
to modeling. What matters in the final analysis, though, is exactly
what matters to the original genic selectionists, and that is the
search for the ultimate beneficiary of the evolution by selection

3.4 Genic Selection: The Pluralists

As we saw in the previous section, the original genic selectionists
had particular problems with their treatment of the interactor. While
they admitted that the “vehicle” was necessary for the
selection process, they did not want to accord it any weight in the
units of selection debate because it was not the beneficiary, but
rather an agent of the beneficiary. Soon, however, there emerged a new
angle available to genic selectionists (Waters

The new “genic pluralism” appears to let one bypass the
interactor question, by, in effect, turning genes into interactors
(Sterelny & Kitcher 1988). The proposal is that there are two
“images” of natural selection, one in which selection
accounts are given in terms of a hierarchy of entities and their
traits’ environments, the other of which is given in terms of
genes having properties that affect their abilities to leave
copies of themselves (Sterelny & Kitcher 1988; see Kitcher,
Sterelny, & Waters 1990, Sterelny 1996a,b; Waters 1986,
Something significant follows from the fact that hierarchical models
or selection processes can be reformulated in terms of the genic
level. These claims have been resisted on a variety of grounds (see
objections in R.A. Wilson 2003, Stanford 2001, Van der Steen & van
den Berg 1999, Gannett 1999, Shanahan 1997, Glennan 2002, Sober 1990,
Sober & Wilson 1998, Brandon & Nijhout 2006, Sarkar 2008).

The big payoff of the genic point of view is:

Once the possibility of many, equally adequate, representations of
evolutionary processes has been recognized, philosophers and
biologists can turn their attention to more serious projects than that
of quibbling about the real unit of selection. (Kitcher, Sterelny,
& Waters 1990: 161)

By “quibbling about the real unit of selection,” here, the
authors seem to be referring to the large range of articles in which
evolutionists have tried to give concrete evidence and requirements
for something to serve as an interactor in a selection process.

As an aside, it is important to note that none of the philosophers are
advocating genic selectionism to the exclusion of other views. What
interests them is a proposed equivalence between being able to tell
the selection story one way, in terms of interactors and replicators,
and to tell the same story another way, purely in terms of
“genic agency”. Thus, they are pluralists, in that they
are not ultimately arguing in favor of the genic view; they are,
however, expanding the genic selectionist view beyond its previous

The pluralists attack the view that “for any selection process,
there is a uniquely correct identification of the operative selective
forces and the level at which each impinges” (Waters 1991: 553).
Rather, they claim, “We believe that asking about the real unit
of selection is an exercise in muddled metaphysics” (Kitcher,
Sterelny, & Waters 1990: 159). The basic view is that “the
causes of one and the same selection process can be correctly
described at different levels” (including the genic one) (Waters
1991: 555). Moreover, these descriptions are on equal ontological
footing. Equal, that is, except for when Sterelny and Kitcher slip over into a
genuinely reductionist genic view, when they state that it is an error
to claim

that selection processes must be described in a particular way, and
their error involves them in positing entities, “targets of
selection,” that do not exist. (1988: 359)

Here they seem to be denying the existence of interactors altogether.
If interactors don’t exist, then clearly a genic level account
of the phenomena would be preferable to, not merely equivalent to, a
hierarchical view.

The pluralists do seem to be arguing against the utility of the notion
of the interactor in studying the selection process. Echoing the
original genic selectionists, their idea is that the whole causal
story can be told at the level of genes, and that no higher level
entities need be proposed or considered in order to have an accurate
and complete explanation of the selection process. But, arguably, the
genic level story cannot be told without taking the functional role of
interactors into account, and thus the pluralists cannot avoid
quibbling about interactors, as they claim (see Lloyd 2005). Nor is
the genic account adequate to all selection cases; the genic account
fails when drift is factored in (Brandon & Nijhout 2006).

