## 1. The Classical Problem of Fitness


 

The leading idea of Darwin's theory of natural selection is
often expressed in terms first coined by Herbert Spencer as the claim
that among competing organisms the fittest survive (1864, 144). If
there is random variation among the traits of organisms, and if some
variant traits fortuitously confer advantages on the organisms that
bear them, i.e., enhance their fitness, then those organisms will live
to have more offspring, which in turn will bear the advantageous
traits. Whence descent with adaptive modification, i.e.,
evolution. Evolution by random heritable variation and natural
selection will explain ever increasing adaptation to given
environments, increasing diversity in the occupation of new
environments, and the complexity of organisms and their parts as their
lineages adapt to one another and to their environments.




But what is fitness and how can one tell when a trait enhances
fitness, or more to the point, when one organism is fitter than
another? Opponents of the theory of natural selection have long
claimed that the theory is so treated by its proponents as to define
fitness in terms of rates of reproduction, thus condemning the
principle of the survival of the fittest to triviality: the claim that
those organisms with higher rates of reproduction leave more offspring
is an empty, unfalsifiable tautology bereft of explanatory power. In
the century and a half since the publication of *On the Origin of
Species* biologists have all too often reinforced this objection
by actually so defining fitness. For example, C.H. Waddington writes,
in *Towards a Theoretical Biology* (1968, 19), that the fittest
individuals are those that are "most effective in leaving
gametes to the next generation." It appears therefore that
evolutionary theory requires a definition of fitness that will protect
it from the charges of tautology, triviality, unfalsifiabilty, and
consequent explanatory infirmity. If no such definition is in fact
forthcoming, then what is required by the theory's adherents is
an alternative account of its structure and content or its role in the
research program of biology.


## 2. Ecological Fitness


 

In an intuitive sense, 'fitness' can refer to the
correspondence between the shape of an object and an empty volume it is
placed in: a square peg fits into a square hole. In a more abstract
fashion, one might refer to the properties of an entity and how they
correspond to the constraints of its context. In a biological setting
one could focus on an organism's traits and how they correspond
to various aspects of the environment the organism is living
in. Following biological usage, call this concept 'ecological
fitness'. (It has also been called 'vernacular
fitness,' cf. Matthen and Ariew 2002.) The
'vernacular' definition is fraught with
difficulties. Suppose, following Dennett (1995) we characterize the
relation '\(x\) is fitter than \(y\)' as follows:



>  
> 
> \(x\) is fitter than \(y\) if and only if \(x\)'s
> traits enable it to solve the 'design problems' set by the
> environment more fully than \(y\)'s traits do.




One may ask, What are these design problems? How many of them are
there? Is there any way of measuring the degree to which \(x\)
exceeds \(y\) in their solution? Answers to these questions
simply reinforce the threat of tautology that faces the theory. To
begin with the notion of "design problems" is vague and
metaphorical; or, if treated literally, design problems will all be
relative to the overarching objective of leaving more
descendants. Thus the definition may simply hide the original problem
of distinguishing fitness from reproductive rates, instead of solving
it.




Second, the number of design problems is equal to the number of
distinct environmental features that affect survival, and of course
reproduction, and this number is probably uncountable. Accordingly,
prima facie, the proposed definition provides no hope of cardinal or
even ordinal measurement that would enable us to predict or explain
quantitatively differences in rates of reproduction, and the
evolutionary processes that depend on these rates. Moreover,
ecological fitness accounts may not have provided a satisfactory story
about how to carve up the relevant reference environment that is
supposed to have an impact on the survival of said organisms (Abrams
2009). It is no wonder that biologists, sensible of the importance of
predictive precision and explanatory testability, have had little
truck with ecological fitness and have defined '\(x\) is
fitter than \(y\)' in terms of quantitatively measurable
reproductive rates. This tendency of course simply adds force to the
original argument. If the only way to make fitness differences
scientifically tractable is to trivialize the theory, so much the
worse for the theory.


## 3. Individual versus Trait Fitness


 

Some philosophers (notably Sober, 2013) have argued that
evolutionary fitness is a property of populations and not of
individual organisms, or alternatively that fitness is a property of
traits and not of the individuals that possess them. Individual
fitness values are, they argue, empirically inaccessible and
predictively useless. If trait fitness is defined in terms of the
average fitness value of individuals bearing the trait, then it will
turn out that there are individual fitnesses and individual fitness
differences, even if it is the case that evolutionary
biologists' interests are confined to trait fitnesses. This
claim has been challenged (cf. Pence and Ramsey 2014): sometimes
biologists estimate trait fitnesses by studying individual fitnesses
(Endler 1986).


