AMER. ZOOL., 29:1067-1074 (1989)
Biology's "Phoenix": Historical Perspectives on the
Importance of the Organism 1
KEITH R. BENSON
Department of Medical History and Ethics, University of Washington,
Seattle, Washington 98195
SYNOPSIS. From Aristotle through the nineteenth century, biology was directed to investigating the organism. In this tradition, natural historians utilized a descriptive methodology to study the structure and function of the organism. By the end of the nineteenth
century, however, a number of factors contributed to reorient biological investigations
methodologically; that is, biologists searched for causal explanations, borrowing methods
from physics and chemistry. These methods have characterized the bulk of biological
research during the twentieth century, thereby ignoring the importance of the organism
as a whole. Several contemporary biologists have critically evaluated this situation and
have attempted to formulate biological methods that would once again consider the entire
organism as the central focus for biological investigation.
From at least the time of Aristotle, natural history, the ancestral form of modern
biology, has held the organism at its central
focus. Certainly Aristotle emphasized this
theme by insisting that the whole of the
organism was the only meaningful subject
of natural history; it was inconceivable and
even irrelevant to study but a part of the
whole structure. The Aristotelian natural
historian, as a result, adopted methods that
involved a complete descriptive natural
history of the organism being investigated.
The primary character of this method was
the Greek interpretation of history as
learning or knowing by inquiry. Essentially
nothing of a descriptive nature about
the organism under investigation should
escape the notice of the.natural historian
(Grene, 1983). But this methodological bias
changed by the twentieth century, however, when the most impressive advances
in biology, the modern version of natural
history, were accomplished by scientists
who probed nature using methods that
were designed to uncover causal explanations behind natural phenomena. Typically, this modern approach involved the
reduction of biological explanations to
principles borrowed from physics and
chemistry: to study the organism, it was
teased into its constituent parts, the phe1
From the Symposium on Is the Organism Necessary?
presented at the annual meeting of the American
Society of Zoologists, 27-30 December 1987, at New
Orleans, Louisiana.
nomena associated with these parts were
explained at the lowest level of organization and, consequently, the emphasis on
the whole of the organism gradually
became lost (Schaffner, 1969).
Unfortunately, the older tradition, with
its descriptive methods from Aristotle, and
the modern interpretation, often described
as reductionistic and mechanistic, have
been depicted as mortal adversaries and
competitors. J. H. Woodger, the major
twentieth-century advocate of the organism, popularized this notion in his 1930
article in the Quarterly Review of Biology.
In histories of biology in the dim future
there will probably be a chapter entitled
"The Struggle for Existence of the Concept of Organicism in the Early Twentieth Century," which will relate how this
concept came to be neglected on account
of the influence of Descartes, how the
metaphysics of natural science in the
Nineteenth Century so completely dazzled biologists that they never dreamed
of regarding organisms as being anything but swarms of little invisible hard
lumps in motion, and how the first
blossoming of the concept of organism
towards the end of the century was
nipped in the bud by the mismanagement of those who advocated it.
(Woodger, 1930-31)
The struggle, which David Hull described
as "more reminiscent of political polemics
and biblical exegesis than science" (Hull,
1067
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KEITH R. BENSON
1974), eventually and inexorably led to the
removal of the organism from center stage
by the twentieth century.
This change in perspective regarding the
organism has been so pervasive in the
twentieth century that the major philosophy of biology texts available at the present time, by David Hull and Michael Ruse,
do not seriously treat the concept of the
organism or any modern variant of organicism, the philosophical approach that
focuses on the whole organism (Ruse, 1973;
Hull, 1974; see also Hull, 1969). Part of
the reason for the disappearance of these
concepts from philosophy of biology is the
nineteenth- and twentieth-century association of the organism and organicism with
vitalism or other schools of thought that
sought to frame theories for the life sciences that were distinct from theories in
the physical sciences. Several more "mainstream" attempts to inject the idea of the
organism into twentieth-century biological
thought also failed to attract a wide following. Among these are numbered E. S. Russell's attempt to return to an Aristotelian
concept of holism; Woodger's complex
philosophical reconstruction for biology
based upon logical empiricism in an attempt
to steer a middle course between mechanism and vitalism a la Claude Bernard
(Woodger, 1929; for critical review see
Ruse, 1975); C. D. Broad's idea of emergent properties dependent on the level of
organization and including mechanistic
ideas; and Ludwig von Bertalanffy's general systems theory that depicted the
organism as dynamic informational processes in toto (Roll-Hansen, 1984).