Let us recall what the interactor question in the units of selection
debate amounts to: What levels of entities interact with their
environments through their traits in such a way that it makes a
difference to replicator success? As mentioned before, there has been
much discussion in the literature about how to delineate and locate
interactors among multilayered processes of selection. Each of these
suggestions leads to slightly different results and different problems
and limitations, but each also takes the notion of the interactor
seriously as a necessary component to understanding a selection

The genic pluralists state that “All selective episodes (or,
perhaps, almost all) can be interpreted in terms of genic selection.
That is an important fact about natural selection” (Kitcher,
Sterelny, & Waters 1990: 160). Thus, the functional claim of the
pluralists is that anything that a hierarchical selection model can
do, a genic selection model can do just as well. Much attention is
paid to showing that the two types of models can represent certain
patterns of selection equally well, even those that are conventionally
considered hierarchical selection. This is argued for using both
specific examples and schema for translating hierarchical models into
genic ones. Let us consider one challenging case here.

Take the classic account of the efficacy of interdemic or group
selection, the case that even G.C. Williams acknowledged was
hierarchical selection. Lewontin and Dunn (Lewontin & Dunn 1960
and Lewontin 1962), in investigating the house mouse, found first,
that there was segregation distortion, in that over 80% of the sperm
from mice heterozygous for the t-allele also carried the t-allele,
whereas the expected rate would be 50%. Second, they also found that
male homozygotes (those with two t-alleles) tended to be sterile (in
several populations they were lethal, but in the populations in
question, they were sterile.) Third, they also found a substantial
effect of group extinction based on the fact that female mice would
often find themselves in groups in which all males were sterile, and
the group itself would therefore go extinct. This, then, is how a
genuine and empirically robust hierarchical model was developed.

What the pluralists want to note about this case is very narrow, that

whether there are real examples of processes that can be modeled as
group selection can be asked and answered entirely within the
point of view. (Kitcher, Sterelny, & Waters 1990: 160)

Just as a warning to the unwary, the key to understanding the genic
reinterpretation of this case is to grasp that the pluralists use a
concept of genetic environment that their critics ignore.

The pluralists tell how to “construct” a genic model of
the causes responsible for the frequency of the t-allele. We must
first distinguish

genetic environments that are contained within female mice that are
trapped in small populations with only sterile males from genetic
environments that are not contained within such females. In effect,
the interactions at the group level would be built in as a part of one
kind of genetic environment. (Waters 1991: 563)

In other words, various very detailed environments would have to be
specified for various different t-alleles and wild-type alleles. In
order to determine the invariant fitness parameter of a specific
allele, let’s call it “A” for example, we would need
to know what kind of environment it is in at the allelic level, e.g.,
whether it is paired with a t-allele. Then we would need to know a
further detailed layer of the environment of “A”, such as
what the sex is of the “environment” it is in. If it is in
a t-allele arrangement, and it is also in a male environment, the
allelic fitness of “A” would be changed. Finally, we need
to know the type of subpopulation or deme the “A” allele
is in. Is it in a small deme with many t-alleles? Then it is more
likely to become extinct. So, as we can see, various aspects of the
allele’s environment are built up from the gene out, depending
on what would make a difference to the gene’s fitness in that
very particular kind of environment. If you want to know the overall
fitness of the “A” allele, you add up the fitnesses in
each set of specialized, detailed environments and weight them
according to the frequency of that environment.

The idea is:

What appears as a multiple level selection process (e.g., selection of
the t-allele) to those who draw the conceptual divide [between
environments] at the traditional level, appears to genic selectionists
of Williams’s style as several selection processes being carried
out at the same level within different genetic environments. (Waters
1991: 571)

The “same level” here means the “genic level,”
while the genetic environments include everything from the other
allele at the locus, to whether the genotype is present in a male or
female mouse, to the size and composition of the deme the mouse is in.
This completes the sketch of the genic pluralist position. We now turn
to its reception.

Genic pluralism’s impact has been largely philosophic rather
than biological (but see Shanahan 1997 and Van der Steen & Van den
Berg 1999). Within philosophy, the view has been widely disseminated
and taught, and a steady stream of critical responses to the genic
pluralist position has been forthcoming. These responses fall into two
main categories: pragmatic and causal.

The pragmatic response to genic pluralism simply notes that in any
given selective scenario the genic perspective provides no information
that is not also available from the hierarchical point of view. This
state of affairs is taken by critics of this type as sufficient reason
to prefer whichever perspective is most useful for solving the
problems facing a particular researcher (Glymour 1999; Van der Steen
& Van den Berg 1999; and Shanahan 1997). The weakness of this
approach as a critique of genic pluralism is that it does not so much
criticize genic pluralism as simply ignore it.