 

It has also been held that trait fitness and fitness difference are
both something more than and different from the average of individual
fitnesses and fitness differences. On this view, trait fitness is a
property of populations and, in part, their population
structure--that is, the ways in which traits are distributed in
the population. An example (to be explored further below) is reflected
in cases where the fitness of a trait depends not just on its
incidence in a population, but also on its variance within. A
trait's variance in a population cannot be reflected in
individual fitness any more than the entropy of a volume of gas can be
reflected in the properties of any of the individual molecules that
compose it and contribute to its entropy. This suggests that trait
fitness is not reducible to, definable in terms of, or even entirely
supervenient on the relationship between individuals (e.g., organisms)
and their environments.


 

The disagreement about whether fitness is a property of biological
individuals (genes, genotypes, organisms, families, populations and
other groups or even species) as opposed to a property of traits of
these individuals, has made significant another debate about the
explanatory role of fitness in the theory of natural selection. Among
those who endorse trait fitness (differences), and not individual
fitness (differences), as a fundamental explanatory factor in natural
selection, there is a dispute about whether its explanatory role
reflects its causal force, or whether trait fitness is a purely
statistical concept employed in the theory of natural selection to
make demographic predictions about future trait distributions, without
entering into any causal nexus among the objects so to speak. Thus,
Matthen and Ariew (2002, 56) write, "Unlike vernacular
[individual] fitness, predictive [trait] fitness is not a cause of
selection, or of evolution for that matter.... [P]redictive
fitness is a measure of evolutionary change not a cause." This
view confers an obligation on those who embrace it to explain how the
theory of natural selection can provide contingent explanations
without trading in causal relations among its explanatory
variables.


## 4. The Propensity Interpretation of Fitness


 

Among philosophers of biology there has been a wide consensus that
the solution to problem of defining individual 'fitness'
is given by treating it as a probabilistic disposition. As such it
causally intervenes between the relationship of environments to
organisms that cause it, and the actual rates of reproduction that are
its effects. Thus, fitness turns out to be a
"garden-variety" dispositional concept like
'magnetic' or 'fragile'. These properties, and
all dispositions are distinguished both from the actual behaviour to
which they give rise--e.g., attracting iron filing or breaking in
the case of magnetism or fragility; some items are magnetic and others
fragile without ever actually attracting iron filings or
breaking. Similarly, an organism can have a probabilistic disposition
to have \(n\) offspring and yet "unluckily" never actually
reproduce.




Dispositional concepts such as 'magnetic' have explanatory
power even though they are defined in terms of causes and effects from
which they are nevertheless distinct, and are realized by the
molecular properties of matter on which they supervene. The fact that
fitness is a probabilistic *disposition* makes for no
special difficulty on this analysis. The charge of tautology against
the theory thus rests on the mistaken demand that an explanatory
variable must always be defined in terms distinct from its causes and
effects. This is a demand shown to be unreasonable by the failed
Logical Positivists' attempts to give the empirical meanings of
theoretical terms independent of their explanatory roles.



*Mutatis mutandis* the same will apply to comparative fitness
differences. These will be dispositions supervening on the complex of
relations between organisms' and environments' manifest
properties (Rosenberg 1978), and will give rise to differential
reproductive rates. Thus, definitions such as the following were
advanced by proponents of this approach (Beatty and Mills 1979,
Brandon 1978):



> 
> 
> \(x\) is fitter than \(y\) in \(E\) \(=\_{df}\) \(x\) has a
> probabilistic propensity \(> .5\) to leave more offspring than \(y\).
> 
> 




Of course, if fitness is a probabilistic propensity, then the fitter
among competing organisms will not always leave more offspring, and
the theory of natural selection will have to be understood as making
the claim that (probabilistic) fitness differences result in
reproductive differences not invariably but only with some
probability. With the inclusion of such propensities, the tautological
nature of the explanation is dissolved since there is no deterministic
path between the propensity to leave more offspring and the actual
reproductive rates. But putting aside the tautology issue, there is
also a scientific reason for favoring propensity approaches: since the
theory of natural selection allows for drift, this qualification on
its claims will be a welcome one.




