AMER. ZOOL., 25:689-694 (1985)
Vertebrate Morphology: Tale of a Phoenix1
CARL GANS
Division of Biological Sciences, The University of Michigan,
Ann Arbor, Michigan 48109-1048
SYNOPSIS. The last 25 years have seen a renaissance in the use of structural principles
in biological study. Analytical methods have been refined and new concepts introduced.
Systematic applications have imposed new demands because cladistic methods have emphasized the need for correct interpretations of individual characters. Developmental
approaches now permit association of characters; however, newly described genetic mechanisms may pose questions about structural criteria for homology. Structural characters
prove significant, both in evaluation of the possible roles of morphological characteristics
and in establishing the reality and level of adaptation. Morphology, ever more, is an area
of active researches promising significant results.
Structure is the first thing that we notice
whenever looking at organisms. Hence, it
should not be surprising that morphology
is an old science. Aristotle, El Kasvini and
Cuvier were first of all morphologists, that
is they used morphological data in diverse
ways in their studies of natural history,
paleontology and physiology. Given this
long and renowned history covering millennia, one may well question the value of
a review concerning only the last quarter
century. Indeed, one may question the
worth of any discussion of this "antique"
and presumably now somnolent field. Has
there been significant progress and if so
did the Division of Vertebrate Morphology
of the ASZ contribute to it? I hope to be
able to show that a change indeed occurred,
that it was significant and that our Division,
our Society, and our Journal have all played
significant roles.
Slightly more than a quarter of a century
ago, a group of far-sighted scholars, including Alfred Romer, Perry Gilbert, D. Dwight
Davis, and Bobb Schaeffer, decided that
vertebrate morphology needed a forum
and a platform. Individual students of morphology were making progress, but in isolation. The wheel kept being reinvented.
Two things were needed: An opportunity
to talk and to exchange ideas and, even
more, a place from which viewpoints could
be expressed and communicated to others.
Professor Romer persuaded the American
Society of Zoologists to provide such a
forum by accepting a Division of Vertebrate Morphology. The first symposium of
the Division graced the first issue of the
American Zoologist and sixteen more symposia have followed.
The aims of founding the section had
been to improve the image of morphology
among the zoological community, and, as
important, to facilitate our own education
by generating conversations and exchanging ideas. It was necessary to engage in an
educational effort directed to other biologists because many of them perceived
morphology as a field in which research
was becalmed in the doldrums, all possibly
interesting discoveries having been made
decades, perhaps centuries ago. Vertebrate morphology had been relegated to
the preprofessional undergraduate curriculum, and presumably anybody could provide instruction in the discipline; morphologists were not needed for this. It was
often taught by colleagues whose primary
research interest lay in paleontology,
behavior, or invertebrate zoology, even by
some who did not then, and had never carried out research of their own. The view
sometimes was that instruction in vertebrate morphology represented merely a
service to the premedical community, a
"proto-anatomy" that the college had to
offer but one which required minimal
training and commitment of its instructors.
' Plenary Lecture for the Division of Vertebrate
Morphology presented at the Annual Meeting of the
American Society of Zoologists, 27-30 December
1984, at Denver, Colorado.
The causes of this situation had been
partly external and partly inherent in the
field. The latter was exemplified by the
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advice, given to me during my postdoctoral
days, not to call myself a morphologist
because morphology represented a losing
proposition. External to the field was the
pressure due to the competition of new
research areas, of exciting discoveries leading to an exponential growth of biological
information, techniques, and the capacity
for asking "new" questions. This generated a conflict between the annually
increasing corpus of facts and hypotheses
that students "needed to know" and the
fixed length of time available for teaching
a biological curriculum.
However, morphology also incorporated an inherent set of faults. Among these
was the anatomical preoccupation with
typology and with morphological events
observed in individual organisms, the lack
of rigor in modern comparison, the lack of
concensus regarding the nature of major
questions and the repetition of data from
textbook to textbook. These internal faults
often reflected the lack of a sound theoretical basis. There was no agreement about
what needed doing, indeed, there existed
little conceptual framework into which
morphological data might usefully be
placed. This led to preoccupation with
detail and a lack of basis for making value
judgments, reflecting the absence of an
order of priority for particular morphological investigations.
Perhaps the most important change that
occurred in morphological research was the
realization that more was needed than mere
description. Elegant characterization of
structure was a beginning, so that competence of technique and presentation
remained essential. However, the understanding of structure demanded not just a
description of topography and composition, but information about formative
influences, an answer to the question why
structures have a particular geometry and
chemistry. Most important in fostering this
approach has been the rediscovery in the
process-oriented sciences that structure
places significant constraints on process.
For instance, it is clear that the physiology
of muscular contraction would still remain
mysterious today, had it not been for electron microscopic observations of the struc-
ture of the overlap and cross-bridging of
actin and myosin filaments.
