Mae-Wan Ho - Biology Department, Open University
Walton Hall, Milton Keynes, MK7 6AA, U.K.
Comparative Psychology, a Handbook, (G. Greenberg and M.
M. Haraway, eds.), pp. 107-119, Garland Publishing, 1998.
The following description of evolution concentrates on an approach that
most connects with comparative psychology, and therefore differs from
standard accounts, which readers may like to consult for a more general
picture. The entry in Encyclopedia Brittanica written by Sewell
Wright (1965) is especially commendable. It is thought-provoking, balanced
and comprehensive, running well over 12 pages of closely printed text. The
present account is much more limited in scope, and is mainly concerned to
bring out those areas of convergence between contemporary evolutionary
theories and comparative psychology that may be fruitfully explored in
Lamarck, Darwin and the neo-Darwinian Synthesis
Evolution refers to the natural (as opposed to supernatural) origin and
transformation of the living inhabitants of the planet earth throughout
its geological history to the present day. Many have speculated on
evolution since the time of the Greeks. The ideas which have come down to
us, however, originate in the European Enlightenment. This period saw the
beginning of Newtonian mechanics, mathematics and other modern scientific
developments, including John Ray's species concept and C. Linnaeus' system
for classifying organisms. The power of rational thought in science to
explain the material universe presented a deep challenge to received
wisdom, especially the biblical account of creation according to the
Christian Church. Evolution by natural processes - as opposed to special
creation by God - was already on the mind of most educated people.
Linnaeus came to accept a limited transformation of species later in his
life; other prominent figures who wrote on the possibility of evolution
include the naturalist, G.L. Buffon and Charles Darwin's grandfather,
The first comprehensive theory of evolution is due to Jean
Baptiste de Lamarck (1809) who was very much a product of the
Enlightenment, both in his determination to offer a naturalistic
explanation of evolution and in his systems approach. Thus, he dealt at
length with physics, chemistry and geology before embarking on presenting
evidence that biological evolution has occurred. He also suggested a
mechanism of evolution, whereby new species could arise through changes in
the relationship between the organism and its environment in the pursuance
of its basic needs, which produce new modifications in its
characteristics that become inherited after many successive generations.
Lamarck's theory was widely misrepresented to be merely "the
inheritance of acquired characters", or caricatured as changes
resulting from the "wish" fulfillment of the organism. Half a
century later, Charles Darwin was to include a number of Lamarck's ideas
in his own theory of evolution by natural selection. The theories of
evolution and heredity are closely intertwined in their historical
development. Just as evolutionists needed a theory of heredity, so plant
breeders in the eighteenth century who inspired Mendel's discovery of
genetics were motivated by the question as to whether new species could
evolve from existing ones. In accounting for change or transformation, it
is also necessary to locate where constancy or stability resides.
Darwin's (1859) theory of evolution by natural selection states that,
given the organisms' capability to reproduce more of their numbers than
the environment can support, and there are variations that can be
inherited, then, within a population, individuals with the more favourable
variations would survive to reproduce their kind at the expense of those
with less favourable variations. The ensuing competition and "struggle
for life" results in the "survival of the fittest", so that
the species will become better adapted to its environment. And if the
environment itself changes in time there will be a gradual but definite "transmutation"
of species. Thus, nature effectively 'selects' the fittest in the same way
that artifical selection practised by plant and animal breeders ensures
that the best, or the most desirable characters are bred or preserved. In
both cases, new varieties are created after some generations.
In addition to natural selection, Darwin invoked the effects of
use and disuse, and the inheritance of acquired characters in the
transmutation of species. It is clear, however, that those Lamarckian
ideas do not fit into the theory of natural selection, and Darwin's
followers all regard the lack of a theory of heredity and variation as the
weakest link in the argument for natural selection. When Mendelian
genetics was rediscovered at the turn of the present century and Weismann
identified the material basis of heredity as the "germplasm" in
germ cells which became separate from the rest of the animal's body in the
course of early development, it seemed to offer a perfect explanation of
how Mendelian genes could be passed on unchanged from one generation to
the next. Darwinism was promptly reinterpreted according to the gene
theory in the 'neo-Darwinian synthesis' from the 1930s up to the 1950s and
60s. This coincided with an extremely productive and exciting period in
the history of biology as the gene theory itself continued to inspire a
series of discoveries that culminated in the DNA double helix and the
The neo-Darwinian synthesis began with the mathematical representation
of genes in populations and in plant breeding (biometrical genetics),
which, together provide a rigorous theory of Darwinian natural selection
in terms of genes for both discontinuous and continuously varying
characters. Systematics and paleontology for their part, defined
phylogenetic relationships and 'adaptive radiations' of the major groups
in accordance with Darwin's dictum of 'descent with modification'. At the
same time, the detailed study of chromosomes together with mutational and
other cytogenetic analyses eventually clarified the molecular basis of
Mendelian genes, which are located to linear arrays on chromosomes.
Heritable variations are generated by random mutations in these genes,
different forms (alleles) of which are subject to natural selection via
the different characters they determine, As the genes, according to
Weismann, are insulated from environmental influences, they are passed on
unchanged to the next generation, except for rare random mutations.
With the identification of DNA as the genetic material and the cracking
of the genetic code in the 1950s and 60s, the 'central dogma' of molecular
biology came to be accepted by most biologists. It states that the
sequence of bases in each DNA is faithfully transcribed into RNA, and the
RNA translated into a specific sequence of amino-acids of a protein in a
one-way information flow; and no reverse information-flow is possible.