But my intent is not to provide a critique
of the failures of biologists and philosophers to create a philosophy of biology that
allows scientists to examine the organism
in its integrated totality. Indeed, I am not
professionally equipped to do so. Instead,
I would like to provide several historical
comments upon the nineteenth-century
divorce of the traditional Aristotelian bond
between whole structures and their function and the subsequent demise of the
organism as a subject of biological inquiry
in the twentieth century. The most impressive impact of the split has been a meth-
odological one. As biology has adopted a
more causal approach to study vital phenomena, the organism has slowly and
benignly disappeared from center stage.
While this gradual change had become virtually completed by the mid-twentieth century, there are several current trends in
biology that appear to offer methodological approaches or techniques and rationale
that will once again encourage biologists
to focus upon the organism. I will conclude
my remarks with a few observations that
indicate such a resurrection of organismic
thinking in contemporary biology may be
occurring at the present time.
The inseparable integrity of structures
and their functions that Aristotle taught at
his Lyceum were modernized in the nineteenth century by the French baron,
Georges Cuvier. Through his teleological
arguments based upon the doctrine of final
causes, Cuvier effectively destroyed and
eliminated the Cartesian heritage of mechanistic explanations that eschewed final
cause arguments from natural history.
Arguing cogently for the uniqueness of
natural history, Cuvier stated:
There is, however, a principle peculiar
to natural history, which it uses with
advantage on many occasions; it is that
of the conditions of existence, commonly
styled final causes. As nothing can exist
without the reunion of those conditions
which render its existence possible, the
component parts of each being must be
so arranged as to render possible the
whole being, not only with regard to itself
but to its surrounding relations. (Cuvier,
1831)
In other words, to understand the structure of the organism the biologist was led,
indeed required, to understand the purpose, design, or function of the structure.
Using these ideas, Cuvier reconstructed
numerous fossil forms from the scattered
bones in the Paris Basin, thereby illustrating the utility of the final cause argument
in natural history (that is, a teleological
explanation) and providing an impressive
method for a generation of comparative
anatomists and paleontologists. Similar to
the methods of the Aristotelian tradition,
BIOLOGY'S "PHOENIX"
Cuvier's method was descriptive. Armed
with final cause arguments, the natural historian became the interpreter of the design
that was observed in the natural world.
The seminal ideas of Cuvier dominated
natural history until 1859, not only in
France but also in England. English natural
theology was consistent with Cuvier's
purposeful nature; the natural world was
designed by a beneficent creator who produced everything in the natural world with
a purpose which could be observed by the
natural historian. The philosopher William Whewell codified the approach by
adopting the Cuvierian tradition and
claiming that the concept of teleology was
an explanatory tool unique to the life sciences; in fact, it marked the essential distinction between the physical sciences and
natural history (Whewell, 1837). Natural
historians were required to adopt methods
of research that examined the natural world
for evidences of design. But these influential ideas had an inherent limitation for
they lacked the orientation that was eventually to lead to the displacement of the
organism's centrality in biological investigations. For Cuvier's and Whewell's definition of function was not physiological;
rather, both referred to function as the
purpose of the structure or its designed
utility. This interpretation did not demand
any causal explanation of phenomena
beyond the observable design; indeed, any
mechanistic explanation of function did not
make sense.
During this same time, beginning in the
1830s, a number of German physiologists,
many trained by Johannes Muller, developed a parallel but distinct tradition
investigating animal function: these physiologists interpreted the function of an
organism in terms of physico-chemical
explanations and, at the same time, selfconsciously avoided any interpretations
that contained references to teleology or
design in nature. Emil du Bois-Reymond
and Hermann Helmholtz, two of the major
spokesmen of this tradition, insisted that
physical and chemical rigor, accomplished
through experimentation, were the desired
goals of physiology. Methodologically, the
German physiologists wanted to examine
1069
isolated physiological phenomena with the
exact tools of physics and chemistry in an
attempt to remove any metaphysical
notions from physiology and replace these
notions with the precise physical laws that
regulated vital function.
Several English physiologists and natural
historians, concerned and dissatisfied with
Whewell's separation of the life sciences
and the physical sciences, began seriously
to question the utility and desirability of
framing a philosophy of science that used
teleology as an "artificial" device to distinguish natural history from the rest of the
sciences. Among these "Young Turks" was
Charles Darwin. Not surprisingly, therefore, Darwin's major opus, On the Origin of
Species, contained several elements which
departed from the teleological viewpoint
and sought to place natural history on a
footing that included both structural considerations and functional investigations.