The other major form of critique of genic pluralism is based on
arguments concerning the causal structure of selective episodes. The
idea here is that while genic pluralism gets the “genetic
book-keeping” (i.e., the input/output relations) correct, it
does not accurately reflect the causal processes that bring about the
result in question (Wimsatt 1980a,b). Some examples of this approach used against the
genic pluralists (including Sober 1990; Sober & Wilson 1994,
1998), also appeal to aspects of the manifestor of adaptations and
beneficiary questions to establish the failure of genic pluralism to
represent certain selective events correctly. Causal concerns are also
raised in some other work (Shanahan 1997, Van der Steen and Van den
Berg 1999, Stanford 2001, and Glennan 2002), though without the focus
on other units questions. The weakness of this line of criticism is
its inability to isolate a notion of cause that is both plausible and
plausibly true of hierarchical but not genic level models. This
feature—that the genic and hierarchical models are so similar as
to be indistinguishable—which appears as an insurmountable
problem in the context of debates about differing causal structure,
turns out to be the locus of critical response to genic pluralism,
which denies that the genic selectionists have any distinct and
coherent genic level causes at all (Lloyd 2005; Lloyd et al.

Genic pluralism presents alleles as independent causal entities, with
the claim that the availability of such models makes hierarchical
selection models—and the ensuing debates about how to identify
interactors in selection processes—moot. Or, in a less
contentious version of the argument, the hierarchical and genic models
are fully developed causal alternatives (Waters 1991). However, in
each case of the causal allelic models, these models are directly and
completely derived from precisely the hierarchical models the authors
reject. Moreover, causal claims made on behalf of alleles are utterly
dependent on hierarchically identified and established interactors
as causes, thus undermining their claims that the units of
selection (interactor) debates are mere “quibbles” and are
irrelevant to the representation of selection processes. Moreover, and
contrary to the claims of pluralists, cases of frequency-dependence,
such as in heterosis and in game-theoretic models of selection,
necessitate selection at higher than genic levels because the relevant
properties of the entities at the genic level are only definable
relative to higher levels of organization. Thus, they cannot be
properly described as properties of alleles nor are they “even
definable at the allelic level.” (Sarkar 2008: 219) In addition,
when drift is taken into account, the genic accounts fail to be
empirically adequate (Brandon & Nijhout 2006).

We can say that the allelic level models are completely derivative
from higher level models of selection processes using the following
guidelines (Lloyd 2005). Two models that are mathematically equivalent
may be semantically different, that is, they have different
interpretations. Such models can be independent from one another or
one may be derivative of the other. In the genic selection case, the
pluralists appear to be claiming that the genic level models are
independent from the hierarchical models. The claim is: although the
genic models are mathematically equivalent, they have different
parameters, and a different interpretation, and they are completely
independent from hierarchical models.

But, despite the pluralists’ repeated claims, we can see from
their own calculations and examples that theirs are
derivative models, and thus, that their “genic”
level causes are derivative from and dependent on higher level causes.
Their genic level models depend for their empirical, causal, and
explanatory adequacy on entire mathematical structures taken from the
hierarchical models and refashioned.

As reviewed above, one example from their own writing comes from the
treatment of the t-allele case, a universally recognized case of three
levels of selection operating simultaneously on a single allele. Right
before the t-allele case, a suggestion is offered that a
Williams’s type analysis could be based on an application of
Lloyd’s additivity criterion for identifying
interactors, which is strictly hierarchical (Waters 1991:
563; Lloyd [1988] 1994: Ch. 5). Thus, the pluralist suggestion is to
borrow a method for identifying potential higher-level interactors in
order to determine the genic environments and thus to have more
adequate genic level models. Similarly, other pluralists resort to a
traditional approach to identifying interactors in order to make their
genic models work. It had earlier been proposed that the statistical
idea of screening off be used to identify which levels of entities are
causally effective in the selection process; i.e., it is a method used
to isolate interactors (Brandon 1982). But some pluralists propose
using screening off to identify layers of allelic environments, and
also show how Sober’s probabilistic causal account could be used
for a genic account (Sterelny & Kitcher 1988: 354).

