Biology and Philosophy (2007) 22:145–153 Ó Springer 2005

DOI 10.1007/s10539-005-9011-9

Book review

How wide and how deep is the divide between population

genetics and developmental evolution?

GÜNTER P. WAGNER
Department of Ecology and Evolutionary Biology
Yale University
New Haven
USA
E-mail: gunter.wagner@yale.edu; phone: +47-55236370; fax: +47-55236379

A review of Ron Amundson’s ‘‘The Changing Role of the Embryo in Evolu-

tionary Thought’’ (2005, Cambridge Studies in Philosophy and Biology)

In the summer of 1988 I participated for the first time in a meeting of the
Society for the Study of Evolution for which Doug Futuyma had organized a
president’s symposium on ‘‘Phylogeny and Evolutionary Processes’’. Doug
kindly invited me to speak at his symposium about the relationship between
development and homology. That was an odd choice, because my career up to
that point was mostly based on my work in mathematical population genetics,
and homology is not a standard topic for a population geneticist. In fact John
Maynard-Smith, in his characteristic candor, approached me during this
meeting and asked: ‘‘How can someone who is able to solve integral equations,
like you, waste his time on such non-sense as homology?’’ Needless to say, I
took this as a compliment. Since then homology has become a hotly debated
subject, fuelled mostly by the advances in evolutionary developmental biology.
Developmental evolution has resuscitated research questions which were
abandoned early in the 20th century when Neo-Darwinian theory of evolution
took over as the dominant form of evolutionary theory. But still, the distrust
between Neo-Darwinian evolutionary biologists, as population geneticists and
developmental biologists is still as real as it was when John Maynard-Smith
was concerned about my mental state. To me, Ronald Amundson’s book is
fascinating to read because the gulf between population genetics and devel-
opmental evolution is one of two main foci of this book, and it is by far the
conceptually most interesting one. I myself living in both worlds, that is in
population genetics as well as developmental evolution, never fully understood
the extent and the scope of this problem; I guess this was a form of denial,
otherwise I would have had to agree with John’s concern for my sanity. And it
is only through my reading of Amundson’s penetrating analysis that I now
more fully appreciate the scope of the problem, and this is the topic I want to
focus on first in this review.
The book ‘‘The Changing Role of the Embryo in Evolutionary Thought’’ has
two main messages. The first is that the standard view of pre-Darwininan and
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para-Darwinian biology by is seriously flawed. This part will be most inter-

esting to historians of biology, since it represents a radical departure from the
reading that was forcefully advanced by Ernst Mayr in the recent decades.
Since I am not a historian, I will only briefly deal with this aspect in the third
section of this review. The second topic is the relation ship between Neo-
Darwinian theory of evolution and developmental evolution. This is the topic I
want to focus on first.

It is hard to reconnect with a distant relative: what keeps evolutionary

and developmental biology apart?