According to Darwin's new theory, all
organisms shared a common ancestry. This
historical commonalty extended to both
structural, or morphological, and functional, or physiological, considerations
(Darwin, 1859). Morphologists sought
ancestral forms that were universal; physiologists searched for unifying functional
processes. Ernst Haeckel, the infamous
"Darwin of Germany," even attempted a
premature fusion of what T. H. Huxley
referred to as the twin aims of biology
(physiology and morphology) by claiming
that the biogenetic law, "ontogeny recapitulates phytogeny," was true because
phylogeny provided the mechanical cause,
in a physiological sense, for the forms produced in ontogeny. Haeckel's problem, of
course, was that his lofty goals for an evolutionary biology could not be placed into
action without resorting to wholesale speculation instead of careful experimental
work.
Haeckel's attempt notwithstanding, the
Darwinian rapprochement between morphology and physiology, which emphasized the historical nature of the organism
whether it was considered in a morphological sense or in a physiological sense, did
not last into the twentieth century. Instead,
a variety of factors led many prominent
1070
KEITH R. BENSON
biologists, especially in the United States,
eventually to abandon the whole organism
and return to a Helmholtzian treatment
emphasizing studies of the function of parts
of the organism, understood in terms of
physico-chemical events. In the main, all
of the factors involved the way in which
biology was done. In other words, the loss
of the organism as the focal point of biological investigation involved changing
methods in biology. I will mention four of
these factors which acted in concert at the
turn-of-the-century to reduce questions of
form and function to physiological explanations, thereby diminishing the importance of the organism as a whole.
The first factor was the growing skepticism over the efficacy of natural selection.
While evolution theory enjoyed widespread acceptance by the 1880s, natural
selection fared less well. What was natural
selection? Did it exist in nature? Was it a
mechanical principle? Was it creative? All
of these questions plagued Darwin's central idea with enough force that natural
selection no longer guided biological investigations by the century's end. True, part
of the turn from natural selection was exacerbated by the speculative excesses of
Haeckel and others who sought ad hoc
alternatives to deal with its problems. Many
young biologists, for example, soon tired
of explanations that lacked any evidence
except from the imagination. But another
major reason was that by this same time
biology had begun to frame successfully a
number of methodological approaches that
could deal with ontogenetic events without
recourse to phylogenetic speculation.
Especially in the United States, studies in
the 1890s emphasized the descriptive
record of development, often without any
reference to the mechanism for evolutionary change.
A second factor was the increasing
importance of instrumental techniques,
especially new microscopical procedures in
embryology, and experimental methods in
biology. In fact, refined microscopes and
new techniques to prepare embryological
specimens led to early criticism of Haeckel's gastraea-theorie and its related ideas of
the deterministic germ layers. By the early
1880s, W. K. Brooks and C. O. Whitman
encouraged their students to examine early
cell developments in their attempt to
understand development without hypothetical speculations. Both mentors, who
were responsible for the education of
essentially all America's leading biologists
at the time, did not turn away from the
centrality of the organism in their own
research nor did they advocate such a redirection to their students. In fact, as more
evidence gathered to indicate the futility
of including speculative phylogenetic considerations in ontogeny, Whitman and
Brooks still insisted that the proper focus
of biological research was on the level of
the organism. Not surprisingly, the
American cytological community, which
emerged from the tutelage of Brooks and
Whitman, was identified by its careful celllineage studies in which embryological
events were painstakingly described from
early fertilization events through development. But these same instrumental and
experimental techniques that characterized the new American research tradition
in cytology also contained methodological
elements that directed the researchers from
the organism as a whole. A major thrust
of embryology became the search for morphological structures that were causal factors in developmental phenomena. Examinations of these structures soon led many
researchers to focus upon the parts of
organisms instead of the entire organism.
A related factor, the third to be considered, was the continued success of physiology in examining natural phenomena in
terms of causal explanations that were
amenable to experimental techniques.
