Metascience Ó Springer 2007

DOI 10.1007/s11016-007-9117-6

SURVEY REVIEW

EVOLUTIONARY BIOLOGY: CAUSES, CONSEQUENCES AND

CONTROVERSIES

Samir Okasha, Evolution and the Levels of Selection. Oxford:

Oxford University Press, 2006. Pp. xi + 263. US$55.00£30.00 HB

Massimo Pigliucci and Jonathan Michael Kaplan, Making Sense of

Evolution: The Conceptual Foundations of Evolutionary Biology.
Chicago: University of Chicago Press. 2006, Pp. vi + 300.
US$28.00 £17.00 PB, $70.00 HB.

By Anya Plutynski

INTRODUCTION

These books address a number of core conceptual issues in evolu-

tionary biology. Okasha’s is a sustained philosophical discussion of
the levels of selection debate, and all its attendant implications –
from the nature of selection to the evolution of the biological hier-
archy itself. Pigliucci and Kaplan’s is a critical overview of fitness
concepts, Ôtargets and units’ of selection, constraints, adaptationism,
function ascription, the adaptive landscape metaphor, and last, but
not least, species concepts. What ties the book together is a critical
stance with respect to hypothesis testing in evolutionary biology.
Of the two, the latter is far more critical. Pigliucci and Kaplan’s
central claim is that there is a ‘‘disconnect between conceptual
understanding’’ of core concepts in evolutionary theory ‘‘and the
way in which these are studied empirically’’ (p. 263). In sum, they
argue that some of the most common methods of testing in evolu-
tionary quantitative genetics are deeply flawed. Okasha, on the
other hand, is more ecumenical, Ôbridging the gap’ between biology
and philosophy of science, rather than using the latter as a tool to
 SURVEY REVIEW

dismantle the former. His aim is to use formal modeling techniques

as a Ôsystematic framework’ for addressing a variety of conceptual
questions about the levels of selection.
Both books are extremely well-versed in evolutionary theory and
practice. Further, neither let current assumptions in biological prac-
tice escape notice or critical assessment. In sum, they are both thor-
ough, insightful discussions, and should serve as touchstones for
any future discussion of either levels of selection, or, for that mat-
ter, hypothesis testing in evolutionary biology.
The levels of selection debate has historically been concerned
with the following issue: under what circumstances are entities at
different levels of the biological hierarchy – genes, chromosomes,
individual organisms, groups, or even species and clades – the Ôsub-
ject’ or Ôunit’ of selection. Selection can potentially operate on any
entity with heritable variation in fitness (Lewontin, 1970), so the
problem is whether and under what circumstances different entities
in the hierarchy meet these conditions and how we ought to assess
cases where there is some ambiguity. So, for example, when are
groups rather than individual organisms subject to selection, and
how do we decide whether one process is simply a Ôby-product’ of
the other? Okasha deftly negotiates the maze of conflicting views,
vocabularies, and conceptual schemes that have been developed to
address this question over the past 25 years. Moreover, he shows
both the advantages and limitations of formal models in assessing
competing claims about multi-level selection processes.
Okasha points out that the debate has focused on the syn-
chronic problem of what level(s) selection is presently acting upon.
Biologists and philosophers have for the most part ignored the dia-
chronic problem of how selection could have shaped the evolution
of biological hierarchies in the first place. In other words, up to
now, most biologists take the fact of the biological hierarchy as
given, not something to be explained. Okasha argues that the hier-
archies themselves – chromosomes, cells, organisms, populations
and species – have evolved, and further, claims that selection at
multiple levels is required for some, though not all, stages in the
evolution of the hierarchy itself. That is, he illustrates how and
why the problem of the levels of selection is relevant to larger con-
cerns about the evolution of all levels of the biological hierarchy.
Okasha’s book is so level-headed, detailed, and exhaustive, that
seeking out controversial arguments is rather difficult. There are a
 EVOLUTIONARY BIOLOGY