One puzzling aspect of developmental evolution is the fascination it holds for

philosophers and historians of science. How shall we explain that a research
program, which only started in earnest during the 1990s, in spite of having deep
historical and conceptual roots, is the subject of quite a number of historical
studies (Raff 2000; Love and Raff 2003; Wagner and Laubichler 2004; Laub-
ichler 2006)? It seems that there can hardly be enough history to warrant a
historical study!
I think one reason why developmental evolution hold that much fascination
with historians is that developmental evolution is an oddity within the broader
history of evolutionary thinking. The standard historical narrative, what
Amundson calls the ‘‘Synthesis historiography’’, is a victory tale of the white
knight of population thinking over the anti-evolutionary dragon of typology.
The latter should be better called structuralist thinking to avoid polemic
overtones. For most of the 20th century population thinking was the only game
in town, but now the hydra of structuralist ideas is lifting its ugly head(s) again
in the form of developmental evolution. And to the dismay of some it is more
vital than ever, establishing a vibrant research program with dedicated research
funding, faculty positions and specialized scientific journals. There is nothing
more successful than success, and for that reason it is hard to ignore what is
going on in developmental evolution.
But more importantly than the oddity of developmental evolution as a
historical phenomenon is the question of the conceptual compatibility between
developmental evolution and the Neo-Darwinian Synthesis based on popula-
tion thinking and its offspring, population genetics. The tension between these
two types of thinking goes back to the very beginning of biology in western
culture. The functionalist tradition going back at least to Cuvier and which has
spawned the modern adaptationist research program, explaining organism by
their ecological functions and (nowadays) population genetics. This was the
dominant form of evolutionary biology during most of the 20th century. On
the other side is the structuralist approach going back at least to Geoffroy St.
Hilliair and which has spawned the first large scale evolutionary research
program after the publication of the Origin of Species, evolutionary mor-
phology (Nyhart 1995); which produced the wealth of comparative anatomical
and embryological knowledge on which the first phylogenetic hypotheses were
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based. But as an approach to the study of evolution this research program was
completely eclipsed by population genetics and affiliated research programs. It
is quite obvious, that developmental evolution is re-connecting to this
intellectual heritage. One can see this in the research topics addressed in
developmental evolution, i.e. the origin of limbs, the origin of the vertebrate
body plan, the evolution of insect wings etc., as well as in the self-character-
ization of practitioners of the field: ‘‘[the Neo-Darwinists] are interested in
species, we [the practitioners of developmental evolution] are interested in
bodies’’ (Rudy Raff; cited by Ron Amundson on p. 253).
Ron Amundson shows that the rise of developmental evolution is inevitably
in conflict with the most cherished metaphysical principles of the Neo-
Darwinian theory of evolution, radical population thinking. Ernst Mayr
considers it the most important intellectual achievement of the Neo-Darwinian
Synthesis (Mayr 1988) and the ontological commitments can be summarized as
a-historic causes (selection) acting on ubiquitous variation, encouraging an a-
historical view of evolution. That may sound strange for a science that aims at
explaining an historical process, evolution of life, but what this means is that
the focus is on immediate causation, i.e. factors which affect the genetic
composition of the population, rather than on historical narratives. Historical
sciences, like paleontology and phylogeny are regarded as ‘‘phenotype exis-
tence’’ studies with little impact on the actual explanation of evolutionary
change. This a-historical focus is also reflected in the training of population
geneticists. I can assure you that one can be a successful population geneticist
without knowing much of life’s history on earth. The second important com-
ponent of the Neo-Darwinian ontology is variation as the most elementary
biological category (Ghiselin 1997). According to this view only variation, be it
genetic or phenotypic, is real, everything else are statistical abstractions or in
the worst case the wrongheaded influence of typological thinking. Notions like
bodyplans and homology make no sense in this ontology, or only as accidental
traces of past adaptations. The center of adaptationist explanations is diversity,
because diversity of the typical results of mutation, selection and drift.
On the other hand the ontology of structuralist thinking is quite different.
There one finds a focus on unity rather than diversity, which reflects the re-
search priorities of comparative anatomy as well as modern developmental
biology. That is a focus on traits that are shared among large groups of species
with deep roots in the phylogeny (i.e. distant ancestors). This ontology asks us
to take seriously concepts like the vertebrate body plan, the tetrapod limb and
the arthropod (or at least insect) segment, i.e. exactly the kind of concepts that
the Neo-Darwinian ontology has taught us to avoid like the devil the holy
water. To avoid derogatory meaning, Amundson calls these concepts ‘‘devel-
opmental types.’’
In a nutshell the problem is this: for the kinds of causes that the Neo-
Darwinan theory accepts as real, i.e. population processes like selection and
drift, the limit of their reach are the limits of species. Species are exactly those
entities that are delimited by the reach of demographic processes as so
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poignantly expressed in the cohesion concept of species (Templeton, 1989).

