THE HOLOGRAPHIC PRINCIPLE IN
BIOLOGICAL DEVELOPMENT AND
3c Dawlish Road, Leyton, London E10 6QB
I would like to introduce the themes of this paper in the form of a dialogue:
Q: How should we build complex forms, such as living things?
A: Organise them as a hierarchy of stable subassemblies, or homologous organs.
Q: Surely the genes are all you need to explain living organisation?
A: But the same organ can be the result of different genes! When we look at the
genes as more than simply stretches of nucleic acid, but see them switching each other
on and off, then a hierarchical organisation emerges spontaneously.
Q: Anyway, hadn’t Darwin explained homology?
A: No, his explanation fails, and the pre-Darwinian understanding of homology is
much closer to the hierarchical approach.
Q: Isn’t there a quantitative approach that explains form?
A: No, form is a qualitative distinction between an inside and an outside. Living
things are autonomous forms, themselves maintaining this boundary.
Q: Is such a boundary a purely material skin?
A: A boundary can be seen as the interface between the parts inside and the rest of the
universe outside, through which information flows.
Q: Can’t an organism be described in isolation?
A: But then it would be a stone! An organism is a process of interaction with its
environment, a process of creating and discovering.
Q: Creating and discovering? Is that a linguistic process?
A: Yes, a living thing is a focus of a linguistic process, where meanings are
recognised and transformed.
Q: Eventually we will be able to reduce form to physics and chemistry, won’t we?
A: Could you reduce the meaning of these words to the chemistry of the ink? The
same form may be realised in many different physicochemical configurations. The
Cartesian method just won’t work.
Q: Do you mean to say that genetic and morphological descriptions of living things
are radically different?
A: Yes, they are complementary yet incompatible. Continuity of morphological
information is a kind of memory without mechanical storage. Without this holistic
memory, the mechanically stored genetic information would deteriorate over time.
Q: I know that many quantitative models of morphogenesis have been proposed. So
how can you say that form is qualitative?
A: Morphogenetic models exhibit bifurcation points, where the system shifts suddenly
from one form to a quite different form.
Q: I feel uncomfortable with this idea of sudden jumps.
A: You feel happy about the sudden jumps in quantum physics, don’t you?
Q: But how do you decide between all the different interpretations?
A: Things become a lot clearer once you understand that the most important thing is
the form of the quantum system, not the energy.
Q: Isn’t that a very organic way of putting things?
A: Yes, the ageing of a living system is much closer to the development of a quantum
process than to anything Newton described.
Q: But how deep could the comparison be?
A: Well, certain forms of the equations for both look very similar, the same equations
that describe a hologram. You can talk about a quantum process as a hierarchy of
surfaces through which information flows.
Q: ‘Surfaces through which information flows’—that’s how you described living
things and their organs, isn’t it?
A: Yes, that’s right! And these surfaces turn out to be holographic.
Q: Oh so that’s where the holographic principle in your title comes from?
A: Yes, the holographic principle may hold the key to bringing quantum physics
together with relativity. Looks like it might bring in life and non-linear systems too!
1. MORPHOLOGICAL STABILITY
The parable of the two watchmakers is first presented by Simon (1962: 470), and has
been variously adapted by Koestler (1967: 45-47) and Allen and Starr (1982: 49-51).
In Simon’s account, the two watchmakers are named Hora and Tempus, whereas
Koestler renames them Bios and Mekhos, and Allen and Starr provide a factual
exemplar of the fictional Hora. Both Hora and Tempus make watches that consist of
1000 parts. However, Hora manufactures his watches in subassemblies of 10 parts
each, whereas Tempus puts his watches together part by part. The workshop is a busy
place, often disturbed by the telephone ringing. Hora and Tempus must leave their
work to answer the telephone, in case it is a new customer on the line. Who gets his
work done more quickly? Hora’s subassemblies are stable in themselves. They do
not fall apart when their maker leaves them to answer the phone. But for Tempus
only the completed watch is stable. A disruption at any stage except the last means he
will have to start from scratch again. Hora’s strategy is the better one for dealing with
disturbances from the environment, since his use of stable subassemblies minimises
the effect of those disturbances. Watches built by Hora as a hierarchy of
subassemblies will come to predominate in the market at the expense of the watches
Living things are not simply aggregates of parts, nor are they indecomposable wholes.