Beginning with the German physiologists
and continuing with Michael Foster's laboratory at Cambridge, H. Newell Martin's
experimental studies of the action of the
heart at Johns Hopkins, and Jacques Loeb's
numerous studies of animal behavior, parthenogenesis, and cell membrane phenomena, physiology provided a clear demonstration of how the methods borrowed
from physics and chemistry could be
applied—with success—to phenomena that
had previously been described in vitalistic
terms. Furthermore, many of the physiol-
BIOLOGY'S "PHOENIX"
ogists (especially Loeb) disparaged the older
morphological tradition in biology that
speculated on the formation of organic
structure. Several of these physiologists
specifically encouraged cytologists and
others to adopt a more causal approach.
Entwicklungsmechanik, or developmental
mechanics, while it has been overworked
by historians of late, is an example of a
causal approach adopted by Wilhelm Roux
and applied to questions of development.
The overt emphasis of this tradition was
function; and function was studied in terms
of the parts of organisms, a much different
orientation than the functional concept of
Cuvier (Rainger et al., 1988).
But despite the increasing success in
dealing with physiological problems or
examining other biological questions with
experimental and instrumental approaches,
many leading biologists were not willing or
anxious to abandon the organism completely. E. B. Wilson, one of America's
foremost cytologists and an important contributor to the formation of the chromosome theory of development, cautioned the
embryological community in the 1906 edition of The Cell in Development and Inheri-
tance, by drawing an interesting analogy
between biology and the physical sciences.
But despite all our theories we no more
know how the organization of the germcell involves the properties of the adult
body than we know how the properties
of hydrogen and oxygen involve those
of water. So long as the chemist and physicist are unable to solve so simple a problem of physical causality as this, the
embryologist may well be content to
reserve his judgment on a problem a
hundred-fold more complex. (Wilson,
1906)
Wilson's colleague, E. G. Conklin, writing
six years later on the "extrinsic and intrinsic factors" in cellular differentiation,
thought that the new view of the "chromosomes as the sole 'bearers of heredity'
. . . [was] too narrow [an] outlook on the
activities of the cell as a whole. It seems to
me incredible that this most general of all
cell functions . . . should be the property
1071
of only a single cell constituent—the chromosomes (Conklin, 1912).
Despite the urgings of Wilson and Conklin for moderation in adopting causal
explanations based on physico-chemical
mechanisms of parts of the organism, T.
H. Morgan's chromosome theory was a
fourth factor that eventually lured the
majority of biologists from considering the
whole of the organism as of central importance. In 1915, Morgan's Mechanism of
Mendelian Heredity was published; now all
the essential functional considerations
could be potentially understood by the
physiological behavior of a structure. All
structural considerations were now understood not from the organism down, but on
the basis of the operation of the genes on
the chromosomes. Eventually, biologists
like Wilson who maintained an organismic
perspective began to entertain the views of
physiologists. In his intriguing book The
Physical Basis of Life (1923), Wilson stated,
the study of protoplasm and the cell may
be destined to pass more and more into
the hands of the physiologist, the physicist and the chemist; and certainly the
rising tide of cell-research in these directions is of good augury for the future
experimental analysis of vital phenomena. (Wilson, 1923)
Later in the same work, he compared the
chromosome theory in biology to the
atomic theory in chemistry and physics.
Still, however, Wilson claimed that
"genetics . . . has of late made remarkable
advances toward the study of the nuclear
organization but leaves unsolved the problem of the 'organism as a whole.' " Nevertheless, he maintained his conviction that
the mechanical tradition in physiology was
most promising for biological investigation.
I do not in the least mean by this that
our faith in mechanistic methods and
conceptions is shaken. It is by following
precisely these methods and conceptions
that observation and experiment are
every day enlarging our knowledge. . . .
(Wilson, 1923)
Morgan, perhaps to no one's surprise, was
1072
KEITH R. BENSON
equally enthusiastic and, in fact, adamant
to adopt the new approach. In his wellknown book Embryology and Genetics (1934),
he noted
the idea that embryology could be placed
on an experimental basis was especially
attractive to those who were familiar with
the great advances that the experimental
method in chemistry and physics had
brought about. [The greatest need is to]
try to discover, despite the amount of
time and labor involved, how far a
knowledge of the chemical and physical
changes taking place in the egg will carry
us toward an understanding of the developmental processes. (Morgan, 1934).