Speciation irreversibly breakes the causal nexus that flows from population
processes. In contrast, however, entities like the tetrapod limb transcend the
limits of species, and there can be no population genetic (meaning ‘‘evolu-
tionary’’) mechanism which lends cohesion to these entities. To a population
geneticist, the assumption of a developmental type implies that the ancestor is
reaching from its grave (or the Lagerstätte) to clutch the throat of several
recent species. This is impossible, at least in the ontology of the Neo-Darwinian
Synthesis and ‘‘da nicht sein kann was nicht sein darf’’ (German for ‘‘since
nothing can be real that is not allowed by law’’) developmental types have to be
illusionary, or at least irrelevant for the causal explanation of evolution. Hence
developmental types can only be the traces of shared ancestry and do not
contribute to an explanation of evolutionary processes.
On the other hand any reference to a developmental type implies that the
feather of a chick and that of an eagle are in a real and biologically relevant way
‘‘the same.’’ This is implied in the research program of developmental evolu-
tion, otherwise expressions like the origin of ‘‘the limb’’ or ‘‘the insect wing’’ or
‘‘the avian feather’’ would be meaningless. It is tempting to suggest, as has been
done many times, that developmental types are defined by their shared devel-
opmental mechanisms and pathways, but things are not that simple. Devel-
opmental mechanisms and pathways have a tendency to shift underneath the
continuing presence of the ‘‘developmental’’ type. For instance, the genetic
machinery that produces segments in grasshoppers is in important ways dif-
ferent from that in a fruit fly (Patel et al. 1992). Genes which are essential for
fruit fly segmentation are not even expressed during segmentation in grass-
hoppers, e.g. even skipped and ftz. But there are also counterexamples, as for
instance the development of feathers, which are distinguished from other epi-
dermal appendages through a suite of ‘‘essential’’ developmental features, like
the fact that all feathers derive from an epidermal tube, unlike hair, and develop
by opening up this tube through a process of patterned cell death (Prum 1999).
Here is the very core of Ron Amundson’s argument, and one which
having identified is a great service to developmental evolution and evolu-
tionary theory in general. There is no explanation for the phylogenetic
stability of developmental types. As long as such an explanation is not
given, which connects to both developmental biology with population
genetic theory, developmental evolution and population genetics remain in
conceptual discontinuity. This is, according to Amundson, and I follow him
in his argumentation, the most urgent theoretical problem in the re-unifi-
cation of development and evolution.

Is there a way out?

