Alan C. Love
Dept. of History and Philosophy of Science
University of Pittsburgh
Pittsburgh, PA 15260
allst39@pitt.edu
DRAFT: 8/20/2001
Evolutionary Morphology, Innovation, and the
Synthesis of Evolutionary and Developmental Biology
Abstract
One foundational question in contemporary biology is how to integrate evolution and development. The
emerging synthesis (evolutionary developmental biology or ‘evo-devo’) requires a meshing of disciplines,
concepts, and explanations (inter alia) that have been developed largely in independence over the past
century. The nature of the hoped for synthesis is not wholly agreed upon due to divergent viewpoints
resulting from this disciplinary independence and, consequently, the mechanics for accomplishing the task
are not clearly specified. This paper utilizes historical investigation for philosophical purposes in order to
explore the question of synthesizing evolutionary and developmental biology.
In the attempt to comprehend the present separation between evolution and development much attention
has been paid to the split between genetics and embryology in the early part of the century with its
codification in the exclusion of embryology from the Modern Synthesis.
This encourages a
characterization of “evo-devo” as the integration of developmental genetics with Neo-Darwinism. But
there is a largely untold story about the significance of morphology and comparative anatomy (also
minimized in the Modern Synthesis). I will attempt to reconstruct part of this story, focusing on the rebirth
of functional (and evolutionary) morphology after the 1950s. Functional morphology is critical for
understanding the development of a concept central to “evo-devo”, evolutionary innovation. Understanding
the story about morphology and innovation reveals a different conception of the foundational problem,
providing alternative ways of conceptualizing the “evo” and the “devo” to be synthesized. 1
1. Introduction and Methodology
“…problems concerned with the orderly development of the individual are unrelated to those of the
evolution of organisms through time…” (Wallace 1986)
One foundational question in contemporary biology is how to integrate/synthesize/unify
evolution and development. The emerging synthesis (evolutionary developmental biology or
‘evo-devo’) requires a meshing of disciplines, concepts, and explanations (inter alia) that have
been developed largely in independence over the past century.2 (Raff 2000) The nature of the
1
I would like to thank Ingo Brigandt, Paul Griffiths, and Jim Lennox for comments on an earlier draft of this paper,
which is the beginning of a larger dissertation project on explanations of the origin of evolutionary novelty since the
Modern Synthesis with special reference to evolutionary developmental biology.
2
There is not universal agreement on the name of the emerging synthesis, with some using “experimental
embryology” (Müller 1991), “developmental evolution”. (Wagner, Chiu, and Laubichler 2000). The name does
matter, (cf. Hall 2000) but I will only utilize evolutionary developmental biology and ‘evo-devo’ in the body of the
paper. The NSF recently established an explicit funding program for ‘evo-devo’ research called the “Evolution of
1
hoped for synthesis is not wholly agreed upon due to divergent viewpoints resulting from this
disciplinary independence and, consequently, the mechanics for accomplishing the task are not
clearly specified. Although a variety of biologists (Ghiselin 1997; Maynard Smith 1998; Mayr
1991; Wallace 1986) and some philosophers (Sterenly 2000) hold that there is no particular
conceptual or empirical difficulty in assimilating recent findings in developmental biology to
contemporary neo-Darwinism, there are a number of reasons to doubt this confidence. (Arthur
2000a;Roberts 2001) The scientists involved in the emerging synthesis called ‘evo-devo’ do not
hold these views for historical, philosophical, and empirical reasons, and therefore I will proceed
with an investigation of the nature of a synthesis of evolution and development rather than an
assimilation of development by evolution.
One way to dissect the foundational problem of bringing evolutionary and developmental
biology back together is through historical investigation. Jim Lennox has recently articulated a
methodological strategy utilizing historical investigation for philosophical purposes he calls the
“phylogenetic approach”. (Lennox 2001) This approach advocates the importance of historical
trajectories to understanding foundational problems in contemporary science through an
exploration of the origins of these problems, attempting to identify focal points where particular
conceptualizations may have led to the present situation. The adjective “phylogenetic” indicates
that the claim is about pathways, not mechanisms. No causal claim is offered about the nature of
scientific theories, concepts, or methods and their interactions. There is a minimal assumption
that the epistemic currency of science (theories, concepts, explanations, etc.) is subject to change
Developmental Mechanisms”, an element within the Division of Integrative Biology and Neuroscience. (Plesset,
Scheiner, and Singer 2000)
2
over time and exhibits relationships of “cognitive descent”.3 As Ernst Mayr has noted, “[e]ach
concept is burdened with the heritage of its past.” (Mayr 1980, 44)4
The formulation of theoretical frameworks in science is highly contingent and subject to
local influences of many different kinds. Foremost among these influences are empirical
considerations, but they are by no means fully determinative and operate in conjunction with
other factors. Alternative pathways were available in the early stages of a now mature science,
some of which were pursued while others were ignored. Often the clues to understanding
contemporary foundational problems are found in those alternatives left by the wayside. The
philosopher of science utilizes her knowledge of and distance from contemporary science in
conjunction with the history of science to isolate the nature of underlying conceptual issues.
Contemporary evolutionary theory is built on the foundation of the Modern Synthesis of
the 1940s, which utilized the mathematical population genetic results of Fisher, Haldane and
Wright to forge a synthesis of experimental and naturalist traditions with natural selection as the
major engine of evolutionary change. (Sterelny and Griffiths 1999, 22-52) This framework was
extended by George Williams and Richard Dawkins into a “gene’s eye view of evolution”
utilizing the principles of the Modern Synthesis. (Sterelny and Griffiths 1999, 55-76) A number
of challenges emerged in the early 1980s, some friendly, some hostile, to the sufficiency of the
synthetic theory. (Burian 1988) A key point of discussion was the relationship between
evolution and development, addressed at a now famous Dahlem conference in 1981. (Bonner
1982) Gould’s work on the history and contemporary significance of heterochrony, (Gould
1977) and the formal model presented shortly after (Alberch et al. 1979), stimulated a vigorous
3
Thus the “phylogenetic approach” does not directly engage the many debates within evolutionary epistemology.
Equally important to a characterization of the phylogenetic approach is a reminder of what it is not. “It is
decidedly not the enterprise of trying to support philosophical conclusions with historical facts.” (Lennox 2001) The
history of science is not a large data set from which to test or confirm pet theses within the philosophy of science.
4
3
conversation about how recent results in developmental biology might impinge on the received
view of evolutionary theory. The publication of a symposium on development and evolution
(Goodwin, Holder, and Wylie 1983) and an entire book devoted to the importance of
developmental genetics for evolutionary change (Raff and Kaufman 1983) permanently carved
out a research niche for the relationship between genes, embryos, and evolution. Further
conferences contributed to this discussion through the interaction of biologists from diverse
disciplinary backgrounds and theoretical propensities. (Raup and Jablonski 1985; Raff and Raff
1987; Wake and Roth 1989a)
In the attempt to comprehend the present separation between evolution and development
much attention has been paid to the split between genetics and embryology in the early part of
the century with its codification in the exclusion of embryology from the Modern Synthesis.
This encourages a characterization of “evo-devo” as the integration of developmental genetics
with Neo-Darwinism.5 But there is a largely untold story about the significance of morphology
and comparative anatomy, also minimized in the Modern Synthesis. I will attempt to reconstruct
part of this story, focusing on the rebirth of functional (and evolutionary) morphology in the
1950s. Functional morphology is critical for understanding the development of a concept
understood as central to “evo-devo”, evolutionary innovation. (Wagner, Chiu, and Laubichler
2000) The meanings of this concept within morphology and comparative anatomy are relevant
to the nature of the disciplinary synthesis of ‘evo-devo’. Understanding the story about
5
E.g., in a chapter on “Development and evolution” in a recent paleobiological treatment of vertebrate evolution, the
heading “Integration of developmental biology with the evolutionary synthesis” only discusses the importance of
Hox clusters from the realm of developmental genetics. (Cf. Carroll 1997, 258-262)
4
morphology and innovation reveals a different conception of the foundational problem,
providing an alternative way of conceptualizing the ‘evo’ and the ‘devo’ to be synthesized.6
2. Synthesis and Integration
“Two approaches seem possible: one, in which the structure of one discipline is compared with that of the
other, and subsequently bringing both together in one structure, and the other, in which the significance of the
concepts of one discipline for the other discipline are considered.” (Dullemeijer 1981)
Although Dullemeijer’s comments pertain to the relationship between functional
morphology and evolutionary biology (see Section 5), it is an apt point of departure for
characterizing the nature of the problems that make the emergence of evolutionary
developmental biology desirable. The first option, where two disciplines are compared and then
brought together, I will call disciplinary integration. (Cf. Bechtel 1986b) This is appropriate
because the result is one disciplinary structure that integrates two distinct disciplines. The
second strategy, where the significance of concepts in one discipline is evaluated for another
(and vice versa), I will refer to as conceptual synthesis, distinguishing both the level at which the
two domains are being compared and the activity that is being engaged in. Integration denotes
bringing together one or more parts into a new entity where the individuality of the original parts
are lost or effaced. Synthesis denotes a blending of one or more parts that may or may not
produce a new entity where the individuality of the original parts is not dissolved, though
potentially transformed.
