2 The Organismic Systems Approach: Evo-Devo and the
Streamlining of the Naturalistic Agenda
Werner Callebaut, Gerd B. Mu
¨ller, and Stuart A. Newman
In this chapter we ﬁrst discuss the emergence of evolutionary developmen-
tal biology (evo-devo) as a response to the essential incompleteness of the
modern synthesis. In the second section, we provisionally characterize evo-
devo in terms of its conceptual framework, methods, and explanatory strat-
egies, and try to introduce some order into the plurality of its theoretical
perspectives. Here we also suggest that a philosophical naturalism com-
mitted to causal-mechanistic explanation is the philosophical theory that
best ﬁts our own organismic systems approach (OSA) to evo-devo and evo-
lution at large. In the third section, we argue that a proper understanding
of evo-devo requires a reconceptualization of the relationship between
what counts as genetic and what as epigenetic. In the fourth section, which
constitutes the heart of the chapter, we sketch some major features of OSA.
Our central concerns are the generic, conditional (i.e., unprogrammed)
generation of primordial organismal form and structure (‘‘origination’’), the
question of evolutionary innovation—how novel elements arise in body
plans—and the factors of organization, that is, how structural elements and
body plans are established. The ﬁfth section deals with some of the major
problems that OSA allows us to address: tempo and mode of phenotypic
evolution, selection and emergence, integration, and inherency. To round
off in the ﬁnal section, we return to more philosophical issues; in particu-
lar, we discuss the kinds of nonreductionistic uniﬁcation that are at stake
in evo-devo in relation to the data- and technique-driven nature of much
As a package, the OSA/naturalistic account allows us to turn the tables on
the adaptationist, gene-centric view and take seriously again Walter Gar-
stang’s dictum (in 1922) that ontogeny does not recapitulate phylogeny,
but rather creates phylogeny (Gilbert 2003a, 777). More speciﬁcally, in
Løvtrup’s (1984, 261) words, ‘‘Inverting Haeckel’s biogenetic law, we may
assert that ontogeny is the mechanical cause of phylogeny. And it must be
In: Integrating Evolution and Development. From Theory to Practice
(Sansom R. and B. Brandon eds.) pp 25-92. MIT Press, Cambridge, 2007.
so, for ontogeny is a mechanical process, while phylogeny is a historical
Until about 1800, biological phenomena were subsumed under two labels:
medicine (comparative anatomy, morphology, and physiology) and natu-
This was a ‘‘remarkably perceptive division’’ (Mayr 1982, 67),
for biology can be divided into the study of proximate or short-term causa-
tion and the study of ultimate causes. The former are the province of func-
tional biology or the physiological sciences, broadly conceived, which seek
answers to ‘‘How?’’-questions; the latter are the subject of evolutionary
biology, which seeks answers to ‘‘Why?’’-questions (Mayr  1961,
1982). Even ‘‘greedy’’ reductionists admit the necessity of taking into ac-
count historical contingencies in evolutionary explanation, and grant that
this circumstance makes biology essentially different from (classical) phys-
Under the spell of Weismannism, informational accounts of ontogeny
such as Mayr’s shift attention away from ontogenetic agency.
dently of Mayr, Tinbergen (1963) recognized that every trait requires both
proximate and ultimate explanation. Inspired by Lorenz’s work in ethol-
ogy, he also realized that these explanations are quite different depending
on whether the explanandum is a single form or a sequence. Tinbergen’s
‘‘four questions’’—now commonly referred to as proximate mechanisms,
ﬁtness advantage, ontogeny, and phylogeny—along with his view that
they are independent yet complementary components of any complete bi-
ological explanation—have become widely accepted not only for animal
behavior, but for biology in general.
The interrelation between proximate and ultimate causation is the cen-
tral problem of any explanatory theory of organismal form (Mu
Hall (2000) characterizes evo-devo, which he views as continuous with the
evolutionary embryology of the nineteenth century, as a way of integrating
proximate and ultimate causes for the origin of phenotypes. Although
embryology—which later came to be called developmental biology—
played an important, if not indispensable, role in the inception of evolu-
tionary theory (Richards 1992, 2002), it was conspicuously absent from
the modern synthesis. Mu
¨ller (2005, 89–90) discusses how the disrepute of
recapitulationism and of neo-Lamarckian beliefs about environmental
inﬂuences on embryogenesis contributed to this ostracism. In the past two
decades, stimulated by a number of explanatory deﬁcits in the prevailing
evolutionary paradigm and by the rise of molecular developmental genet-
26 Werner Callebaut, Gerd B. Mu
¨ller, and Stuart A. Newman
ics, developmental considerations have come to the fore again with a ven-
geance (Laubichler and Maienschein, chapter 1, this volume).
The success story of the modern synthesis is being told and retold every
day by both the popular scientiﬁc media and the professional Darwin in-
dustry. (For more or less critical assessments, see Mayr and Provine 1980;
Depew and Weber 1985, 1995; Burian 1988; Futuyma 1988; Gayon 1989;
Smocovitis 1996; Weber 1998; Keller 2000a; Gould 2002.) Yet a sentiment
has accumulated in the last two decades that extant evolutionary theory, in
which the reigning mode of explanation is genetic (Lewontin 2000a) and
adaptationist (Gould and Lewontin 1979), represents an ‘‘unﬁnished syn-
thesis’’ (Eldredge 1985; Reid 1985).
The synthetic theory of evolution
worked well at the population genetic level it concentrated on, but popula-
tion genetics is far from the whole story.
The modern synthesis was
increasingly found to run into difﬁculties when it came to explaining char-
acteristics of phenotypic evolution such as biased variation, rapid changes of
form, the occurrence of nonadaptive traits, or the origination of higher-
level organization such as homology and body plans (Mu
¨ller and Newman
1999; Laubichler 2000; Wagner and Laubichler 2004; Mu
Evo-devo, broadly conceived, is addressing seriously Viktor Hamburger’s
(1980) complaint that the modern synthesis treated the processes of ontog-
eny as a ‘‘black box.’’ Current calls for a ‘‘new evolutionary synthesis’’ that
would genuinely incorporate development (Carroll 2000; Gilbert 2003a,
777–779), or for a straightforward ‘‘developmental synthesis’’ (Amundson
1994), revive Waddington’s lifelong but ultimately unsuccessful attempt
to forge a ‘‘ﬁnal’’ uniﬁcation of embryology and evolution ( Wilkins 1997;
Keller 2000b, 251; Van Speybroeck 2002).
Gene-centered biology comes
dangerously close to ofﬁcially long-rejected preformationism.
by the close mapping between genotype and phenotype in many kinds of
modern organisms, it takes an organism’s morphological phenotype—the
physical, organizational, and behavioral expression of an organism during
its lifetime—to be ‘‘determined’’ by its genotype—the heritable repository
of information that ‘‘instructs’’ the production of molecules whose interac-
tions, in conjunction with the environment, generate and maintain the
phenotype. It thus portrays the development of individual organisms as
the unfolding of a ‘‘genetic program’’ alleged to reside in the fertilized
(For critical assessments, see, e.g., Varela 1979; Atlan and Koppel
1989; Rose 1998; Moss 2002; Robert 2004.) Yet, as one dissenter puts it,
‘‘The organism does not compute itself from its genes. Any computer that
did as poor a job of computation as an organism does from its genetic ‘pro-
gram’ would be immediately thrown into the trash and its manufacturer
The Organismic Systems Approach 27
would be sued by the purchaser’’ (Lewontin 2000a, 17). The evolutionary-
theoretical version of the notion of genetic program usually remains
unchallenged even in glosses on neo-Darwinism that otherwise disagree
over such issues as the tempo and mode of phenotypic evolution, the de-
gree to which genetic change can result from selectively neutral mecha-
nisms, and the universality of adaptation in accounting for complex traits
(but see Neumann-Held and Rehmann-Sutter 2006).
Life did not necessarily require DNA to get started (see, e.g., Rosen 1990,
Goodwin 1994, Maynard Smith and Szathma
´ry 1998, Fry 2000, and Hazen
2005, for reviews of theories of the emergence of biological order). How-
ever, it has long entered a regime in which genes are not only indispens-
able for both development and evolution, but have become increasingly
privileged—though never in an absolute sense (Maynard Smith and Szath-
´ry 1995, chap. 6; Gilbert 2003b; Newman 2005). We thus agree with
Schaffner (1998) that the developmental systems perspective (DSP)
too far in claiming that other developmental resources are ‘‘on a par’’ with
genes (Grifﬁths and Gray 1994, 283; cf. Oyama 2000 on ‘‘parity of rea-
soning’’). As Gilbert (2003b, 349) observes, DSP has generally failed to
distinguish between instructive and permissive inﬂuences on epigenetic
The ofﬁcial ‘‘interactionist consensus’’ (Robert 2004) pays
lip service to the realization that genes alone are insufﬁcient for develop-
mental agency (see, e.g., Gray 1992 and Moss 2002 for forceful argu-
ments to this effect), but require the genotype of the developing cells to
interact with their cellular environment for the production of phenotypes.
Yet dominant practice still largely disregards the generative—and hence
explanatory—roles the phenotype per se plays in many biological phenom-
ena. This is true in at least two important ways.
First, at the developmental level, there is no basis for assuming that infor-
mational models according to which ‘‘all the relevant information’’ resides
in the genomic DNA sufﬁce to capture all or even most of the relevant
developmental data (Sarkar 2000). In light of this fundamental limitation
of the informational account of ontogeny, Keller’s (2000b, 245) suggestion
that genetics and molecular biology are ‘‘committed to the goals of causal-
mechanistic explanation’’ must be qualiﬁed. She claims that the ‘‘long-
sought efﬁcient causality’’ came to biology ‘‘with the identiﬁcation of
genes (coupled with the causal properties attributed to them in prevailing
notions of ‘gene action’), and with the more deﬁnitive identiﬁcation of
DNA as the carrier of genetic information (coupled with the notion of a
‘genetic program’).’’ But only on particular contemporary philosophical
interpretations of causation, such as the view that a causal process involves
28 Werner Callebaut, Gerd B. Mu
¨ller, and Stuart A. Newman
the transfer of (a particular token of) information from one state of a
system to another (the so-called conserved-quantity view: Dowe 1992,
2000; Salmon 1994; Collier 1999), can the informational account of ontog-
eny be considered causal.
Genuine causal analysis, taking fully into
account epigenetic and environmental determinants, remains as indis-
pensable as ever—remember Entwicklungsmechanik (Laubichler and Maien-
Second, a similar limitation exists at the evolutionary level, where a full
understanding of selection requires that we capture the regulatory pheno-
typic structures and functions of species. Again the informational picture
must remain incomplete: ‘‘One can construct mathematical ‘laws’ of genet-
ics within the information picture, but one cannot assert that they apply,
nor understand the limits of their application, nor understand the alterna-
tive possibilities where their application breaks down, without recourse to
the details of the causal picture’’ (Hahlweg and Hooker 1989, 85–86.
evolutionary biologists, the emerging focus on developmental mechanisms
is ‘‘an opportunity to understand the origins of variation not just in the se-
lective milieu but also in the variability of the developmental process, the
substrate for morphological change’’ (von Dassow and Munro 1999, 307).
Adding a causal-mechanistic dimension to, say, the historical study of char-
acter evolution also allows one to test evolutionary hypotheses more rigor-
ously (Autumn, Ryan, and Wake 2002). Note that the great debates within
evolutionary biology focus on the causal mechanisms of evolutionary
change rather than on the elucidation of particular phylogenetic relation-
ships (Atkinson 1992). Opposing developmental biology to evolutionary
biology, then, in terms of the distinction between causal-mechanistic
explanation (answering ‘‘How?’’-questions) versus functional explanation
(answering ‘‘Why?’’-questions) would be an oversimpliﬁcation.
‘‘Dawkinsspeak’’ has by now become so prevalent in our media-driven
culture that it may no longer be trivial to point out that, for instance in
the case of our own species, there simply aren’t enough genes to ‘‘determine’’
the phenotype in the simplistic ways envisaged by most behavioral geneti-
cists and evolutionary psychologists, among others. For instance, genes
cannot incorporate enough instructions into the structure of the hu-
man brain to ‘‘program’’ an appropriate reaction to most—let alone all—
conceivable behavioral situations. As Ehrlich (2000, 124) reminds us, there
are roughly 100–1,000 trillion connections (synapses) between more than a
trillion nerve cells in our brains; that is, ‘‘at least 1 billion synapses per gene,
even if every gene in the genome contributed to creating a synapse.’’ Ehr-
lich concludes: ‘‘Clearly, the characteristics of that neural network can be
The Organismic Systems Approach 29
only partially speciﬁed by genetic information; the environment and cul-
tural evolution must play a very large, often dominant role in establishing
the complex neural networks that modulate human behavior.’’
It may be too early to say how modest or revolutionary the changes in
our thinking about evolution occasioned by evo-devo will be (see Gilbert
2003b). But it is certainly timely to observe the profoundly paradoxical na-
ture of the gene-centrism that characterizes the currently dominant evolu-
tionary paradigm. Its fatalist view of phenotypes as ‘‘vehicles’’ that are the
prisoners of their genes (Dawkins’s ‘‘lumbering robots’’) reigns supreme at a
time when the genomes of plants, animals, and increasingly also humans
are dramatically transformed by human agency in the name of health, eco-
nomic proﬁt, and other societal aims, and when ﬁndings in molecular
biology itself (e.g., Lolle et al. 2005) call into question the very ‘‘Central
Dogma’’ that the fatalist view requires. There is much to be said, then, for
Tibon-Cornillot’s (1992, 17) diagnosis of this paradox as a crisis of the neo-
Darwinian paradigm (cf. also Strohman 1997).