few rather quick dismissals, elliptical arguments, and (admitted) ap-

peals to intuition here and there, but in the end the conclusions are
eminently sensible and relatively uncontroversial.
In stark contrast, Pigliucci and Kaplan’s book comes in with
guns blazing, marshalling controversial claims left and right. They
argue for radical reconsideration not only of the conceptual foun-
dations of evolutionary biology, but also of standard methods of
testing in evolutionary quantitative genetics. Some of their argu-
ments will no doubt ruffle the feathers of practising biologists.
Other claims, however, are more Ôphilosophical’ and less likely to
move biologists to change their thinking. For instance, at the cen-
tre of Pigliucci and Kaplan’s arguments is a critique (following
Matthen and Ariew, 2002) of the Ôforce’ metaphor, and the associ-
ated claims that selection and drift are decomposable causal forces.
One worry (which they acknowledge) is that biologists who will
take these issues seriously are in the (philosophically inclined)
minority. That is, most biologists will simply dismiss this discussion
as not terribly relevant to biological practice or theory.
However, Pigliucci (himself a biologist) and Kaplan argue that
this Ôphilosophical’ worry is connected to larger methodological is-
sues. In particular, they argue that thinking about selection as a
Ôforce’ (for instance) has led to methods of testing hypotheses in
evolutionary quantitative genetics that are deeply problematic.
Many of Pigliucci and Kaplan’s concerns about hypothesis testing
are surely ones that practising biologists ought to take seriously.
Indeed, this is where the book shines; the discussions of hypothesis
testing in Chapters 2, 4, and 10, should, I suggest, be studied care-
fully by not only most entering graduate students in evolutionary
biology, but philosophers of science as well. Pigliucci and Kaplan
draw attention to problems with inferring cause from correlation,
and are critical of classical statistics and tests of null models. While
they cover other interesting and worthwhile topics, one wishes that
they had devoted more time to an analysis and discussion of meth-
ods of path analysis and structural equation modelling, and a com-
parison and contrast of this with other methods. Whatever
conceptual confusions biologists are subject to, how they frame and
test hypotheses is a concern that is philosophically deeply interest-
ing, and relevant to both theoretical and practicing biologists, not
merely philosophers.
 SURVEY REVIEW

OKASHA ON LEVELS OF SELECTION

Okasha defends multi-level selection theory – the view that selec-

tion can and does operate at more than one level (sometimes simul-
taneously) in the biological hierarchy. He does this by developing a
systematic framework for assessing when and how selection is act-
ing at different levels. At the core of this framework are two for-
mal models, the Price Equation, and, what Okasha calls the
Ôcontextual’ approach. The Price model, he argues, is a simple,
general model that both Ôlays bare’ the essential elements of the
natural selection process – a covariation between character and
fitness. The first half of the book is a detailed explication and anal-
ysis of the formal models; the second half is relatively independent
of this discussion, and addresses larger conceptual issues concern-
ing, e.g., the Ôgene’s eye view’, group selection, species selection,
and hierarchical selection theory. Indeed, the book might well be
treated as two relatively separate discussions; and it’s not clear that
the earlier discussion of formal modelling strategies contributes
very much to the latter.
First, however, Okasha defends Lewontin’s three criteria for
selection – heritable variation in fitness – and argues that Price’s
model nicely captures all three. Further, he shows how the Price
approach allows one to represent the combined effects of a two-level
selection process in a single scheme. This allows Okasha to assess
cases of what he terms Ôcross-level byproducts’ of selection. In some
cases, what appears to be selection at one level is simply a
Ôby-product’ of a selective process operating at some different level.
One of the central projects of the book is to sort out how we ought
to assess these problematic cases. Okasha discusses a variety of
alternative attempts to identify the level at which selection is acting
– the Ôadditivity’, Ôscreening off’, Ôemergent character’, as well as the
Ôemergent relation’ criteria – and argues that none of these is whol-
ly satisfactory (though the first and second have merits in specific
contexts). He also considers pluralism – the view that there is no
Ôfact of the matter’ as to which level selection is acting, which he
rejects in favour of the realist view that there is (almost) always a
fact of the matter.
Okasha describes a useful way to clarify the levels of selection
debate – Damuth and Haisler’s (1998) distinction between two
kinds of multi-levels selection, what they call, MLS1 versus MLS2.
 EVOLUTIONARY BIOLOGY