Naturally, a complete taxonomy allows for disciplinary synthesis and conceptual
integration, where the former produces a new discipline without dissolving those from which it
6
A number of proposals for the integration (or synthesis) of evolution and development have been made. (Atkinson
1992; Burian 1986; Gilbert, Opitz, and Raff 1996; Horder 1989; Smith 1992) The argument in the present paper
differs in emphasizing the possible role of morphology based on a history of science rationale.
5
was synthesized and the latter refers to how more than one concept can be merged into a single
new concept for various purposes. The taxonomy is hierarchically inclusive in that disciplinary
integration and synthesis subsumes both conceptual integration and synthesis, but the conceptual
level can be tackled without necessary implication for the disciplinary level.7 Defending this
taxonomy is not my present aim, and one might immediately want to extend it with more levels
such as theories or explanations, which would force at least some reevaluation of the hierarchical
relations and implications. (Table 1) These issues have been discussed extensively elsewhere
with respect to many different scientific disciplines. (E.g. Bechtel 1986a) Instead I want to zero
in on the level of concepts to approach the issues at stake in “evo-devo”, assuming that the
conceptual level typically has implications for the disciplinary level.8
Evolutionary developmental biology is usually conceived of as a disciplinary synthesis,
hierarchically inclusive in the above sense.9
“For evolutionary developmental biology (EDB or ‘evo-devo’) is not merely a fusion of the fields of
developmental and evolutionary biology, the grafting of a developmental perspective onto evolutionary
biology, or the incorporation of an evolutionary perspective into developmental biology. EDB strives to
forge a unification of genomic, developmental, organismal, population, and natural selection approaches to
evolutionary change. It draws from development, evolution, paleaeontology, molecular and systematic
biology, but has its own set of questions, approaches and methods.” (Hall 1999, xv)
Analyzing all of these suggested interrelations is beyond the scope of any one essay. A more
manageable task is to try and determine the mutual significance of one or more concepts for
evolutionary developmental biology in the mode of conceptual synthesis. Ron Amundson has
produced an insightful analysis of the concept of constraint in evolutionary and developmental
7
E.g., accomplishing conceptual synthesis does not mandate disciplinary synthesis or integration and it may be
undesirable, impractical, or impossible.
8
One parallel theme, which will not be a part of my analysis, is unification. This narrative theme has recently been
carefully discussed (Smocovitis 1996) and is obviously related to synthesis and integration, as discussed above.
Briefly, I take unification to be a synthesis claim about all biological disciplines, thus something much larger than a
disciplinary synthesis simpliciter, however complex.
6
studies, revealing that evolutionary practitioners interpret constraint as ‘constraint on adaptation’
and researches in development understand it as ‘constraint on form’. (Amundson 1994; 2001) I
have tried elsewhere to bring together the concepts of developmental constraint and adaptive
landscape in specific explanations of biological phenomena. (Love 2001)
On the assumption that concepts have a historical lineage, a concept must be tracked
across time and not just in the present.10 If the concept is utilized in a discipline not taken to be
“central” to the emergence of evolutionary developmental biology, we will have cause to
recommend a reconsideration of this discipline and its theories, concepts, etc., in the project of
synthesizing evolutionary and developmental biology. I am proposing that understanding the
historical trajectories of concepts within evolutionary and developmental biology is critical to
disentangling the problem of synthesizing them in the present and identifying one or more
putative solutions.
3. Exclusion Historiographies and ‘Evo-Devo’
“Curiously, the only group of biologists not participating were the developmental biologists. In Germany, in
France, in England (with the exception of Waddington) and in the United States they were opposed to the
synthesis on a Darwinian basis. They were all Lamarckians.” (Mayr 1997)
It is an oft-repeated historical claim that embryology was excluded from the Modern
Synthesis (Hamburger 1980), or least did not want to participate. (Mayr 1993) This exclusion is
perceived as a source of the foundational problems attending contemporary evolutionary theory
9
Bechtel’s notion of disciplinary integration brings this out by pointing to conceptual integration and synthesis that
emerges from interdisciplinarity. (Bechtel 1986b, 38-47) For a related discussion of the integration of idealized
models, see Mitchell 2001.
10
Thus, this technically adds a third dimension, time (synchronic vs. diachronic), to our taxonomy. (Cf. Table 1)
7
that require the synthesis called evolutionary developmental biology.11 The historical trajectories
of genetics and embryology, their split and various relations, or lack thereof, have been
documented by many historians. (Allen 1985, 1986; Gilbert 1978; Maienschein 1987; Sapp
1987) Much of this story transpires in the first three decades of the 20th century as genetics
became an autonomous discipline. The writings of T.H. Morgan helped codify the division,
ironic given his own participation in both areas of research. (See Morgan 1926a, 1926b)
Assuming genetics and embryology were separate by about 1935, the tight connection
between population genetics and evolutionary theory in the Modern Synthesis helps explain the
exclusion of embryology. Although some participants in the Evolutionary Synthesis had
resources for bringing embryology into the discussion, by and large this simply did not occur.
Julian Huxley’s training in experimental embryology would have made him a likely candidate
for discussing the importance of development for evolution in his contribution to the synthesis.
(Huxley 1942) Although he acknowledges development in his “three aspects of biological fact”
(“the mechanistic-physiological aspect: how is the organ constructed, how does the process take
place?” [40]), he tips his hand by equating this aspect with the transmission of hereditary factors
when applying the three aspects to evolution. (Cf. Huxley 1942, 41)
The genetics and embryology exclusion historiography is not incorrect in its details. The
concern arises over how it is put to use. If evolution is understood primarily in terms of genetics
(which is not unusual given the welding of evolutionary theory to population genetics in the
Modern Synthesis), then the synthesis of evolutionary and developmental biology is a synthesis
between genetics and embryology. The dramatic results pouring forth from studies in
11
Exclusion historiography is only one way of approaching the historical rationale for a new synthetic approach.
Other developments in biology, such as cladistic systematics, could not have been part of the Modern Synthesis in
the 1940s since they emerged at a later date. Thus, one could also characterize the synthesis in terms of those things
that are later developments that need to be included.
8
developmental genetics seem to provide the needed materials for constructing this synthesis,
providing exactly the bridge that is needed between genetics and embryology. (Carroll 1995;
Gehring 1998; Lawrence 1992)
This viewpoint can be seen in a couple different places. In his well-respected textbook
on developmental biology, Gilbert says:
“In the 1990s, the techniques of molecular biology enabled biologists to discover (1) homologous
regulatory genes such as Pax6 that control the development of the same organs thoroughout [sic] the
animal kingdom, (2) homologous developmental pathways whose functions can change between organisms
or between cells of the same organism, and (3) the changing patterns of the homeotic gene expression that
allow different parts of the body to have different structures and functions. Such discoveries have
converged to form a developmental evolutionary synthesis that incorporates the population genetic
approach but which expands evolutionary theory to explain macroevolutionary phenomena as well. …We
are at a remarkable point in our understanding of nature, for a synthesis of developmental genetics with
evolutionary biology may transform our appreciation of the mechanisms underlying evolutionary change
and animal diversity.” (Gilbert 1997, 614)
Gilbert implicitly equates the population genetic approach with evolution and sees
developmental genetics as the key missing component for the synthesis. Some of these notions
are further revealed in an accompanying diagram in the text. (Gilbert 1997, 915; Figure 1) Here
comparative anatomy is assumed to have been a part of the Modern Synthesis when it usually is
understood as having been excluded. (See below, Section 4)
Another window on this viewpoint is seen in the work of Arthur’s study of evolutionary
developmental biology.
“The goal of evolutionary developmental biologists is to explain the causality of this pattern, through
consideration of how natural selection (the domain of population genetics) interacts with the genetic
architecture of development (the domain of developmental biology).” (Arthur 1997, 32)
“…the picture that [the developmental geneticists] ultimately produce (of which our current view is
fragmentary but enticing) is likely to be the most important remaining input into evolutionary theory.” (43)
Here population genetics is equated with evolutionary studies and developmental genetics is the
“missing link”. This perspective is enhanced through a diagram of the “circle” of evolutionary
theory (Arthur 1997, 287; Figure 2) The major part of the missing developmental component is
9
developmental genetics. It is not clear what the role of comparative anatomy (morphology) is,
the major component found under the heading “Classical Evidence of Evolutionary Pattern”.