To set the scene for our discussion of OSA, we will in the subsequent two
sections consider some of the requirements for evo-devo to become a ma-
ture scientiﬁc ﬁeld. (For a fuller treatment, we refer to Mu
¨ller and Newman
Evo-Devo: A Clash of Weltanschauungen?
Reﬂecting on the renewed interest in the relationship between evolution-
ary biology and developmental biology that awoke in the 1980s, Atkinson
(1992, 93) speculated that their reunion ‘‘may result in a new subdiscipline
of biology, if there is a set of unique concepts and methods which tie the
various research approaches together.’’ Although we think more is involved
in the articulation of evo-devo than conceptual and methodological issues,
we discuss concepts and methods in turn as a ﬁrst approximation to evo-
devo and add two more issues: its explanatory strategies and what we call
Elements of a Conceptual Framework for Evo-Devo
Anticipating current attempts to differentiate evo-devo from more estab-
lished research in developmental biology and evolutionary biology (Gil-
bert, Opitz, and Raff 1996; Hall 2000; Raff 2000; Wagner, Chiu, and
Laubichler 2000; Robert, Hall, and Olson 2001; Amundson 2005; Burian
¨ller 2005, 2006), Atkinson (1992) suggested that concepts such
as bauplan (Riedl 1978), canalization (the reduced sensitivity of a phenotype
30 Werner Callebaut, Gerd B. Mu
¨ller, and Stuart A. Newman
to changes or perturbations in the underlying genetic and nongenetic fac-
tors that determine its expression: Wagner, Booth, and Bagheri-Chaichian
1997; Wilkins 1997; Gibson and Wagner 2000), and developmental con-
straints (see below) may serve in such a capacity.
Today we must add several more concepts to this list. One is inherency,
the propensity of biological materials to assume preferred forms (Newman
and Comper 1990; Newman and Mu
¨ller 2006). Another is evolvability, the
intrinsic potential of certain lineages to change during the course of evolu-
tion (Wagner and Altenberg 1996; Gerhart and Kirschner 1997; Conrad
1998; Kirschner and Gerhart 1998; Newman and Mu
¨ller 2000, Schank and
Wimsatt 2001; Hansen 2003; Earl and Deem 2004; Wagner and Laubichler
2004; Deacon 2006).
Still another crucial concept is developmental modu-
larity (Wagner 1996; von Dassow et al. 2000; Gilbert and Bolker 2001;
Stelling et al. 2001; Schlosser and Wagner 2002; Hall 2003; Burian 2005;
Callebaut and Rasskin-Gutman 2005). Developmental systems are decom-
posable into components that operate largely according to their own,
intrinsically determined principles. These components can be selected
phenotypically. A developmental module consists of a set of genes, their
products, their developmental interactions, and their interactions with
epigenetic factors, including the resulting character complex and its func-
tional effect. The genes affecting the modular character complex are typi-
cally characterized by a high degree of internal integration and a low
degree of external connectivity—that is, pleiotropic relations are largely
within-module. These modules, Brandon (1999, 177) claims, are the units
of evolution by natural selection. Whether this verdict will bring the units
and levels-of-selection debate to a stop remains to be seen. At any rate, as a
principle connecting the genetic and epigenetic components of evolving
developing repertoires, modularity has the potential to assume a central
role in the evo-devo framework (von Dassow and Munro 1999).
Most important, from our perspective, we should add evolutionary origina-
tion,innovation, and novelty, a set of interrelated concepts collectively called
the ‘‘innovation triad’’ (Mu
¨ller and Newman 2005). In this domain, it is
suggested, evo-devo could make its most pertinent contribution to evolu-
tionary theory. We return in a later section to these concepts and the cen-
tral role homology plays in them.
It should be noted that Wagner et al. (2000, 829) distinguish between the
contributions evo-devo makes to the agenda of established research pro-
grams, such as the evolution of adaptations, and the genuine contributions
of evo-devo, such as developmental constraints, evolutionary innovations,
and the evolution of development in general.
The Organismic Systems Approach 31
This much being said, it should be granted that evo-devo is still in search
of a clear conceptual framework in which the aforementioned concepts, as
well as related ones such as robustness—the capacity of organisms to com-
pensate for perturbations (Fontana 2002; de Visser et al. 2003; Kitano
2004; A. Wagner 2005; Hammerstein et al. 2006)—can be integrated in a
logically coherent and cautiously parsimonious way. A ﬁrst necessary step
in this direction may be to elucidate what speciﬁcally constitutes a develop-
mental mechanism (von Dassow and Munro 1999; Salazar-Ciudad, Newman,
´2001, Salazar-Ciudad, Jernuall, and Newman 2003). Increased
clarity on what the proper questions and goals of evo-devo should be is an-
other urgent desideratum, and may actually be easier to reach than one
might expect (Wagner et al. 2000; Robert, Hall, and Olson 2001; Fontana
Comparative developmental biology, experimental developmental biology
¨ller 1991), and evolutionary developmental genetics are the methods
most commonly relied on in evo-devo. These methods clearly are not
unique to evo-devo (Mu
¨ller 2006), and one should not assume that their
combined application will automatically yield unproblematic, novel results
(see von Dassow and Munro 1999). When Haeckel proposed his views on
recapitulation, the union of evolution and development he envisaged was
primarily one of descriptive sciences. For Haeckel, as for Darwin before
him, comparative embryology served as the source of knowledge in the
construction of phylogenies (Richards 1992). Although the nexus between
development and evolution may remain descriptive to a large extent (Nijh-
out, chapter 3, this volume), developmental biology (e.g., Gerhart and
Kirschner 1997; Hall 1999; Gilbert 2003a; Carroll, Grenier, and Weatherbee
2004) has come a long way and today offers a wealth of causal-mechanistic
theories and models—also, but not only, because it has become molecular
(Robert, Hall, and Olson 2001; Mu
¨ller 2005, 2006).
Biologists have long recognized that the evolvability of development is
the key to morphological evolution. But molecular genetics is only now
producing the substantial characterizations of developmental regulatory
processes that make it possible to analyze them comparatively with regard
to common molecular characteristics across a wide range of species ( Wil-
kins 2001; Carroll, Grenier, and Weatherbee 2004).
In an attempt to zero in on the role of developmental mechanisms in
evolutionary processes, and in particular evolutionary innovation, Wagner,
Chiu, and Laubichler (2000) propose a checklist for establishing a causal
32 Werner Callebaut, Gerd B. Mu
¨ller, and Stuart A. Newman
link between molecular developmental evolution and phenotypic evolu-
tion. First, what is the developmental mechanism that accounts for the
derived character (or character state)? More precisely, does the identiﬁed
mechanism account speciﬁcally for the derived character state, or is it
responsible for more fundamental and more ancient, plesiomorphic, char-
acter states within the lineage? Second, does the developmental mecha-
nism for the derived character (or character state) map to the same node
on the phylogeny as the derived character (or character state)? Coincidence
is the ﬁrst test of the causal efﬁcacy of the mechanism in the evolutionary
process. Only mechanisms that were active in the ancestor can account for
the evolutionary origin of the character. The test for this may be difﬁcult
because of the recency bias built into cladistic character reconstruction
methods: by the very nature of the cladistic method applied to recent spe-
cies, the deepest node that in principle can be reconstructed is the most re-
cent common ancestor of the extant clade ( Wagner, Chiu, and Laubichler
2000, 824). Third, what are the developmental changes that occurred at the
origin of the derived character (or character state)? As Wagner and col-
leagues see it, the study of the sequence evolution of developmental regula-
tory genes is a powerful tool for detecting candidate mutations that may be
responsible for developmental and phenotypic transformations, yet this
method has inherent limitations. Fourth, are the genetic differences sufﬁ-
cient to cause the derived character (or character state)? Advances in trans-
genic technology ‘‘make the thought of performing these experiments less
crazy than they were a few years ago’’ (p. 828).
If the answers to all these questions support a hypothesis about the
developmental mechanism for the origin of a novel phenotypic charac-
ter, the conclusion is ‘‘all but unavoidable that this mechanism in fact
was instrumental in causing the origin of the derived character (or char-
acter state) (Wagner, Chiu, and Laubichler 2000, 829).’’ What we call
evolutionary developmental epigenetics is as relevant here as the more familiar
evolutionary-developmental genetics (see below for instantiations).
The Explanatory Strategies of Evo-Devo
From an epistemological point of view, what current evo-devo seems to be
largely lacking is a way to get from the knowledge of parts (entitities and
their properties) and what they do (process, activity)—knowledge that a
ﬁeld like developmental genetics increasingly provides—to a full-ﬂedged,
formal understanding of developmental phenomena. ‘‘Mechanism, per se,
is an explanatory mode in which we describe what are the parts, how they
behave intrinsically, and how those intrinsic behaviors of parts are coupled
The Organismic Systems Approach 33
to each other to produce the behavior of the whole’’ (Von Dassow and
Munro 1999, 309). This commonsense deﬁnition of mechanism implies
an inherently hierarchical decomposition (Von Dassow and Munro 1999, 309;
cf. Glennan 1996, 2002a, 2002b, on mechanism as interaction of parts;
Machamer, Darden, and Craver 2000, 13–18, on mechanism as activity;
Callebaut 2005a on the ubiquity of nearly decomposable systems in na-
ture), which has historically been unattainable to developmental biologists
because their knowledge of the parts was insufﬁcient.
Instead, for expla-
nation we still rely primarily on a sort of local causation: ‘‘The operational
approach of developmental genetics, for instance, takes for granted the or-
ganism as a working whole, with no general assumptions about the nature
of developmental mechanisms beyond the empirical fact that some frac-
tion of mutations have discrete, visible effects. Developmental genetics
begins with an induced anomaly (a mutation) and a (hopefully discrete)
consequence, then proceeds to decipher a perturbation-to-consequence
chain’’ (Von Dassow and Munro 1999, 309). This kind of account allows
a description of what parts (genes and their products) do to each other,
but it ‘‘doesn’t articulate any sense of the mapping from genotype to phe-
notype, which is what we ultimately want’’ (p. 309; see also Hall 2003).
An alternative explanatory strategy focuses on the epigenetic factors that
are causal in the evolution and organization of phenotypes. Here the ge-
neric physical properties of cells and tissue masses and their self-organiza-
tional properties are given priority over the molecules used in these
¨ller and Newman 2003a, 2005, Newman 2005; Newman and
¨ller 2000, 2005).
Our discussion up to now may have suggested that evo-devo is more
monolithic than it actually is. In fact, various accounts of evo-devo exist,
which in part reinforce one another, but in part also compete (box 2.1).
Gene selectionism (e.g., Cronin 1991; Williams 1966, 1992) provides the
antiposition for all these views, as well as for a number of additional, com-
plementary perspectives (box 2.2). It holds that the organism is but ‘‘the
realization of a programme prescribed by its heredity’’ ( Jacob 1970, 2) and
that ‘‘the details of the embryonic developmental process, interesting as
they may be, are irrelevant to evolutionary considerations’’ (Dawkins
1976, 62; but see Maynard Smith 1998). Recent work on niche construc-
tion (Laland, Odling-Smee, and Feldman 1999; Odling-Smee, Laland, and
Feldman 2003), to the extent that it pays lip service to development only
(Wimsatt and Griesemer, chapter 7, this volume), would also seem to be-
34 Werner Callebaut, Gerd B. Mu
¨ller, and Stuart A. Newman
long to the gene selectionist paradigm, and so does the extended replicator
perspective of Sterelny, Smith, and Dickison (1996).
A complication arises from the circumstance that not just competing
theories—broad intellectual perspectives—are at stake. Process structural-
ism, self-organizational approaches to complexity, the dialectical account,
or DSP—to name but a few examples—are typically presented as ‘‘pack-
ages’’ that not only include their own methodology and explanatory strat-
egies, but are embedded in a broader ‘‘philosophy.’’