Hence, the pluralists all use the same methods for isolating relevant
genic-level environments as others do for the traditional isolating of
interactors. What, we may ask, is the real difference? Both can be
seen as attempting to get the causal influences on selection right,
because they are using the same methods. What is different is that the
genic selectionists want to tell the causal story in terms of genes
and not in terms of interactors and genes. Moreover, they propose
doing away with interactors altogether, by renaming them the
genic-level environments. Are we to think that renaming changes the
metaphysics of the situation?

It seems that levels of interaction important to the outcome of the
selection process are being discovered in the usual ways, i.e., by
using approaches to interactors and their environments, and that that
exact same information is being translated into talk of the
differentiated and layered environments of the genes.

The issue concerning renaming model structures is especially confusing
in the genic pluralists presentations, because they repeatedly rely on
an assumption or intuition that, given an allelic state space, we are
dealing with allelic causes. This last assumption is easily traced
back to the original genic selectionist views that alleles are the
ultimate beneficiaries of any long term selection process (Williams
1966; Dawkins 1982a,b); thus, the genic pluralist argument rests
substantially on a view regarding the superior importance of the
beneficiary question, which has been clearly delineated from the
interactor question, above.

Let us summarize the consequences of derivativeness in terms of the
science and metaphysics of the processes discussed. First, the genic
pluralists end up offering not, as they claim, a variety of genuinely
diverse causal versions of the selection process at different levels.
This is because the causes of the hierarchical models, however
determined, are simply transformed and renamed in the lower level
models, but remain fully intact as relevant causes at the full range
of higher and lower levels. More importantly, no new allelic causes
are introduced. Second, while genic models may be derived from
hierarchical models, they fail to sustain the necessary supporting
methodology. Third, the lack of genuine alternative causal accounts
destroys the claims of pluralism or, at least, of any interesting
philosophical variety, since there are no genuine alternatives being
presented, unless you count renaming model structures as
metaphysically significant (see also Okasha
Thus, the picture of proposing an alternative
“interactor” at the genic level is not fulfilled (vs.
Sterelny & Kitcher 1988). Perhaps the best way to save the
pluralist vision is to appeal to the work on neighbor selection
(Godfrey-Smith 2008),
which can be cast within a pluralist program. This effort is to revive
and discuss an alternative fashion of modeling altruism or group
benefit, within the terms of a lower, individual level (see the
discussion in
section 3.1, Genic Selection: The Originators).

There is a further complication with respect to the nature of the
genic selection models put forward by genic pluralists. These models
function under the presupposition that they are at least
mathematically equivalent to hierarchical models. This claim has
largely depended on the work of Dugatkin and Reeve in establishing
this equivalence (Dugatkin & Reeve 1994, Sterelny 1996b, Sober
& Wilson 1998, Sterelny & Griffiths 1999, Kerr &
Godfrey-Smith 2002a, Waters 2005). However, foundational work has
indicated that this equivalence does not in fact hold. In Dugatkin and
Reeve and the rest of this literature, comparison of population
genetic models was largely based on predictions of allele frequency
changes; in other words, if two models made the same predictions as to
the changes of allelic frequencies in a given situation, then the
models are equivalent. However, this is an overly simplistic method
for testing model equivalence which pays little mind to the details of
the models themselves. When the notion of representational adequacy of
the models is taken into account, specifically through the inclusion
of parametric and dynamical sufficiency as important points of
comparison, this equivalence between genic and hierarchical models
disappears (Lloyd, Lewontin, & Feldman 2008; Lewontin 1974; see
group selection
for more on formal equivalence).

Parametric sufficiency concerns what state space and variables are
sufficient to capture the relevant properties of a given system, while
dynamical sufficiency

concerns what state space and variables are sufficient to describe the
evolution of a system given the parameters being used in the specific
system. (Lloyd, Lewontin, & Feldman 2008: 146; Lewontin 1974)

Utilizing these concepts allows for a more detailed and meaningful
evaluation of a given mathematical model. And under such an analysis,
the claims regarding the equivalency of genic and hierarchical models
cannot be sustained. Since allelic parameters and the changes in
allelic frequencies depend on genotypic fitnesses, the genic models
claimed to be equivalent to the hierarchical models are neither
parametrically nor dynamically

3.5 Units of Evolutionary Transition

In our preceding discussions of units of selection, we have restricted
ourselves to situations in which the various units were
pre-established entities. Our approach has been synchronic, one in
which the relevant units, be they genes, organisms, or populations,
are the same both before and after a given evolutionary process.
However, not all evolutionary processes may be able to be captured
under such a perspective. In particular, recent discussions regarding
so-called “evolutionary transitions” present a unique
complication to the debates over units and levels of selection.