In their current incarnations developmental evolution and population genetics

are conceptually incompatible, as argued by Amundson, and eventually
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something has to give. Is there any way thinkable in which this conflict can be
resolved? At this point I want to step back from reporting on Amundson’s
book and respond to his challenge with my view as a scientist who would like
to see this problem resolved. I do not pretend to have THE answer or even an
answer, because I do not, but at this point the question rather is where there are
points of contact or proximity between population genetics and developmental
evolution at which bridge building might be successful.
Let us start with the conceptual toolbox of population genetics, after all it
has the longer history of contributing to the understanding of evolutionary
processes, and it is also where my scientific home base is located. I said earlier
that the basic ontological level for population thinking is natural variation and
the population processes which act on inter-individual variation. In classical
population genetic models usually only a hand full of variants are considered,
say two loci with two alleles, or a simple ensemble of genetic variations, like
polygenic additive variation of quantitative traits. But everyone knows that
these models are simplifications, and nothing in population genetic theory
keeps us from developing models of larger and more complex sets of genetic
and phenotypic variants. In fact, one of the founding fathers of the Neo-
Darwinian Synthesis, Sewall Wright, has led the way toward the modern
developments that seek to do that. It is the notion of adaptive landscapes, and
the underlying genotype space that paved the way for modern population
genetics. The mathematical abstractions, which seek to capture larger sets of
complex genetic variations are variously called configuration spaces (Stadler
1996), in analogy to their close mathematical kin in statistical physics, or
adaptive landscapes (Gavrilets 2004) and phenotype landscapes (Rice 2004;
Salazar-Ciudad and Jernvall 2004). Once this step is done, the one from simple
models of genetic variation, to those which allow for more complex models, all
kinds of things fall out naturally, which otherwise would look mysterious.
The key to understanding these configuration space models is that the
relationship between genetic states (possible genotypes) and phenotypes is a
many to few relationship. Each phenotype can be realized by a large number of
genotypes. This is obvious in the case of macro-molecular phenotypes, like the
secondary structure of RNA or the structure of proteins. In fact much of the
inspiration of these types of model does derive from research into the rela-
tionship between nucleotide and amino acid sequences and the corresponding
molecular 3-D structures (Stadler et al. 2001). It is also intuitive that not all
phenotypes can have exactly the same number of genotypes coding for them.
This has been shown explicitly for RNA secondary structure (Schuster et al.
1994), but even developmental models of tooth morphogenesis show the same
characteristic (Salazar-Ciudad and Jernvall 2004). It is also obvious that
phenotypes which can be realized by many more genotypes (i.e. have higher
genetic entropy, so to say) are easier to evolve than phenotypes which can only
be realized by a small set of genotypes (Stadler et al. 2001). Intriguingly, the
shapes of teeth that have higher entropy, according to a model of tooth
development (Salazar-ciudad and Jernvall 2004), are also those which evolved
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first, probably because they are more easily ‘‘found’’ by mutations. Tooth
shapes with lower entropy evolved only later in response to specific adaptive
needs, as for instance grazing.
In a similar way, it is also clear that for a phenotype to evolve into another,
the derived phenotype needs to be genetically accessible from the ancestral one.
Again, following the Neo-Darwinian way of thinking, accessibility is deter-
mined by the number of genotypes realizing the ancestral phenotype that can
mutate to the new phenotype. Again it is intuitively clear that not all pheno-
types can be reachable from each other phenotype with equal probability. If
there are many genotypes of A that can mutate to give the derived phenotype B
but only very few which can mutate to phenotype C, it is more likely to evolve
B from A than C (Stadler et al. 2001). All of a sudden we are talking about
developmental constraints, and developmental types without having crossed an
impermissible conceptual divide.
The point of this little mental exercise is that one can think of many if not all
the problematic concepts from developmental evolution (developmental types,
developmental constraints etc) as reflecting variational properties of genotypes
‘‘coding’’ for a certain phenotype, or if one prefers a more abstract language,
developmental types reflect the local topology of the genetic/developmental
configuration space. Developmental constraints reflect limited mutational
accessibility from a given ancestral phenotype/genotype. Developmental types
can be thought of as large areas of the genetic configuration space with only
few pathways leading in or out (like a fish trap, hence epigenetic traps sensu
(Wagner 1989)) (Wagner and Stadler 2003). Evolution is shaped by both, the
variational properties of genotype and organisms as well as the functional
needs and the natural selection which results from it.
So far I have used language that should be comfortable to population
geneticists: I talked only about genotypes and phenotypes, not development.
But the rub is this: the essential topological features of the phenotypic con-
figuration space I talked about above (how many genotypes represent the same
phenotype, how many genotypes can mutate to give another phenotype etc.),
are determined by the developmental process. Now a militant Neo-Darwinist
could say development is also encoded in the genotype, and to a very large
extend she would be right. But this is ultimately not the point. The point is that
the variational properties, sketched above, cannot be understood at the genetic
level alone. One needs to understand the dynamics of developmental interac-
tions, how the genome is interacting with the environment, for instance, to see
what is going on (Schlichting and Pigliucci 1998; West-Eberhard 2003). The
topological properties of configuration and phenotype landscapes can only be
understood through insights into developmental mechanisms. And this is the
reason why, ultimately, developmental biology is indispensable for the expla-
nation of evolutionary patterns. Here is a point of contact with population
thinking, entirely consistent with the basic assumptions of the Neo-Darwininan
theory of evolution, but also transcending it, in that developmental mecha-
 151

nisms become a necessary factor in the explanatory narrative (Wagner 2000;

Wagner et al. 2000).
Now we need to come back to reality and say that all that might be exciting,
at least it is to me, but it is not yet scientific reality. Whether theory
development will play out that way is an open question, but the point here is
not to give a definite answer. The point is to show that there are plausible
conceptual bridges between developmental biology and evolutionary biology
that circumvent the apparent incompatibility between them. This section was
not written to contradict Ron Amundson’s analysis. To the contrary, it owns
its focus to the powerful and penetrating analysis of the very real conceptual
difficulties, and is roughly consistent with what Ron imagines the solution
ought to be. Ron thinks of a theory of say limb development that covers what
is common among all tetrapod limbs as well as the variants that are possible
within that common framework (p. 230f). Ultimately I agree with Ron, but I
have a specific vision of how to go about overcoming this problem. But a vision
is not the same as knowing or having achieved this synthesis, and we need to
remain humble in the face of biological reality: nature loves to hide.

Was everyone before Darwin really an Idiot?