With population genetics basically equated with evolutionary theory (“Neo-Darwinism” in the
circle), comparative anatomy along with aspects of paleontology and comparative embryology
appear to be observers, not participants in the new discipline of ‘evo-devo’.
Although the previous two examples were from the writings of scientists, the framing of
the problem in terms of embryology and genetics can also be found in the work of
philosophers.12 Amundson’s main investigative question and concluding remarks in a recent
paper implies the bridge of developmental genetics.
“Was the success of the Evolutionary Synthesis a factor in the increase of interest among embryologists in
the study of developmental genetics? … Unification of developmental with evolutionary biology has not yet
been achieved despite the advances in developmental genetics.” (Amundson 2000, 315, 327)
In the introduction to the symposium on ‘evo-devo’ published in American Zoologist, Burian
sees the control of eye formation by a conserved genetic module as a prominent example of how
evolutionary developmental biology is unfolding.
“The extraordinary rich details regarding integrated units that function in development, with controls that
are preserved through even hundreds of millions of years, provide us with the materials to bring
developmental, evolutionary, and genetic techniques to bear on old, but transformed, problems. This
triangulation, I believe, will be the key to the success or failure of Evo-Devo.” (Burian 2000, 714)
Burian’s triangulation observation follows after a variety of historical comments that imply that
the key disciplinary split was between embryology and genetics in the early 20th century (Burian
2000, 713), made more explicit in an earlier article. (Burian 1997) As before, it is not inaccurate
to draw attention to these facets, but it may be a distortion to imply that the key rapprochement
12
Other scientists perceive developmental genetics as the critical factor in awakening an interest in the project of
reuniting evolutionary and developmental biology. (Cf. Raff 2000, 75)
10
for evolutionary developmental biology is between developmental biology and genetics.13 The
issue is not the correctness of the history for understanding the ancestry of evolutionary
developmental biology. It is the use of the history as the primary narrative for guiding the
present construction of ‘evo-devo’ that runs the danger of forgetting others who were left out of
the synthesis, who might be critical to normatively directing its formulation today.
4. Morphology and the Modern Synthesis
“There exists …a generally silent group of students engaged in biological pursuits who tend to disagree with
much of the current thought [i.e. the Modern Synthesis] but say and write little because they are not
particularly interested, do not see that controversy over evolution is of any particular importance, or are so
strongly in disagreement that it seems futile to undertake the monumental task of controverting the immense
body of information and theory that exists in the formulation of modern thinking. … Wrong or right as such
opinion may be, its existence is important and cannot be ignored or eliminated as a force in the study of
evolution.” (Olson 1960)
Given the traditional exclusion historiography of genetics and embryology, it may be
somewhat surprising that the targeted groups of Olson’s description are morphologists and
paleontologists. Olson goes to great lengths in his discussion to make space for alternative
conceptions of evolution that were not strictly part of the Modern Synthesis, emphasizing the
tendency to consider one or more discipline’s conceptual stance more legitimate by excluding
alternative stances from other disciplines. He was keenly aware of the lack of “elasticity” in the
selection theory in conjunction with its seeming ability to explain everything. The burden of
proof was shifted from showing that an alternative explanation for a phenomenon was possible to
demonstrating that the phenomenon could not be sufficiently handled by the synthetic theory.
13
A side effect of the genetics and embryology exclusion historiography is a disproportionate focus on individuals
such as C.H. Waddington (Amundson 2000; Gilbert 1991, 2000) and Boris Ephrussi (Amundson 2000; Burian,
Gayon, and Zallen 1991), who can be seen as early participants in the bridge area of developmental genetics. In
comparison, I.I. Schmalhausen has received less attention (but see Allen 1991 and Gilbert 1994).
11
“Morphologists and paleontologists feel this, perhaps, more strongly than other students of
biology…The extent of assumption, interactions of assumptions, and the degrees of extrapolation
give a sense of uneasiness when the animals and their structures are foremost in mind.” (Olson
1960, 530)
Although a valiant attempt has been made to show the importance of morphology in the
Modern Synthesis in the British context (Waisbren 1988), the key distinction is between the
potential to contribute and actual contribution. Goodrich, Huxley, and de Beer all were
potential sources of morphological thinking to be incorporated in the synthetic theory, but none
of them can be said to have actually made a significant contribution. We have already seen that
Huxley diminished the significance of development and this is equally true of his work on
allometry, as well as de Beer’s work on heterochrony, by attributing both to rate-genes. (Huxley
1942, 525-543; cf. Churchill 1980) Everyone respected the vertebrate morphological research of
E.S. Goodrich but there is no evidence that the framers of the synthetic theory saw his work as a
contribution. de Beer’s Embryos and Ancestors (1958) [1st edition, 1930] played a significant
role in reinvigorating interest in the connection between development and evolution in the 1960s,
but this book was not central to the articulation of the Modern Synthesis. Evolutionary
morphology is much more explicit in de Beer’s textbook, Vertebrate Zoology (1967) [1951] (1st
edition, 1928), but this also was not part of the discussions in the 1940s. Maybe this was a
function of national difference that a primarily American context for the synthesis did not
overcome. Regardless of the existing resources, those morphologists who could make key
contributions to the Modern Synthesis did not.
A qualitatively stronger thesis is that because morphology is descriptive, it could not have
made a contribution to the synthetic theory.
12
“To many it has seemed enigmatic that morphology contributed virtually nothing to the synthetic theory of
evolution. … Morphology has contributed so little primarily because it has had so little to contribute. It is a
descriptive science of form, and only when conjoined with other disciplines does it tell us anything about
causes. …morphology tends to be the sort of discipline that will follow, rather then lead, in the
development of evolutionary theory.” (Ghiselin 1980)
The Modern Synthesis was focused on the mechanism of evolutionary processes and
morphology simply could not tackle the causal question. Ghiselin attributes the difficulty of
morphology not just to its descriptive orientation but also to metaphysical trappings such as
essentialism and the search for laws following the model of physical science. Coleman’s
companion analysis largely concurs: “The role of morphology in the formation of the
evolutionary synthesis was negligible.” (Coleman 1980, 174) He also points out that
morphologists failed to connect their work to genetic mechanisms. Similarities in general
characteristics were detailed in order to reconstruct the history of life while ignoring population
diversity. Variation was an unimportant phenomenon, signaled by the metaphysical inclinations
towards idealistic philosophy of many morphologists.
In a review of the Mayr and Provine volume on the Evolutionary Synthesis, David Wake
comments that, “[t]hose who feel that morphology and embryology stood outside the synthesis
should read Schmalhausen.” (Wake 1981, 1257)14 There is no doubt that Schmalhausen’s
Factors of Evolution (1986) [1949] was much more integrative with respect to embryology and
morphology and this is expected considering his own morphological training under Severtsov.
(Adams 1980) But it is also true that Schmalhausen’s work was not genuinely a part of the
synthesis, which may have been due to a perception that it was in conflict with the work of
Waddington. (Wake 1986) The important concept of norm of reaction (adaptively interpreted)
played a significant role in Schmalhausen’s thinking. (Cf. Sarkar 1999) Stabilizing selection acts
on “adaptive norms”, assumed to be hereditary because they are characteristics of particular
13
genotypes, which are initially shaped by external factors but become integrated over time into a
system of internal factors of development, insulated from environmental perturbations.
(Schmalhausen 1986 [1949], 2-5) The history of life is a “progressive” liberation from these
external factors with a commensurate anchoring of the phenotypic plasticity in autonomous
ontogenetic processes that are reliable.
A likely candidate for a contribution to the synthesis from the ranks of morphology in the
American context is D.D. Davis. His article in the report from the 1947 Princeton meeting of the
Committee on Common Problems of Genetics, Paleontology, and Systematics, opens with a
familiar refrain in real time: “Recent syntheses of current evolutionary thought have, almost
without exception, ignored comparative anatomy completely or considered it only very
obliquely.” (Davis 1949, 64) Despite his claim of a reciprocal relationship between the findings
of genetics and morphology, Davis never provides an account of why morphology is important
for genetics. Davis acknowledges that morphologists have not thought in terms of “populations”
but sees a remarkable congruence of ideas between population geneticists and evolutionary
morphologists. (76) There is no explicit challenge to the synthetic theory of evolution and the
article can be interpreted as a guide to perceiving morphology and comparative anatomy as
consistent with the aims of other domains within the Modern Synthesis.