The question arises however of what sort of a probabilistic propensity
the definition invokes. One candidate that has not found much favour
among philosophers is that the probability invoked by the definition
is long run relative frequency. To begin with, owing to periods of
environmental and genetic instability, actual frequencies may vary
rapidly while still approaching their long run relative frequencies
(conditional on the counterfactual assumption that environment and
genes had been stable). This makes it difficult to confirm measures of
fitness so defined. Moreover, treating single case probabilities as
long run relative frequencies is subject to a long-standing objection. In the
biological case it is particularly serious owing to the role of small
numbers (e.g., founder effects) in evolution. Finally, if long run
relative frequencies reflect dispositions of organisms or populations
to leave descendants, the question arises whether these dispositions
are grounded on some occurrent properties or not. If not then long run
relative frequencies turn out to be or immediately give way to
objective chances. (See Earman 1985, 149.)




Some philosophers have argued that fitnesses are precisely such
objective chances. Brandon and Carson (1996) held that here, as in
quantum mechanics, we find a brute unanalyzable probabilistic
dispositional property of a particular item, which generates the long
run relative frequencies. It is indeed the case that among
philosophers of quantum mechanics some hold that probabilistic
propensities can explain actual frequencies [cf. Railton 1978, 216],
and some hold that they do so via a detour into long run relative
frequencies. But few are comfortable with such arguments and adopt
them only because, at the level of the quantum mechanical
probabilistic propensities are indispensable and irreducible
[cf. Lewis, 1983]. Proponents of probabilistic propensities in biology
may envision two possibilities here. One is that probabilistic
propensities at the levels of phenomena that constitute the biological
are the result of quantum probabilities "percolating up"
in Sober (1984) and Brandon's and Carson's (1996) phrase;
the second is that there are brute unexplainable probabilistic
propensities at the level of fitness differences (Brandon and Carson
1996). No one doubts the potential biological significance of quantum
percolation. It may well be an important source of mutation
[cf. Stamos 1999 for a discussion]. But the claim that it has
a *significant* role in most fitness differences is not
supported by any independent evidence [cf. Millstein 2000 and Glymour
2001 for a discussion]. The claim that there are brute probabilistic
propensities at the level of organismal fitness differences is only
slightly more tenable. No one has adduced any evidence that, for
instance, the probabilistic generalizations about the behaviour of
animals that ethology and behavioural biology provide, are irreducibly
probabilistic, instead of simply expressions of the current state of
our knowledge and ignorance of the causes and conditions of the
behaviour in question.




Rosenberg and Kaplan [2005] advance an alternative account of the
nature and source of objective chances in Darwinian processes, arguing
that they are not quantum mechanical in origin but are identical to
the objective chances that operate in the processes described by the
second law of thermodynamics. Of course this suggestion trades one
problem for another, since the source of thermodynamic chances is a
vexed question in the philosophy of physics.




There is however a much more serious issue facing the propensity
definition of fitness: it has long been held to be difficult to pin
down the specific mathematical expression of the probabilistic
propensity that is supposed to constitute fitness altogether. The
difficulty reflects features of natural selection that we must
accommodate. Failure to deal with these difficulties leads inexorably
to the conclusion that far from providing the theoretical meaning of
fitness, the probabilistic propensity "definition" is a
set of an indefinitely large number of
operational *measures* of fitness; moreover,
identifying these measures often turns on assuming as understood just
what the theory of natural selection sets out to explain. And if this
is so, the probabilistic propensity definition will not defuse the
threat of triviality facing the theory of natural selection. We review
here the research program of delivering a propensity definition of
fitness that has sought to deal with these difficulties.


 

The first thing to notice about the "definition"



> 
> 
> \(x\) is fitter than \(y\) in \(E\) \(=\_{df}\) \(x\) has
> a probabilistic propensity \(> .5\) to leave more offspring
> than \(y\)




is that it is of course often falsified. That is, there are many
circumstances in which the organism of greater fitness has the
propensity to leave fewer immediate offspring than the organism of
lower fitness; as when for example, the larger number of a bird's
chick all die owing to the equal division of a quantity of food which
would have kept a smaller number viable. More generally, as Gillespie
(1977) has shown, the temporal and/or spatial variance in number of
offspring may also have an important selective effect. Take a simple
example from Brandon (1990). If organism \(a\) has 2 offspring
each year, and organism \(b\) has 1 offspring in odd numbered
years and 3 in even numbered ones, then, *ceteris paribus*,
after ten generations there will be 512 descendants of \(a\) and
243 descendants of \(b\). The same holds if \(a\) and
\(b\) are populations, and \(b\)'s offspring vary between 1
and 3 depending on location instead of period.