In both cases, there are what Okasha calls Ôparticles’ and Ôcollec-
tives’ – where the latter are higher level units in which the particles
are Ônested’. In MLS1, particles are focal units – units whose
demography gets tracked – in MLS2, both particles and collectives
are focal units. Fitness of a collective in MLS1 is average fitness of
particles within the collective, whereas in MLS2, collective fitness is
defined independently, for instance, in terms of its own Ôreproduc-
tion’ – e.g., producing more groups.
Okasha uses the Price Equation as a way of parsing causal
dynamics in these two cases. The Price Equation treats average
character change in some character (say, height), from one genera-
tion to the next as a function of the sum of the covariance of that
trait and fitness, and the average parent–offspring deviation (trans-
mission fidelity). However, he points out that the equation is a sta-
tistical, not causal decomposition of the factors involved in
selection. In other words, the equation describes correlations be-
tween fitness and character value, but these correlations may or
may not reflect a causal link. In other words, the correlation may
be due to Ôindirect’ as opposed to Ôdirect’ selection – or, selection
Ôof’ a trait, as opposed to selection Ôfor’ a trait (p. 25).
In the end, Okasha concludes that there is ‘‘no fully general
solution to causally decomposing evolutionary change’’(p. 157), at
least in one of two evolutionary scenarios he discusses (MLS1), but
he does think that one or other approach better parses the causal
dynamics of evolution in specific cases. That is, in his view, assess-
ment of where selection is acting in any particular case will always
depend on the biological facts on the ground. This seems sensible.
However, it is a bit disappointing if one (perhaps naively) hoped
that the Price Equation might provide an unequivocal solution.
Why, then, bother with the formal analysis?
An advantage of the Price approach is that it is, as Okasha
argues, a general model of evolution at any level – i.e., it does not
require at the outset that we model evolution as change in gene fre-
quencies. Moreover, the Price approach does allow one to represent
selection acting simultaneously at different levels. However, while
(formally) it is a beautiful thing, apparently it’s quite difficult to
apply in practice.1 In the end, it’s unclear whether the Price Equa-
tion provides a Ôsystematic framework’ for addressing the levels
question; it might be better to say that it provides a framework for
1
Thanks to Fred Adler and Stephen Peck for pointing this out.
 SURVEY REVIEW

representing our prior (biologically informed) intuitions about

where the causal action is.
One issue that Okasha might have addressed in rather more de-
tail is when and if we can correctly infer that the Price Equation
does track a causal relationship. That is, Okasha does not clarify
how we get from the world to the formalism; an example may have
been useful here. To be charitable, the question of the application
of the Price Equation in practice is not really part of Okasha’s lar-
ger project. However, it may have been useful to discuss a concrete
example (for an illustration, see Weinig et al., 2007).2
Other issues Okasha addresses in the book include: how are we to
demarcate Ôlevels’ in the hierarchy – is Ôinteraction’ between parts of a
collective sufficient or necessary for individuation of levels? If not
interaction, then what exactly should count? How do the Ôbook-keep-
ing’ and other objections to the Ôgene’s eye’ view fare, given this dis-
tinction? Under what circumstances, if any, can selection act on
species or clades? Finally, may the Ôgenic’ versus Ôhierarchical’ ap-
proach to the major evolutionary transitions be reconciled, and if so,
how does multi-level selection theory assist in this reconciliation?
Okasha addresses these issues with characteristic subtlety and rigour.
While all these questions cannot be addressed in one review, they are
definitely worth examining in further detail.

PIGLIUCCI AND KAPLAN ON CAUSE AND CORRELATION

Pigliucci and Kaplan’s book opens with a discussion of Shipley’s

(2000) wonderful example of the Balinese puppet theatre, where
shadows of elaborate three-dimensional wooden puppets are pro-
jected onto a screen. Spectators do not see the puppets, but only
their shadows. Similarly, they argue that quantitative biologists
only have access to the Ôstatistical shadows’ of selective processes.
The true Ômechanisms’ of selection, in their view, are causal interac-
tions between organisms and their environments. What they call
Ôpredictive’ or Ôformal’ fitness, drawing on Matthen and Ariew’s
(2002) distinction, is simply Ôthe difference from one in the mean
ratio of growth rates’ in a subpopulation of individuals with a vari-
ant of some trait. They contrast this with Ôinformal fitness’ (also
called Ôindividual fitness’), which is ‘‘about the relationship between
2
Thanks to Joe Dickenson for this reference.
 EVOLUTIONARY BIOLOGY