The separation of structural units into
their components and the reassembly of
the components to explain the properties
of organs have contributed significantly to
our understanding of structure. Important
in fostering this successful achievement
during the past quarter century has been
the exponential increase of techniques and
tools. What once took years to design, build
and apply is now available "off the shelf."
Every issue of our journals provides new
examples of the application of old tools in
new ways and of the development of new
ones. Our meetings, in bringing morphologists together, result not only in interchange of ideas, but accelerate the transition from a situation where a technique is
used in but one laboratory to its widespread employment. Conversations in
which there is an exchange of ideas have
proved to be critical to the success of our
Division.
In short, morphology is again a vital
component in most areas of vertebrate
study. This is true not only within the
American Society of Zoologists, but
throughout biology; indeed, the study of
morphology has become important not only
for the study of vertebrates but also for
that of invertebrates, plants and even subcellular entities.
Modern morphology derives benefit
from, and contributes to, three viewpoints:
1) phylogeny, 2) developmental biology and
3) functional influences. I propose to treat
these areas by reviewing emergent principles rather than by citing the key papers
of the last quarter century.
PHYLOGENY
Phylogeny implies the recognition of
organismic diversity and a concern with
organismic relationship. In linking Recent
animals and the occasional fossil, attempts
are made not just to classify them but to
do so in a natural (i.e., evolutionary) framework. Recently, some of the many, often
more-or-less intuitive, previous practices
have been codified into a methodology
commonly referred to as cladistics. Signif-
VERTEBRATE MORPHOLOGY
icant in this approach is the division of phenotypic features into those that also characterized those organisms from which
members of a radiation derived and those
that were presumably derived within the
new radiation. The importance of this
approach to morphology is twofold. First,
the reliance on individual phenotypic characters, rather than on the overall similarity
of a set, has placed a premium on the accuracy of the morphological data used to generate phylogenies. Secondly, phylogenies
prove to be fundamental for any acceptable pattern of morphological description.
Most important for an understanding of
phylogeny must be the a priori recognition
that variation may affect all characters of
all organisms. The shared-derived aspects
that are diagnostic for a particular radiation can only be recognized ex post facto by
reviewing the species comprising a radiation; they cannot be determined a priori by
inspection of individual specimens. Hence,
comparison becomes essential and one
needs to examine and quantify the conditions appearing in all members (or as many
as possible) of the radiation of interest.
It is no longer acceptable to assume that
particular species are "typical" and present
an overall state characteristic for a particular assemblage. This invalidates the popular didactic procedure, ascribed to T. H.
Huxley, among others, of using certain
species of a class or phylum as "types." The
idea that Paramecium caudatum serves as a
prototype for ciliate protozoans, Lumbricus
terrestris as a prototype for annelids, and
Rana pipiens as a prototype for the amphibians is most misleading whenever taken
beyond basic education.
Reconsideration of such usage should
remind us that single characters often provide misleading or confusing taxonomic
clues and should not be randomly assembled into morphological series. Only within
single lineages will the "intermediate"
states, observed in the Recent, be likely to
model the "intermediates" that have
occurred in history. Hence, discussion of
the transformation of one character without consideration of adjacent ones, in other
words ignoring the systematic basis of the
sequence, incorporates major risk of error.
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Consequently, morphological analysis has
to proceed in a taxonomic framework, and
the animals to be compared must be
selected with phylogeny in mind. Many systems need to be described in multiple
species before some level of certainty may
be achieved.
The converse of this is that the recognition of states of morphological similarity
(i.e., whether the observed similarity represents homoplasy, homology, or the various degrees of analogy) requires more
detailed morphological analysis than is
often accorded it. Use must be made of the
tools and methods of several (traditionally
non-morphological) disciplines; morphometry, electron microscopy, mapping of
cells, histochemistry and electron probe
approaches may have to be applied. Mechanisms of morphogenesis and pattern formation in development must be considered. Gestalt impressions of structure,
being unlikely to be adequate themselves,
are likely to lead to inadequate definition
of phenotypic states and will inevitably
generate inadequate phylogenies.
Analysis of character states (establishing
whether characteristics defined are "good")
again demands not only an appropriate
conceptual basis but also the skills and
meticulous attention to significant detail
for which morphology has long been
known. Test and confirmation of morphological states require that their anatomy be
checked on multiple specimens. More than
in the past, we have to recognize that not
just the mean characteristic but the variants and extremes of the range represent
important data. Variability of structure is
a defining taxonomic character, whatever
its level, so that careful description remains
essential. However, as the aims of description have changed and diversified, the
needs have become more demanding. For
instance, documentation for systematic
analysis is not an end in itself, but must be
couched in terms that permit easy comparison of the assembled data with those
likely to be needed for additional species
and groups. In short, descriptive elegance
is insufficient by itself; we must keep the
"customer" in mind in characterizing
structure.