 

Accordingly, we need to change the "definition" to
accommodate the effects of variance:



> 
> 
> \(x\) is fitter than \(y\) \(=\_{df}\) probably \(x\) will have more
> offspring than \(y\), unless their average numbers of offspring are
> equal and the temporal and/or spatial variance in \(y\)'s
> offspring numbers is greater than the variance in \(x\)'s, or
> the average numbers of \(x\)'s offspring are lower than
> \(y\)'s, but the difference in offspring variance is large
> enough to counterbalance \(y\)'s greater number of offspring.
> 




It is also the case that in some biologically actual
circumstances--for example, in circumstances in which mean
fitnesses are low, increased variance is sometimes selected for
(Ekbohm, Fagerstrom, and Agren 1979). As Beatty and Finsen (1987)
further showed, our "definition" will also have to
accommodate "skew" along with offspring numbers and
variance. Skew "appears" when one of the
"tails" of the distribution contains more observations and
the median is therefore shifted away from the normal. Our
"definition" of fitness must take these conditions into
account on pain of falsity. One simple way to do so is to add a
*ceteris paribus* clause to the definition. But the question
must then be raised of how many different exceptions to the original
*definiens* need to be accommodated. If the circumstances
under which greater offspring numbers do not make for greater fitness
are indefinitely many, then this "definition" will be
unsatisfactory.


 

Some proponents of the propensity definition recognize this difficulty
and are prepared to accept that at most a "schematic"
definition can be provided. Thus Brandon writes (1990, 20):



> 
> 
> We can ... define the adaptedness [a synonym for expected
> fitness] of an organism *O* in an environment *E* as
> follows:
> 



 \[

A^\*(O,E) = \sum P(Q\_i^{OE})Q\_i^{OE} - f(E,\sigma^2).

\]

 

Here \(Q\_i^{OE}\) are a range of possible offspring numbers in
generation \(i\), \(P(Q\_i^{OE})\) is the probabilistic propensity to
leave \(Q\_i^{OE}\) in generation \(i\), and most important \(f(E,
\sigma^2)\) is "some function of the variance in offspring
numbers for a given type, \(\sigma^2\), and of the pattern of
variation" (1990, 20). Brandon means "some function or
other, we know not what in advance of examining the case."
Moreover, we will have to add to variance other factors that determine
the function, such as Beatty and Finsen's skew, or the
conditions which Ekbohm, Fagerstrom, and Agren identify as making
higher variance adaptive, etc. Thus, the final term in Brandon's
definition will have to be expanded to \(f(E,\sigma^2,\ldots)\), where
the ellipsis indicate the additional statistical factors which
sometimes combine with or cancel the variance to determine fitness
levels.




But how many such factors are there, and when do they play a non-zero
role in fitness? The answer is that the number of such factors is
probably indefinitely large. The reason for this is given by the facts
about natural selection as Darwin and his successors uncovered
them. The fact about selection which fates our
"definition" either to being forever schematic or
incomplete is the "arms-race" strategic character of
evolutionary interaction. Since every strategy for enhancing
reproductive fitness (including how many offspring to have in a given
environment) calls forth a counter-strategy among competing organisms
(which may undercut the initial reproductive strategy), the number of
conditions covered by our *ceteris paribus* clause, or
equivalently the number of places in the function
\(f(E,\sigma^2,\ldots)\) is equal to the number of strategies and
counter-strategies of reproduction available in an
environment. Brandon writes, "in the above definition of
\(A^\*(O,E)\), the function \(f(E,\sigma^2)\) is a dummy function in
the sense that the form can be specified only after the details of the
selection scenario have been specified" (20). But, besides the
fact Brandon admits, that the function \(f\) will differ for different
\(O\) and \(E\), \(f\) will have to be expanded to accommodate an
indefinite number of further statistical terms beyond
variance. Schematically, it will take the form
\(f(E,\sigma^2,\ldots)\). Again, adapting Brandon's notation,
none of the members of the set which express his multiply generic
"definition" of "adaptedness" or
"expected fitness", 
\(\{\Sigma P(Q\_i^{OE})Q\_i^{OE} - f\_1(E,\sigma^2, \ldots)\), 
\(\Sigma P(Q\_i^{OE})Q\_i^{OE} - f\_2(E,\sigma^2, \ldots)\), 
\(\Sigma P(Q\_i^{OE})Q\_i^{OE} - f\_3(E,\sigma^2, \ldots)\), 
\(\ldots\}\), 
is in fact a definition of either term. It is the set of operational
measurements of the property of comparative fitness.