What is missing from a constructive account of the importance of morphology in his
1949 article can be partially recovered in a later discussion. (Davis 1960) In an attempt to
delineate the proper goal of comparative anatomy, Davis consciously steers clear of idealistic
notions found in the phylogenetically oriented morphology of the Gegenbaur School. Davis
rejects the claim that comparative anatomy cannot contribute to questions of evolutionary
14
Even though Smocovitis addresses the ‘exclusion’ of embryology from the Modern Synthesis, she does not
discuss the exclusion of morphology. (Cf. Smocovitis 1996, 191-196)
14
causality and he locates the main reason for the failure of morphology to contribute to biological
theory in transnational misunderstanding. This misunderstanding occurred in part because the
subtle meanings of morphological concepts were hard to grasp outside of the German speaking
context and German anatomists failed to grasp key aspects of Darwinism. The scientific
qualification for comparative anatomy shifts the focus of morphologists from structural
similarity to structural difference.
“If comparative anatomy is to qualify as a science it must, like any other science, offer a rational
explanation for the phenomena with which it deals. The phenomena of comparative anatomy are not the
observed structure of vertebrates, but the observed differences between the structure of one vertebrate and
another. …its proper goal is …to explain the observed variations in [the common structural] plan.” (46)
The “major” differences focussed on by comparative anatomists are based on the same
mechanism as those minor phenotypic variations described by population geneticists. The
problem is simply demonstrating how the mechanism operated in a particular case. The
contribution of morphology to a causal understanding of evolution is at a level inaccessible to
laboratory genetic studies using the same causal mechanism. Adaptation is the a main
explanandum of morphology, just as in other aspects of biology, but operating at higher
taxonomic levels: “we are dealing with adaptation, with functional mechanisms, and differences
in structure are meaningless unless they can be correlated with differences in function.” (49)
After identifying structural differences correlating these differences with function and it relation
to organismal habits and behavior, the last step is to figure out whether or not the morphological
traits in question are under direct or indirect genetic control. This way lies the “salvation” of
comparative anatomy. (50)
The presence of Davis and his arguments for a functional approach to morphology reveal
that it was not just comparative anatomy per se that was excluded but rather a research
perspective often associated with morphology. The exclusion of this perspective is evident in an
15
editorial decision made in the early stages of the journal Evolution, identified in an analysis of
Ernst Mayr’s pivotal role at this juncture. (Cain 1994) Shortly after the inception of Evolution,
Rainer Zangerl, a vertebrate anatomist, submitted an article on the importance of comparative
anatomy for evolutionary studies. (Zangerl 1948) Drawing heavily on German idealist
morphologists, Zangerl argued that concepts such as morphotype and structural plan were
important for evolutionary theory. The outlook was clearly typological:
“In morphology, the norm is the morphotype which is an abstraction of the actual form variety within a
group of organisms of the same structural plan. It is arrived at by abstraction …disregarding all the
numerous peculiarities of form in the individual representatives of the group, and including only those
features that are unspecialized and mutually present in all…” (Zangerl 1948, 357)
Zangerl illustrates the existence and significance of morphotypes through a study of turtle skulls.
The second half of the paper is an argument to the effect that holism, with its focus on the
organism, is a necessary component of evolutionary biology. “It is in this basic realm where
morphology must and can make an important contribution to the future development of ultimate
theoretical thinking in biology.” (372)
After a long editorial process conducted among Mayr and others, it was finally decided
that the paper should be published. When a rebuttal of Zangerl was submitted a year later, it was
returned with the explanation that, “the editorial board had agreed it would serve “no good
purpose” to continue with that “discussion””. (Cain 1994, 420) Typological comparative
anatomy was not to be a part of the conversation in the journal Evolution, effectively silencing its
role as a contributor of theoretical perspective to evolutionary discussion in the post-Synthesis
context. Comparative anatomy and morphology in the service of paleontological studies
(Schaeffer 1948), phylogenetic studies (Gregory 1950), and morphometrical analysis (Olson and
16
Miller 1951) were acceptable as long as they were conducted within the theoretical perspective
of the synthetic theory of evolution, implicitly or explicitly.15
5. Functional and Evolutionary Morphology
“In 1956 anatomy was moribund; the field of functional and evolutionary morphology barely existed as a
scientific discipline.” (Wake 1982)
The significance of morphology in 19th and early 20th century biological research,
including evolutionary theory, has recently been reconsidered by a number of authors. (Bowler
1996, Maienschein 1991, Nyhart 1995) Here I want to draw attention to the period after the
Modern Synthesis, congruent with Wake’s remarks about the status of comparative anatomy in
the early 1950s. David Wake’s retrospective comments seem odd when there are presently
dense textbooks filled with rich examples of functional anatomical studies in an evolutionary
framework. (Walker and Liem 1994) The thread of continuity with the period prior to 1950 is
found in individuals like D.D. Davis who articulated an agenda for morphology that was
distinctly functional in orientation, pulling away from the traditional emphasis on structure apart
from function. (Davis 1960) Wake identifies a reductionist research outlook as a factor in the
decline of comparative anatomy in the first half of the 20th century but he also notes that the
exclusion of morphology from the Modern Synthesis played a critical role. (Wake 1982, 604-5)
The return of functional morphology was tightly connected with the increasing emphasis
on an experimental approach. (Gans 1985; Hanken and Wake 1991; Wake 1982) New
techniques such as mechanical and chemical sensors, force plates, and electromyography led to a
15
The contribution of Bernard Rensch can be understood in a similar way. (Rensch 1959) Although a zoologist
trained in a context congenial to comparative morphology, his comprehensive study comports with the synthetic
theory of evolution and focuses on the importance of allometric growth. But his use of the notion of “type” and its
idealist connotations come under the suspicious eye of architects of the Modern Synthesis. (Cf. Simpson 1949, 184)
17
proliferation of data that was then analyzed through new computer technology. Unsuspected
aspects of morphological performance were discerned through studying the unused capacities of
functional systems. Explicit connections were made with phylogenetic considerations (thus
leading to evolutionary morphology) as well as developmental studies.16 Knowing the history
and development of a structure became integral to discerning its function(s). As Gould noted at
the outset of the ICSEB symposium in 1974 on the “Evolutionary Development of Form and
Symmetry”, “[d]uring the past decade, like a thief in the night, morphology has surreptitiously
become interesting again.” (Gould 1974, 401; see also Wake 1982 for further details)17
In addition to the experimental approach, philosophical aspects of the nature of and
relations between functional and evolutionary morphology were addressed. (E.g. Bock and von
Wahlert 1965; Dullemeijer 1974) At the forefront of these discussions was an articulation of the
form-function relation, foundational to all morphological investigation. Another crucial
component of articulating the foundations of morphology was the erosion of any simplistic
equivalence between functional morphology and standard biomechanical studies. One reason for
this is the historical turn that emphasized the significance of phylogenetics for functional
morphology, thereby making it more evolutionary in nature. George Lauder, emphasizing that a
diachronic approach was essential to morphology, cogently argued for the importance of
historical analysis in morphology in the early 1980s. (Lauder 1981, 1982) An important aspect
of historical analysis was specifying a way to test hypotheses about morphological innovations.
(Lauder and Liem 1989)
16
Functional morphology is not equivalent to evolutionary morphology, although a variety of practitioners now see
the two intricately intertwined through the necessity of a historical perspective. (See Dullemeijer 1981)
17
Gould’s comments are a reminder that an important connection exists between morphology and paleontology,
already indicated by Olson (1960). A full exploration is beyond the scope of the present paper but important sources
connected with the my discussion include Raup (1972) and Seilacher (1973). (See also Olson 1960)
18
In a review of the state of morphology in 1985, Liem and Wake gave the following
definition of evolutionary morphology: “We define functional and evolutionary morphology as
that field of biology that studies the evolution of form and function by combining comparative
and experimental methods of analysis.” (Liem and Wake 1985, 366) They advocated a view
where it is necessary to include both extrinsic and intrinsic determinants of “design”.18 Within
the extrinsic factors, structural analysis, functional analysis, and experimental ecological analysis
are necessary components. Under the intrinsic heading, phylogenetic and historical analysis,
analysis of biological repetition, and ontogenetic analysis are essential components. The latter
component (ontogenetic analyses) receives the most thorough treatment with special attention to
the importance of epigenetic (not genetic) processes that generate stable morphological
patterns.19 Heterochrony is invoked as a potential source of the origin of morphological
novelties and the research program outlined for morphology seems to be immediately relevant to
evolutionary developmental biology. Developmental genetics is not explicitly discussed.