They are loosely coupled, or near decomposable (see Simon, 1962, 1973; Koestler,
1967: 64-65; Allen and Starr, 1982: 70-74). Living things consist of sub-wholes,
parts in relation within the whole. A kidney is defined in terms of its function within
the body, but may also be transplanted from one body to another. Its function within
the body is an aspect of its partness, the fact that it can be transplanted an aspect of its
wholeness. Koestler (1967: 48) describes such semi-autonomous sub-wholes as
holons (from Greek: holos, meaning whole, and -on as in electron, proton). ‘The
evolutionary stability of sub-assemblies—organelles, organs, organ-systems—is
reflected by their remarkable degree of autonomy or self-government. Each of
them—a piece of tissue or a whole heart—is capable of functioning in vitro as a
quasi-independent whole, even though isolated from the organism or transplanted into
another organism. Each is a sub-whole which, towards its subordinated parts, behaves
as a self-contained whole, and towards its superior controls as a dependent part.’
Koestler (1974: 62).
‘Among possible complex forms, hierarchies are the ones that have time to evolve’
(Simon, 1962: 473). Simon’s conclusion from the watchmaker parable has been
tested recently in evolutionary computing. The final solution of a problem specified
for a population of genetic algorithms emerges from a synthesis of several partial
solutions, known as building blocks. Wagner (1995) draws the following lesson for
the evolution of living things: ‘... a system consisting of building blocks has a much
better chance to be improved by mutation and natural selection than an unstructured
system ... Hence the building block hypothesis can explain why it makes sense to
organize a complex organism into individualized characters called homologues.’
Living things consist of a wide variety of standard parts (Raff, 1996: 330), building
blocks (Wagner, 1995) or modules (Wagner and Altenberg, 1996). ‘The most
fundamental principle of evolutionary strategy, related to the watchmakers’ parable, is
the standardisation of subassemblies ... Animals and plants are made out of
homologous organelles like the mitochondria, homologous organs like the gills and
lungs, homologous limbs such as arms and wings. They are the stable holons in the
evolutionary flux’ (Koestler, 1967: 135, 139).
Riedl introduces a concept of morphological stability, or fixation, to account for the
fact of homology: ‘Actually, every homologue is characterised by the fact that it
shows adaptive freedom in only a few directions, but fixation in many others. If this
were different, if every character were free to change in every direction, the living
world would appear as a random chaotic mixture of patterns, as chaos, and the single
relationship left among representatives would not relate to common ancestry but only
to common functions, such as analogous limbs, horns, wings, jaws, and so forth’
(Riedl, 1977: 354; cf. Alberch, 1982: 315-316). Parts of organisms possess a stability,
which permits us to recognise relationships between them that are not the result of
2. METABOLIC STABILITY
‘A living thing is a complex net of interactions between thousands or millions of
chemical species’ (Kauffman, 1969: 437; 1970: 18). How is it possible for an
organism to arrive at a stable metabolism among these chemical species? The answer
lies in how the organism is able to construct a number of specialised compartments as
it develops, the different cell types. It then has at its disposal a range of environments
in which specialised metabolic reactions can take place. The problem of metabolic
stability is a problem of cellular differentiation.
Kauffman (1969, 1970) describes cellular differentiation in terms of the Jacob-Monod
theory of gene expression. Genes are modelled as binary switches, turning each other
on or off. Each gene executes a certain Boolean operation on its own state, on or off,
and the states of the genes connected to it in order to generate the state at the next
point in time. Connections among genes are randomly assigned. Kauffman discovers
how, with these model genomic networks, the behaviour of the system is related to its
connectedness. With one connection the behaviour is frozen, the activities of the
genetic elements are not coordinated. When the number of connections is large, chaos
reigns and the array does not reach a stable pattern of activity. However, when the
number of connections is poised at two, complex behaviour emerges. Here the system
of elements divides into a number of functionally isolated subsystems, loosely
coupled to each other, each of which settles down into a regular pattern of gene
activity. Metabolic stability emerges out of randomness. Kauffman is able to
introduce perturbations to test this stability, either by changing the state of a particular
gene, or by altering its Boolean function. Genes will generally return to the same
state cycle, or shift to a limited number of other cycles (Kauffman, 1969: 463; 1970:
34). The emergent subsystems are therefore ‘poised’, that is, they are to transform
into a very limited number of other subsystems (Kauffman, 1992). This is the very
nature of differentiation. Remarkably, the number of subsystems for a particular
number of genes is of the same order of magnitude as the number of cell types found
in organisms possessing that number of genes. Kauffman concludes that the genomes
of organisms may indeed be constructed more or less randomly, and rely on the order
that spontaneously emerges from such randomness for their coordination.