Biology in the twentieth century has witnessed the continued extension of Morgan's bias and has carried the "experimental method in chemistry and physics" deep
into biological phenomena. A few biologists in the 1930s and 1940s paid "lip-service" to organismic interpretations in biology, including F. R. Lillie, Ross Harrison,
E. E. Just, and, continuing into the present
time, Barbara McClintock. Additionally,
Ernst Mayr and other systematists maintained research programs that necessarily
involved investigations of the organism. But
mainstream and "cutting-edge" biology
continued to examine parts of organisms,
isolated systems, biochemical pathways, and
to devise and test biological models. The
invasion of biology by chemists and physicists in the 1930s and 1940s, including
the ruminations of Erwin Schroedinger and
the work of Max Delbruck, influenced the
methodological commitment to the study
of physicochemical processes of parts of
organisms rather than examination of the
parts in their organismal context. This
approach bore substantial and luxuriant
fruit. Most notably, James Watson and
Francis Crick adopted this method in their
molecular research to develop a physical
model for DNA. In a classic example of
understatement given the success of the
work of Watson and Crick, they wrote in
their 1953 paper in Nature that "it has not
escaped our notice that the specific pairing
we have postulated immediately suggests a
possible copying mechanism for the genetic
material" (Watson and Crick, 1953). The
next two decades only underscored the
modesty of their claims for the model and
its attendant methods from physics and
chemistry.
The continued success of the physicochemical approach in biology effectively
drowned any cries to return to biology
based on the organism. In fact, the philosopher Ernst Nagel wrote in a 1951 paper
entitled "Mechanistic Explanation and
Organismic Biology,"
The central thesis of this paper is that
none of the arguments advanced by
organismic biologists establish the inherent impossibility of physico-chemical
explanation of vital processes. (Nagel,
1951)
In other words, all conceivable organismic
alternatives could be reduced to molecules in motion. But despite more than
eight decades of success, there is a reemergence of biologists who maintain the
centrality of the organism and desire the
inclusion of organismic thinking in modern biology. Allow me to provide a few
examples.
Some of the most cogent arguments for
reexamining the role of the organism in
modern biology come from evolutionary
biologists. David Wake, Gerhard Roth, and
Marvalee Wake provided such an argument in the Journal of Theoretical Biology in
1983. In this article, they stated that evolutionary biology lacks sufficient explanatory theory, and that the field would benefit from the introduction of a formulation
from organismal biology which views the
organism as a self-produced and self-maintained (autopoetic) system, which changes
or stabilizes itself with respect to internal
dynamics (Wake et al., 1983). Influencing
Wake and his colleagues is the work of
Francisco Varela, H. R. Maturana, and R.
Uribe, which has been critical of the tendency of modern biology to examine isolated phenomena. Instead, Varela et al.
insist that biology should focus upon the
organization of living beings (Varela et al.,
1974). They claim that all isolated biological phenomena are component parts that
are secondary to the establishment of the
1073
BIOLOGY'S "PHOENIX"
unitary organization of a living system. In
fact, the properties of the component parts
of a living system do not determine its
properties as a unity; the properties of a
self-maintaining system are determined by
the unitary organization (Varela, 1979).
Another exciting area in biology that
begins and ends its discussion of living phenomena with the organism is biomechanics. While investigators in this field do not
eschew physical and chemical laws and certainly examine with care the constituent
parts of organisms, their main goal is to
examine how the whole of the organism
operates. Mimi Koehl provided an apt
description of the objectives of biomechanics in the American Zoologist (1984).
We who use an engineering approach in
morphological studies are accused of
thinking that all organisms are beautifully designed for the functions they perform. In fact, biomechanics, like physiology, is just a way of trying to unravel
how organisms work. I hope to illustrate
. . . that biomechanics is a useful experimental tool that enables morphologists
to study in a quantitative and predictive
way how the performance of organisms
depends on their structure. (Koehl, 1984)
ism demand or even suggest that molecular
considerations or physico-chemical explanations are unwarranted. Indeed, much of
our understanding of the organism is based
on these models of research. However, it
may be time to reexamine the organism in
light of what we now know to frame a more
sophisticated and satisfying organismic
biology that leaves behind such loaded
terms as "vitalism," "reductionism," and
"mechanism." This will not be an easy task.
Borrowing from Woodger, who cribbed
from G. K. Chesterton (in his remarks on
Christianity), "[the organism] has not been
tried and found wanting; it has been found
difficult and not tried" (Woodger, 193031). Perhaps in the near future exciting
work will reveal that biology's phoenix, the
organism, is beginning to reemerge from
the ashes of its death and burning in the
first half of the twentieth century into its
full plumage by this century's end.
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