 

Philosophers dissatisfied with this conclusion have continued to
search for a propensity definition of fitness that is
counterexample-free and not schematic or generic in Brandon's
sense. A promising candidate is due to Pence and Ramsey (2013). A
brief account is given here.


 

Consider all the possible daughter lineages or lines of descent from
some individual, \(o\). Call each of the possible lineages \(\omega\)
and the set of them \(\Omega\). For each lineage \(\omega\_i\) the
probability that \(o\)'s actual daughter population is
\(\omega\_i\) will be \(Pr(\omega\_i)\). \(F\), the fitness of \(o\),
will not be given by weighted sums of possible daughter populations at
a specific generation in the future, but rather by this value over the
long run, as the number of generations increases without limit. The
definition of individual fitness, \(F\), is then given by the
following equation (Pence and Ramsey 2013, 862; equation (4)):




\[
F = \exp \left( \lim\_{t \to \infty} \frac{1}{t} \int\_{\omega\in
\Omega} Pr(\omega ) \cdot \ln(\phi(\omega ,t)) \mathrm d \omega
\right)
\]


(where \(\phi(\omega ,t)\) is a function that gives the size of a
daughter population at some future time \(t\)). Of course if every
possible daughter lineage becomes extinct eventually then in the limit
\(F = 0\), and if some populations fluctuate wildly, \(F\) may not
converge to a stable value in the limit either. But there are
conditions under which the limit as the number of generations goes to
infinity is guaranteed to exist and under which \(F\) is well-defined
(see Pence and Ramsey 2013, 862).




This equation is also subject to some further conditions Pence and Ramsey
argue are biologically reasonable, for example that selection is
density dependent, that there is an extinction threshold of some
population size below which extinction obtains, and most important
that the population dynamics are non-chaotic. Pence and Ramsey show
how their definition avoids all of the problems discussed above, as
well as some other counterexamples to previous proposals, owing to its
incorporating and combining all possible daughter populations over
indefinitely many reproductive generations. They also show that a
general version of the same equation has been independently derived by
mathematical biologists, and they argue that so defined, fitness has a
substantial role to play in biology, especially the field of
"adaptive dynamics". They show how standard operation
fitness measures biologists employ can be derived from the definition,
including the simple geometric and arithmetic means, along with their
higher moments (variance, skew, etc.) when multi-generational effects
are present. Thus, for example, Pence and Ramsey's proposal has
the result that an organism with a probability of reproducing one
offspring per generation equal to 1 will be fitter than an organism
with a .5 probability of 0 offspring and a .5 probability of 2
offspring, since the second organism's possible lines of descent
will all have a probability of extinction that approaches 1 as time
approaches infinity.


 

Suppose that the Pence and Ramsey proposal adequately deals with the
counter-example problems that confronted earlier probabilistic
propensity definitions of fitness. The question of whether this
definition is adequate for trait fitness as well as for individual
fitness and fitness differences remains. To begin with there is matter
of whether the definition merely provides units in which to measure
fitness the way that plainly operational definitions do, by contrast
with definitions of dispositions in terms of their occurrent
bases. The supervenience of fitness on a vast and heterogeneous base
makes such a reductive definition impossible and as we have seen the
ecological characterization in terms of "design problems"
has its limits as well. Moreover, some have argued that the propensity
definition is at most only a component of the meaning of trait
fitness. As noted above, some philosophers (e.g., Ariew and Ernst
(2007, 296)) argue that trait fitness is often a matter of population
size and structure and conditions of genetic heritability, and these
factors are "extrinsic to the causal properties of the
individual" in its local environment. From this conclusion it
seems an easy matter to infer that as it functions in the theory of
natural selection, trait fitness may not be causal force at all. It
may, after all, be a "book-keeping" notion, one which
allows us to make predictive inferences without having any
"biological reality".