This strengthens "Weismann's barrier", which is supposed to
strictly forbid environmental influences, or any experience in the
life-time of the organism to directly, i.e., predictably, affect its
genes. In the new orthodoxy which reigned over the next 20 years, the
organism tended to be seen as no more than a collection of genes, its
development, the unfolding of a 'genetic programme' encoded in
the genome. Random mutations give rise to mutant characters and natural
selection allows the fittest mutants to survive and reproduce.
Environmental changes give new selective forces and evolution is thereby
guaranteed. Dawkins (1976) has pushed this reductionistic trend to its
logical conclusion in proposing that organisms are automatons controlled
by 'selfish genes' whose only imperative is to replicate at the expense of
other 'selfish genes'. E.O. Wilson (1975) extended neo-Darwinian theory to
animal and human societies to define the new discipline of sociobiology,
which poses the paradoxical question (i.e., paradoxical within
neo-Darwinism): how could altruistic behaviour evolve (given that genes,
and the behaviour they control are fundamentally selfish)?
This paradox disappears, of course, when one rejects the ungrounded
assumption that selfishness or competitiveness is fundamental to the
living world. Animals engage in competitive or aggressive acts, but that
does not mean there are inherent qualities of competitiveness and
aggressiveness which can account for those acts. Furthermore, examples of
cooperation among animals far outstrip those of competition. Kropotkin
(1914) has given abundant evidence of the natural sociality of all animals
which is independent of genetic relatedness. Thus, one could invert E.O.
Wilson's question and ask, why do animals compete, given their natural
sociality? This highlights the sociopolitical underpinnings of all
scientific theories. Darwinism is no exception, for it is all of a piece
with the Victorian English society preoccupied with competition and the
free market, with capitalist and imperialist exploitation.
Darwin and Lamarck, The Genetic versus the Epigenetic Paradigm
History has the habit of creating heroes and anti-heroes, and so Darwin
triumphed while Lamarck bore the brunt of ridicule and obscurity. The
reason is that the theories of the two men are logically
diametrically opposed. Darwin's theory is natural selection, and
selection entails a separation of the organism from its environment. The
organism is thus conceptually closed off from its experience, leading
logically to Weismann's barrier and the central dogma of the
genetic paradigm, which is reductionistic in intent and in actuality.
Lamarck's theory, on the other hand, is of transformation arising
from the organism's own experience of the environment. It requires
a conception of the organism as open to the environment - which it
actually is - and invites us to examine the dynamics of transformation, as
well as mechanisms whereby the transformation could become 'internalized'.
Hence it leads logically to the epigenetic approach, which embraces the
same holistic, systems thinking that Lamarck exemplifies (Burkhardt,
The Genetic Paradigm and neo-Darwinism
Neo-Darwinism is a theory based on genes, G.C. Williams (1966) states
explicitly,"...In explaining adaptation, one should assume the
adequacy of the simplest form of natural selection, that of alternative
alleles in Mendelian populations." (p.4) Natural selection on
alternative alleles can only be a valid description of reality when the
following abstractions of the genetic paradigm are assumed to be true: (a)
genes determine characters in a straightforward and additive way, (b) they
are stable and, except for rare random mutations, are passed on unchanged
to the next generation, and (c) there is no feedback from the environment
to the organism's genes. All three assumptions have been demonstrated to
Assumption (a) was known to be false since the beginning of the
neo-Darwinian synthesis, and to some of the most prominent 'architects' of
the grand synthesis such as Sewell Wright (1969; 1978) and Ernst Mayr
(1963). Wright argues that selection relates to the organism as a
whole, or to the social group, not to single genes except as a net
resultant. He saw that the major source of variability is in the
recombination of already existing genes into a great number of different
genotypes, many of which would occupy equivalent "adaptive peaks"
in a "fitness landscape". Mayr, on the other hand, insists that
natural selection acts on "co-adapted gene complexes" as a
whole, and remains highly critical of 'beanbag [population] genetics' such
as that of R.A. Fisher (1930) and J.B.S. Haldane (1932), which deals with
selection of single genes. However, that still leaves both the "fitness
landscape" and the "co-adaptive gene complex" undefined,
and with little impact on the study of evolution in the mainstream, where
it is customary to identify a character, then assume there is a
hypothetical gene (or set of genes) responsible for it, which may be
selected in isolation from everything else.
Critics point out that the mapping between genes and the organisms'
characters (phenotype) in development is nonlinear and non-additive (as it
would already be when one takes Wright and Mayr seriously), and that the
organism as a dynamical system is subject to universal generative
principles not immediately dependent on the genes. Neo-Darwinists counter
that these are only "developmental constraints" which limit, to
some extent, the action of natural selection, but that natural selection
still plays the creative role in evolution (Bonner, 1981). There have been
serious attempts to use developmental findings to trace phylogenetic
relationships (Humphries, 1988; Wake, 1990; D.B. Wake, 1991) although the
theoretical relationship between ontogeny and phylogeny is still not
adequately understood by most systematists (Ho, 1988a; Wake, 1994).
Assumptions (b) and (c) effectively separate the organism from the
environment, which has the role of the 'selector'. Of course, most people
accept that the environment also interacts with the organism, causing
changes in its characteristics. However, it is supposed that the
environment as 'interactor' can be neatly separated from the environment
that selects, for so long as the germline genes are stable, and do not
change with the environment, then it is irrelevant how the rest of the
body is affected. As only the genes are passed on in evolution, it also
means that evolution is separate from development. Maynard Smith and
Holliday (1979) have indeed declared that the gift of Weismannism to
evolutionary (i.e., neo-Darwinian) theory is that development can be
safely ignored. As we shall see, these assumptions are no longer tenable.