In this sense, evo-devo perspectives may be likened to (certain com-
ponents of) paradigms, in which a characteristic set of metaphors play
Main evo-devo packages
The main contributors to evo-devo combine theoretical, methodological, and
epistemological perspectives with a genuine research practice. Following Gil-
bert 2003b, we view core evo-devo as encompassing both the program to ex-
plain evolution through changes in development and the program to reframe
evolutionary biology more drastically along developmental lines (e.g., Raff
1996, 2000; Hall 1999, 2000; Gilbert 2003a; see ﬁgure 2.2). Gene regulatory evo-
lution is a research program that arises from the methodical application of
comparative molecular genetics to developmental biology. Its principal aim is
the elucidation of the ‘‘developmental genetic machinery’’ (Arthur 2002) and
the evolution of gene regulation. Presently it represents the most widespread
and empirically productive approach to evo-devo (e.g., Akam 1995; Holland
2002; Carroll et al. 2004; Holland and Takahashi 2005; Davidson 2006). Epige-
netic evo-devo is the main subject of the fourth section of this chapter. Process
structuralism (e.g., Ho and Saunders 1979; Goodwin et al. 1983; Goodwin 1984,
1994; Webster and Goodwin 1996; cf. Depew and Weber 1995, Grifﬁths 1996,
and Eble and Goodwin 2005) is a largely ahistorical approach that aims to
explain form in terms of morphogenetic laws and generative principles. It
regards organisms as ﬁtting into timeless categories (‘‘natural kinds’’), similar
to the periodic table of elements. Approaches to the self-organization of biologi-
cal complexity abound and are multifarious, ranging from Heinz von Foerster’s
‘‘order through noise,’’ elaborated by Henri Atlan (e.g., Atlan and Koppel
1989; Fogelman Soulie
´1991), to Stuart Kauffman’s ‘‘adaptation on the edge
of chaos’’ (e.g., Kauffman 1985, 1992, 1993, 1995) to the Prigogine school in
far-from-equilibrium thermodynamics (e.g., Prigogine and Nicolis 1971; Prigo-
gine and Goldbeter 1981; Nicolis 1995; cf. Camazine et al. 2001). Depew and
Weber (1995) provide an excellent review (see also Callebaut 1998; Richard-
The Organismic Systems Approach 35
Additional evo-devo perspectives
Structural modeling (SM) extends the explanation of phenotypic evolution from
ﬁtness considerations alone—the classical approach—to the topological struc-
ture of phenotype space as induced by the genotype-phenotype map (e.g.,
Fontana and Schuster 1998; Stadler and Stadler 2006). SM focuses on key
aspects of evo-devo, but does not offer a representation of organismal develop-
ment per se. The regulatory networks of gene expression and signal transduc-
tion that coordinate the spatiotemporal unfolding of complex molecules in
organismal development have no concrete analogue in the RNA sequence-to-
structure map. Yet the RNA folding map implements concepts like epistasis
and phenotypic plasticity, thus ‘‘enabling the study of constraints to varia-
tion, canalization, modularity, phenotypic robustness and evolvability’’ (Fon-
tana 2002, 1164). The dialectical account of biology urges thinking in terms of
the organic construction of environments and the interpenetration between
organisms and environments rather than adaptation (Levins 1968; Rose
1982a, 1982b, 1998; Rose et al. 1984; Levins and Lewontin 1985, 2006; Lew-
ontin 1996, 2000a; Rose and Rose 2000; cf. Godfrey-Smith 2001b). Systems
biology aims at explaining life mechanistically at the system (primarily cell)
level. Whereas older work in this area, most notably biological cybernetics,
had to concentrate on phenomenological analysis of physiological processes
(cf. also Piaget, below), systems biology can take advantage of the rapid
progress in molecular biology, furthered by technologies for making compre-
hensive measurements on DNA sequence, gene expression proﬁles, protein-
protein interactions, and so on (e.g., Kitano 2001, 2002, 2004; Bruggeman
et al. 2002; Hood and Galas 2003; Krohs and Callebaut 2007). Extant systems
biology calls for a better awareness of the importance of organizing principles,
in particular hierarchical organization (Mesarovic 1968; Newman 2003b;
Mesarovic et al. 2004). Jean Piaget’s attempt at a cybernetic synthesis (Celle
et al. 1968; Piaget 1971, 1978, 1980), aptly summarized by Parker (2005)
(see also Hendriks-Jansen 1996), is listed here as early attempt to articulate a
phenotype-centered theory of biological and cognitive development and evo-
lution—presumably ﬂawed by Piaget’s endorsement of Lamarckian inheri-
tance (Deacon 2005; but see Hooker 1994). Griesemer’s reproducer perspective
(RP) is a process perspective that aims at understanding development, inheri-
tance, and evolution by way of analyzing the processes that take place
throughout an evolutionary hierarchy of levels of productive organization.
The core idea of RP is material overlap: offspring form from organized parts of
parents, such as cells, rather than by the copying of traits (Griesemer 2000a,
2000b, 2005, 2006b; Wimsatt and Griesemer, chapter 7, this volume). Repro-
ducers can be important units of culture and cultural evolution, despite the
36 Werner Callebaut, Gerd B. Mu
¨ller, and Stuart A. Newman
exemplary heuristic and uniﬁcatory roles (see Jablonka 2000), and typically
also a negative role—demarcation from other approaches.
(1996, 1) words,
All sciences, but especially biology, have depended on dominant metaphors to in-
form their theoretical structures and to suggest directions in which the science can
expand and connect with other domains of inquiry. Science cannot be conducted
without metaphors. Yet, at the same time, these metaphors hold science in an eter-
nal grip and prevent us from taking directions and solving problems that lie outside
(See also Nijhout 1990; Lewontin 2000a, chap. 1.) Metaphors also mediate
between speciﬁc scientiﬁc cultures and culture at large (see, e.g., Schlanger
1971; Haraway 1976; Tibon-Cornillot 1992).
Although one may be tempted to cluster the various approaches to evo-
devo even further—thinking of, for instance, Goodwin’s (1994) vindica-
tion of Kauffman’s (1985, 1993) nonlinear models, or the tendency of
advocates of DSP to portray the critical work of Lewontin and his associates
as belonging to it (e.g., Oyama 2000, 8; Gray 2001, 200; Grifﬁths and Gray
2005, 418–419), or the suggestion that generative entrenchment (Wimsatt
2001) provides DSP with an ‘‘engine’’ (Robert 2004, 126)—the conceptual
and methodological differences between these approaches remain consider-
able. We feel that in this incipient stage of the articulation of evo-devo it is
wiser to cherish and cultivate conceptual and social variety than to apply
common assumption that culture depends on transmission of units that are in
some other way nonbiological. The developmental systems perspective (DSP) is
characterized in notes 10 and 11, and its ‘‘engine,’’ Wimsatt’s generative en-
trenchment, in note 34. Caporael’s (1997) core conﬁgurations model, based on
human morphology and ecology in human evolutionary history, substitutes
the concept of repeated assembly (of organisms, groups, habits, and so forth)
for nature-nurture dualism. For Caporael, core conﬁgurations of face-to-face
groups are the selective context for uniquely human mental systems (cf. also
Wimsatt and Griesemer, chapter 7, this volume). A comparison of Caporael’s
and other recent calls for a ‘‘cognitive evo-devo’’ (e.g., Herna
´ndez Blasi and
Bjorklund 2003) with OSA falls beyond the scope of this chapter.
The Organismic Systems Approach 37
Our distinction between the main evo-devo packages and additional per-
spectives on evo-devo is mostly based on considerations such as the ﬁt be-
tween ideas professed and actual research practice, which is most obvious
in the former case (with ‘‘practice’’ typically preceding ‘‘theory’’). In con-
trast, the holistic incantations of the advocates of a dialectical biology, to
take this example, often seem quite disconnected from their own research
practice, which may be decidedly reductionistic. Or, in the case of DSP,
most of the important research that its advocates invoke as endorsing their
perspective (Grifﬁths and Gray 2005, 417–418), such as Gilbert Gottlieb’s
work in developmental psychobiology and Timothy Johnston’s in learning
theory, predates the articulation of their own perspective (see, e.g., John-
ston 1982), which makes it difﬁcult if not impossible to assess DSP’s con-
structive (e.g., heuristic) potential at present (see Godfrey Smith 2001a).
Other considerations to make our distinction are straightforwardly socio-
logical: intellectual distance to core evo-devo (quantiﬁable by means of bib-
liometric methods), perspectives that are at present advocated by a single
person or small group, or those that are currently taken by many to be ob-
solete (the Piagetian cybernetic synthesis). Evo-devo has incorporated
many of the arguments of the critics of the synthetic theory but seems
more successful at marrying its theory and practice than most of its
Griesemer (2000a, 2002) usefully distinguishes between theories, per-
spectives, and images. Following Levins (1968), he views theories as ‘‘col-
lections of models and their robust consequences’’ that represent and
interpret phenomena (Griesemer 2000a, 350; cf. Wimsatt 1997 and Giere
1999). Theoretical perspectives coordinate models and phenomena; such
coordination is necessary because phenomena are complex, our scientiﬁc
interests in them are heterogeneous, and the number of possible ways of
representing them in models is too large. Adequate theorizing may require
a variety of perspectives and models—a point worth keeping in mind in
discussing what the ‘‘right’’ account of evo-devo is. Genetic determinism
is an instance of a perspective. Theoretical perspectives are expressed in
images that specify preferred lines of abstraction from phenomena of inter-
est and prioritize principles in terms of which models may be constructed
to represent phenomena. Weismannism has been a historically immensely
powerful image of the genetic-determinist perspective, as was Watson’s
central-dogma diagram in the second half of the twentieth century. Many
biologists (e.g., Hood and Galas 2003) today still think of the genetic-
program image as heuristically fruitful.
38 Werner Callebaut, Gerd B. Mu
¨ller, and Stuart A. Newman
What is an image, speciﬁcally? One function of Kuhnian exemplars is to
make phenomena intelligible to students, researchers, and the public at
large. (That the genetic-program image is catchy is plain enough.) Images
that display a mechanism, especially if they are visual, are particulary apt
to engender intelligibility, because they ‘‘show how possibly,how plausibly,
or how actually things work’’ (Machamer, Darden, and Craver 2000, 21).
The intelligibility of an image must not be confounded with the correct-
ness of an explanation: images often will convince us even if, as (shorthand
for) explanations, they are misleading; see de Regt’s (2004) discussion of
understanding. Intelligibility typically also evokes emotions, which in turn
may act as positive or negative motivators.
Coming back to the general issue of evo-devo packages, we must ask to
what extent the close links that are often suggested between speciﬁc theo-
retical notions and speciﬁc metalevel views are really robust or even inevi-
table or rather the result of the contingencies of one’s scientiﬁc and
philosophical education, social background, or standing. This question is
important because, as, for example, Maienschein (2000) has shown for
several of the preformation-versus-epigenesis debates in the eighteenth
and nineteenth centuries, ‘‘epistemology (can) actually . . . drive the science’’
(p. 123). Smith (1992, 433) exempliﬁes a tendency to posit the existence
of a neorationalist, ‘‘European view of metatheory,’’ which is taken to be
‘‘more holistic and less empirical than its American counterpart’’ ( p. 449).
He associates this view with Riedl’s and Wagner’s systems-theoretical anal-
yses (e.g., Riedl 1978; Wagner 1986) as well as with Goodwin’s process
structuralism (e.g., Goodwin 1984, 1994). Although there is some truth in
Smith’s view (Callebaut 1998), his picture is too undifferentiated. For
instance, Riedl’s evolutionary epistemology, which he viewed as an integral
part of his theoretical biology (Riedl 1978; Wagner and Laubichler 2004),
ultimately comes closer to Humean empiricism, with its emphasis on
regularity rather than causation-as-production, than it resonates with the
scientiﬁc-realist view that now dominates Anglo-American philosophy of
biology (Callebaut 2005b). On the other hand, Hooker (1995, 227) and
Mahner and Bunge (1997, 294–299), among others, have argued convinc-
ingly that there is no need to accept such a dichotomy as suggested by
Smith. OSA assumes that one can resituate neo-Darwinian processes within
a complex systems framework without going to either empiricist or ratio-
nalist extremes (see Depew and Weber 1995; Robert 2004).
Against the background of evo-devo packages, the issue of the modesty
or ambition of the various perspectives is not merely a tactical question,
The Organismic Systems Approach 39
let alone a rhetorical ﬂourish. At stake are the actors’ deepest methodologi-
cal, epistemological, and metaphysical convictions, their scientiﬁc ethos,
and perhaps even their politics and ideology. (See, for instance, Ruse 1999,
who discerns a steady increase in the inﬂuence of epistemic values and a
concomitant diminution of wider cultural inﬂuences in the history of evo-
lutionary theorizing since Erasmus Darwin.) Contrast, for instance, George
Williams’s or Edward Wilson’s gene-selectionist austerity (Williams 1966,
1985, 1992; Wilson and Lumsden 1991) with Gould’s pluralist playful-
Compare Maynard Smith’s (1998, 45) ‘‘Reductionists to the Right,
Holists to the Left,’’ whose moral is that ‘‘it pays to be eclectic in our choice
of theories,’’ being ‘‘reductionist in one context and holist in another.’’ As
scientiﬁc realists, we are tempted to add that one should also realize that in
the absence of any direct access to the Truth, it is ultimately on the success
or failure of scientiﬁc careers as proxies for truth that bets are taken (see
Hull in Callebaut 1993, 303; Hull 2001, 171, 182–183). No wonder that
debates will at times be harsh! Difﬁculties in communication between the
contending parties stem in part from the boundary work that accompanies
scientiﬁc discipline building (Galison and Stump 1996; Harre
´2005). An im-
portant task incumbent on philosophers and historians of biology will be
to probe how deeply entrenched the metacommitments of the advocates
of the various perspectives on evo-devo really are.
Reversing Foreground and Background: From Genetics to Epigenetics
In the introduction, Sansom and Brandon see the exclusion of develop-
ment from the study of evolution for much of the twentieth century as
the result of regarding evolution as a change in the genomes of a popu-
lation over time.
On the selﬁsh-gene view, ‘‘natural selection looked
through the organism right to the genome,’’ rendering the process of devel-
opment epiphenomenal to the process of evolution. On this construal, the
evolution of development of a full-ﬂedged organism was but a Ruse (in
both meanings of the word) of natural selection to increase the ﬁtness of
individual genes. This view has many ﬂaws—the ‘‘beanbag’’ assumption,
the assumption that genes are self-replicating, and so on— which have
been sufﬁciently exposed that we can dispense with their discussion here
(see, e.g., Lewontin 2000a, the papers in sections A and B of Singh et al.