That is the question one should have asked oneself when reading the, in the
meantime standard historiographies of evolutionary biology such as Ernst
Mayr’s The Growth of Biological Thought (Mayr 1982). As briefly mentioned
above, the cartoon version of the history of biology has it that there was the
dark age in which the greatest minds of western culture were held hostage to
the vile philosophical ideas of idealism, or what ever it was called at a time. The
stranglehold of these philosophical preconceptions where keeping biological
research confined in the unenlightened dungeon of typology and species fixism.
And then, out of the blue sky of Southern England, comes the genius that set
biology free by breaking the shackles of idealism and replacing them with the
wings of population thinking. Ron Amundson makes two simple observations
that essentially destroy this tale. Fist, pre-scientific ideas about life did not
include fixed species. In fact the earliest accounts of the living world is a chaos
of suggested transformations between the inanimate and the animate worlds, in
which mice grow out of old rags, and mosquitos from dew drops as well as one
kind of organism form others, like ducks from fallen leaves. The idea that
species are real immutable entities was not forced onto the minds of biologists
by philosophical ideas but the result of a systematic but now forgotten
empirical research program. It included common garden experiments to
determine how far the environment can modify organisms. This was largely
done by botanists, but the conceptual impact has reached all of biology.
Furthermore it is not too hard to appreciate, that the hypothesis of species
fixism was a necessary step towards evolutionary theory. The argument goes
like this: if species can be transformed into any other organisms, then it does
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not make sense to study the structure of biological diversity, since there will be
no rhyme or reason to it. If, whoever, species are real entities, which have their
limits of variation, then the pattern of diversity is a legitimate research
objective. Out of that grew systematics and taxonomy, i.e. the study of
biological diversity. The work of systematists then led to the discovery of
patterns that cried out for an explanation. The explanation then was evolu-
tionary theory. This in a nutshell is the narrative that Ron is proposing. And it
is a narrative which makes much more sense and is more satisfying than the
narrative of the struggle between good (Darwin) and evil (typology). Now to
me it is hard to believe that anyone could have fallen for this narrative
structure, except that an antagonistic narrative makes good entertainment.
Could we ever really believe that centuries in which the foundations for modern
sciences have been laid in physics and chemistry and mineralogy, and certainly
also in anatomy and neurobiology, that other branches of science where
populated only by idiots? I certainly fell for it, no I ate it, because it gave
identity and meaning to my efforts to make a contribution to science.
This latter observation finally brings me to a point that still bothers me even
about the alternative historiography offered by Ron. At some points in the
book, Ron freely admits to his personal bias in favor of structuralist thinking,
he is after all a philosopher and I guess as such he is attracted to the more
subtle intellectual texture than crude reductionism and adaptationism. So far
so good, but he also admits, in print, to want his narrative ‘‘to come out right’’
for the structuralists, in this case developmental evolution. But what are we
doing here? Is this Hollywood? Where is our scholarly objectivity? What worth
is history of biology if we write history to fit our predilections? I know that Ron
did not intend it to come across that way, but the exact answer of what it
means to write a history of science eludes me. Which is fine, since I am not a
historian, as my friend Manfred Laubichler likes to remind me when ever he
has a chance, but I am a consumer of history of science and as such I request
some intellectual consumer protection.
OK, to be entirely honest, I did discuss this problem with Ron and there is
an answer that I can accept. First there are real disagreements between Ron
and say Mayr about historical fact. These include the question whether 19th
century taxonomy was essentialist in its methods or not? Was essentialism the
reason for the belief in species fixism? These are questions of fact and these
need to be discussed in a scientific manner. But there is still the part of making
the narrative ‘‘coming out right’’ for this or that camp. This is a question of
trying to connect modern developments, like developmental evolution, to
earlier historical periods. Is it possible to see these modern developments as
conceptually continuous with movements in the 19th century? These are not
strictly questions of fact, but of interpretation. But why would a scientist care?
I think the benefit of these narratives lies in the perspective and even wisdom
one can gain about conflicts and controversies in contemporary science. How is
it that population geneticists get so upset about developmental evolution?
What aspect of their belief system is affected by these recent developments?
 153

Maybe I am stating the obvious, but it certainly was not obvious to me. But
Ron’s book was perhaps one of the most inspiring I have read in many years.

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