The demise of the genetic paradigm and revival of the epigenetic
The assumptions that genes are stable, and that they are insulated from
environmental influences, are pivotal to the genetic paradigm and
neo-Darwinian theory. They were inspired by Weismann's theory of the
germplasm which, however, has been flawed from the start. Plants do not
have separate germ cells at all, for every somatic cell is potentially
capable of becoming a germ cell, and that is why plants can be propagated
from cuttings. Most animals also do not have germ cells that separate from
the rest of the body early in development (Buss, 1989). Furthermore, there
is no evidence that the genes in germ cells are stable, or immune from
environmental influences once they have separated from the rest of the
body. Evidence that genes are neither stable nor immune from direct
environmental influence has been accumulating over the past 20 years in
the findings of molecular genetics. They reveal hitherto unsuspected
complexity and dynamism in cellular and genic processes involved in gene
expression, many of which serve to destabilize and alter genomes within
the lifetime of all organisms (Steele, 1979; Pollard, 1984; Ho, 1987;
Rennie, 1993). This is in direct contradiction to the static, linear
conception of the central dogma that previously held sway.
A complicated network of feed-forward and feedback processes has to be
traversed just to express one gene or synthesize a single protein
(reviewed by Rennie, 1993; Kendrew, 1995). For a gene is not a continuous
sequence of DNA which can be transcribed and translated mechanically with
fidelity. It is actually interrupted in many places, and the bits must be
properly joined together in order to make a functional protein. Instead of
a linear causal chain between DNA and protein, there is a bewildering
profusion of other proteins regulating transcription, and alternative
starts and stops are often involved just to produce the RNA, which is then
subject to a vast array of alternative choppings and changings or further
editing by yet other proteins, before it is ready to be translated.
Translation is similarly subject to its own batallion of regulatory
factors, and the genetic code itself can be recoded or read in alternative
ways by the cellular machinery to make the protein. After that, a spectrum
of post-translational processings intervene before the finished product is
ready for transport to its final destination accompanied by still other
proteins acting as 'chaperones'. It is clear that no gene ever functions
in isolation. It becomes increasingly difficult to define and delimit a
gene, as multitudinous causal links criss-cross and interramify
throughout the entire epigenetic net, ultimately connecting the expression
of each gene with that of every other.
The genome itself is embedded within the epigenetic net, and is far
from stable or insulated from environmental exigencies. A large number of
processes appear to be designed especially to destablize genomes during
the life-time of all organisms, so much so that molecular geneticists have
been inspired to coin the descriptive phrase, "the fluid genome".
Mutations, insertions, deletions, amplifications, rearrangements,
recombinations, gene-jumpings, and gene-conversions keep genomes in a
constant state of flux in evolutionary time (Dover and Flavell, 1982).
Genes are found to jump between species that do not interbreed, being
carried by mobile genetic elements, viruses or microorganisms, which can
exchange genes at a prolific rate, as witnessed by the rapid horizontal
spread of antiobiotic resistance in bacteria. Parasites that infect more
than one species are also vectors for horizontal gene transfer. A
particular genetic element - the P-element - has spread to all species of
fruitflies in the wild within the span of less than 50 years, probably
carried by a parasitic mite (Rennie, 1993). These 'fluid genome' processes
are by no means entirely stochastic or meaningless, but are subject to
physiological and cellular control. Gene jumping, recombination and other
alterations of the genome are frequent responses to stress or starvation
in non-dividing cells that enable them to adapt or adjust to new
Similarly, cellular processes regularly inactivate whole batteries of
genes by chemically marking them during normal development, or imprint
them with binding proteins that alter the expression of the genes
(Sapienza, 1990). Some of these marks and imprints are created early in
development and may be passed on to the next generation via the germ
cells. These instances of 'epigenetic inheritance' already constitute a
substantial body of literature (comprehensively reviewed by Jablonka and
Epigenetic inheritance is just one aspect of the (previously forbidden)
reverse information flow - from the environment to the genomes - of which
there is now abundant evidence. The genomes of higher organisms contain a
high proportion of both functional and nonfunctional (pseudo)genes that
have arisen by reverse transcription of processed and mutated RNA
sequences back to DNA which is then re-inserted into the germline genome.
This process was predicted long ago by Nobel laureate, Howard Temin
(1971), who discovered the reverse transcription enzyme in a large class
of RNA retroviruses that are related to the mobile genetic elements
present in all genomes. The immune system may be particularly active in
using this mechanism to incorporate, into the germline, new antibody genes
that have been generated by mutations in somatic cells during immune
responses against foreign antigens (Rothenfluh and Steele, 1993).
Despite the correlation of genetic changes with physiological or
cellular states, many still regard these genetic changes to be the result
of random mutations which are then subject to internal or external
selection. 'Internal' selection is merely another name for physiological
interactions that ultimately give the required change, which is often
highly predictable and repeatable. Plants exposed to herbicides, insects
to insecticides and cultured cells to drugs, are all capable of changing
their genomes repeatably by specific mutations or gene amplifications that
render them resistant to the noxious agent (Pollard, 1988). Starving
bacteria and yeast cells respond to the presence of (initially)
non-metabolizable substrates by greatly enhanced, specific mutational
changes in the required enzymes compared to other 'non-selected' enzymes.