2001, or Robert 2004). For our purposes in this chapter it will sufﬁce to
elaborate on the keywords causation (agency), emergence, and pluralism in
the sense of a multilevel, hierarchical theory of natural selection, taking
Gould’s (2001) account as our point of departure. Together, we contend,
40 Werner Callebaut, Gerd B. Mu
¨ller, and Stuart A. Newman
these concepts force evo-devo to take epigenetic considerations—in the
sense of ‘‘epigenesis’’—as primordial for the organismic perspective, leav-
ing it to others (there are plenty) to speak for the gene.
Replication must be displaced from the prominent role it plays in the gene-
centric view of Williams, Dawkins, and Co. because it is not, and cannot
be, the locus of agency. In Gould’s (2001, 213) words, ‘‘Units of selection
must be actors within the guts of the mechanism, not items in the calcu-
lus of results.’’ Griesemer’s reproducer perspective (see box 2.2) begins to
pave the way for a full-ﬂedged philosophical account of evolutionary-
developmental processes as causal-mechanical processes, which can be
based on genetic, epigenetic (ﬁgure 2.1), and environmental causation.
The philosophical view that best ﬁts the causal-mechanistic account
of explanation endorsed by OSA is a variety of philosophical naturalism,
scientiﬁc realism, which holds that (1) the world has a deﬁnite, mind-
independent structure (ontological or metaphysical realism), (2) scientiﬁc
theories are descriptions of their intended domain (whether observable or
not) that are capable of being true or false (semantic realism), and (3) mature
and predictively successful theories are well conﬁrmed and approximately
true of the world (epistemic optimism) (Psillos 2003, 60ff.; cf. Salmon 1984,
Bhaskar 1989, Callebaut 1993, and Hooker 1995). Scientiﬁc realism com-
bines the modest claim that there is a world that is independent from us,
Epigenesis (after Mu
The Organismic Systems Approach 41
largely unobservable, which science attempts to map, with the more ‘‘pre-
sumptuous’’ claim that science can nonetheless succeed in arriving at a
more or less faithful representation of the world, enabling us to know
some (not necessarily ‘‘the’’) truth about it (Psillos 2003, 61)—a position
that cannot be argued for from idealist, empiricist, and most constructivist
premises (constructive realism being an exception; Giere 1988).
The causal-mechanistic account of explanation relinquishes the long-
dominant covering-law account that viewed explanation as ‘‘subsumption’’
under one or more universal laws. (For example, that Newton’s proverbial
apple fell from the tree was taken to be explainable as an instantiation of
his law of gravity in conjunction with appropriate initial and boundary
conditions.) Instead, explanation is now accounted for in terms of mecha-
nistic models (Salmon 1984, 1989, 1994, 1998; Bechtel and Richardson
1993; Glennan 1996, 2002a, 2002b; Machamer, Darden, and Craver
2000), capacities, powers, or propensities (Fisk 1973; Cartwright 1989; Ellis
1999), and, taking into account human cognitive limitations, ‘‘major fac-
tors’’ (Wimsatt 1974, 1976). This is not to say that functional/teleological
explanation can be dispensed with at all levels, but the hope is that they
can be rephrased so as to ﬁt the general causal explanatory mold (see Sober
1993, 82–87, on naturalizing teleology and the distinction between onto-
genetic and phylogenetic adaptation). Similarly, when, say, OSA interprets
homologues as ‘‘attractors’’ of morphological design, this begs for an expla-
nation, not of how the event to be explained was in fact produced, but
of ‘‘how the event would have occurred regardless of which of a variety of
causal scenarios actually transpired’’ (Sober 1983, 202ff.); also see our dis-
cussion of inherency below. Such ‘‘equilibrium explanations’’ (Sober) pres-
ent disjunctions of possible causal scenarios, but the explanation does not
specify which of them is the actual cause. Another complication with
causal explanation, which we can only mention here without discussion,
considers the desideratum that biological research should substitute for
past causes the ‘‘traces’’—state variables; see, for example, Padulo and Arbib
1974—left in the present by the operation of those causes (cf. Elster 1983,
33, and note 29).
Gene-centrism counterfactually supposes that genes ‘‘build organisms’’ en-
tirely in an additive fashion without nonlinear interactions among genes
and their products, or for that matter, the physical processes that govern
the material systems of which gene products are only one portion ( New-
man 2002). However, the fact of emergence is indisputable: ‘‘This aspect
42 Werner Callebaut, Gerd B. Mu
¨ller, and Stuart A. Newman
of the question is empirical but also entirely settled (and never really con-
troversial): organisms are replete with emergent properties; our sense of
organismic functionality and intentionality arises from these emergent fea-
tures’’ (Gould 2001, 213; see Schlanger 1971; Pluhar 1978; Minati and Pessa
2002; Hooker 2004). Thus Dawkins’s colorful metaphors of selﬁsh genes
and manipulated organisms ‘‘could not be more misleading, because he
has reversed nature’s causality: organisms are active units of selection;
genes, although lending a helpful hand as architects, remain stuck within’’
(Gould 2001, 213–214). Hull’s (1982, 1988) apt replacement of Dawkins’s
replicator-vehicle distinction by replicators and interactors, respectively,
ﬁne-tunes Lewontin’s (1970) formalization of evolution as ‘‘heritable varia-
tion in ﬁtness,’’ but needs to be complemented by an account of what is
materially transferred in evolution and development—Griesemer’s ‘‘repro-
ducer perspective,’’ inspired by Maynard Smith’s account of units of evolu-
tion in the 1980s, whose key principle is multiplication (see box 2.2).
Individuals need not replicate themselves to be units of selection; it sufﬁces
that they contribute to the next generation by hereditary passage, and
‘‘magnify’’ their contributions relative to those of other individuals (Gould
2001; cf. Lewontin 1996 and Griesemer 2000a). Selection, then, occurs
‘‘when this magniﬁcation results from the causal interaction of an evolution-
ary individual (a unit of selection) with the environment in a matter that
enhances the differential reproductive success of the individual’’ (Gould
2001, 216, emphasis in the original). Emergence, by contrast, can be seen
as a by-product of dynamic systems (development) under evolutionary
modiﬁcation, regardless of whether selection or other factors initiate the
The modern synthesis was neither a consensus in favor of, nor a consensus
against, a hierarchical concept of evolution. However, among the pioneers
of the synthesis, Sewall Wright’s thinking was paradigmatically hierarchical
(Gayon 1989, 36). Wright’s inﬂuence has clearly been instrumental in the
comeback of group selection, which recently ‘‘has risen from the ashes
to receive a vigorous rehearing’’ (Gould 2001, 216; see, e.g., Wade 1978,
Wimsatt 1980, Sober and Wilson 1998, and Griesemer 2000c). This revival
rests on two proposals that Gould and others believe can serve as center-
pieces for a general theory of macroevolution: (1) the identiﬁcation of evo-
lutionary individuals as interactors, causal agents, and units of selection,
and (2) the validation of a hierarchical theory of natural selection based
on the recognition that evolutionary individuals exist at several levels of
The Organismic Systems Approach 43
organization, including genes, cell lineages, organisms, demes, species, and
clades (Gould 2001, 216). A multiple-level view of evolution was also vin-
dicated quite independently by the biologists and founders of general
systems theory such as Ludwig von Bertalanffy (e.g., 1968) and Paul
Weiss (e.g., 1970), who in turn inﬂuenced Riedl (1978), Wagner (1986),
and OSA, and contributed to the current rise of systems biology (see box
Reclaiming the phenotype, understood as a multilevel, hierarchical sys-
tem, as the central concern of biology, we must qualify Smith and San-
som’s (2001) contention that ‘‘evolution has resulted in organisms that
develop.’’ Relocating the causal nexus in epigenetic processes, we call for
equal consideration of the proposal that development has resulted in popula-
tions of organisms that evolve. The next section will be an elaboration of this
reversal of foreground and background. We propose to call the approach to
evolution that seeks to incorporate the issues of causation, emergence, and
pluralism with respect to levels into the formal framework of evolutionary
theory the organismic systems approach.
The Organismic Systems Approach (OSA)
Evo-devo, eco-devo (Gilbert 2001), systems biology, and other concepts
of organismic evolution contribute to OSA. At present the core conceptual
framework is being provided by evo-devo. Contrary to unilinear, quasi-
monocausal concepts of evolution such as genetic determinism, evo-devo
as the empirical and theoretical analysis of the causal connection between
embryological/developmental and evolutionary processes is immanently
dialectical (ﬁgure 2.2). On the one hand, evo-devo is interested in the fac-
tors that together explain the origination of ontogenetic systems and the
mechanisms that account for their subsequent modiﬁcation. On the other
hand, it investigates the ways in which the properties of ontogenetic
processes inﬂuence the course of morphological evolution (see Raff 2000;
How can OSA contribute to an extended evolutionary synthesis? A num-
ber of conceptual and methodological issues were mentioned above as part
of the evo-devo packages. In this section we concentrate on epigenetic evo-
devo concepts, leaving a treatment of and comparison with other work for
another occasion. In our view, the most salient contributions of OSA are
plausible theoretical and, where possible, also empirical accounts of: (1)
the generation of primordial organismal form and structure (origination),
(2) how novel structures arise in phenotypic evolution (innovation), (3)
44 Werner Callebaut, Gerd B. Mu
¨ller, and Stuart A. Newman
why not all the design options of a phenotypic space are realized (con-
straints), and (4) the causal processes that together make for the organiza-
tion of the integrated phenotype (homology). In this chapter we can only
discuss these issues in an abbreviated form; for a more complete survey, see
Origination of Primordial Organ Forms and Body Plans
According to OSA, the correlation of an organism’s form with its genotype,
rather than being a deﬁning condition of morphological evolution, is a
highly derived property. This implies that other, nongenetic causal deter-
minants of biological morphogenesis have been active over the course of
evolution. Here it is necessary to distinguish between those mechanisms
that are involved in the primary generation of ﬁrst metazoan structures
and body plans, origination (discussed in this section), the later modiﬁca-
tion of these arrangements by the processes of innovation (discussed in
the following section), and variation, the mode of change dealt with most
successfully by the neo-Darwinian paradigm.
Plasticity of form and developmental trajectory in modern-day organisms
(West-Eberhard 2003) provides the starting point for this novel perspec-
tive on the origination of more ancient forms. Protists, fungi, plants, and
animals such as arthropods and mollusks, may exhibit radically different
forms in different environments or ecological settings. Candida albicans,
for example, a fungal pathogen in humans, does not seem to have a
The dual structure of evo-devo. The two subagendas, evo-devo and devo-evo, address
different kinds of questions (from Mu
The Organismic Systems Approach 45
‘‘default morphology’’ (Magee 1997); rather, it is able to switch among
forms ranging from single budding cells, to threadlike hyphae, to strings
of yeastlike cells plus long separated ﬁlaments (‘‘pseudohyphae’’), depend-
ing on the local environment. In mice, the number of vertebrae can de-
pend on the uterine environment: fertilized eggs of a strain with ﬁve
lumbar vertebrae preferentially develop into embryos with six vertebrae
when transferred into the uteri of a six-vertebra strain (McLaren and
Michie 1958). Tadpoles of the frog Rana temporaria undergo signiﬁcant
changes in body and tail morphology within four days when subjected to
changed predation environment (Van Buskirk 2002).
Neo-Darwinian interpretations of these phenotypic polymorphisms pres-
ent them as speciﬁcally evolved adaptations and therefore sophisticated
products of evolution. The different phenotypes of an organism with a
given genotype are thus considered to be outcomes of subroutines of an
overall genetic program that evolved as a result of distinct sets of selective
pressures at different life-history stages. Alternatively, they are seen as man-
ifestations of an evolutionary ﬁne-tuned ‘‘reaction norm,’’ or as products of
evolution for evolvability. According to OSA, in contrast, much morpho-
logical plasticity is a reﬂection of the inﬂuence of external physicochemical
parameters on any material system and is therefore primitive and inevitable
rather than programmed (ﬁgure 2.3 and box 2.3).
Viscoelastic materials such as clay, rubber, lava, and jelly (soft matter: de
Gennes 1992), are subject (by virtue of inherent physical properties) to
being molded, formed, and deformed by the external physical environ-
ment. Most living tissues are soft matter, and all of them are also excitable
media—materials that employ stored chemical or mechanical energy to
respond in active and predictable ways to their physical environments
(Mikhailov 1990). Much organismal plasticity results from such material
Ancient organisms undoubtedly exhibited less genetic redundancy, met-
abolic integration, homeostasis, and developmental canalization than
modern organisms and were thus more subject than the latter to external
molding forces. Hence it is likely that in earlier multicellular forms mor-
phological determination based on an interplay of intrinsic physical prop-
erties and external conditions was even more prevalent than it is today. In
the scenario envisioned by OSA, then, morphological variation in response
to the environment is a primitive, physically based property, carried over to
a limited extent into modern organisms from the inherent plasticity and
responsiveness to the external physical environment of the viscoelastic
cell aggregates that constituted the ﬁrst multicellular organisms.
46 Werner Callebaut, Gerd B. Mu
¨ller, and Stuart A. Newman
Spheres and tissue layering from in vitro combinations of cells with different surface
tensions (dyne/cm) (after Foty et al. 1996).