The centrality of morphology for evolution has been forcefully, if not uniquely, argued
for by Rupert Riedl. (Riedl 1983) “Morphology contains the methodology of scientific
comparison, namely, the distinction between essential similarities (homologies) and accidental
similarities (analogies).” (206) A typological approach to morphology is innate because our
“hereditary cognitive apparatus” allows us to correctly identify and make comparisons of natural
kinds. Although Riedl’s views on why morphology is central to evolutionary biology are
debatable, his book Order in Living Organisms (1978) is cited as an early treatment of the
18
Here design is understood as “the organization of biological structure in relation to an hypothesized function.”
(Lauder 1982, 58)
19
“To understand ontogenetic trajectories one must understand epigenetics and developmental dynamics. One of
the most intriguing aspects involves the complex nonlinear interactions during development. Small changes in
development control parameters can be amplified during ontogeny to give dramatically different morphological
results. It is this final point that has led to the recent excitement in analyzing ontogeny in relation to evolutionary
morphology and phylogeny.” (Liem and Wake 1985, 376)
19
intersection between evolution and development. Importantly, his students (e.g. Günter Wagner
and Gerd Müller) are key players in the current discussion surrounding evolutionary
developmental biology.
Apart from Riedl’s arguments, the resurgence of interest in functional morphology has
not necessarily translated into a tangible effect on evolutionary theory.
“The data of morphologists and some of their interpretations are important, even “indispensable” for
evolutionary biology, but I do not yet see integration of morphology into the central themes of evolutionary
biology at the level of understanding the processes responsible for the evolutionary modification of form
and function.” (Wake 1982, 609)
Part of this impact was perceived at the fourth meeting of the ICSEB where the relation between
the impact of functional morphology and biomechanics on evolutionary biology was discussed.
(Wake 1991) Wake (1992) reviews the breadth and scope of current studies in evolutionary
morphology drawing attention to the reintroduction of whole-organism approaches, comparative
biology, and architectural/constructional constraints. Two factors that affect this impact are
more explicit attention to methodological issues in functional morphology, such as the building
and testing of models (Homberger 1988), and the study of the role of ecology in the actual
performance of morphological trait complexes. (Wainwright and Reilly 1994) The significant
interface between morphological studies and the emerging synthesis of evolution and
development was also explored in a variety of papers at the 2nd International Symposium on
Vertebrate Morphology in 1986. (Splechtna and Hilgers 1989) Not a single presentation (30
total) focused on the findings from developmental genetics.
6. Innovation and Novelty
“There are fashionable problems and there are neglected problems in any field of research. The problem of the
emergence of evolutionary novelties has undoubtedly been greatly neglected during the past two or three
decades, in spite of its importance in the theory of evolution.” (Mayr 1960)
20
The origin of novel structures and functions is an old problem in evolutionary biology,
going back to Darwin himself. (Darwin 1964 [1859], 179-203)20 Standard examples usually
include the turtle carapace (cf. Burke 1989), avian flight (Cracraft 1990), vertebrate feeding
systems (Roth and Wake 1989), as well as more recent examples such as centipede segment
number. (Arthur 2000b) Ernst Mayr’s seminal article helped bring the topic back under
consideration in the post-Synthesis context. (Mayr 1960) In expected fashion, Mayr tries to
show how evolutionary novelty can be handled within the context of the synthetic theory of
evolution without recourse to saltationism/macromutationism, assuming a dichotomy of
explanations between saltation and gradualism. He also distinguishes the problem of the origin
of novelty from the problem of the origin of new taxa, even though his definition is suggestive of
a connection that continues to the present day.21 Mayr’s functionalist approach to biological
investigation leads him to a tentative functional definition of novelty (“…any newly acquired
structure or property which permits the assumption of a new function”), in contrast to the
structural definition of classical comparative anatomy.
At about the same time, Bock applied a functional morphological perspective in his study
of double jaw articulation in birds (Bock 1959), illustrating Mayr’s point that the transfer of
function for the origin of novelty can take place in the presence of a structural duplicate. (Mayr
1960, 362) Working within the context of the synthetic theory of evolution, Bock attempted to
account for the secondary basitemporal articulation in the avian mandible (the medial brace) that
prevents the jaw from disarticulating under strong forces during feeding activity (such as
skimming for fish). The concept of preadaptation plays a central role in Bock’s argument: “A
20
Evolutionary innovations are not equivalent to evolutionary transitions, the latter being a species of the former.
(See Szathmáry and Maynard Smith 1995)
21
structure is said to be preadapted for a new function if its present form which enables it to
discharge its original function also enables it to assume the new function whenever need for this
function arises.” (201)22 Bony knobs on the basitemporal plate which served as attachment
points for cervical muscles were preadapted for the secondary articulation of the medial brace
due to their position and projection with respect to the entire basitemporal plate. Interestingly,
Bock invokes Schmalhausen’s theory of stabilizing selection to account for how the articulation
could have arisen non-genetically and later been brought under genetic control during ontogeny.
His functional morphology of avian jaw articulation is a good example of the early connection
between the origin of novelty and morphological investigation in the post-Synthesis context.
Proponents of evolutionary developmental biology see their nascent synthesis as a prime
avenue for exploring unanswered questions about the origin of evolutionary novelties.23
“Questions on the nature of homology, …the origin of novelties and ultimately a complete understanding
of evolution lie before this young discipline [i.e. ‘evo-devo’] (Raff 2000, 79)
“...finding answers to what constitutes an evolutionary innovation …and how developmental mechanisms
have changed in order to produce these innovations are major issues in contemporary evolutionary
developmental biology.” (Olsson and Hall 1999, 612)
“…DE [developmental evolution] may lead to a mechanistic explanation of the origin of evolutionary
innovations and the origin of body plans…. Evolutionary innovations and the evolution of body plans are
hard to understand in population genetic terms since they involve radical changes in the
genetic/developmental architecture of the phenotype. …evolutionary innovations are outside the scope of
any current research program. Through its contribution to the solution of that question, DE genuinely
expands the explanatory range of evolutionary theory. We think that this is the one area where DE will
have its most lasting impact on evolutionary theory and biology in general. …we see in the problem of
innovation and the evolution of body plans a unique opportunity for DE to develop its own independent
identity as a research program.” (Wagner, Chiu, and Laubichler 2000, 820, 822)
Some researchers in evolutionary developmental biology emphasize innovation precisely
because traditional population genetic analysis is incapable of offering the desired explanation.24
21
“…any newly arisen character, structural or otherwise, that differs more than quantitatively from the character that
gave rise to it.” (Mayr 1960, 351)
22
Bock’s paper took the discussions of preadaptation in Simpson (1953) and Davis (1949) as points of departure.
23
Recent textbooks on evolution and development devote entire chapters to novelty. (See Gerhart and Kirschner
1997, ch. 5; Hall 1999, ch. 13)
22
Wagner et al. incline towards the significance of epigenetic dynamics in relevant ontogenetic
processes as the source of the origin of morphological innovations. (See Newman and Müller
2000)25 Elsewhere, Wagner uses the concept of “explanatory force” (sensu Amundson 1989) to
try and demonstrate that although both population genetic and developmental genetic are
mechanisms contributing to evolutionary processes, one or the other may have more explanatory
force for a particular phenomenon. (Wagner 2000) 1:1 sex ratios are wholly accounted for
within population genetic without recourse to developmental mechanisms but eyespots on
butterfly wings are inexplicable apart from an understanding of gene expression patterns during
ontogeny. Evolutionary developmental biology makes an essential contribution to the innovation
of an “eyespot organizer” that gives rise to butterfly wing coloration patterns.
An important variant on the concept of innovation is key innovation, referring to the
capacity of a morphological change to elicit a significant adaptive radiation. One of the most
famous examples is the pharyngeal jaw apparatus in cichlid fish, allowing a massive proliferation
in African lake habitats by specialization of feeding structures. “The innovation (or novelty)
emerged as a new functional and morphological reorganization and subsequent integration of
existing branchial muscles, nerves and bones resulting in an ever increasing efficiency of
function.” (Liem 1973, 432; see also Liem 1980, 1990) The adaptive complex of these fish that
conferred the competitive advantage in feeding capacity was identified using functional
morphological experimentation, such as electromyography. Although subsequent work has
24
“…in the case of evolutionary innovations, the specific developmental functions of the genes involved are an
important part of the explanatory narrative. To state that a genetic mutation led to a favored character, which, in
turn, was selected is utterly uninformative in explaining innovation.” (Wagner, Chiu, and Laubichler 2000, 822-3)
25
Newman and Müller (2000) argue that external physico-chemical factors shaped morphology, generating
innovations, prior to the existence of a genetic architecture that later allows for a fixed inheritance of the
morphology and its construction rules. Their position is strikingly similar to that of Schmalhausen (1986) [1949] in
the sense that phenotypic plasticity induced by environmental conditions becomes insulated from the change of
external factors by internalizing the production of the phenotype within a genetic substratum. Thus epigenetic, not
genetic, factors are critical to the origin of morphological innovation.