They are hence referred to as "directed mutations" (Foster,
1992; reviewed by Symonds, 1994). Finally, selection in any form has been
ruled out in the predictable and repeatable genetic changes which occur
simultaneously and uniformly in all the cells of the growing
meristem in plants exposed to fertilizers, which are then stably inherited
in subsequent generations (Cullis, 1988). The genetic paradigm has
collapsed under the weight of its own momentum in the burgeoning new
genetics. With the demise of the genetic paradigm, neo-Darwinian theory
has likewise lost its foundation.
Beginning in the early 1970s and just before the recent revelations in
molecular genetics, there has already been a general revival of the
epigenetic approach. This comes from workers in divers disciplines, all
focussing on the development of the organism as the key to understanding
evolution (Lovtrup, 1974; Gould, 1977; Ho and Saunders, 1979; 1984;
Alberch, 1980; Webster and Goodwin, 1982). Many share Lamarck's holistic
conception of the organism developing and evolving in concert with its
ecological (biosocial and physicochemical) environment; a few even
recognized that the mutual feedback interrelationships between organism
and environment may extend to directed genetic changes. The new genetics
seems to bear out Lamarck's basic propositions, although the precise
cellular or epigenetic mechanisms mediating non-random, directed genetic
changes are not yet understood.
Epigenetic Theories of Evolution
There are a number of different epigenetic theories of evolution, some
predating the neo-Darwinian synthesis. One common starting point for all
epigenetic theories is the developmental flexibility of all organisms. In
particular, it has been observed that artificially induced developmental
modifications often resemble (phenocopy) those existing naturally
in related geographical races or species.Thus, it seems reasonable to
assume that evolutionary novelties first arose as developmental
modifications which somehow became stably inherited (or not, as the case
may be) in subsequent generations.
An early proponent of an epigenetic theory was Baldwin (1896) who
suggested that modifications arising in organisms developing in a new
environment produce "organic selection" forces which are
internal to the organism, and which act to stabilize the modification in
subsequent generations. Another notable figure was Richard Goldschmidt
(1940), who questioned the orthodox neo-Darwinian account that new species
originate as the result of the accumulation, by natural selection, of
small single gene effects over geological time, for he saw abundant
evidence of 'unbridgeable [genetic] gaps' between natural species. He
proposed therefore, that evolutionary novelties arise from time to time
through macromutations producing "hopeful monsters" that
can initiate new species. In his defence, he was at pains to point out
that monsters are hopeful because of the inherent organization of
the biological system that tends to 'make sense' of the mutation. More
recently, Lovtrup (1974) advocates a similar theory of evolutionary
novelties, or major phyletic groups, coming into being by macromutations.
One important reason for focussing on development is that developmental
changes are far from random or arbitrary (Ho and Saunders, 1979; 1984;
Alberch, 1980; Webster and Goodwin, 1982). Instead, they are determined by
the dynamics of developmental (epigenetic) processes which are amenable to
mathematical description. The set of possible transformations is highly
constrained so that particular transformations may be predictably linked
to specific environmental stimuli. This is the basis for 'structuralism in
biology' (Webster and Goodwin, 1982; Lambert and Hughes, 1984; Goodwin
et al, 1989), or 'process structuralism' (Ho and Saunders, 1984;
Ho, 1988a) which proposes a rational taxonomy of biological forms and a
natural system of classification based on the dynamics of processes that
generate the forms (Ho, 1990; Ho and Saunders, 1994). The dynamics of the
processes are themselves subject to contingent complexification in the
course of evolution, by virtue of the lived experience of the organisms
themselves. We cannot go into details about that here, except to point out
that directed genetic changes in given environments are proving to be just
as nonrandom as morphological changes, and hence, possibly subject to
comparable systemic constraints (Ho, 1987).
Waddington's theory of genetic assimilation
The most influential recent figure among the 'epigenetic evolutionists'
is Waddington (1957), who attempted to accommodate 'pseudo-Lamarckian'
phenomena within neo-Darwinism in his theory of genetic assimilation. Like
all Darwinian and neo-Darwinian evolutionists, he wanted to explain the
origin of adaptive characters, i.e., characters that seem to be
fitted to the functions they serve.
First, Waddington conceptualizes the flexibility and plasticity of
development, as well as its capacity for regulating against disturbances,
in his famous 'epigenetic landscape' - a general metaphor for the dynamics
of the developmental process. The developmental paths of tissues and cells
are seen to be constrained or canalized to 'flow' along certain
valleys and not others due to the 'pull' or force exerted on the landscape
by the various gene products which define the fluid topography or
structure of the landscape (Fig. 1). Thus, certain paths along valley
floors will branch off from one another to be separated by hills
(thresholds) so that different developmental results (alternative
attractors) can be reached from the same starting point. However, some
branches may rejoin further on, so that different paths will nevertheless
lead to the same developmental result. Genetic or environmental
disturbances tend to 'push' development from its normal pathway across the
threshold to another pathway. Alternatively, other valleys (developmental
pathways) or hills (thresholds) may be formed due to changes in the
topography of the epigenetic landscape itself.