From the pre-Mendelian to the Mendelian world
Interchangable, generic forms resulting from multicellular aggregates, with no
ﬁxed, heritable relation between genotype and phenotype
Stabilized, heritable forms resulting from an increasingly ﬁxed matching be-
tween genotype and phenotype established by natural selection
Source: Newman and Mu
The Organismic Systems Approach 47
The correspondence of a given genotype to one morphological pheno-
type, as typically seen in higher animals (but less so in multicellular pro-
tists, fungi, and plants), will be exceptional, then. Such close mapping can
result from an evolutionary scenario in which the developmental mecha-
nism by which a phenotype is generated changes from being sensitive to
external conditions to being independent of such conditions. If modern
organisms are ‘‘Mendelian,’’ in the sense that genotype and phenotype are
inherited in close correlation, and that morphological change is most
typically dependent on genetic change, then the organismic systems hy-
pothesis includes the postulate that there was a ‘‘pre-Mendelian world’’ of
polymorphic organisms at the earliest stages of metazoan evolution whose
genotypes and morphological phenotypes were connected in only a loose
fashion (box 2.3; see also Newman 2005).
In this exploratory period of organismal evolution, the mapping of geno-
type to morphological phenotype would have been one-to-many, rather
than one-to-one. This changed as the subsequent evolution of genetic
redundancies (e.g., A. Wagner 1996) and other mechanisms supporting re-
liability of developmental outcome forged a closer linkage between genetic
change and phenotypic change. In particular, natural selection that fa-
vored the maintenance of morphological phenotype in the face of environ-
mental or metabolic variability, produced organisms characterized by a
closer mapping of genotype to phenotype—that is, the familiar Mendelian
world. But even as body plans and other major morphological features,
such as the bauplan of the vertebrate limb ( Newman and Mu
became locked in by the accumulation of reinforcing genetic circuitry,
ﬁne-tuning of details of organismal, and particularly organ morphology
continued (and continues) to occur through an interplay, albeit diminished
in effect, of genetic and nongenetic factors.
Cell-cell adhesion is an evolutionary novelty that was the sine qua non
of the earliest multicellular forms. Adhesivity is unlikely to have been strin-
gently regulated with regard to expression levels on the occasion(s) when
it ﬁrst appeared. Subpopulations of cells in multicellular aggregates with
adhesive differentials exceeding a threshold level will sort out, leading
to multilayered structures (Steinberg and Takeichi 1994)—morphological
novelties that would have been objects of natural selection. The stabili-
zation of differential adhesion was thus probably among the earliest
examples of biochemical differentiation to have become established in the
metazoan world. Differential adhesion was coupled variously with cell po-
larity, inherent physical attributes and behaviors of cell aggregates (includ-
ing diffusion and the formation of gradients), biochemical oscillation, and
48 Werner Callebaut, Gerd B. Mu
¨ller, and Stuart A. Newman
standing wave formation. It would thus have generated a panoply of mor-
phologically distinct forms—multilayered, hollow, segmented, separately
and in combination (ﬁgure 2.4)—that is, novel organisms with the capacity
to populate correspondingly new ecological niches (see Newman et al.
2006 for a more detailed account).
Evolutionary Innovation and Morphological Novelty
Once primordial structures and body plans had originated, phenotypic evo-
lution proceeded through variation and innovation. OSA recognizes a dis-
tinction between these two processes. As a consequence, morphological
novelties, such as feathers, eyes, or skeletal elements (box 2.4), represent a
speciﬁc class of phenotypic change that differs from adaptations (Mu
and Wagner 2003; Mu
¨ller and Newman 2005; Wagner and Lynch 2005). It
also holds that the processes underlying the generation of novelties are
qualitatively different from the standard mechanisms of variation—that is,
Repertoire of generic forms. Virtually all the features seen in early development of
modern metazoan organisms can be attributed to the composition of one or more
of the pattern-forming mechanisms with differential adhesion (Newman 1994). The
combined effects of the various physical properties that were generic to the earliest
multicellular aggregates considered as chemically excitable, viscoelastic soft matter,
ensured the production of a profusion of forms.
The Organismic Systems Approach 49
variation (plus selection) is considered to produce adaptation, whereas the
outcome of innovation (plus selection) is novelty.
The treatment of the innovation and novelty problem depends to a great
extent on how phenotypic novelties are deﬁned (Mu
¨ller 2002; Love 2003).
Several deﬁnitions have been proposed,
but an operational deﬁnition
favors the use of a morphological-character concept and of homology crite-
ria: a morphological novelty is ‘‘a structure that is neither homologous to
any structure in the ancestral species nor homonomous to any other struc-
ture of the same organism’’ (Mu
¨ller and Wagner 1991, 243). This deﬁnition
is narrow, excluding characters that deviate only quantitatively from the
ancestral condition and that may often be regarded as novelties in a func-
tional sense, but it permits identiﬁcation of unambiguous cases of morpho-
logical novelty. Examples that satisfy the deﬁnition exist in all tissues and
organ systems of plants and animals, such as, in the latter case, the skeletal
system (box 2.4).
Focusing on novelties selected in accordance with this deﬁnition, it
becomes possible for evo-devo to address empirical questions concerning
the initiating conditions and the speciﬁc mechanistic processes responsible
for the generation of a particular novelty. Here OSA does not give priority
to the notion of genetic program that tacitly or overtly underlies the tradi-
tional account. Mutational change unavoidably accompanies any kind of
phenotypic evolution, if only as a consolidator of change, but is not neces-
sarily causal for the inception of new complex traits, except probably in
rare cases of mutations with large and coordinated pleiotropic effects. OSA
Examples of morphological novelties
Panda’s ‘‘thumb’’ (panda bears)
Panda’s ‘‘7th digit’’ (panda bears)
snout bone (boars)
third forearm bone (golden mole)
ﬁbular crest (theropod dinosaurs, birds)
preglossale (passerine birds)
patella (birds, mammals)
Source: After Mu
¨ller and Wogner 1991.
50 Werner Callebaut, Gerd B. Mu
¨ller, and Stuart A. Newman
argues that the majority of novelties result from higher-level organizational
properties, epigenetic interactions, and environmental inﬂuences that arise
during the modiﬁcation of established developmental systems. In this
sense, novelties would be epigenetic by-products of the systems properties
Among the initiating causes of innovation feature: natural selection, be-
havioral change (Mayr 1958, 1960), symbiotic combination (Margulis and
Fester 1991), and environmental induction (Gilbert 2001; West-Eberhard
2003). OSA holds that, whatever the initiating conditions, the speciﬁcity
of the resulting novelty is determined by the systems properties of develop-
ment. In the case of natural selection, for instance, it is clear that selection
cannot act on characters that are not yet in existence, and hence selec-
tion cannot directly cause novelty (see the subsection on ‘‘Selection and
Emergence’’ below). Rather, as has been argued in several different con-
texts, novelties often arise as developmental side effects of selection, which
acts on such parameters as body shape, size, or proportions, through the al-
teration of developmental processes—for example, the modiﬁcation of cell
behaviors or of developmental timing (Hanken 1985; Mu
¨ller 1990; Mu
and Wagner 1991; Newman and Mu
¨ller 2000). In these and earlier views
(Schmalhausen 1949) selection is regarded as a facilitating factor or as a
general boundary condition rather than a direct cause of novelty.
The speciﬁc developmental mechanisms of novelty generation can also
be multiple. Morphological novelties can be based on innovations at the
molecular or cellular levels of development, including the establishment
of new developmental interactions, or on the redeployment of existing
developmental modules at a new location in the embryo. Other possibil-
ities include the subdivision or combination of developmental modules, or
the developmental individualization of serial structures such as teeth, verte-
brae, or hair (Mu
¨ller and Wagner 2003). Currently the bulk of empirical re-
search is focused on the evolution of new gene regulatory interactions and
the recruitment of genes and gene circuits into new developmental func-
tions, as seen in a growing number of examples (Shapiro et al. 2004; Colo-
simo et al. 2005). Understanding the kinetics (Bolouri and Davidson 2003),
dynamics (Cinquin and Demongeot 2005), and topological aspects (von
Dassow et al. 2000; Salazar-Ciudad, Newman, and Sole
´, and Newman 2001, Salazar-Ciudad, Jernvall, and Newman
2003) of developmental gene regulation and their correlation with mor-
phogenetic events will be central in this endeavor. But as argued above, it
will be equally necessary to elucidate the speciﬁc epigenetic conditions of
novelty generation such as the role of biomechanics.
The Organismic Systems Approach 51
In summary, by considering the emergence and transformation of devel-
opmental mechanisms as an evolutionary problem in its own right,
OSA arrives at the view that epigenetic mechanisms, rather than genetic
changes, are the major sources of morphological novelty in evolution.
Phenotypic evolution is limited and biased by developmental constraints
that are contingent for all phylogenetic lineages (Maynard Smith et al.
1985). Constraints represent a central evo-devo principle (Streicher and
¨ller 1992; Amundson 1994; Eberhard 2001; Mayr 2001, 198–200; Wag-
ner and Mu
¨ller 2002), and hence are covered by OSA, but need not be dis-
cussed in detail here, because their role is widely accepted and now belongs
to the standard picture (Schwenk and Wagner 2003). The relaxation or
breaking up of constraints, which may be required in instances of innova-
tion, is an important phenomenon that is readily accommodated by OSA.
Possible mechanisms of constraint relaxation include mutational events or
neutral phenotypic drift (Mayr 1960). But even in closely studied cases the
interpretation of whether or not developmental constraints had to be over-
come for the origination of an innovation can be difﬁcult (cf. Eberhard
2001 versus Wagner and Mu
¨ller 2002). Certainly constraints should not be
understood as mere limitations to phenotypic variation, since they can also
provide taxon-speciﬁc opportunities for novelties to arise. A novelty can
result from a constrained developmental system, not because genetic or
developmental variation is relaxed, but precisely because the system is un-
able to respond by variation and is forced to transcend a developmental
¨ller 1990; Streicher and Mu
¨ller 1992). This can provide
heightened potentialities for innovation in particular areas of phenotypic
character space (Roth and Wake 1989; Arthur 2001).
The three features of OSA discussed above all pertain to the phenotype
in evolution. Consequently, OSA takes the organization of the phenotype
as its conceptual hallmark, in contrast to evolutionary theories that
concentrate on gene frequencies in populations. The explanation of the
genotype-phenotype relationship, not as an abstract statistical correspon-
dence but in terms of mechanistic processes of structural organization, is
the concern of OSA. In this it takes the evolution of characters and char-
acter states as realities and proposes that once generic morphological
templates and novelties emerged through the interplay of epigenetic and
genetic factors, they served as organizers in the further evolution of the
52 Werner Callebaut, Gerd B. Mu
¨ller, and Stuart A. Newman
phenotype and, at the same time, of their regulatory mechanisms in
This summary of OSA’s position regarding the evolution of organization
requires further speciﬁcation. The kind of organization most relevant to
this perspective is the generation, integration, and ﬁxation of morphologi-
cal building elements that result in evolutionarily stable body plans. These
are the terms in which OSA represents the homology problem in evolution-
ary theory. It assumes that the constructional components have an orga-
nizing role in organismal evolution, a position that has been labeled the
‘‘organizational homology concept’’ (Mu
¨ller 2003; Love and Raff 2005).
The concept holds that, as more and more constructional detail is added,
the already ﬁxated and developmentally individualized parts (homologues)
serve as accretion points for new components added in the evolving body
plans. Furthermore, the homologues that initially arise from generic prop-
erties of cell masses, and later from conditional interactions between cells
and tissues, provide ‘‘morphogenetic templates’’ for an increasing bio-
chemical sophistication of cell and tissue interactions (Newman and Mu
ler 2000). Although their co-option by the evolving genome results in
the so-called genetic ‘‘programs’’ of development, the dynamics of these
genetic control systems would involve stabilizing and ﬁne-tuning the mor-
phogenetic templates already present. Hence the sequence of gene expres-
sion changes associated with the generation of pattern and form during
embryogenesis would be a consequence, not a cause, of phenotypic organi-
zation. At their ﬁnal stage, the organizational homology concept asserts,
homologues become autonomized—that is, the constructional building
elements of the phenotypes become independent from their molecular
and developmental underpinnings and come to act as attractors in body
plan evolution (Striedter 1998).
The organizational homology concept brieﬂy summarized here is a bio-
logical homology concept (Roth 1984; Wagner 1989), because it refers to
the biological mechanisms that underlie the origination of homology,
rather than to the genealogical and taxonomic aspects that are emphasized
in historical homology concepts. Organizational homology recognizes the
role of developmental constraints, but gives priority to the active contribu-
tions of organizing processes rather than to passive limitations.
The empirical approach to organization prompts the use of new, compu-
tational tools that can accurately represent the relationship between gene
activation, cell behavior, and morphogenesis. A host of such tools are being
developed (e.g., Jernvall 2000; Streicher et al. 2000; Streicher and Mu
2001; Costa et al. 2005; Weninger et al. 2006). The data obtained by these
The Organismic Systems Approach 53
and other techniques can be used to derive formal models of the principles
relating genotype and phenotype, with the capacity to make testable pre-
dictions about the evolution of organization (Salazar-Ciudad, Newman,
´2001; Salazar-Ciudad, Sole
´, and Newman 2001; Britten 2003; Bis-
sell et al. 2003; Nijhout 2003; Rasskin-Gutman 2003).