variation in some particular trait and some particular physical pro-

cess’’ (pp. 23, 18).
They also claim that biologists move too quickly from claims
about the former to the latter without sufficient empirical support.
Further, they argue that genuine support for such claims is rather
difficult to come by: ‘‘the only way to discover predictive fitness of
traits is with replicates of the population of interest’’ (p. 81). In
natural populations, obviously, this cannot be done; they are effec-
tively claiming that we can only estimate formal fitnesses for bacte-
ria in a chemostat (if then!). One concern is that this seems to set a
rather high standard for estimating fitnesses. Surely, we can gener-
ate useful hypotheses based on statistical data, that can then be
substantiated by further empirical work?
In the end, Pigliucci and Kaplan seem willing to grant this, but
grudgingly: ‘‘[if] properly used, [regression analysis] can conve-
niently summarise information and suggest causal hypotheses to be
tested by other means’’(p. 53). That is, statistical studies might
serve to frame hypotheses about selection (which are later substan-
tiated by careful ecological detective work). Arguably, biologists
themselves are fairly well aware of the limits of multivariate statis-
tics in establishing causality. In citations that Pigliucci and Kaplan
mention, biologists have been critical of swift moves from correla-
tion to causation; yet Pigliucci and Kaplan argue that Ômost’ biolo-
gists do not Ôwalk the talk’, and that this is largely due to thinking
of selection and drift as Ôforces’.
The argument for this latter claim is not altogether persuasive:
it’s not clear that the use of multivariate statistics grows directly
out of thinking of selection as a Ôforce’. Of course, if we think of
evolutionary factors like selection and drift as causes, then presum-
ably we can partition these causes and measure their effects; this is
the upshot of the Newtonian analogy (see Stephens [2004] for a re-
view of the decomposition issue). However, it seems that Pigliucci
and Kaplan are concerned with two separate issues – first, concern-
ing the metaphysics of causation, or, whether population level pat-
terns – such as patterns of change in distribution of frequency of
traits over time – are causal. Second, they are concerned with an
epistemic issue; i.e., the question of whether Ôformal’ fitnesses genu-
inely track Ôinformal’ fitnesses in practice. These are, arguably, two
different questions that should be kept separate.
 SURVEY REVIEW

Regarding the metaphysical question, Pigliucci and Kaplan draw

upon a common intuition that all and only physical interactions,
e.g., between organisms and their environments, are Ôtrue causes.’
However, there are (arguably) other senses of causation; e.g.,
supervenient causal processes, (see Shapiro and Sober, forthcoming;
Millstein, forthcoming). These are what we appeal to when we ex-
plain, say, why gambling causes one to lose money, or why taking
a smaller sample size resulted in a misleading result. If one can
grant that such (distributed, population level) processes are causal,
then it will not strike one as altogether implausible that selection is
a cause.
Regarding the epistemic question, it is, of course, possible to
generate models that represent the relative significance of selection
and drift (see Okasha’s book); whether such models are always (or
ever) further substantiated by good Ôecological detective work’ is a
different matter. Pigliucci and Kaplan are correct that statistical
approaches Ôcannot succeed alone’ in, for instance, ‘‘directly infer-
ring anything about the genetic architecture of a population or
trait, or the causal story of how that structure got to be the way it
is’’ (p. 111). Yet, this issue is relatively independent of whether
selection (or drift) are properly understood as Ôcauses’ of evolution.
The book’s greatest strengths are in its criticism of classical sta-
tistics, and a push for use of path analysis, structural equations
modelling, and other methods of testing. Along the way, they make
a number of persuasive and commendable additions to the philo-
sophical literature on other core issues. The chapters on adapta-
tionism, functions, criticisms of evolutionary psychology and
species concepts would serve as excellent introductory surveys for
new students of philosophy of biology; they are clear, and thor-
ough, introducing the relevant new additions to the literature, par-
ticularly developmental systems theory. They argue (as does
Amundson, 1994) that constraints are not Ôcounter’ to selection,
but are part of the developmental processes that selection acts
upon in the first place. They argue that other Ôdevelopmental’
resources apart from genes may have functions, on an etiological
account of functions. All these chapters are insightful, and could,
indeed, stand as separate reviews of these issues.

Department of Philosophy
University of Utah
Salt Lake City,USA
 EVOLUTIONARY BIOLOGY

REFERENCES

Amundson, R. ‘‘Two Concepts of Constraint: Adaptationism and the Challenge

from Developmental Biology’’, Philosophy of Science 61 (1994), pp. 556–578.
Damuth, J. and I.L. Haisler. ‘‘Alternative Formulations of Multi-Level Selection’’,
Biology and Philosophy 3 (1998), pp. 407–430.
Lewontin, R. ‘‘The Units of Selection’’, Annual Review of Ecology and Systematics 1
(1970), pp. 1–18.
Matthen, M. and A. Ariew. ‘‘Two Ways of Thinking About Fitness and Natural
Selection’’, Journal of Philosophy 49 (2002), pp. 55–83.
Millstein, R. ‘‘Natural Selection as a Population–Level Causal Process’’, forthcom-
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Shapiro, L. and E. Sober. ‘‘Epiphenomenalism – The Do’s and the Don’ts’’,
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71 (2004), pp. 550–570.
Weinig, C., J.A. Johnston, C.G. Willis and J.N. Maloof. ‘‘Antagonistic Multilevel
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(2007), pp. 58–67.