## 5. Fitness as a Propensity and the Principle of Natural Selection




The Pence-Ramsey proposal holds out the prospect of dealing with a
serious difficulty that long daunted the probabilistic propensity
definition of fitness. For the counterexamples it deals with made
impossible any attempt to turn a generic probabilistic schema for
fitness into a complete general definition that is both applicable and
adequate to the task of vindicating the truth of the principle of
natural selection (PNS):



> 
> 
> PNS : If \(x\) is fitter than \(y\), then probably \(x\) will have
> more descendants than \(y\).




Note that if we cannot give anything more than a generic schema for
'\(x\) is fitter than \(y\)', then the PNS cannot be
expressed as a synthetic proposition with a truth-value and so cannot
figure as a general law. These problems had suggested to some
philosophers that we need to rethink the cognitive status of the
theory of natural selection altogether.


 

Brandon, for example, has argued that the theory of natural selection
should not be viewed as a body of general laws, but as the
prescription for a research program. As such its central claims need
not meet standards of testability, and fitness need not be defined in
terms that assure the nontriviality, testability, and direct
explanatory power of the theory of natural selection. In that sense,
Brandon makes common cause with the later Popper. Popper originally
argued the claim that the theory of natural selection was
unfalsifiable pseudoscience. Later he came to hold that theory of
natural selection was a scientifically respectable but nevertheless
untestable organizing principle for biological science (Brandon 1990,
139-140).




On this view, in each particular selective scenario a different
specification of the schematic propensity definition of fitness
figures in the antecedent of a different and highly restricted
principle of natural selection that is applicable only in that
scenario. Properly restricted to the right function and the right set
of statistical features of its reproductive rate for a given
environment, this version will be a highly specific claim about
natural selection for the given population in the given
environment.




The notion that there is a very large family of principles of natural
selection, each with a restricted range of application, will be
attractive to those biologists uncomfortable with a single principle
or law of natural selection, and to those philosophers of science who
treat the theory of natural selection as a class of models. On the
"semantic approach" to the theory of natural selection,
each of the substitution instances of the schematic principle of
natural selection generated by a particular specification of the
propensity definition of fitness is treated as a definition of a
different Darwinian system of population change over time. See Lloyd
1994, Beatty 1981, and Thompson 1989 for exposition of this
position. The evolutionary biologist's task is to identify which
definition is instantiated by a population in an environment.


 

For every such definition instantiated by a population, there is the
synthetic truth that the members of the population, or all of its
subpopulations, instantiate the definition, and the further broader
truth that many populations of otherwise diverse species instantiate a
small sub-set of the models, and the yet broader truth that all
populations instantiate one of this set of really quite similar
models. Presumably, all these statements of varying degrees of
generality need explanation. Consequently, those who resist the
"semantic interpretation" of theories argue that we might
as well treat each as a substitution instance of the principle of
natural selection generated by a different probabilistic propensity
measure of fitness as a distinct empirical generalization to begin
with instead of a model-theoretic definition. But, one will want to
ask, does this set of generalizations with similar antecedents and
identical consequents have something in common, which in turn explains
and unifies them, or are they the fundamental principles of the theory
of natural selection? The question is obviously rhetorical. For each
of the members of the set of functions that turn the definition-schema
for fitness into a complete property is a measurement of the fitness
of some actual or potential individuals or populations. Each is a
measurement appropriate to its particular environmental circumstances,
a measurement inappropriate for the same or different individuals at
different locations or times in the same environment.




One alternative is to allow that the PNS is a necessary truth but
continue to hold that it has explanatory content, and can figure in
causal explanations of evolutionary outcomes. This is a view advanced
by Sober (see Sober 2002) and examined in Lange and Rosenberg
(2011). As we shall see in the next section, another possibility is to
relativize reproductive rates in favor of another universal measure of
fitness.


## 6. How the Problems of Defining Biological Individuality Affect the Notion of Fitness


 