The importance of the epigenetic landscape is that its topography is
determined by all of the genes whose actions are inextricably
interlinked, and is not immediately dependent on specific alleles of
particular genes (Ho and Saunders, 1979). This is in accord with what we
know about metabolism and the epigenetic system, particularly as revealed
by the new genetics. Hence, it has evolutionary consequences other than
those predicted by the selection of individual genes. The epigenetic
landscape captures the complex nonlinear dynamics of the developmental
process, which has been explored mathematically in greater detail since,
and its evolutionary consequences made explicit (Saunders, 1992). For
example, it accounts for 'punctuated equilibria' (Eldredge and Gould,
1972) - the observation in the fossil record of evolutionary stasis over
long geological periods punctuated by the sudden appearance of new species
or of rapid morphological change. It also shows how large organized
changes can occur with a relatively small disturbance, or how continuously
varying environmental parameters can nevertheless precipitate
discontinuous phenotypic change.
Thus, when a population of organisms experience a new environment, the
following sequence of events may take place.
(a) A novel response arises during development in a large proportion
of the organisms in a population exposed to a new environmental
Because the topography of the landscape is not the property of specific
alleles of individual genes but the collective property of all the genes,
it is expected that a large proportion of the population will respond.
This corresponds to the normal developmental pathway being 'pushed' over a
threshold, or a new pathway appearing by a change in topography of the
(b) If this response is adaptive, then there will be natural selection
for its "canalization", i.e. it deepens in intensity and becomes
regulated so that a more or Iess uniform response results from a range of
intensity of the environmental stimulus. This involves a change in the
epigenetic landscape so that the valley constraining the new developmental
path deepens and regulates against disturbances.
(c) After some generations, the response becomes genetically
assimilated, in that it arises even in the absence of the stimulus. This
would entail a further change in the topography to bias the original
branch point in favour of the new pathway, so that the new phenotype will
persist in the absence of the environmental stimulus.
Waddington was not very specific as to the mechanisms involved either
in canalization or in genetic assimilation, except to argue that because
they are advantageous there would be selection for them presumably through
suitable "modifier" genes, i.e., genes which modify the
expression of the character ( or the topography of the epigenetic
landscape). He and his colleagues have carried out experiments showing
that artificial selection for the new character could result in
canalization and genetic assimilation.
Ho et al (1983) questioned the assumption that genic selection
is necessary for canalization and genetic assimilation, and in a series of
experiments, demonstrated that heritable cytoplasmic effects may be
involved in canalization in the absence of selection for
the new character. Heritable cytoplasmic effects were first demonstrated
by Jollos (1921) early this century. Developmental biologists are also
familiar with observations indicating that changes in cytoplasmic
organization could be stably inherited independently of nuclear or
cytoplasmic DNA (Malancinski, 1990). Recently, Chow et al (1994)
demonstrated that heritable cytoplasmic effects are induced by a low serum
culture medium which predispose entire populations of cultured cells to
malignant transformation in subsequent generations. However, these studies
do not give any clue to the mechanisms involved in cytoplasmic effects.
Cytoplasmic effects may be due to a dynamic equilibrium of genic and
cellular processes (a cellular or gene expression state) that is a
property of the whole system, in which case, they may prove
elusive to conventional methods that attempt to identify single, localized
molecular causes. They may involve (many) genes being marked and other
epigenetic inheritance of varying memory spans, as Jablonka and Lamb
Heredity and evolution in the light of the new genetics
How should we see heredity in the light of the new genetics? If the
genome itself is so dynamic and fluid, where does heredity reside? It is
clear that heredity does not reside solely in the DNA of the genome. In
the first instance, it resides in an epigenetic cellular state - a dynamic
equilibrium between interlinked genic and cellular processes. But even
that is an abstraction and reification. It cannot be assumed that heredity
is exhausted at the boundary of cells or organisms. For as organisms
engage their environments in a web of mutual feedback interrelationships,
they transform and maintain their environments which are also passed on to
subsequent generations as home ranges and other cultural artefacts (Oyama,
1986; Gray, 1988). Embedded between organisms and their environment are
social habits and traditions, an inseparable part of the entire dynamical
complex that give rise to the stability of the developmental process, and
which we recognize as heredity (Ho, 1988b). Heredity is thus distributed
over the whole system of organism-environment interrelationships, where
changes and adjustments are constantly taking place, propagating through
all space-time scales in the maintenance of the whole, and some of these
changes may involve genomic DNA. Thus, the fluidity of the genome is a
necessary part of the dynamic stability, for genes must also be able
to change as appropriate to the system as a whole.
What implications are there for evolution? Just as interaction and
selection cannot be separated, so neither are variation (or mutation) and
selection, for the 'selective' regime may itself cause specific variations
or 'adaptive' mutations. The organism experiences its environment in one
continuous nested process, adjusting and changing, leaving
imprints in its epigenetic system, its genome as well as on the
environment, all of which are passed on to subsequent generations. Thus,
there is no separation between development and evolution. In that
way, the organism actively participates in shaping its own development as
well as the evolution of its ecological community.
While the epigenetic approach fully reaffirms the fundamental holistic
nature of life, it can give no justification to simplistic
mechanistic ideas on arbitrary effects arising from use and disuse or the
inheritance of acquired characters. Organisms are above all, complex,
nonlinear dynamical systems (Saunders, 1992), and as such, they have
regions of stability and instability that enable them to maintain
homeostasis, or to adapt to change (or not as the case may be). The
appearance of novelties and of mass extinctions alike in evolutionary
history are but two sides of the same coin, we cannot be complacent about
the capacity of organisms to adapt to any and all environmental insults
that are perpetrated. The dynamics of the developmental process ultimately
holds the key to heredity and evolution, in determining the sorts of
changes that can occur, in its resilience to certain perturbations and
susceptibility to others.