Kauffman (1983: 218) explains how a compartmented organisation of the genome is
advantageous in evolution: ‘Selective evolution [evolution by natural selection]
requires the capacity to accumulate partial successes sequentially. Were the genome
organized such that a small change in connections could alter coordinated dynamical
patterns of gene activities throughout the network preservation of past favourable
combinations of activities would be difficult. Accumulation of partial successes
requires either genuinely isolated subsystems, hard to maintain in a scrambling
genome, or functionally isolated subsystems which are otherwise loosely coupled, as
arise inevitably in these model genomes. Selective modification of the combinations
of gene activities in one functionally isolated subsystem would not alter the dynamics
of the remaining system, hence allowing piecewise evolution of favourable new cell
types.’ Kauffman’s findings harmonise very well with Simon’s proposal that
hierarchically organised, near-decomposable systems are the most likely to evolve.
As Wagner (1995) perceives, each subsystem is a partial success, or building block, to
which new improvements can be added. Kauffman’s model of cellular differentiation
is discussed in the chapter on modularity in Raff (1996: chapter 10). Cell types are
described as modular units of gene expression (Raff, 1996: 328).
3. THE HIERARCHY OF TYPES
‘What can be more curious than that the hand of man, formed for grasping, that of a
mole for digging, the leg of the horse, the paddle of the porpoise, and the wing of the
bat, should be all constructed on the same pattern, and should include the same bones,
in the same relative positions’ (Darwin, 1859 [1968: 415]). The forelimbs of the
different mammals are homologous and overall, the mammals, indeed all vertebrates,
show the same plan of organisation, or unity of type.
The bones in the forelimbs of mammals maintain the same relative positions: ‘An
organ is sooner altered, atrophied, or annihilated than transposed’ (Geoffroy Saint-
Hilaire, 1818: xxx; translated in Appel, 1987: 99). The criterion for their homology is
the principle of connections. Geoffroy Saint-Hilaire discovered this principle through
his attempt to establish the homology of the opercular bones, the bones that cover the
gill opening in fishes. By considering only their connections, he reached the
conclusion that the opercular bones are located in the middle ear of mammals, as the
malleus, incus and stapes (Geoffroy Saint-Hilaire, 1818: 37). Similarly, by
considering its connections to bones of the ankle, the horse’s hoof is the enlarged nail
of the third toe (Goodwin, 1994: 131).
The explanation of homology that Darwin proposes is that the two structures trace
back to a structure in the common ancestor (see also, Ghiselin, 1976): ‘If we suppose
that the ancient progenitor, the archetype of all mammals, had its limbs constructed on
the existing general pattern, for whatever purpose they served, we can at once
perceive the plain signification of the homologous construction of the limbs
throughout the whole class’ (Darwin, 1859 [1968: 416]). Darwin’s explanation
assumes that bodily organs are replicated and handed on entire from generation to
generation. But we know that this is not the case: ‘Only replicators like genes pass
on their own structure to their descendants directly. Morphological structures are not
replicators ... The notion of continuity of descent is not problematic for genes but is
less clear for organs’ (Wagner, 1989b: 55, 56).
There are two possible ways of revising the Darwinian explanation of homology:
1. The homology of structures in different animals is due to the same genes
handed down from the common ancestor.
2. Homologous structures form from the same cells in development.
However, counterexamples can be given to both explanations:
1. ‘In the fruit fly Drosophila there is a particular gene which governs the
formation of the eyes and there is an allelomorph (a mutant alternative) of this
gene which in the homozygous state produces an eyeless condition. Now [T.
H.] Morgan showed that, if a pure homozygous eyeless stock is inbred, the
other genes in the gene complex, by reassortment, may come to be recombined
in such a way that they will deputise for the missing normal eye-forming
allelomorph, and lo and behold flies appear in the “eyeless” stock with the
eyes as good as ever! These eyes must surely be regarded as homologous with
the eyes of normal flies, yet their production is not controlled by the same
genes’ (Hardy, 1965: 212). This is the phenomenon of genetic piracy (Roth,
2. ‘... in one species of frog (Rana fusca) the lens of the eye can only be induced
by the presence of the optic cup; in another species (Rana esculenta) while it
can be induced by the optic cup, it is also formed in its proper place if the
optic cup is removed—formed apparently in relation to the developing whole
animal’ (Hardy, 1965: 213). ‘Phylogenetically homologous characters need
not share common pathways of ontogenetic development’ (Wagner, 1989b:
58). Between species, the origin of cellular material, the precise sequence of
events or specific inducers, have all been found to vary.