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CARL GANS
DEVELOPMENT
Development, which is, in part, a
descriptor for ontogeny, is concerned with
the processes by which structures are generated. It is generally regarded as a discipline of its own. The field is represented
by a separate Division of our Society and,
indeed, of other societies. However, besides
representing an independent approach,
evidence about ontogeny represents part
of the traditional test for the kind of similarity which we refer to as homology.
Whereas the developmental path has always
been a test for similarity, recent emphasis
has led to its study in many more species
and to a search for the meaning of slight
differences in developmental patterns.
Initially ontogeny was viewed as a gradual transition, for example, of ovum to
mesoderm to somite to vertebra. The gradually changing developmental sequence was
assumed to reflect a process inherent to a
particular group of organisms and to provide the touchstone for assessing the characteristics. An additional implication was
that the similarity, seen whenever stages
among species were shared, implied commonality of descent. The later in ontogeny
the divergence appeared among embryos,
the closer the posited phylogenetic relationship.
However, it has long been known (though
often ignored) that the multiple structures
of an individual species may differ in their
rates of unfolding. Recently concepts such
as heterochrony, neoteny and paedogenesis which refer to this differential development have attracted renewed interest.
Reference is also being made to shifts in
developmental rates, and changes that may
involve addition and loss (expression or
non-expression of stages). In short, even
though the development of an organism
through a sequence characterized by the
formation and genesis of the major germ
layers represents an important and powerful descriptive tool, we have begun to
recognize that the components of organisms do not march in lock-step to a germlayer drum. Documentation of diversity in
some developmental aspects and commonality (or constancy) in others led to new
views on gastrulation and other developmental aspects. New techniques, such as
isotope and chemical labelling and transplantation using embryos of species with
cells that bear natural markers, have
allowed us to test assumptions that have
critical implications for understanding
structural and phylogenetic patterns.
Two other aspects of development are
relevant to the correlation of genetical and
morphological distance. We know that relatively minor changes early in development may have profound effects on the
phenotype. Hence morphological change
only proceeds at rates that need not correlate strictly with rates of genetical (mutational) change. More important for our
analyses is that such correlations may differ
for the major subgroups of vertebrates and
perhaps for the tissue types upon which the
comparisons are founded.
All of these aspects clearly extend beyond
the tools and concepts of morphology itself;
they reflect the usage of data from molecular genetics and experimental embryology. What must be of concern to the morphologist and becomes ever more
important, is the question whether development indeed involves a "gradual unrolling" or whether the process involves only
a misleading impression of continuity.
There is evidence that both genetic
instructions and developmental processes
are organized into patterns of subroutines.
Those subroutines that control developmental stages, whether early, intermediate
or late, may be replaced or their expression
may be altered. Under such circumstances,
the architecture of the final product (process, phenotype) is maintained. (For
instance, intercalation of the mammalian
morula does not modify the later similarity
of their developmental processes to those
of birds.) Should such observations prove
to have generality, they would have profound implications, not only for morphology. The implication is that equivalent
structural geometry and perhaps equivalent biochemical composition of organelles
can be produced by different sets of genetic
instructions, perhaps even for whole
organisms or for particular aspects thereof.
If this is so, we will need to reconsider the
VERTEBRATE MORPHOLOGY
basis upon which statements regarding
homology may be made; even more, it
should cause us to question recognition of
shared-derived states and consequently our
ability to construct phylogenies. Certainly,
it would force us to re-examine some of
the fundamental assumptions of morphological change.
In short, data on developmental processes have a profound bearing on the
interpretation of morphological data.
Indeed, our morphological problems and
approaches may help those studying development to frame their questions. Furthermore, we should not be surprised to find
profound convergence among the discoveries of developmental biology and of many
branches of morphology.
FUNCTION
Structure, whether expressed as topography or chemistry, permits process. The
nature of the relation between structure
and function remains an important question. Indeed, how do they affect each other?
A first conclusion derives from the observation that any phenotypic aspect likely
permits multiple processes. It is clearly
impossible to derive the process proceeding in a particular organism from mere
examination of its structure, a problem that
plagues the reconstruction of the biology
of fossils. Even in the consideration of populations rather than individuals, it is necessary to come to terms with the observation that animal constructions may be
excessive; at any moment, they may permit
more than the minimal current demands
of the environment. Hence, worthwhile
correlation can only be made if both process and structure are subject to observation and measurement.
Over the last twenty-five years, we have
observed the development of literally dozens of new and increasingly facile techniques for analyzing and defining the function of structures: important physiological
approaches to the central nervous system,
cinefluoroscopy, mechanical and chemical
sensors, force plates and electromyography. Furthermore, many studies have
shown that measurement of routinely
observed motions may not always be
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enough. We must establish whether the
normally unused capacity of the system is
important. Thus, adaptation may produce
reduced cost of metabolic maintenance, or
increased peak locomotor effectiveness;
indeed it may provide combinations of both
of these for a single species. Hence, it is
useful to plan manipulation and test of the
phenotype in order to establish its absolute
capacity and not just the level of its current
utilization.