In previous sections, we remarked on the difficulty of identifying the
precise propensity that could, according to some, ground fitness
ascriptions. Moreover, it is often difficult to isolate the
populations where the evolutionary change is occurring. This is in
part an operational problem, but for many biological systems, this
difficulty may in fact reveal a deeper ontological issue. Thinking
about fitness in reproductive terms depends on the possibility of
identifying offspring (or successive replicators) and populations of
them. For most Metazoans, this appears to be relatively
straightforward. But how are we to treat the evolution of colonies,
clonal organisms and symbionts (and hypothetically ecosystems)? Many
philosophers have argued that our philosophy of biology's usual
bestiary does not reflect some of the complex organisation actually to
be found in nature (J. Wilson 1999, D.S. Wilson and Sober 1989,
Godfrey-Smith 2009, O'Malley and Dupre 2007, Bouchard and
Huneman 2013) For many biological systems, organismal boundaries seem
arbitrary ways to carve up the biological world. Those boundaries may
merely reflect an impoverished way of thinking about biological
individuality (Pradeu 2012, Haber 2013). Many biological individuals
are in fact complex arrangements of other individuals. When these
individuals belong to a single species (ex. some eusocial insects) a
gene selectionist view according to which fitness is understood as the
differential reproductive success of alleles may be available. But in
the case of multi-species communities (e.g., fungus-termite colonies),
allelic success will not track evolutionary change since some of the
adaptations are not fully biotic (Bouchard 2009). Moreover, it has
been argued (Turner 2004, Bouchard 2004, 2008) that some individuals
that are adapting are not reproducing at all.


 

Biological individuality is much more varied and heterogeneous than
previously believed and this additional complexity puts pressure on
the notion that reproductive success can act as a 'universal
currency' of fitness. The difficulties of establishing
reproductive success for some clonal organisms, for collectives of
organisms and for multi-species assemblages has led some biologists
and philosophers to entertain alternative concepts of fitness. Leigh
Van Valen, in his attempts to develop a theory of evolution that would
allow for the evolution of whole communities (Van Valen 1975, 1989,
1991), suggested that fitness as energy control could explain the
evolution of a broader range of biological systems. "Rather than
saying that natural selection is expected differential reproduction,
we should say that it is expected differential expansion" (Van
Valen 1989, 7). By 'expansion' Van Valen doesn't
mean expansion in physical space (although that may occur) but
expansion in resource or energy space. In this approach, energy is
seen as the 'universal currency': a fitter community is
one that controls more energy than another community. For
'simpler' biological systems such as sexual species with
discrete generations, increased reproductive success is a good proxy
for increased energy success and therefore previous measurements and
models of reproductive output remain useful but their explanatory
exhaustiveness is relativized. Although energy can seem to be a
universal measure of fitness that could apply to the all the varied
types of biological individuals that can emerge, it's not clear
that Van Valen's approach can be as universal as desired since
it has difficulty explaining increases in efficiency in energy control
(see Bouchard 2004 chap 3 for analysis). This has motivated Bouchard
(2004, 2008, 2011) to argue for an account of evolution focusing on
differential persistence (reminiscent of Thoday 1953). Bouchard (2004,
2008, 2011) argues that Persistence Through Time of a lineage is the
property maximized by evolution by natural selection: maximization of
relative reproductive success or maximization of energy control are
only two dominant strategies for persistence increase (see Bourrat
2014 and Doolittle 2014 for related approaches). In this approach
(lineage) \(X\)is fitter than (lineage) \(Y\) if \(X\)has a higher
propensity to persist for \(Z\) amount of time than \(Y\). Some of the
problems of propensities remain, but we gain a way to assess
ecological fitness (probability of persistence) in a way that can be
independent of reproductive success. Persistence is the overarching
design-problem. Increased reproductive potential is but one powerful
way to increase one's potential to persist.


 

The question of how to define biological individuality is an
ontological question about what individuals can evolve in response to
natural selection. Many biological systems differ in form and in
function from our garden variety Metazoans. How are we to understand
the evolution of symbiotic communities involving bacteria with lateral
gene transfer? How are we to make sense of the complex traits of
eusocial insects? Not all these emergent individuals qua individuals
replicate. Whether it's by focusing on energy or persistence (or
some other account) a complete understanding of fitness should reflect
that fact--or accept that it cannot alone account for some
adaptive change in the biological world.


## 7. Ecological Fitness and the Problem of Evolutionary Drift


 

The difficulties that face both the subjective probability view of
fitness and the probabilistic propensity definitions of fitness are
serious enough to make the notion of "ecological fitness"
worth revisiting. Recall that on this view '\(a\) is fitter than
\(b\) in \(E\)' is defined as '\(a\)'s traits result
in its solving the design problems set by \(E\) more fully than
\(b\)'s traits.' The terms in which this definition is
couched are certainly in as much need of clarification as is
'fitness'. It is cold philosophical comfort to point out
that definitions have to stop somewhere, that the definition of a
theoretical term must be distinct from the operational measure of the
property it names, and that testability is not a matter of theory
meeting data one proposition at a time. In consequence none of these
considerations have convinced philosophers of biology to accept the
design problem definition, and to give up the project of defining
fitness by reference to its effects in reproduction. Nevertheless,
there does appear to be important biological work that the ecological
fitness concept can do, and which no definition of fitness in terms of
differential reproductive rates--actual, expected, or
dispositional--can do.