Genetic and epigenetic paradigms in the study of behaviour
We are now in a position to examine the parallels in the study of animal
behavior, where a similar divide between the genetic and epigenetic
paradigms occurs. In the classical view due to Lorenz (1965), which is
shared to some extent by Tinbergen (1963), the development of behaviour
consists of a largely autonomous sequence of maturation of central neural
mechanisms controlling the animal's behavioural repertoire. The
environment, insofar as it enters in development, does so in the form of
specific stimuli serving to release preformed patterns of behaviour from
central inhibition. A strict dichotomy is thereby maintained between the
'innate' and 'acquired' components of behaviour, the 'innate' being
equated with species-typical or instinctive behaviour. This fits easily
within the genetic paradigm in terms of genes controlling behaviour in a
more or less straightforward and mechanical manner. Much of the theorizing
in sociobiology is based on just such an assumption, despite apologies to
the contrary. In opposition to the theory of Lorenz, comparative
psychologists such as Lehrman (1956) and Schneirla (1965; 1966), have
shown that the 'innate' and 'acquired' are inextricably confounded. And
that applies even to so-called instinctive behaviour.
In a classic study on the chick, Kuo (1966) showed how the embryonic
heartbeat is instrumental in stimulating and entraining the raising and
lowering of the head (resting on the heart), whose movements extend to the
beak opening and closing, then to swallowing the amniotic fluid later on.
The embryo not only develops an integrated sense of itself, but also a
series of coordinated movements that are the tangible precursor of
so-called instinctive behaviour. Similarly, Gottlieb (1963) showed how
isolated wood ducklings learn to recognize the call of its conspecifics at
hatching simply through hearing its own call while still in the egg. Thus,
there is no preformed set of behaviour encoded in the genes waiting to be
released. Even an isolated animal is subject to self-stimulation arising
from its own activities beginning early in embryogenesis, which in turn
generates complex behavior. (This demonstrates the fallacy of isolation
experiments that are still carried out by ethologists and sociobiologists
to-day in an attempt to prove that particular behaviours are innate or
The aim of comparative psychology, according to Schneirla, is to
discover the similarities and differences between phylogenetic
levels in how behavior is organized. This requires careful studies on the
ontogeny of species-typical behaviour which deal with the problem of
organization. Maturational (biological) processes are inextricably linked
with the experiential, each in turn defining and transforming the other.
Through the interplay of maturational and experiential processes, the
physiological and 'meaningless' become psychological and meaningful by
social reinforcement. There is thus a continuum linking the
genetic/metabolic with the social and pyschological. A full understanding
of how organisms evolve must ultimately take on board the whole spectrum
of interrelationships (Tobach and Greenberg, 1984; 1988).
Comparative psychology is thoroughly epigenetic in its holistic
attention to many levels of living organization, and its emphasis on how
complex behaviour is generated during development through the formative
influence of experience. Recently, Gottlieb (1992) has extended
comparative psychology to consider how new behaviour defines new
functions, and hence, new morphologies in evolution. This same step has
been taken by developmental psychologist Piaget some years ago.
Piaget (1979) rejected the idea that there is an innate cognitive
structure which allows us to make sense of reality. Instead, much of his
prodigious volume of work is devoted to showing how cognitive abilities
are developed through the child's own activities in exploring and
experiencing the world. One of his preoccupations in biology is to
undertand why form is so-well suited, or adapted to the 'function' it
serves. In his last works, Piaget (1979) returned to the study of biology
in order to consider the evolutionary problem which he regards as
insoluble within the neo-Darwinian framework: how is it that the form of
an organ is invariably accompanied by the behavioural repertoire
appropriate to its use? It stretches credulity to imagine, for example,
that the woodpecker first got a long beak from some random mutations
followed by other random mutations that made it go in search of grubsin the bark of trees. The only explanation for this coincidence of
form and behaviour in the execution of function is that the two must have
evolved together through the organisms' experience of the environment.
Experience, as we have seen, never involves the organism in a purely
passive role. Organisms generally act (more than just behave)
so as to give themselves the greatest chance of survival. This is brought
about by various means ranging from avoidance reactions in unicellular
organisms to the purposive or directed explorations of higher organisms.
Thus, a change in habit may be the efficient cause of the change in form,
which in turn accounts for the fit between form and function. If it is
true that organisms generally act so as to maximize their prospects for
survival, it follows that the resulting modification of form will most
likely be 'adaptive'. The 'adaptation' will involve feedback effects on
its physiology, which include changes in gene expression, or in the genes
themselves. On the other hand, organisms may also act and develop
'maladaptively', as human beings, in particular, seem capable of doing.
The epigenetic approach, dynamic holism and the new organicism
The epigenetic paradigm which encompasses both comparative psychology
and biology may be broadly characterized as follows:
1. Development occurs by epigenesis, in which the experience of the
organism's environment enters as necessary formative influences,
there being no preformation or predetermination in the genes.
2. Evolutionary changes are initiated by developmental changes.
3. These developmental changes are non-arbitrary, being determined by
the dynamics of the epigenetic system itself.
4. Developmental changes may be assimilated into the new organism/
environmental system as a whole, which set the parameters for further
5. Epigenesis mediates between the biological and social levels serving
to integrate the two into a structural and functional whole.
6. Development and evolution are continuous, with the organism
participating in shaping its own developmental and evolutionary history.