Evolutionary transition is “the process that creates
new levels of biological organization” (Griesemer 2000c:
69), such as the origins of chromosomes,
multicellularity, eukaryotes, and social groups (Maynard-Smith and
Szathmáry 1995: 6–7). These transitions all share a
common feature, namely that “entities that were capable of
independent replication before the transition can replicate only as
part of a larger whole after it” (Maynard-Smith and
Szathmáry 1995: 6).

Evolutionary transitions create new potential levels and units of
selection by creating new kinds of entities that can have variances in
fitness. Thus, it is the “project of a theory of evolutionary
transition to explain the evolutionary origin of entities with such
capacities” (Griesemer 2000c: 70). However, since such cases involve the evolutionary
of a given level of selection, traditional synchronic
approaches to units and levels of selection, which assume the
pre-existence of a “hierarchy of entities that are
potential candidates for units of selection”, may be
insufficient, since it is the evolution of those very properties that
allow entities to serve as, for example, interactors or replicators
that is being addressed (Griesemer 2000c: 70). Such a task requires a
diachronic perspective, one under which the properties of our
currently extant units of selection cannot be presupposed.

…[A]s long as evolutionary theory concerns the function of
contemporary units at fixed levels of the biological
hierarchy…, the functionalist approach may be adequate to its
intended task. However, if a philosophy of units is to address
problems going beyond this scope—for example to problems of
evolutionary transition,… then a different approach is
needed. (Griesemer 2003: 174)

The “reproducer” concept (discussed in
section 2.2),
which incorporates the notion of development into the treatment of
units and levels of selection, is a step toward meeting the goal of
addressing such evolutionary transitions, and

the dependency of formerly independent replicators on the
“replication” of the wholes—the basis for the
definition of evolutionary transition … is a
developmental dependency that should be incorporated into the
analysis of units. (2000c: 75)

Those adopting the reproducer concept argue that thinking in broader
terms of reproducers avoids the presupposition of evolved coding
mechanisms implicit to the concept of replicators. In the case of
evolutionary transitions, this allows us to separate the basic
development involved in the origin of a new biological level from the
later evolution of sophisticated developmental mechanisms for the
“stabilization and maintenance of a new level of
reproduction” (Griesemer 2000c: 77).

Explaining evolutionary transitions in Darwinian terms poses a
particular challenge: “Why was it advantageous for the
lower-level units to sacrifice their individuality and form themselves
into a corporate body?” (Okasha 2006: 218). On one analysis,
three stages of such a transition, each defined in terms of the
connection between fitness at the level of the collective and the
individual fitness of its component particles, are identified (Okasha
2006: 238). Initially, collective fitness is simply defined as average
particle fitness. As fitness at the two levels begins to be decoupled,
collective fitness remains proportional to average particle fitness,
but is not defined by it; at such a stage, “the emerging
collective lacks ‘individuality’, and has no
collective-level functions of its own” (Okasha 2006: 237).
Finally, collective fitness “starts to depend on the
functionality of the collective itself” (Okasha 2006:
237–8; see Okasha 2015 for a representation of this in terms of
causal graphs).

On this analysis, the different stages of an evolutionary transition
involve different conceptions of multi-level selection (Okasha 2006,
2015). Using the distinction defended by Lorraine Heisler and John
Damuth (Heisler & Damuth 1987; Damuth & Heisler 1988) in their
“contextual analysis” of units of selection, this analysis
claims that early on in the process of an evolutionary transition,
multi-level selection 1 (MLS1), in which the particles themselves are
the “‘focal’ units” upon which selection
directly acts, applies. However, by the end of the transition, both
the collectives and the particles are focal units of selection
processes, with independent fitnesses, a case of Damuth and
Heisler’s multi-level selection 2 (MLS2) (Okasha 2006: 4). An
easy way to capture this distinction is that, under MLS1, the lower
level particles are the interactors as well as the replicators, while
in MLS2, both the upper level collectives as well as the particles are
interactors. Thus, the issues surrounding evolutionary transitions
involve both the interactor question and the replicator question.
Understanding evolutionary transitions hence provides additional
significance to Damuth and Heisler’s distinction:

Rather than simply describing selection processes of different sorts,
which should be kept separate in the interests of conceptual clarity,
MLS1 and MLS2 represent different temporal stages of an
evolutionary transition. (Okasha 2006: 239)

On a different approach, evolutionary transitions are seen as the
appearance of a “new kind of Darwinian population”, of
“new entities that can enter into Darwinian processes in their
own right” (Godfrey-Smith 2009: 122). These transitions involve
a “de-Darwinizing” of the lower-level entities such that

an initial collective has come to engage in definite high-level
reproduction, and this has involved the curtailing of independent
evolution at the lower level. (Godfrey-Smith 2009: 124)

This can be accomplished in a variety of ways, such as through the
bottleneck caused by the production of new collectives from single
individuals, coupled with germ-line segregation (as in the transitions
to multicellularity), or by a single member of the collective
preventing all other members from reproducing (for example, among
eusocial insects), or by single member having primary but not total
control over the other constituents (as in the evolution of
eukaryotes) (Godfrey-Smith 2009: 123–124).

These processes all involve restrictions on the ability of the
lower-level entities to function as interactors and replicators, and
the emergence of upper-level collectives as both interactors and
replicators. The degree to which lower-level entities are thus
restricted can vary. For example, somatic cells are still capable of
bearing individual fitness, of outcompeting neighboring cells, and of
producing more progeny. Thus, they are not yet
“post-populational”; they “retain crucial Darwinian
features in their own right” (Godfrey-Smith 2009: 126). However,
they are dependent on the germ-line cells for the propagation of new
collectives, and thus their ability to act as replicators is
necessarily curtailed. Thus, in order to prevent subversion and
encourage cooperation, such a transition requires both the
generation of benefit” and the
alignment of reproductive interests
(Godfrey-Smith 2009: 124, with terminology from Calcott 2008; see
Booth’s 2014 analysis of heterokaryotic Fungi using
Godfrey-Smith’s approach). For example, in the case of
multicellularity, the latter can be accomplished by “close
kinship within the collective” (Godfrey-Smith 2009: 124).

In a useful analysis of the volvocine algae, other hierarchical
selectionists use optimality modeling at the group level to search for
a group level adaptation, in aid of modeling evolutionary transitions
(Shelton & Michod 2014b). They look for selection and adaptation
at the higher level in their model of transition, which contrasts
other views that look only for selection at the higher level, but not
for engineering adaptations. The emphasis is on the distinction
between fortuitous group benefit and real group adaptation. In places,
however, they seem to embrace the product-of-selection definition of
group adaptation, even though they are committed to denying its
applicability (2014b: 454). Their point is to decompose levels of
selection and adaptation using a model organism to get evolutionary
emergency of levels, i.e., evolutionary transition.

Thus, there are a variety of philosophical approaches to analyzing
evolutionary transition on offer, whether in terms of reproducers,
multilevel selection, or Darwinian populations. The essential
diachronic nature of the problem poses a unique challenge, and
involves not just the interactor and replicator (or reproducer)
questions, but also the questions of who is the beneficiary of the
selection process, and how that new level emerges.

4. Conclusion

It makes no sense to treat different answers as competitors if they
are answering different questions. We have reviewed a framework of
four questions with which the debates appearing under the rubric of
“units of selection” can be classified and clarified. The
original discussants of the units of selection problem separated the
classic question about the level of selection or interaction (the
interactor question) from the issue of how large a chunk of the genome
functions as a replicating unit (the replicator question). The
interactor question should also be separated from the question of
which entity should be seen as acquiring adaptations as a result of
the selection process (the manifestor of adaptation question). In
addition, there is a crucial ambiguity in the meaning of adaptation
that is routinely ignored in these debates: adaptation as a selection
product and adaptation as an engineering design. Finally, we can
distinguish the issue of the entity that ultimately benefits from the
selection process (the beneficiary question) from the other three

This set of distinctions has been used to analyze leading points of
view about the units of selection and to clarify precisely the
question or combination of questions with which each of the
protagonists is concerned. There are many points in the debates in
which misunderstandings may be avoided by a precise characterization
of which of the units of selection questions is being addressed.

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