To see what these tasks are, consider the question, How do we decide
whether a divergence from a long run relative frequency prediction
about fitness differences is a matter of drift, a disconfirmation of
the hypothesis of natural selection, or a reflection of a
mismeasurement of fitness differences to begin with? Suppose we
measure the fitness differences between population \(a\) and
population \(b\) to be in the ratio of 7:3 (e.g., \(w\_a = 1\), \(w\_b =
.428\)) and suppose further that in some generation, the actual
offspring ratio is 5:5. There are four alternatives: (a) the fitness
measure of 7:3 is right but there was drift--i.e., the initial
conditions at this generation are unrepresentative of those which
obtain in all relevant generations; (b) the fitness measure of 7:3 was
incorrect and there was no drift; (c) both drift and wrong fitness
measure or (d) the principle of natural selection is
disconfirmed. Ignoring the fourth alternative, how do we discriminate
among the first three of these?




In the absence of information about the initial conditions of the
divergence, there is only one way empirically to choose between
alternatives (a)-(c). This way requires that there are
ecological fitness differences, and that we can detect them. Suppose
that fitness differences were matters of probabilistic differential
reproductive success (no matter what interpretation of probability is
adopted). Then the only access to fitness differences is via
population censuses in previous generations (since these form the
bases of the probabilities). Suppose that this census does indeed show
a 7:3 ratio between as and bs in the recent past. In order to exclude
the absence of fitness differences instead of drift, as the source of
the current generation's 5:5 outcome, we need to be able to
establish that the 7:3 differences in previous populations were not
themselves the result of drift. But this is the first step in a
regress, since we began with the problem of discriminating drift from
mismeasures of fitness. To solve the initial problem, we now have to
assure ourselves that the 7:3 ratios in the past were not the result
of drift. Whence the regress. *Of course the problem does not arise
if we have access to fitness differences independently of previous
population censuses*. And this access we have, at least in
principle, if fitness is a matter of differences in the solution of
identifiable design problems, that is, if there is such a thing as
ecological fitness and it is (fallibly) measured by probabilistic
propensities to leave offspring.




Once we have access to ecological fitness differences, we can, at
least in principle, decide whether the divergence from predicted
long-run relative frequencies, especially where small populations are
concerned, is a matter of drift or reflects our ignorance either of
ecological fitness differences or the unrepresentativeness of the
initial conditions of individual births, deaths, and
reproductions.




This result also has important implications for the interpretation of
the theory of natural selection as one wholly about populations, and
not also about individual fitness differences, discussed above
(individual versus trait fitness). Note that the problem of
distinguishing drift from selection in ensembles--i.e., large
populations--has the same character, and is in principle
susceptible to the same solution as the problem of drift makes for
evolution among lineages with small numbers of individual members. We
can distinguish drift from selection in ensembles as well, *if*
we accept that there is such epistemic access to ecological fitness
differences and to the initial conditions of births, deaths and
reproductions, taken one at a time, and we accept that these
individual-differences aggregate into ensemble-differences.




Because populations no matter how large are always finite in size,
there is always some drift which needs to be distinguished from
fitness differences. Thus even in population biology there is in the
end no substitute for ecological fitness and no way to dispense with
its services to the theory of natural selection. And since ecological
fitness is ultimately a relationship between organisms (or
individuals) taken two at a time, the theory is as much a set of
claims about individuals as it is about populations.




This line of reasoning highlights the next phase of the debate. From a
discussion about fitness, the debate has evolved into a general debate
concerning the nature of natural selection and drift. A number of
alternative views have emerged in thinking about these topics. Some
(e.g., Walsh, Lewens, Ariew, and Matthen) think about natural
selection solely as population wide patterns caused by non selective
processes: this view deprives fitness of any causal or explanatory
power. Others (e.g., Millstein and Stephens) see fitness and natural
selection as a cause, operating at the population level, to bring
about the differential reproduction rates. Finally others argue that,
if it is to play an explanatory role in our theory, fitness has to be
an individual and causal concept. As these debates suggest, far from
being merely a 19th century slogan, understanding the
meaning of the "survival of the fittest" is of
philosophical and biological urgency.