Schneirla shared obvious sympathies with the work of epigeneticists
such as Waddington, Kuo, and Lehrman. However, he chose to refer to his
own approach as "dynamic holism", with emphasis on the concept
of 'integrative levels': the idea that there are behaviors or activities
specific to levels of integration which cannot be reduced to the
components at a lower level. For example, Schneirla (1966) points out that
ants are capable of situation-specific behavior which gives rise to the
social level of organization, while mammals exhibit an integrative
solution of problems which is characteristic of the psychosocial
level of organization. This recognition of level-specific phenomena does
not imply a separation of distinct, disconnected levels. On the contrary,
it acknowledges the continuity between them and behoves us to pay
attention to all levels and their interconnections.
In reaction to the recent spread of neo-Darwinian genetic determinism
into the social sciences, Many sociologists and psychologists have argued
that the social and psychological are separate and independent of the
biological. I have shown how neo-Darwinian genetic determinism is no
longer tenable within biology, while an alternative approach explicitly
recognizes the mutually dependent, mutually defining and transforming
relationship between the biological and the psychosocial.
The epigenetic paradigm has transformed into a contemporary movement in
that I shall refer to as the 'new organicism'. It attempts to connect
biology with non-equilibrium physics, chemistry and mathematics, offering
greater precision to ideas of living organization, of organic wholeness
and complexity (Nicolis and Prigogine, 1989; Saunders, 1992; Ho, 1993;
Kaufman, 1993; Goodwin, 1994). In particular, the organism is seen as a
coherent domain thick with activities over all space-time scales
which are interlocked and intercommunicating; hence the organism itself
has no levels nor preferred levels (Ho, 1993), 'levels' being our
own construct for making sense of the entangled whole. A new alliance
between psychology and organicist biology is timely in presenting a
picture of evolution that is consonant with empirical findings as well as
with our deepest experience of nature's unity.
Alberch, P. (1980). Ontogenesis and morphological diversification.
Am. Zool., 20, 653-667.
Baldwin, J.M. (1896). A new factor in evolution. Am. Nat. 30,
Bonner, J.T. ed. (1982). Evolution and Development,
Burkhardt, R. (1977). The Spirit of Systems, Harvard
University Press, Cambridge, Mass.
Buss, L. (1987). The Evolution of Individuality, Princeton
University Press, Princeton, N.J.
Chow, M., Yao, A. and Rubin, H. (1994). Cellular epigenetics:
topochronology of progressive "spontaneous" transformation of
cells under growth constraint. Proc. Natl. Acad. Sci. USA 91,
Cullis, C. A. (1988). Control of variations in higher plants. In
Evolutionary Processes and Metaphors (M.W. Ho and S.W. Fox, eds.),
Darwin, C. (1859). On the Origin of Species by Means of Natural
Selection or the Preservation of Favoured Races in the Struggle for Life,
Dawkins, R. (1976). The Selfish Gene, Oxford University
Dover, G. A. and Flavell, R.B. eds. (1982). Genome Evolution,
Academic Press, London.
Eldredge, N. and Gould, S. J. (1972). Punctuated equilibria: an
alternative to phyletic gradualism. In Models in Paleobiology (T.J.M.
Schopf, ed.), Freeman, New York.
Fisher, R.A. (1930). The Genetical Theory of Natural Selection.
Clarendon Press, Oxford.
Foster, P.L. (1992). Directed mutations: between unicron and goats.
J. Bacteriol. 174, 1171-1716.
Goldschmidt, R.B. (1940). The Material Basis of Heredity,
Yale University Press, New Haven.
Goodwin, B.C. (1994). How the Leopard Changed Its Spots,
Orion Books, London.
Goodwin, B.C., Webster, G. and Sibatani, A. eds. (1989). Dynamic
Structures in Biology, Edinburgh University Press, Edinburgh.
Gottlieb, G. (1963). A naturalistic study of imprinting in wood
ducklings (Aix sponsa). J. Comp. Physiol Psychol, 56, 86-91.
Gottlieb, G. (1992). The Genesis of Novel Behavior, Oxford
University Press, Oxford.
Gray, R. (1988). Metaphors and methods in evoluionary theory In Evolutionary
Processes and Metaphors (M.W. Ho & S.W. Fox, eds.), Wiley,
Haldane, J.B.S. (1932). The Causes of Evolution. Longmans,
Ho, M.W. (1987). Evolution by process, not by consequence:
implications of the new molelcular genetics on development and
evolution. Int. J. Comp. Psychol. 1, 3-27.
Ho, M.W. (1988a). How rational can rational morphology be? A
post-Darwinian rational taxonomy based on the structuralism of process.
Rivista di Biologia 81, 11-55.
Ho, M.W. (1988b). Genetic fitness and natural selection: myth or
metaphor. In Proc. 3rd Schneirla Conference, Lawrence Erlbaum,
Ho, M.W. (1990). An exercise in rational taxonomy. J. theor. Biol.
Ho, M.W. (1993). The Rainbow and the Worm: The Physics of
Organisms, World Scientific, New Jersey.
Ho, M.W. and Saunders, P.T. (1979). Beyond neo-Darwinism: an
epigenetic approach to evolution. J. theor. Biol., 78, 673-691.
Ho, M.W. and Saunders, P.T. eds. (1984) Beyond neo-Darwinism.