Major Evolutionary Problems Addressed by OSA
OSA addresses a number of issues that are sidestepped by the received
theory. OSA’s explanatory focus is on phenotypic evolution. Homology,
homoplasy, novelty, modularity—to name the principal ones—are pheno-
typic phenomena that are not speciﬁcally dealt with in the neo-Darwinian
framework and by its population-genetic methods. In OSA these problems
are regarded as central and are explained on the basis of mechanistic pro-
cesses rather than statistical associations with abstract gene frequencies.
Therefore, OSA-based models can be predictive not about which characters
are going to be maintained in a population (the neo-Darwinian selection
focus) but about what is likely to arise structurally. In addition, OSA
addresses a number of long-standing issues in the neo-Darwinian discourse.
Tempo and Mode of Phenotypic Evolution The punctualism-gradualism
debate receives renewed attention in OSA because development has non-
linear system properties that can result in punctuated events even when
submitted to continuous change. Taking these properties into consider-
ation, instances of rapid change of form are not only possible but are to be
expected. The burst of morphological diversiﬁcation recorded in the early
Cambrian fossil record, for instance, rather a conundrum for any gradual-
istic theory, becomes much more easy to explain in a developmental
framework that considers generic mechanisms of form generation. The
framework of OSA suggests a pre-Mendelian phase of organismal evolution
that conceivably laid the basis for this ‘‘Cambrian explosion’’ and the rapid
elaboration (on the geological time scale) of the modern metazoan body
plans that followed (Newman and Mu
¨ller 2000; Newman 2005). The ﬁrst
morphologically complex multicellular organisms, represented by the Ven-
dian fossil deposits, appear to have been ﬂat, often-segmented, but appar-
ently solid-bodied creatures. The concurrence of polarized cells with the
multicellular state has the inevitable physical consequence of producing
organisms with distinct interior cavities. Body cavities thus were a topolog-
ical innovation permitting new geometric relationships among tissues and
facilitating the origination of tissue multilayering, including triploblasty.
54 Werner Callebaut, Gerd B. Mu
¨ller, and Stuart A. Newman
The mobilization of additional physical processes (differential adhesion,
molecular diffusion, biochemical oscillation, Turing-type reaction-diffusion
coupling) would have spurred the rapid elaboration of all the modern body
plans within a space of perhaps 25 million years during the 100 million
years following the advent of the Vendian forms (Newman 1994, 2005).
That this could have occurred with little or no genetic evolution may also
provide a resolution to the paradox (within the neo-Darwinian framework)
of the conservation of the ‘‘developmental-genetic toolkit’’ (Carroll et al.
2004) across all animal phylogeny (Newman 2006).
Selection and Emergence Neo-Darwinism is about the dynamics of alleles
in populations as determined by mutation, selection, and drift. A theory
based on the dynamics of alleles, individuals, and populations must assume
the prior existence of these entitities. But selection cannot set in until there
are entitities to select. This is the problem of innovation, which was previ-
ously often referred to as ‘‘emergence.’’ Although frequently mentioned as
a property of complex systems such as development (e.g., Boogerd et al.
2005), emergence remained without representation in evolutionary theory.
OSA’s mechanistic concept of innovation ﬁlls this void by moving beyond
the neo-Darwinian focus on variation-selection dynamics.
In this context, Fontana and Buss’s (1994a, 1994b) modeling of an ab-
stract chemistry implemented in a l-calculus-based modeling platform is
highly relevant. In their model world (see also box 2.2) the following fea-
tures are generic, and hence would be expected to reappear if the ‘‘tape’’
of evolution were run twice: (1) hypercycles of self-reproducing objects
arise; (2) if self-replication is inhibited, self-maintaining organizations arise;
and (3) self-maintaining organizations, once established, can combine
into higher-order self-maintaining organizations. Darwinian selection pre-
supposes the existence of self-reproducing entitities; but self-maintaining
organizations can arise in the absence of self-reproducing entities. According to
Fontana and Buss (1994a, 761),
self-reproduction and self-maintenance are shared features of all extant organisms,
barring viruses. It is not surprising, then, that there has been little attention paid to
the generation of one feature independently of the other. While selection was surely
ongoing when transitions in organizational grade occurred in the history of life
[Griesemer 2000c], our model universe provides us the unique opportunity to ask
whether selection played a necessary role.
Their ﬁndings indicate that it need not. They conclude that ‘‘separating
the problem of the emergence of self-maintenance from the problem of self-
reproduction leads to the realizazion that there exist routes to the generation
The Organismic Systems Approach 55
of biological order other than that of natural selection’’ (cf. Goodwin 1984,
Integration In a theoretical framework that does not account for the
generative and the emergent, there is no major requirement to deal with
integration, and consequently such proposals were dismissed (e.g., Wad-
dington’s assimilation). In OSA innovation and novelty play a central role,
and, consequently, integration is reemphasized. Here the problem is how
novelties are accommodated into the preexisting, tightly coupled, con-
structional, developmental, and genetic systems of a taxon, to ensure
their functionality and inheritance. Integration is likely to take place
through different mechanisms, acting among and between different levels
of organization—genetic, developmental, phenotypic, and functional.
Waddington (1956, 1962) anticipated genetic integration, following from
selection acting on the genetic variation that will arise with the spreading
of a novel character. Today this corresponds in part to the notion of co-
option during which orthologous and paralogous regulatory circuits ac-
quire new developmental roles over the course of evolution ( Wray 1999;
Wray and Lowe 2000; Carroll et al. 2004). The consequential genetic
integration will increasingly stabilize and overdetermine the generative
processes, resulting in an ever-closer mapping between genotype and phe-
notype. Such transitions can be interpreted as a change from emergent
to hierarchical gene networks (Salazar-Ciudad, Newman, and Sole
´, and Newman 2001).
OSA provides for the possibility that not all integration necessarily rests
on early genetic ﬁxation. Many phenotypic characters can be experimen-
tally suppressed by changing the epigenetic conditions of their formation
and, on the other hand, experimentally induced modiﬁcations in one sub-
system of development can be accommodated by other subsystems even
when the initial change is dramatic. On the basis of this evidence it is
argued that epigenetic integration will usually come ﬁrst, and may sufﬁce
to maintain a novelty for long evolutionary periods, without any need for
genetic ‘‘hardwiring’’ of the new interactions. But the epigenetic patterns
of integration may also provide the templates for subsequent genetic inte-
gration (Newman and Mu
¨ller 2000; Mu
¨ller 2003b). Epigenetic integration
‘‘locks in’’ the novel characters that arose as a consequence of the mecha-
nisms discussed earlier and thus will generate stability (and even herit-
ability) of new building units in organismal body plans. Similar concepts
emphasizing epigenetic integration are generative entrenchment (Wimsatt
1986, 2001) and epigenetic traps (Wagner 1989).
56 Werner Callebaut, Gerd B. Mu
¨ller, and Stuart A. Newman
Inherency If the morphological organization of organisms is (in an evolu-
tionary sense) predictable to a certain degree from the material properties
and generative rules of their constituent tissues (compare Vermeij 2006 on
the predictability of evolutionary innovations), then an additional princi-
ple is added to the external selectionism paradigm of neo-Darwinism. This
principle we propose to call inherency (Newman and Mu
¨ller 2006). ‘‘Some-
thing is inherent either if it will always happen (e.g., entropy) or if the
potentiality for it always exists and actuality can only be obstructed’’ (Eck-
stein 1980, 138–139).
In the evolutionary context inherency means that the morphological
motifs of modern-day organisms have their origins in the generic forms
assumed by cell masses interacting with one another and their microenvir-
onments, and were only later integrated into developmental repertoires by
stabilizing and canalizing genetic evolution.
Therefore, in OSA, the causal
basis of phenotypic evolution is not reduced to gene regulatory evolution
and population genetic events, but includes the formative factors inherent
in the evolving organisms themselves, such as their physical material prop-
erties, their self-organizing capacities, and their reactive potential to exter-
nal inﬂuence. Whereas neo-Darwinism from Monod (1971) to Williams
(1985, 1992) and Gould (2002) emphasized the contingency of evolution
(as does DSP with respect to development: Oyama, Grifﬁths, and Gray
), the watchword of OSA becomes inherency.
Regarding individual development, inherency deﬁes the ‘‘blueprint’’ or
‘‘program’’ notions that abound in present accounts. Cell collectives and
tissue masses take on form not because they are instructed to do so but
because of the inherent physical and self-organizational properties of inter-
acting cells. This does not mean that genes have no role or that gene regu-
lation is unimportant in development. Of course cell properties and cell
interaction of all organisms, ancient and modern, depend on the molecules
that genes specify, but the resulting biological forms and speciﬁc cell
arrangements are not encoded in any deterministic fashion in the genome
(Neumann-Held and Rehmann-Sutter 2006). Inherency locates the causal
basis of morphogenesis in the dynamics of interaction between genes, cells,
and tissues—each endowed with their own ‘‘autonomous’’ physical and
functional properties (ﬁgure 2.1).
Epistemological and Pragmatic Aspects of Evo-Devo
Will developmental biology only (re)supplement evolutionary biology, or
could evo-devo eventually prompt a fundamental theoretical rethinking of
The Organismic Systems Approach 57
evolution itself (see Depew and Weber 1995)? The honest but easy his-
torian’s answer is, of course, that it is too early to tell (Hull 2006), but as
participating scientists and philosophers we have a different ax to grind.
Scenarios in terms of ‘‘modesty’’ versus ‘‘ambition’’ have been suggested.
A caveat seems in order here. The task the proponents of an extended,
‘‘evo-devo synthesis’’ face may be so formidable that even achieving more
modest aims may turn out herculean. A historical perspective is useful here.
Amundson (1994, 576) reminds us that ‘‘evolutionary biology was built on
a huge black box—Darwin could never have written the Origin of Species if
he had not wisely bracketed the mechanism of inheritance.’’ One of the
great advantages of Mendelian genetics in the early decades of the twen-
tieth century, it is often thought, was that it ‘‘bypassed the uncharted
swamp of development’’ (Hull 1998, 89). But today the situation looks rad-
Pre-Synthesis Darwinians at least realized the need for a theory of inheritance,
although they doubted that Mendelism was that theory. Most post-Synthesis neo-
Darwinians do not require developmental biological contributions to evolution
theory [e.g., Wallace 1986]. Developmentalists may or may not be able to demon-
strate that a knowledge of the processes of ontogenetic development is essential for
the explanation of evolutionary phenomena. (Amundson 1994, 576)
Provided developmentalists can demonstrate this, and offer well-founded
developmental evolutionary explanations, the result will be ‘‘a dramatic
synthesis of divergent explanatory and theoretical traditions,’’ Amundson
concluded. We feel the time to attempt such a synthesis has come, al-
though its contours are most likely going to differ greatly from the received
view of explanatory theory reduction that centered on ‘‘imperialism and
competition for primacy and fundamentality’’ (Griesemer 2006).
What kind of explanatory uniﬁcation
can evo-devo in general and OSA
in particular reasonably be expected to contribute to?
Arthur (1987, 182),
pondering whether biologists can realistically aspire to a ‘‘biological Grand
Uniﬁed Theory’’ as a long-term aim, suggested that ‘‘biology can transcend
its biospheric origins and develop principles that will apply to life wherever
we encounter it.’’ He offered principles of self-organization and homeo-
static regulation as good candidates. In a similar vein, Kauffman (1993,
22–23) envisages a synthesis of evolutionary biology and developmental
biology that would be based on the identity of generative mechanisms
(see Goodwin 1984; Eble and Goodwin 2005):
The task of enlarging evolutionary theory would be far more complete . . . if we could
show that fundamental aspects of evolution and ontogeny had origins in some mea-
58 Werner Callebaut, Gerd B. Mu
¨ller, and Stuart A. Newman
sure reﬂecting self-organizing properties of the underlying systems. The present
paradigm is correct in its emphasis on the richness of historical accident, the fact
of drift, the many roles of selection, and the uses of design principles in attempts
to characterize the possible goals of selection. . . . the task must be to include self-
organizing properties in a broadened framework, asking what the effects of selection
and drift will be when operating on systems which have their own rich and robust
Kauffman’s vision provides one attractive interpretation of what the long-
term unifying function of evo-devo might be. But at present, the actual
and conceivable interrelations between the dominant selectionist paradigm
and the paradigm of self-organization are still quite unclear (box 2.5).
It is fair to say that the contribution to a uniﬁed theoretical biology most
workers in the ﬁeld of evo-devo currently envision is more modest. Rather
than some grand uniﬁcation scheme, what they have in mind can perhaps
be rendered best in terms of Darden and Maull’s (1977) concept of an
‘‘interﬁeld.’’ In their analysis, a scientiﬁc ﬁeld is an area of science con-
sisting of a central problem,adomain consisting of items taken to be facts
related to that problem, general explanatory factors and goals providing
expectations as to how the problem is to be solved, techniques and methods,
and often (but not necessarily) also concepts, laws, and theories that are re-
lated to the problem and attempt to realize the explanatory goals. If devel-
opmental biology and evolutionary biology—or more correctly, a number
of their subdiscipines that are relevant to evo-devo
—are regarded as
ﬁelds, evo-devo might be regarded as an ‘‘interﬁeld’’ that borrows resources
from one ﬁeld (say, a developmental analysis of homology) to solve a
Possible interrelations between natural selection (NS) and self-organization (SO)
nNS, not SO, drives evolution.
nSO constrains NS.
nSO is the null hypothesis against which evolutionary change is to be
nSO is an auxiliary to NS in causing evolutionary change.
nSO drives evolution, but is captured and ﬁxated by NS.
nNS is itself a form of SO.
nNS and So are two aspects of a single evolutionary process.