23
qualified these conclusions (Jensen 1990), the importance of the adjective “key” is meant to
point to the adaptive significance of a morphological innovation, which may also be considered a
synapomorphy for a monophyletic clade and explain the relative abundance of species within a
larger family of organisms.
Another good example of a key innovation is the hypocone in the dentition of mammals.
(Hunter and Jernvall 1995) The hypocone is a cusp additional to the triangular upper molar teeth
that have evolved repeatedly in mammalian lineages. Although the phenotypic change required
to produce a hypocone is minimal, analysis of lineage diversification reveals that the mammalian
species with hypocones are extremely diverse, correlated with the advantage obtained in
herbivorous adaptive niches. The evolution of dental cusps has recently been studied from a
developmental perspective, revealing how the variation in tooth structure is morphogenetically
produced. (Jernvall 2000) An analysis of seal populations reveals that discrete variation in cusp
number (3-5) is generated in a biased fashion through small developmental changes. By
implication, the production of the key innovation of the hypocone is a product of the capacity of
evolvability exhibited in the ontogenetic processes of mammalian tooth formation.
The concept of innovation is not without difficulties. It has been linked (with
controversy) to the origin of higher taxa, the proliferation of diversification, and evolvability.
(See Hunter 1998) Some have questioned the ontological status of the characters typically taken
to be innovations, pointing out that they are largely artifactual. (Cracraft 1990) Part of this
difficulty would be addressed by agreement on the character concept in biological research
(Wagner 2001), and the importance of a delineated character concept is in part driven by an
attempt to genuinely identify “new” characters in actual lineages. (Wagner, Chiu, and Laubichler
2000) In some sense evolutionary innovations can be seen as the origin of particular
24
homologies. (Müller and Newman 1999) But some evolutionary innovations appear to not be a
consequence of epigenetic mechanisms overcoming developmental constraints. Eberhard’s
study of moveable abdominal lobes in male sepsid flies reveals multiple origins of this
innovation due to sexual selection rather than developmental mechanisms. (Eberhard 2001)
One of the motivations for the angle I have taken in this paper is the article by Müller and
Wagner that attempts to “restructure” the concept of novelty. (Müller and Wagner 1991) They
intentionally avoid the “phenomenological” notion of key innovations discussed above because it
is not the “central problem”. “We concentrate on the generative aspect of morphological
innovations in the process of evolution.” (231; cf. Raff et al. 1990) Three conceptual approaches
are identified in past discussions of novelty: functional concepts, genetic concepts, and
developmental concepts. Although the authors locate themselves in the latter domain (cf.
Müller 1990, 1991), they try to rebuild the concept of novelty from the ground up. “A
morphological novelty is a structure that is neither homologous to any structure in the ancestral
species nor homonomous to any other structure of the a same organism.” (Müller and Wagner
1991, 243) They claim their definition is more broad than those previously offered but
simultaneously recognize that the reference to homology makes the import of the definition
controversial.
A full analysis of Müller and Wagner’s proposal is needed but for the present I want to
note two things. First, if concepts are historical entities subject to change and bearers of their
ancestral baggage, the attempt to restructure the concept by ignoring one of its major features is
wrongheaded. The “phenomenological” characterization of key innovations is still a part of
detecting and isolating morphological novelty, especially in the fossil record (e.g. hypocones),
and it would have been better to mark their task as clarification rather than restructuring.
25
Neither author is unsympathetic with the themes presented thus far in the paper about the
importance of morphology for evolutionary biology, especially given their close ties with Riedl.
Second, by ignoring the notion of key innovations in their discussion they miss the subtle
interconnections between the functional, genetic, and developmental concepts they argue are a
part of traditional accounts of innovation. Novelty has been treated in a plurality of biological
disciplines including genetic, developmental, morphological, physiological, and paleontological.
(Nitecki 1990) If evolutionary developmental biology is a disciplinary synthesis, then it is a
natural strategy to see what kind of conceptual synthesis might occur with respect to
evolutionary novelty. One relevant disciplinary connection is between functional morphology
and developmental biology (Liem and Wake 1985). It is also apparent in the importance of
linking the generative processes that produce morphology with the ecological factors that affect
both the norms of reaction that obtain for a species and the nature of the fitness value of the
morphological trait through the notion of performance. (See below)
7. Reconsidering the disciplinary synthesis of evolutionary developmental biology
“…the success of the synthetic theory in unification of highly diverse areas has gained for it remarkably wide
acceptance. Such success and agreement, while natural, pose certain dangers—danger that matters pertinent
to the area of study may be missed, obscured, or deemed unimportant if they are peripheral to the central
construction; danger that actually relevant fact and inference that cannot be incorporated in the theory will be
summarily dismissed as inapplicable; and danger of expenditures of vast amounts of time and energy in much
too limited contexts.” (Olson 1960)
Most advocates of evolutionary developmental biology would argue that Olson put his
finger on an important point with respect to the Modern Synthesis. But what about the ‘evodevo’ synthesis currently under construction? Where do success and agreement pose similar
dangers? Of four prospective trends identified in a recent editorial in Evolution and
26
Development, Wray identifies more conscious interdisciplinarity as an important future direction
for evolutionary developmental biology.26 Although he mentions paleontology, embryology,
systematics, life histories, phylogenetics, and genetics, morphology is absent.27
My argument thus far can be summarized as follows. First, there is a foundational
problem in contemporary biology in the synthesis of evolution and development. This
foundational problem is traceable to historical factors such as the exclusion of embryology from
the Modern Synthesis. But since morphology was also excluded, there may be more to the
foundational problem. Evidence for this is seen when evolutionary biology has been conceived
of predominantly in population genetic terms, leading to an overemphasis on developmental
genetics as the route to synthesis. (Wagner’s discussion of the innovation of the “eyespot
organizer”, emphasizing the inability of traditional explanatory accounts and the essential need
to understand developmental mechanisms, trades on a distinction between population genetics
and developmental genetics.) If we focus on particular concepts, the notion of innovation or
novelty is taken be central to evolutionary developmental biology. Since disciplinary synthesis
hierarchically suggests conceptual synthesis or integration, the inclusion of morphology as a
discipline in the synthesis encourages a reevaluation of how its notion of innovation bears on the
one desired in ‘evo-devo’. Conversely, the historical connection between morphological studies
and novelty suggests that morphology should be explicitly considered as a participating
discipline within the emerging synthesis.
An objection might be raised that the focus on developmental genetics as the bridge
between evolution and development is an outcome of being concerned about the mechanism of
evolution, rather than the fact or pathway of evolution. But functional morphology is critical to
26
The other three are denser phylogenetic sampling, shorter timescales, and an emphasis on gene interactions.
27
understanding how organisms and their characters work in natural and artificial environments.
(Wainwright 1994) Also, the importance of a rigorous phylogeny for understanding a particular
lineage reveals that pattern is essential for an analysis of process. (Fink 1982) The inability to
explain a particular evolutionary novelty does not license the implication that the results of
morphological investigation are unimportant for understanding the mechanism of evolution.
Rather, morphological research is a conceptual step towards the explanation. (Cf. de Beer 1958,
171) In a recent article (Arthur 2000a), notes that the mutation/selection regime excludes the
mechanism of developmental reprogramming that can occur in ontogeny.28 Aspects of
developmental reprogramming include heterochrony (change in timing), heterotopy (change in
location), heterotypy (change in type), and heterometry (change in amount). Although each of
these can have a genetic basis, they might also be initiated by ecological factors or through
epigenetic processes, signaling a lacuna in neo-Darwinian accounts of evolutionary mechanisms.
The importance of functional morphology in particular, and morphology more generally,
for evolutionary developmental biology often comes from practitioners in these disciplines. At a
1991 discussion of evolutionary developmental biology, David Wake (salamander biologist and
functional morphologist) led the discussion on the relation between development and
morphological evolution, which concentrated on questions such as, “What can evolutionary
morphology and systematics offer students of development?” (Wake et al. 1991, 584) With
respect to evolutionary novelties, the concern of morphologists with complex structures provides
an appropriate intersection for evolution and development. (Atchley and Hall 1991; Wake and
Roth 1989b) It is worthwhile to briefly consider three ways that the inclusion of morphology in
27
In fairness, Wray also mentions phenotypic plasticity, which can be considered a part of morphology, but his
discussion clearly omits the functional and evolutionary morphology described earlier.
28
A similar notion, “ontogenetic repatterning”, was elucidated by Roth and Wake 1989.
28
‘evo-devo’ might alter how the synthesis is conceptualized: typology, phenotypic plasticity, and
explanatory integration.