Introduction to the New Evolutionary Paradigm, Academic Press,
Ho, M.W. and Saunders, P.T. (1994). Rational taxonomy and the natural
system- segmentation and phyllotaxis. In Models in Phylogeny
Reconstruction (R.W. Scotland, D.J. Siebert and D.M. Williams,
eds.), pp. 113-124, The Systematics Association Special Volume 52,
Oxford Science, Oxford.
Ho, M.W. , Tucker, C., Keeley, D. and Saunders, P.T. (1983). Effects
of sucessive generations of ether treatment on penetrance and expression
of the bithorax phenocopy. J. exp. Zool. 225, 1-12.
Humphries, C.J. ed. (1988). Ontogeny and Systematics,
Columbia University Press, New York.
Jablonka, E. and Lamb, M.J. (1995). Epigenetic Inheritance and
Evolution - The Lamarckian Dimension, Oxford University Press,
Jollos, V. (1921). Experimentelle Protistenstudien I. Untersuchungen über
Variabilität und Vererburg bei Infusorien. Arch. für
Protistenkunde 43, 1-222.
Kaufman, S. (1993). Origins of Order: Self-Organization and
Selection in Evolution, Oxford University Press, Oxford.
Kendrew, J. ed. (1995). The Encyclopedia of Molecular Biology,
Blackwell Science, Oxford.
Kropotkin, P. (1914). Mutual Aid: A Factor of Evolution,
Extending Horizon Books, Boston, Mass.
Kuo, Z,Y, (1966). The Dynamics of Behavior Development: An
Epigenetic View, Random House, New York.
Lambert, D. M. and Hughes, A.J. (1984). Misery of functionalism:
Biological function, a misleading concept. Rivista di Biologia
Lehrman, D.S. (1956) On the organization of maternal behavior and the
problem of instinct. In L'Instinct dans le Comportement des Animaux
et de l'Homme, pp 475-514, Masson, Paris.
Lorenz, K. (1965). Evolution and Modification of Behavior.
Univ. Chicago Press, Chicago.
Lovtrup, S. (1974). Epigenetics, John Wiley & Sons,
Malacinski, G.M. ed. (1990). Cytoplasmic Organization Systems,
McGraw Hill Publishing Co., New York.
Maynard-Smith, J. and Holliday, R. (1979). Preface to Evolution
of Adaptation by Natural Selection (J. Maynard-Smith and R.
Holliday, eds.), The Royal Society, London.
Mayr, E. (1963). Animal Species and Evolution, Belknap Press,
Nicolis, G. and Prigogine, I. (1989). Exploring Complexity,
R. Piper Gmbh & Co., KG Verlag, Munich.
Oyama, S. (1986). The Ontogeny of Information, Cambridge
University Press, Cambridge.
Piaget, J. (1979). Behaviour and Evolution, Routledge and
Kegan Paul, London.
Pollard, J. (1984). Is Weismann's barrier absolute? In Beyond
neo-Darwinism. Introduction to the New Evolutionary Paradigm (M.W.
Ho and P.T. Saunders, eds.), Academic Press, London.
Pollard, J.W. (1988). The fluid genome and evolution. In
Evolutionary Processes and Metaphors (M.W. Ho and S.W. Fox, eds.),
Rennie, J. (1993). DNA's new twists, Scient. Am. March,
Rothenfluh, H.S. and Steele, E.J. (1993). Origin and maintenance of
germ-line V genes. Immunology and Cell Biology 71, 227-232.
Sapienza, C. (1990). Parental imprinting of genes. Scient. Am.
Saunders, P.T. (1992). The organism as a dynamical system. In Thinking
About Biology (W. Stein and F.J. Varela, eds.), Addison-Wesley,
Schneirla, T.C. (1966). Behavioral development and comparative
psychology Quart. Rev. Biol 41, 283-302.
Schneirla, T.C. (1965). Aspects of stimulation and organization in
approach/withdrawal processes underlying vertebrate behavioral
development. In Advances in the Study of Behavior (D.S.
Lehrman,, R. Hinde nad E. Shaw, eds), pp 1-71, Academic Press, New York.
Steele, E.J. (1979) Somatic Selection and Adaptive Evolution,
Symonds, N. (1994). Directed mutation: a current perspective. J.
theor. Biol. 169, 317-322.
Temin, H.M. (1971). The protovirus hypothesis: speculationson the
significance of RNA-directed DNA synthesis for normal development and
for carcinogenesis. J. Nat. Can Inst. 46, III-VII.
Tinbergen, N. (1963). On aims and methods of ethology, Z..
Tierpsychol. 20, 410-433.
Tobach, E. and Greenberg, G. eds. (1984). Behavioral Evolution
and Integrative Levels, Lawrence Erlbaum, New Jersey.
Tobach, E. and Greenberg, G. eds. (1988). Behavior and Evolution,
Lawrence Erlbaum, New Jersey.
Waddington, C.H. (1957). The Strategy of the Genes, Allen and
Wake, D.B. (1991). Homoplasy: the result of natural selection, or
evidence of design limitations? Am. Nat. 138, 543-567.
Wake, M.H. (1990). The evolution of integration of biological
systems: an evolutionary perspective through study of cells, tissues,
Wake, M.H. (1994). The use of unconvensional morphological characters
in analysis of systematic patterns and evolutionary processes. In
Interpretating the Hierarchy of Nature (O. Rieppel, ed.), Academic
Press, New York.
Webster and Goodwin (1982). The origin of species: a structuralist
approach. J. Soc. Biol. Struct. 5, 15-47.
Williams, G.C. (1966). Adaptation and Natural Selection,
Princeton University Press, Princeton.