Source: Adapted from Depew and Weber 1995; cf. Kauffman 1993, 1995; New-
man and Mu
¨ller 2000; and Richardson 2001.
The Organismic Systems Approach 59
problem in another ﬁeld (in our example, the evolution of homology). This
may look modest enough, yet, as some of the historical case studies of
Darden and her group document (e.g., Darden 1991; Darden and Craver
2002; cf. also Darden 1986), such humble beginnings can engender quite
revolutionary breakthroughs. (On a much grander scale, one could think
here of the transition of biochemistry to molecular biology in the 1930s,
and the migration of physicists and chemists into biology as stimulated by
the Rockefeller Foundation; e.g., Abir-Am 1982.) Evo-devo, as we have pre-
sented it here, will require nothing less than a rethinking of the funda-
mentals of developmental as well as evolutionary biology—not in any
philosophically ‘‘foundational’’ sense, but in the much more down-to-
earth terms of Wimsatt’s ‘‘generative entrenchment’’ of ideas.
Most historians and at least some philosophers of biology hold that evo-
lutionary biology is not a uniﬁed science, and that the modern synthesis
was not so much a conceptual/theoretical as an institutional synthesis
(e.g., Smocovitis 1996; Burian 2005). Moreover, as already indicated, the
ideal of ‘‘the’’ unity of science as envisaged by the logical empiricists and
epitomized in Schaffner’s (1993) account of reduction/replacement is no
longer taken for granted, to put it mildly (Dupre
´1983, 1993; Rosenberg
1994; Galison and Stump 1996). If Cartwright (1999, 1) is right, ‘‘The laws
that describe this world are a patchwork, not a pyramid.’’ In biology as else-
where, reduction does not work in practice (Hull 1973; cf. Longino 2000);
physicalist reduction, namely, the reduction of all the theories of complex
objects to physics, is humanly impossible due to our bounded rationality.
Further obstacles to uniﬁcation are related to the data-driven nature of
much contemporary research. ‘‘Since World War II,’’ Patrick Suppes (1979,
17) wrote almost thirty years ago, ‘‘the engines of empiricism have vastly
outrun the horse-drawn carriages of theory.’’ See, for example, Henry
(2003) on the tensions between data- and hypothesis-driven approaches to
systems biology. The current ‘‘reign of theory pluralism’’ (Suppes 1978) is
in part a consequence of this ‘‘Baconian’’ bias toward inductive knowledge
If the postmodernist fashion to celebrate the end of the unity (singular)
of science (singular) was all there was to it, the rhetoric of evo-devo enthu-
siasts calling for a developmental synthesis would be shallow indeed. But
we take it that the one-sided ideology of uniﬁcation dear to the positivists
has only been replaced by an equally misplaced, exclusive focus on the
factors in scientiﬁc practice that tend to diversity and separate scientiﬁc dis-
courses (Radnitzky 1987, 1988; Reisch 2005). A more balanced view should
60 Werner Callebaut, Gerd B. Mu
¨ller, and Stuart A. Newman
also take into account the unifying tendencies that are a consequence of
regimes and practices of experimentation and instrumentation. These,
according to Hacking (1996, 69), ‘‘have been more powerful as a source of
unity among diverse sciences than have grand uniﬁed theories.’’ Instru-
ments (Clarke and Fujimura 1992) are speedily transformed from one disci-
pline to another, not according to theoretical principles but in order to
interface with phenomena. As an example, Hacking mentions the tunnel-
ing electron microscope: at ﬁrst thought suitable only for metallurgy, it
has expanded into cell biology ‘‘in ways not all that well thought-out, and
sometimes by accident’’ (p. 69). We propose that techniques like rheologi-
cal analysis of tissues and model tissues that address the physical aspects
(Forgacs and Newman 2005), time-resolved quantitative PCR that addresses
the temporal gene expression aspects (Zhang et al. 2006), and ‘‘deconstruc-
tive’’ comparative knockout analysis in in vivo and in vitro systems (Lall
and Patel 2001; Liu and Kaufman 2005) could play similar unifying roles
with respect to the ‘‘archeology’’ of evo-devo genetics— that is, the record
of the primitive genetic toolkit.
Another topic for philosophical investigation that could deepen and en-
rich evo-devo’s self-understanding is the vexing role of laws in biology and,
intimately related to that, the function of natural kinds in biological mod-
eling and theorizing (Grifﬁths 1996; Wagner 1996; Laporte 2004); see also
the recent debate on the ‘‘myth of essentialism’’ in the history and philos-
ophy of biology (Amundson 2005, 2006; Hull 2006). According to Cart-
wright (1999, 1), the laws of nature ‘‘do not take after the simple, elegant
and abstract structure of a system of axioms and theorems.’’ One extreme
position wants to dispense with biological laws altogether on the ground
that even in the practice of physics they play negligible roles only (see
Giere 1999). The other extreme position, represented by certain process
structuralists, is that developmental biology will deliver the goods. Thus
Eble and Goodwin (2005) write: ‘‘The successes of evolutionary devel-
opmental biology suggest that the comparison of historical and develop-
mental kinds in developmental morphospace may soon generate more
immediate insight into the nature of evolution than the comparison of his-
torical and adaptive kinds in ﬁtness landscapes.’’ OSA’s view of inherency
clearly situates it more toward the latter end of the spectrum, but exploring
these fascinating issues transcends the bounds of this chapter.
Here again, as for most of the themes we have explored, a pluralism of
approaches seems desirable. The historian of biology Evelyn Fox Keller
(2000a) has plausibly characterized the previous century as ‘‘The Century
The Organismic Systems Approach 61
of the Gene.’’ We are currently witnessing a growing awareness among
biologists that some of the foundational features of the reigning evolution-
ary paradigm, in particular its genetic determinism and adaptationism, re-
quire substantial revision and need to be complemented by other concepts
and theories. We hope to have convinced readers that evo-devo, and more
speciﬁcally our organismic systems approach to evolution and develop-
ment, including its naturalistic philosophical outlook, have the potential
to contribute to a truer picture of life on this earth.
1. It is worth noting that when Treviranus published his Biologie, oder Philosophie der
lebenden Natur fu
¨r Naturforscher und A
¨rzte in 1802, the possibility of integration he
envisaged was based on the eighteenth-century change in generation theory from
preformationism to epigeneticism. ‘‘Biology and epigenesis were born together and
grew up together’’ (Depew 2005).
2. ‘‘A biological explanation should invoke no factors other than the laws of physics,
natural selection, and the contingencies of history. The idea that an organism has a
complex history through which natural selection has been in constant operation
imposes a special constraint on evolutionary theorizing’’ (Williams 1985, 1 –2). See
3. ‘‘The functional biologist deals with all aspects of the decoding of the pro-
grammed information contained in the DNA of the fertilized zygote. The evolution-
ary biologist, on the other hand, is interested in the history of these programs of
information and in the laws that control the changes of these programs from gener-
ation to generation. In other words, he is interested in the causes of these changes’’
(Mayr  1988, 26). According to Weismann’s doctrine, all causality other than
that due to environments, which is ignored at the level of the individual cell or or-
ganism, can be traced to germ or genes; ‘‘the body or phenotype is a causal dead
end’’ (Griesemer 2002, 98).
4. In principle, that is; in practice, adaptationists in behavior and cognition studies
tend to shun proximate questions (Callebaut 2003).
5. In the 1950s, when the phrase ‘‘synthetic theory’’ was not as common as it would
become later, quite a few authors used to refer to the ‘‘selection theory of evolution,’’
‘‘neo-Darwinism,’’ or sometimes ‘‘neo-Mendelism’’ instead. According to Gayon
(1989, 4), ‘‘Such a terminological hesitation clearly indicates that there is indeed a
major theoretical commitment in the synthetic theory: It is fundamentally a general
consensus on a genetic theory of natural selection.’’ The issue of adaptationism can-
not be pursued in this chapter; see, for example, Antonovics 1987; Amundson 1994;
Rose and Lauder 1996; Ahouse 1998; Orzack and Sober 2001; Andrews, Gangestad,
62 Werner Callebaut, Gerd B. Mu
¨ller, and Stuart A. Newman
and Matthews 2002. We have found useful Sober’s (1998, 72) characterization of
adaptationism as the claim that ‘‘natural selection has been the only important cause
of the most phenotypic traits found in most species.’’
6. Thus, on Lewontin’s (2000b, 193–194) view, ‘‘It is not within the problematic of
population geneticists to discover the basic biological phenomena that govern evolu-
tionary change. . . . The basic phenomena are already provided . . . by biological dis-
coveries in classical and molecular genetics, cell biology, developmental biology,
and ecology. Nor is it within the problematic of observational population genetics to
discover the ways in which the operation of these causal phenomena can interact to
produce effects. The elucidation of the structure of the network of causal pathways,
and of the relation between the magnitudes of these elementary forces and their
effects on evolution, is an entirely analytic problem.’’ Because we lack the necessary
observational power (and, in practice, will always lack it), it also ‘‘cannot be the task
of population genetics to ﬁll in the particular quantitative values in the basic struc-
ture that will provide a correct and testable detailed explanation in any arbitrary
case. . . . Rather, the task of population genetics is to make existential claims about
outcomes of evolutionary processes and about signiﬁcant forces that contribute to
these outcomes.’’ Lewontin’s pessimistic conclusion is that ‘‘there is an inverse rela-
tion between the degree of speciﬁcity of these existential claims and the size of the
domain to which they apply.’’
7. Gayon (1989, 4–5) noted that there are basically two ways of criticizing the
synthetic theory as a whole: (1) to attack natural selection as the ultimate factor
controlling all evolutionary processes; (2) to contest the tacit subordination between
the diverse ﬁelds of research. With a few exceptions such as OSA, which points to the
problems of origination of traits and qualitative phenotypic change as the major
blind spots of the synthetic theory (Mu
¨ller and Newman 2003a), biologists engaged
in the evo-devo enterprise adopt the second strategy.
8. If not vitalism: As Varela (1979, 5) once pointed out, pushing all the properties
pertaining to a coherent, cooperative whole such as the functioning cell into the
DNA, which now contains some abstract description of the ‘‘teleogenic project’’ of
the cell, brings one close to the vitalists, who insisted on a simular reduction of the
characteristics of life to some component other than the cooperative relations of
the cellular unity.
9. In developmental biology this notion has gained seeming conﬁrmation in ﬁnd-
ings that successive developmental steps are typically triggered by episodes of new
gene expression and that experimental alteration of gene expression frequently leads
to changed developmental outcome. In evolutionary biology the tenet that genes de-
termine form is essentially equivalent to the reigning neo-Darwinian paradigm: (1)
evolution is the hereditary transmission of phenotypic change; (2) genes are the
medium of heredity; (3) the sum of selected genes therefore speciﬁes and determines
the phenotypic differences between organisms (Newman and Mu
The Organismic Systems Approach 63
10. We prefer this label (following Griesemer 2000a) to the more common ‘‘develop-
mental systems theory’’ (DST) because, as Grifﬁths and Gray (2005, 417) acknowl-
edge, what we are talking about here is really ‘‘a general theoretical perspective on
development, heredity and evolution’’ intended to facilitate the study of the many
factors that inﬂuence development without reviving ‘‘dichotomous’’ debates over
nature or nurture, and so on. ‘‘While theories yield models for explaining, theoretical
perspectives yield guidelines for theorizing and for modeling’’ (Garcı
´a Deister 2005,
28). We will elaborate on the notion of ‘‘perspectives’’ later.
11. Grifﬁths and Gray (2005, 420–424) argue that the criticism of the parity thesis
coming from evo-devo is based on a misunderstanding (see also Gray 2001). But their
own whiggish rendering of the history of evo-devo (‘‘EDB [evolutionary develop-
mental biology], whose growth as a discipline has been closely tied to discoveries in
developmental genetics, has embraced a conception of the developmental system as
an emergent feature of the genome’’ (p. 421); cf. Arthur 2002) contributes little to
solving this and other disagreements between DSP and evo-devo.
12. Another inﬂuential interpretation of causation, the manipulationist or interven-
tionist account, views causal and explanatory relationships as potentially exploitable
for purposes of manipulation and control (Woodward 2003; cf. Hacking 1983; Pearl
2000). Exploring these and other, often competing views of the nature of causation for
a better understanding of causal processes in evo-devo remains a task for the future.
13. Goodwin (1984) accused the synthetic theory of having neglected the important
lessons of developmental mechanics for evolution. Neo-Darwinism treated embryo-
genesis as an aspect of inheritance, considering that a certain category of occasional
causes (genes) ultimately determine form. Thus no room was left for the general
principle of biological organization. On Goodwin’s alternative view, the process of
natural selection acting on genes is subordinated to an ‘‘intrinsic dynamics of the
living state’’ (see Gayon 1989, 24).