Most of all, the experience of the past
twenty-five years continues to make it clear
that the functional capacity of organisms
reflects many previously unsuspected roles
(functional aspects viewed by selectkn).
Indeed, the rate of discovery of the roles
which structures serve seems to have
increased. This confirms yet again that the
diversity of processes utilized by organisms
is sufficient to overtax the predictive capacity of the human mind. Many roles are only
disclosed whenever organisms are studied
in a field setting, i.e., observed while they
are operating under circumstances for
which the roles appear to have been
selected. Repeatedly, field observations
indicate that animals cannot afford onefunction/one-structure designs. It is the
rule rather than the exception that each
role will utilize multiple structures and that
each structure inevitably supports multiple
roles.
Recently, we have seen superficially
plausible arguments, attacking the reality
of adaptation. Even some colleagues, for
whose work adaptationist data have and
continue to be central, now pontificate
against the adaptationist "programme."
Most such arguments address the often
simplistic, short-hand overstatements in the
popular and didactic literature. They refer
to cases in which the fit of structure to role
is assumed to be poor and stress situations
in which alternative hypotheses were omitted. However, neither the possibility of
alternatives nor imperfect matching of
structure and role represent disproof of
adaptation.
We should not be surprised to find that
no structure is perfect and that few structures are optimized to any particular role.
Indeed, it is the obverse that should cause
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CARL GANS
surprise, namely the observation that many
roles are so pervasive that their influence
seems very obvious. It is commonplace to
see different animals exhibit similar
responses to function, even if nonhomologous structures are involved, seemingly
independent of the genetic and developmental bases of the phenotypic aspect. This
observation has been important for many
advances in physiology. It permits studies
of the correlates of function with but limited concern with homology. Hence, I consider it moot and unnecessary to have to
document that structure and function are
correlated. However, test of the closeness
of the match and establishment of the basis
for observed differences in the degree of
matching remain important tasks. In short,
how close is the function-structure correlation, the match between the phenotypic
and functional surfaces, and what is the
basis of the observed differences in congruence?
Any attempt at such matching encounters the recent resurrection of arguments
concerning the significance of constraints,
be they developmental, ecological, physiological, functional or genetic. Constraint
is posited whenever the response to selection for one aspect is limited by the effect
of another. Clearly, constraints must affect
most systems and there is little merit to
arguments about their reality. The important issue is not the reality of their existence, but the determination of the importance of particular constraints in the
specific case being studied. Thus, the number and arrangement of salamander or frog
tarsals must reflect phylogeny, ontogeny
and function (in turn involving aspects, such
as habitat and size of the animal).
CONCLUSIONS
Over the last quarter century, morphologists have become richer in tools, richer
in the availability of animals and richer in
innovativeness and diversity of concepts
and approaches. For all attributes of structure we have increased and/or broadened
the bases on which we may make comparisons. Although they have been treated
independently above, phylogeny, devel-
opment and function are all likely to exert
influence on every attribute of the phenotype. Hence, any attempt to understand
structure must consider all of them in parallel. Myopic restriction to one or another
subset limits the robustness of answers.
This does not mean that every technique
has to be applied in every laboratory. It
does imply that morphologists must be cognizant as to what is happening in many
areas. They must keep in mind the broad
range of potential questions and the broad
range of available tools. We are trying to
study natural phenomena and we must
allow any specific phenomenon to teach us
about the tools that need to be applied in
a particular context. Sometimes we may
wish to stimulate colleagues into providing
answers to important subsets of the questions we generate. Sometimes we may ask
them to train us or permit us to carry out
ancillary studies as visitors to their laboratories. Limitation of morphological
approaches only to the techniques learned
decades before at somebody's knee is no
longer an acceptable approach.
I hope that this brief review has shown
that the study of structure is far from staid.
Morphology is bubbling. Recent active offshoots include biomechanics, neuroscience, bioengineering and parts of sports
medicine. We have seen and continue to
see that morphological principles and data
are critical to an understanding of physiology, ecology, cytology and evolution.
Clearly, the founders of the Division of
Vertebrate Morphology put their money
on the right horse, as morphology has
remained the key to the study of biology.
The phoenix may be an incomplete metaphor. Indeed, it was not morphology, but
only its reputation, that had to rise from
the ashes.
ACKNOWLEDGMENTS
I thank the officers of the Division of
Vertebrate Morphology for inviting me to
present this lecture and D. Carrier, P. F.
A. Maderson and P. Pridmore for multiple
comments on versions of this manuscript.
The presentation was supported by NSF
DEB 8121229.