The distinction between population and typological thinking was introduced by Ernst
Mayr to identify the unique perspective Darwin introduced to biological investigation. (Mayr
1959, 2-5) He traced typology back to the ancient Greeks connecting it with idealism and
essentialism. In his estimation, the two viewpoints are the source of almost every controversy in
evolutionary theory and are mutually exclusive.29 Researchers who were inclined to think
‘typologically’ were bothered that their entire research was being effectively confined to the preDarwinian rubbish heap. Olson expressed the worry concisely: “The statement is made, in
effect, that those who do not agree with the synthetic theory do not understand evolution and are
incapable of so doing, in most cases because they think typologically.” (Olson 1960, 526) This
is not an exaggeration, as Mayr’s own comments demonstrate.30 The worry extends directly to
the introduction of ontogenetic considerations into theorizing about evolution: “Any author who
uses findings from the ontogeny of an individual to prove one or another evolutionary theory
proves thereby that he completely misunderstands the working of evolution. To extrapolate from
the individual to the evolutionary “type” and its fate is, of course, still another manifestation of
typological thinking.” (Mayr 1959, 8)31 Those seeking similarity in the pattern of evolution have
29
“The ultimate conclusions of the population thinkers and of the typologist are precisely the opposite. For the
typologist, the type (eidos) is real and the variation an illusion, while for the populationist the type (average) is an
abstraction and only the variation is real. No two ways of looking at nature could be more different.” (Mayr 1959,
2) The incompatibility has even been utilized as an organizing theme in the study of the morphologist Gegenbaur
(Coleman 1976), where typology is seen as a remnant of pre-Darwinian thinking that took much time to slough off.
“Conversion” was necessary to genuinely adopt descent theory because the morphologist’s types could not be
legitimately evolutionary. (Coleman 1976, 151)
30
“I have devoted so much space to the presentation of the populationist viewpoint because the modern evolutionary
theory can only be understood in the light of population thinking. (Mayr 1959, 4) Mayr attributes the bulk of
difficulties in the construction of the Modern Synthesis to typology/essentialism. (Cf. Mayr 1980, 13, 17, 18, 29)
Although a study of the historical origins of this distinction similar to Beatty’s discussion of the ultimate/proximate
causation distinction (Beatty 1994) would be useful, it is beyond the scope of the present paper.
31
It is important to note that this is a different line of reasoning than Mayr gives elsewhere for why ontogenetic
studies cannot contribute to evolutionary theory. Mayr often invokes the distinction between ultimate and proximate
29
not grasped their own typological predilections or the fact that contemporary evolutionary theory
is primarily concerned about variation and diversity.
Mayr both implicitly and explicitly tied typology to an underlying philosophical
essentialism and idealism. While it is true that a variety of essentialism was a barrier to
evolutionary thinking, it is not clear that typological thinking must be essentialist. Amundson
has identified the ironic consequence of associating typological thinking with idealism;
transcendental anatomists like Geoffroy become idealists and materialists simultaneously!
(Amundson 1998, 159)32 Mayr’s connection between essentialism, typology, and idealism
became the core philosophical commitments of anti-evolutionism and anti-Darwinism, both in
the past and present. But if we shift the main analytical trope from evolution/creation to
teleology/morphology, one can make better sense of the history and present challenges to the
Modern Synthesis from developmentally oriented researchers. (Amundson 1998)
Recent philosophical treatments of the notion of essence suggest that it can be salvaged
as a way of positing natural kinds without appeal to an essential microstructural essence. (Boyd
1999; Griffiths 1999) Natural kinds can be understood as homeostatic property clusters that
evolve over time or historical essences (relationally defined) with detectable counterfactual
force, where the important consideration is the role these natural kinds play in the referential
practice of scientists. Once the necessary link between typology and essentialism is severed, the
importance of typological thinking from morphological investigation becomes a live issue.
Typological and population thinking are compatible but different viewpoints on the function-
causation to reveal that the investigations by developmental biologists of proximate causes cannot provide the
ultimate causal explanation needed. (Mayr 1994a, 1994b; see also Beatty 1994)
32
When Riedl brought the decline of morphology to the attention of Ernst Mayr, Mayr responded, “Morphology is
nothing but German idealistic philosophy.” (Riedl 1983, 206)
30
form complexes that make up organisms.33 Some have even argued that it is impossible to do
morphological investigation apart from an archetypal concept. (Young 1993; see also
Dullemeijer 1974) The requisite dependence on a priori assumptions in biological investigation
makes many researchers chary of any typological notions.
The issue of typology is directly important for understanding evolutionary innovation
because the criticism that innovations are artifacts is attributed to typological thinking. (Cracraft
1990) Mayr’s original discussion attributed all saltational explanations of novelty as a residue of
typological thinking. (Mayr 1960) His gradualism in the post-Synthesis context led him to
characterize the problem of evolutionary novelty in terms of population genetics.34 Typological
research strategies have also been a part of recent criticisms of evolutionary developmental
studies of the putative phylotypic stage in vertebrates. (Richardson et al. 1997) In a theoretical
discussion of the status of developmental archetypes, Richardson et al. acknowledge that there
are some advantages to the typological approach but they are cautious about the pitfalls that are
supposedly associated with understanding types as more than artifactually selected clusters of
conserved features. (Richardson, Minelli, and Coates 1999) The desire for biological laws is
parried with the reminder that generalizations in biology are riddled with exceptions. Although
they argue for “alternatives” to typologism, their main suggestion is that typological models
33
Although Olson was groping for something like compatibility between typological and population thinking, his
attempts were basically ignored. (“…the attention of the morphologist tends to be centered upon form and involves
to some extent a typological aspect—typological in that there is some rather concrete, visual image involved.
Students with this point of view are not quite the unreconstructed villains of the field of evolution as those described
by Mayr (1959). But there is the strong tendency to think in terms of morphology as characteristic of an animal, that
there is a form representative of a species and metric characters characteristic of a genus. What often may appear to
be a purely typological view is not, in fact, based on a disregard or ignorance of population concepts and variability
but upon initial concern with stages in evolution represented by some genus or species, or even a representative of
some higher category.” (Olson 1960, 535)
34
“The problem of the emergence of evolutionary novelties then consists in having to explain how a sufficient
number of small gene mutations can be accumulated until the new structure has become sufficiently large to have
selective value.” (Mayr 1960, 357)
31
reflect the reality of variation and diversity; a compatibility thesis for population and typological
thinking aims for exactly this result.
One way for typology to reenter is through a strict distinction between pattern and
process in the history of life. (Brady 1994; Dullemeijer 1980; Rieppel 1988) Once we restrict
our attention to pattern, “[t]he basic goal of comparative anatomy is to determine regularities of
structural organization that enable a classification and understanding of the ordered diversity of
form.” (Shubin and Alberch 1986, 377) Notions such as the “tetrapod limb” can be understood
as scientific idealizations or abstractions, defined by patterns of relations that obtain among the
relevant components and processes. (Cf. Amundson 2001) In other words, the tetrapod limb is
typologically characterized by historical essences relationally defined. The study of the
morphogenesis of the tetrapod limb by Shubin and Alberch reveals that the intersection of
evolution and development is precisely where you would expect typological thinking to be
necessary.
“…this typological and static approach is not opposed to evolution or even to natural selection. …it does
not draw from evolutionary mechanisms based on environmentally defined selection and random mutation. The
quest for a general set of principles of form is legitimate if we exchange the metaphysical concept of the
Bauplan for a mechanistic one based on principles of morphogenesis and internal integration.” (Shubin and
Alberch 1986, 377)
The tetrapod limb is not an “artificial” construct but a significant suite of conserved characters in
evolution that is generated by morphological processes and results in discrete forms due to
developmental constraints. It must be understood in terms of its stable internal relations across
all tetrapods and not just with respect to the diversity of relations manifested in the population of
a particular species.35
35
“…talk of the urodele limb is not just a way of referring to the limbs of urodeles. Like the bauplan, the urodele
limb is an abstract theoretical construct that expresses shared patterns of development. (Amundson 2001, 321)
32
With respect to phenotypic plasticity, we have already noted that Schmalhausen’s work
was largely neglected in the post-Synthesis context, either for lack of awareness or assumed
similarity with Waddington’s work. But the importance of selection on a norm of reaction that is
initially environmentally induced but later genetically “hard-wired” (Waddington’s genetic
assimilation) is at the forefront of discussions of the origin of morphological innovation.
(Newman and Müller 2000) Distinctives of phenotypic evolution and norms of reaction have
also been recently discussed, emphasizing that the origin of novelties can be achieved via a
rearrangement of existing genetic architecture. (Schlichting and Pigliucci 1998) The importance
of the ecological context for ontogeny itself (outside of laboratory studies), as well as the
evolution of development, is a key part of understanding the origins of novelty. (Cf. Gilbert
2001, van der Weele 1999) West-Eberhard (1989) has explicitly argued for the importance of
phenotypic plasticity, in both behavior and morphology, as a factor in the generation of novelty.