14. For example, Dawkins’s (1976) account of evolution in terms of his replicator-
vehicle distinction ‘‘does not provide resources to identify empirically the physical
avatars of his functional entities. We know that the informational genes are tied to
matter and structure, but if evolutionary theory—to be generally enough to cover
cultural and conceptual change—must be devoid of all reference to concrete mecha-
nisms, it cannot follow from the theory, for example, that genes are inside organisms
or are even parts of organisms, as Dawkins’s language suggests. Strictly, only the cor-
relations between replicator and vehicle due to causal connections of a completely
unspeciﬁed sort can be implied by such a theory. Striving to get matter and speciﬁc
structure out of the theory in order to make it apply to immaterial realms may thus
leave it bankrupt as an account of causal connection for the material, biological
cases’’ (Griesemer 2005, 79).
15. One standard way to characterize how sciences differ from each other is to spec-
ify the modes of explanation they require. Physics is ‘‘the standard instance and
64 Werner Callebaut, Gerd B. Mu
¨ller, and Stuart A. Newman
model of a science using causal explanation’’ (Elster 1983, 18), but the realm of
causal explanation, which invokes antecedent causes, extends to the life sciences,
psychology, social science, and even the humanities. Whereas physics is not
normally viewed as having room for explanation in terms of (actual) future conse-
quences of a phenomenon, functional explanation is the hallmark of evolutionary
biology and plays a more limited role in other biological disciplines, including bio-
chemistry (Rosenberg 1985), as well as in the social sciences. (Notice that ‘‘func-
tional biology’’ as referred to at the beginning of this section uses causal, not
functional explanation.) Intentional explanation is crucial in the social sciences and
humanities only; its role in cognitive ethology is controversial (see, e.g., Sterelny
16. For Gerhart and Kirschner (1997), evolvability is the capacity of a process to
generate nonlethal functional variation on which selection can act. In our own
epigenetic framework, evolvability is interpreted in an entirely different fashion. It
represents the continued efﬁcacy of epigenetic processes in a lineage—some of them quite
ancient, others of more recent origin—and as such is tied to primitive morphoge-
netic plasticity. Genetic evolution will tend to suppress such evolvability and buffer
the development of form ( Newman and Mu
¨ller 2000, 306).
17. Although one can say with Wagner et al. (2000, 821) that development ‘‘can
be seen as another set of biological characters that evolve,’’ our emphasis on the pri-
macy of epigenetic mechanisms suggests that the evolution of development cannot
be adequately captured within the reigning, gene-centric neo-Darwinian paradigm
and should therefore be at the heart of the evo-devo enterprise.
18. As Robert, Hall, and Olson (2001, 957) note, ‘‘The aims of evo-devo are not
carved in stone,’’ which is exactly what one would expect of an evolutionary account
of science a
`la Hull (1982, 1988). Yet the lists of aims of evo-devo of Hall (2000) and
Wagner et al. (2000) map almost one-to-one onto one another.
19. But see Brandon (1990, 185; 1996, 192–202), who disagrees that mechanism
implies an inherently hierarchical decomposition. Although we are largely sympa-
thetic with Brandon’s (1996, 179ff.) attempt to construe a mechanistic philosophy
that would allow biologists to avoid the ‘‘false choice’’ between reductionism and
holism, we would prefer not to equate mechanism with ‘‘causal pattern’’ (p. 194),
but rather leave some ﬂesh on the bones such as a speciﬁcation of the material(s)
out of which a mechanism is constructed (cf. Griesemer 2005, 62, n. 1). See also
Kauffman (1971) and Wimsatt (1974, 1980) on ‘‘articulation-of-parts’’ explanation.
Tabery (2004) suggests that the aforementioned notions of mechanism as interaction
and as activity may complement each other.
20. See Britten’s (2003) ‘‘(only) details determine’’ thesis, according to which devel-
opment is entirely determined by self-assembling individual genes and molecules
(‘‘details’’) that interact as a result of a long process of natural selection.
The Organismic Systems Approach 65
21. Given the inﬂationary use of the term paradigm that followed the popularization
of Thomas Kuhn’s views, many historians and philosophers of science have become
wary of the term, but biologists (e.g., Wilkins 1996; Strohman 1997) are reempower-
ing it. The feature we have in mind was captured best in the so-called disciplinary
matrix (Kuhn 1970). As a kind of scientiﬁc Weltanschauung, disciplinary matrices
are acquired largely implicitly during scientiﬁc education, in which the learning of
‘‘exemplars’’—archetypal applications of symbolic generalizations or theories to
phenomena—is of paramount importance. Commonness of vocabulary and ‘‘sym-
bolic generalizations’’ notwithstanding, scientiﬁc communities with different exem-
plars will hold different theories, and hence will ‘‘view the world differently.’’ Still,
according to Kuhn, depending on one’s exemplars one will also tend to ask different
questions and hold different values. (For a critical assessment, see Suppe 1977, 138–
151.) At the level of Weltanschauungen, biological discourse is heavily imbued with
22. ‘‘The reason why competition, selﬁsh genes, struggle, adaptation, climbing peaks
in ﬁtness landscapes, doing better and making progress, are so important as meta-
phors in neo-Darwinism is because they make sense of evolution in terms that are
familiar to us from our social experience in this culture’’ (Goodwin 1994, 168).
23. Hooker (1994) has argued for this middle-of-the-road position in painstaking
detail in the case of Piaget’s biology and genetic epistemology. In a similar vein,
Amundson (1993) has shown for the debate between behaviorists and cognitivists
in psychology that paradigmatic packages are not necessarily as monolithic as they
are often presented as being. More generally, Bhaskar (e.g., 1978) has made a case
for a critical realism as ‘‘an appropriate metaphilosophy for an adequate account of
science’’ on which philosophy will ‘‘play two essential roles—namely as a Lockean
underlabourer and occasional midwife, and as a Leibnizian conceptual analyst and
potential critic’’ (Bhaskar 1989, 82).
24. ‘‘My memory of Steve [Gould] is indelibly tied to the celebration of diversity—
diversity of approaches, of explanations, of organisms, and of people’’ (Wake 2002,
2346). However, see Newman 2003a for a discussion of Gould’s tendency to over-
privilege genetic causation at the ontogenetic level and nongenetic causation at
the behavioral level. Longino (2000, 282) points out the political desirability of epis-
temological pluralism as ‘‘a philosophical epistemology that recognizes the local
character of prescriptive epistemologies associated with particular approaches.’’ Such
a sensibility for local epistemic cultures is lacking in E. O. Wilson’s (1998) call for the
uniﬁcation of all human knowledge by means of consilience, the (inductive) proof
that everything in our world is organized in terms of a small number of fundamental
natural laws—his deep concern for the conservation of biodiversity notwithstanding.
25. Epigenetics is here meant as a collective term for all nonprogrammed factors
of development (Newman and Mu
¨ller 2000). Note that there are fundamental differ-
ences in usage between the ‘‘epigenesis’’ of developmental biology and the ‘‘epige-
66 Werner Callebaut, Gerd B. Mu
¨ller, and Stuart A. Newman
netics’’ of gene regulation (Griesemer 2002; Mu
¨ller and Olsson 2003; Jablonka and
26. Naturalism has many roots that reach back to Aristotle and include the philo-
sophical traditions of empiricism and materialism, Spinoza, and the American
pragmatists. Despite the multiplicity and variety of its formulations, a concise and
consistent characterization of (‘‘streamlined’’) naturalism seems possible today. Nat-
uralism regards philosophy as continuous with science (Callebaut 1993), requires
philosophical assertions to be testable (Hull 2001, part III ), shuns a priori and tran-
scendental arguments (Callebaut 2003, 2005b), and considers scientiﬁc explanations
as paradigmatic naturalistic explanations (Giere 1988, 2006; Hull 1988, 2001). A con-
sistent naturalism is a methodological rather than an ontological monism and can
best be understood in terms of methodological maxims rather than metaphysical
doctrines, which makes it difﬁcult to deﬁne naturalism positively (Giere 2006). The
open-ended character of naturalism dovetails nicely with mechanism, which on a
rather common understanding is also agnostic with respect to ontological commit-
ments (Brandon 1996, 192ff.; cf. Bechtel and Richardson 1993 or Callebaut 1993).
27. For a more detailed discussion see Mu
¨ller and Newman 2005. The uses of homol-
ogy and the organizational homology concept are discussed in Mu
28. See Conway-Morris 2003, 505, which refers to the ‘‘still unresolved’’ problem of
inherency ‘‘whereby much of the potentiality of structures central to evolutionary
advancement, e.g. mesoderm, neural crest, are already ‘embedded’ in more primitive
29. This is not to be confounded with contingency as understood in logic or, for that
matter, sociology (e.g., Luhmann 1984), where something is considered contingent if
it is neither necessary nor impossible—which is not identical to ‘‘possible,’’ for what
is necessary must also be possible. As regards historical contingency, we should
be aware that we are entering a conceptual mineﬁeld. Historical contingency has
been associated with chance (Monod 1971), irreversibility (Georgescu-Roegen 1971)
or ‘‘lock-in’’ (W. B. Arthur 1989), and nonrepeatability (Elster 1976). It has been
equated with randomness and stochasticity (Chaisson 2001), and has even been con-
ﬂated with the epistemological notion of unpredictability (Gould 1989, 2002; but see
Vermeij 2006). Gould described historical explanations as taking ‘‘the form of narra-
tive: E, the phenomenon to be explained, arose because D came before, preceded by
C, B, and A. If any of these stages had not occurred, or had transpired in a different
way, then E would not exist (or would be present in a substantially altered form, E 0,
requiring a different explanation’’ (Gould 1989, 283; all further quotes in this note
are from this page). But, given A–D, E ‘‘had to arise’’ (italics ours), and is in this sense
nonrandom. Yet ‘‘no law of nature enjoined E’’; any variant E 0arising from altered
antecedents would have been equally explainable, ‘‘though massively different
in form and effect.’’ For Gould, then, contingency means that the ﬁnal result is
‘‘dependent . . . upon everything that came before —the unerasable and determining
The Organismic Systems Approach 67
[sic] signature of history.’’ Superﬁcially, one could think that Gould combined an
epistemological notion of contingency, unpredictability, with an ontological one,
which Oyama (2000, 116) dubs ‘‘causal dependency.’’ But to us, ‘‘unerasable and
determining signature of history’’ suggests that the past leaves its traces in the pres-
ent, which takes us back to epistemology or at least makes for a more complicated
picture (‘‘How much of the past do we have to know to understand the present?’’). It
seems to us that interpreting contingency in terms of stochasticity (Chaisson) is
equally problematic—viewed from Gould’s perspective, that is —because one would
now have to rule out stochastic processes that are memoryless (the Markov property:
the present state of the system predicts future states as well as the whole history of
past and present states). We are assuming here that models and theories that exhibit
time lags have a more prominent role to play in biology than in the physical
sciences, because the structural knowledge that would enable us to disregard the
more ancient causes (A–C in Gould’s schema) has not been attained (yet?).
30. Oyama (2000, 116) argues for ‘‘a notion of development in which contingency is
central and constitutive, not merely secondary alteration of more fundamental, ‘pre-
31. If, as scientiﬁc realists, we consider the covering-law account of explanation
ﬂawed because mere subsumption is not explanation yet, we must also point out
that not all the nonreductionistic accounts of uniﬁcation that are currently in vogue
are necessarily explanatory (see Halonen and Hintikka 1999).
32. As R. L. Carroll (2000) argues, an expanded evolutionary synthesis needs to inte-
grate new concepts and information not only from developmental biology, but from
systematics, geology, and the fossil record as well.
33. We agree with Gilbert (2003b, 348) that ‘‘not all parts of developmental biology
and not all parts of evolutionary biology are involved in these new unions,’’ al-
though we do not share his emphasis on developmental genetics and population
genetics. The situation is actually more complicated since ‘‘paleontology, morpho-
metrics, QTL mapping, ecology, life history strategy research, and functional mor-
phology’’ (and, we would add, biophysics) are also involved. If evo-devo is taken to
include ecological considerations (Gilbert 2001; Gilbert and Bolker 2003; Hall et al.
2004), thist list must be expanded even further.
34. Von Baer’s ‘‘laws of development’’ may be summarized under the general
principle ‘‘Differentiation proceeds from the general to the particular.’’ Wimsatt’s
‘‘developmental lock’’ model of generative entrenchment (GE) formalizes this principle
(Wimsatt 1986). The model sustains, among other tenets, that features expressed ear-
lier in development (1) have a higher probability of being required for features that
will appear later; (2) will, on average, have a larger number of ‘‘downstream’’ features
dependent on them; (3) are phylogenetically older; (4) are more likely to be widely
distributed taxonomically than features expressed later in development. Features
68 Werner Callebaut, Gerd B. Mu
¨ller, and Stuart A. Newman
that are deeply generatively entrenched, if ‘‘mutated,’’ are likely to cause major
developmental abnormalities. GE, which allows for environmental information to
be generatively entrenched, has been applied to the innate-acquired distinction
(Wimsatt 1986, 1999), evo-devo (Schank and Wimsatt 2001; Wimsatt 2001), concep-
tual evolution (Griesemer and Wimsatt 1989), and the ‘‘evo-devo of culture’’ ( Wim-
satt and Griesemer, chapter 7, this volume), among other domains; see also table 2.2.
35. The physical correlate of a higher-level property or kind is typically massively
disjunctive, making it vanishingly unlikely that the properties or kinds of higher lev-
els will enter into the kinds of universal laws characteristic of physics or chemistry.
36. For Hacking, mathematical tools have played a similar role as pragmatic uniﬁers
since the day of Descartes, Newton, and Leibniz. A nice contemporary example is the
steady expansion of game theory since its inception in the 1940s, from a theory of
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