Novel morphology can emerge across a norm of reaction through exposure to new environmental
influences and later be canalized into a stable ontogenetic outcome. These innovations might
explain the origin of higher taxonomic distinctions.
Functional morphology makes a contribution to the discussion by way of the concept of
performance. (Arnold 1983; Emerson and Arnold 1989)36 Understanding the performance of a
complex structure over its norm of reaction in its natural environment is importantly deciphered
by laboratory experimentation that goes beyond the naturally exhibited performance range. 37
Once we have disconnected typology and essentialism, we can also discuss the kinds of reaction
36
“[The] notion that when the selection acting on a trait is formally expressed as the statistical relationship between
the trait and fitness, then selection can be factored into two parts: a performance gradient representing the effect of
the trait on some aspect of performance,…and a fitness gradient representing the effect of performance on fitness.
The point of this distinction is that even when effects on fitness cannot be measured, it will often be possible to
measure effects on performance.” (Arnold 1983, 347)
37
See Ferry-Graham and Lauder 2001 for a representative discussion of the functional morphology of aquatic prey
capture in ray-finned fishes.
33
norms observed without implicitly holding that they obtain independent of environmental
fluctuation; i.e. there is no assumed “natural” state. (Sober 1994 [1980]) Species essentialism
does not reenter by the back door.
Ultimately, the most basic rationale for an inclusion of morphology in evolutionary
developmental biology when trying to understand the composition, construction, and interactions
of organisms is the desire for integrated explanations.38 Thus, the disciplinary synthesis of ‘evodevo’ and any of its theoretical synthesis by-products can be seen as a means to the end of
producing explanatory integration. (Table 1) The difficulty is deciding on what is in need of
explanation. I would argue that an organism-centered (rather than gene-centered) view of
biological investigation drives a number of advocates of evolutionary developmental biology.
Those who are motivated primarily by the explanatory power of the mechanisms of
developmental genetics will likely find the argument for the importance of morphology oddly
curious. I cannot adjudicate this deep divide in the precise nature of the explanandum but it is
critical to perceive that it makes a difference in the continuing project of synthesizing
evolutionary and developmental biology. If the explanandum is not organisms, then it is likely
that components such as functional morphology will be sidelined. (Cf. Benson 1989) Many
functional morphologists do not work on the prevalent model organisms where the genetic
architecture and ontogeny have been finely dissected. The role of research on non-model
organisms in the future is a key component of how evolutionary developmental biology will
evolve that is highlighted by the work of functional and evolutionary morphologists.
Maybe the discussion of the disciplinary synthesis of evolutionary developmental biology
is a barrier to the goal of integrated explanation. Maybe we should characterize the task of
38
“The most important benefit of an integrated approach to the evolution of development is that it produces a more
complete picture.” (Wray 2000, 126)
34
evolutionary biology as the “multidimensional analysis” of evolving lineages. (Wake and Larson
1987) A truly integrated explanatory strategy requires emphasis on functionalist and structuralist
themes (cf. Amundson 2001), and explicit attention to molecular and cell biology, population
genetics, developmental biology, ecology, and phylogenetics (inter alia). Discipline level
considerations are crucial because they involve laboratory space, funding, and other necessary
aspects of the material practice of biologists. But it should not be forgotten that disciplinary
issues of synthesizing disparate research communities might be both a help and a hindrance to
producing integrated explanations of biological phenomena.
Recent discussions of evolutionary developmental biology have begun to highlight the
significance of morphology. The tool of morphometrics was displayed at a recent symposium on
evolutionary developmental biology (Roth and Mercer 2000),39 as well as the important relation
between morphology and systematics. (Mabee 2000; cf. Arthur 1997, 71-77) Although some
discussions of evo-devo include paleontology rather than morphology as a component of the
disciplinary synthesis (e.g. Raff 2000), comparative anatomy is distinguished from paleontology
in other representations. (Wagner, Chiu, and Laubichler 2000). Brian Hall has not only
recognized the role of functional morphology (Hall 1999, 396), but he has also engaged the issue
of typology. He explicitly rejects the typological/populationist thinking dichotomy (398), and
simultaneously advocates the reality of a “phylogenetic suite of characters that typifies a taxon.”
(Hall 1997, 462)
8. Concluding Remarks
39
Roth and Mercer recognize the potential of morphometrics for bringing morphology into the discussion: “Most
exciting is the conceptual link that morphometric characterizations may be able to provide between morphology and
the genetic, developmental, and evolutionary processes and factors that influence it.” (Roth and Mercer 2000, 809)
35
“No phenomenon has ever been found in organic nature that cannot be interpreted within the framework of the
modern, synthetic theory of evolution.” (Mayr 1959)
Many biologists have expressed dissatisfaction with the “unfinished” synthesis for one or
more reasons. (E.g. Eldredge 1985) Other’s claim that the Evolutionary Synthesis was a failure,
possibly hindering progress in evolutionary biology, and thus requires an explicit dismantling.
(Antonovics 1987) Mayr’s confidence can only be maintained in the present with mental
gymnastics that induce more than mild discomfort. Most proponents of evolutionary
developmental biology express a similar dissatisfaction with the Modern Synthesis, always quick
to note that embryology was not a component. But if evolutionary innovation is a central
concept in ‘evo-devo’, and the history of the concept of innovation is bound up in morphological
study, then the exclusion of morphology from neo-Darwinism directs our attention to the nature
of the evolutionary biology that is to be synthesized with developmental biology.40 Put
differently, the synthesis of meanings for the concept of innovation in evolutionary
developmental biology directs our attention to the need for explicitly considering the role of
morphology in constructing ‘evo-devo’.
I have suggested that one controversial area of reevaluation is typology, both in its nature
and relationship to population thinking in the contemporary context, but there are other
ramifications.41 Included among these ramifications are conceptual connections between
innovation and dissociability (Raff and Raff 2000), evolvability (Kirscher and Gerhart 1998),
homology (Laubichler 2000; Müller and Newman 1999), macroevolution (Erwin 2000; Hunter
1998; Leroi 2000; Thomson 1992), model organisms (Arthur 1999), modularity (Bolker 2000;
40
“Prima facie, it appears that synthesizing developmental biology and Neo-Darwinism is a much more difficult
prospect than synthesizing developmental biology and evolutionary theory more broadly construed.” (Robert 2001,
4)
41
van der Weele points to difficulties that an integration of evolutionary and developmental biology might inherit by
utilizing Mayr’s proximate/ultimate cause distinction. (van der Weele 1999, 73-90)
36
Raff 1996), preadaptation (Bock 1959), and syn/apomorphy (Liem 1990). Equally important are
the post-synthesis disciplinary developments that were not present in the construction of the
synthesis. Cladistic systematics, and phylogenetics more generally, have been given increasing
emphasis in recent ‘evo-devo’ studies. (Arthur 1997; Mabee 2000; Raff 1996, 2000) Other
interdisciplinary links include functional morphology and paleontology (Thomason 1995).
Again, historical and philosophical questions need to be considered jointly to determine both the
present state of the synthesis, as well as the desired state, regardless of their current fit.
If we have the same concern as those at an early discussion surrounding the nature of the
new discipline of ‘evo-devo’, namely that “evolutionary developmental biology should not be
reduced to the functioning of genes” (Wake et al. 1991, 588), then considering the historical
absence of morphology can mitigate against the tendency to conceptualize the synthesis of
evolution and development in terms of developmental genetics.42 This paper has been
exploratory in nature, pointing in the direction of further philosophical analysis based on
historical exploration rather than providing a definitive conclusion. The relative absence of
morphology in the Modern Synthesis and later evolutionary theory is one thing; any necessity to
think typologically to adequately capture biological phenomena is another. It should be clear
that a philosophical analysis of the emerging synthesis of evolutionary developmental biology
requires an understanding of the historical development of the disciplines, theories, explanations,
and concepts. Any foundational problem in biology can be more adequately disentangled
through attention to the phylogenetic pathway by which it arose, providing clues to articulating
normative philosophical aims for contemporary science.
42
Novelty is not immune from this tendency as some discussions focus primarily on the co-option and recruitment
of genes. (E.g. Ganfornina and Sánchez 1999)
37
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Levels
Integration
Synthesis
Discipline
Disciplinary Integration
Disciplinary Synthesis
Theory
Theoretical Integration
Theoretical Synthesis
Concepts
Conceptual Integration
Conceptual Synthesis
Explanations
Explanatory Integration
Explanatory Synthesis
Table 1
48
Figure 1
49
Figure 2
50