One also runs into problems applying the Darwinian criterion of homology to
repeated elements in the body. Lankester (1870) claims that the fore and hind limbs
of land vertebrates cannot be homologous, rather they are analogous, responding
independently to the same functional requirements. Since fore and hind limbs do not
trace back to the same structure in the vertebrate ancestor, then they cannot be
homologous, according to Lankester. The Darwinian criterion stretches one’s
credibility when one thinks of structures repeated through the body: ‘If we admit the
homology between any scale x of an individual trout and any scale, say y of a salmon,
and between this scale y in the salmon and scale z in the trout, then how can we
logically deny that homology exists between scales x and z on the body of the same
trout!’ (Hubbs, 1944: 294). Consider structures repeated across the axis of the body.
Common sense tells us that our left hand is the mirror image of our right. Darwin
would have us believe that left and right hands trace back to a single structure in a
one-sided animal! Reductio ad absurdum.
The Darwinian approach assumes we have atomic parts that are passed on from
generation to generation: ‘In the simplest case phylogenetic homology is a one-to-one
mapping from the characters of one species onto characters of another species. A
one-to-one mapping implies that in each species all characters can be recognised
individually’ (Wagner, 1989b: 57). However, a living thing is not a composite of
inert atoms. Its loosely coupled organisation emerges from a dynamic interplay
between conflicting tendencies: ‘Every holon has the dual tendency to preserve and
assert its individuality as a quasi-autonomous whole; and to function as an integrated
part of an (existing or evolving) larger whole. This polarity between the self-assertive
and integrative tendencies is inherent in the concept of hierarchic order; and a
universal characteristic of life. The self-assertive tendencies are the dynamic
expression of holon wholeness, the integrative tendencies of its partness’ (Koestler,
The distinctiveness of an element, the fact that we can recognise its identity across
numerous organisms, derives from its wholeness, the tendency of a holon to assert
itself. If an element cannot be recognised individually, this lack of distinctiveness
emphasises the partness of the holon, its tendency to integrate itself among other
elements as part of a larger whole, such as a series. We may understand serial
homology in this light: ‘The phenomenon of serial resemblance is in fact an
expression of the capacity of repeated parts to vary similarly and simultaneously. In
proportion as in their variations such parts retain this capacity the relationship is
preserved, and in proportion as it is lost, and the parts begin to vary independently,
exhibiting differentiation, the relationship is set aside’ (Bateson, 1894: 569). When
elements of a series vary similarly and simultaneously they cannot be recognised as
distinct. They remain parts integrated into the larger whole, the series. When
elements differentiate, they become individually recognisable and thus assert
themselves as wholes distinct in themselves. The first element in the vertebral series
asserted itself, weakening its integration into the rest of the series, and became
individualised as the axis in tetrapods. Whether an element appears as a part or a
whole depends on the broader context.
All teleost fishes have a recognisable palatine bone, in the context of the
palatopterygoquadrate arch, but vary in the extent to which parts of the palatine are
developed. Hence, we can describe a number of states of the palatine bone, recording
differences in the shape and orientation of the boss and prong, for example. States
within a character represent divergent differentiations of parts within the context of
whole. A character representing the presence or absence of the palatine describes the
expression or suppression of the self-assertive tendency of the holon, the acquisition
or loss of its individuality. For example, the prootic and epiotic of reptiles lost their
separate individualities and fused to form the mammalian petrosal, which then in its
turn has followed its own path of differentiation.
A good example of where members of a series have individualised is the thorax of
insects (Wagner, 1986: 151; 1989a: 1162; 1989b: 63). The thorax most probably
arose as a differentiation of segments 7, 8 and 9 in the annelid-like ancestors of
insects. However, the thorax as an entity in itself is not homologous to the
corresponding segments in centipedes, which have remained closer to the annelid
form. ‘The thorax is the unit differentiated from the rest of the body in terms of
appendages and internal anatomy, a condition not found in centipedes’ (Wagner,
1986: 151; 1989a: 1162; 1989b: 63). There is no direct homologue with the thorax in
the segments of the centipedes—we cannot establish a one-to-one mapping. The
thorax represents a new condition of form, a new autonomous whole, which serves to
“individuate” the taxon Insecta (in the sense of von Baer, 1828; see Rieppel, 1994:
Nelson (1989) suggests that instead of taxa being seen as groups of units, such as
species or organisms, they should be seen as relationships. A taxon is a relationship
inherited by organisms, and a homology, then, is a relationship inherited by parts of
organisms. ‘Conceived as relationships, taxa and homologies do not literally descend
from one another. Taxa come into being with organisms that literally descend’
(Nelson, 1989: 281). A taxon is not a group of organisms tracing back to an ancestral
organism, but a type, a relationship inherited by organisms. Homology is not the
tracing back of structures to an ancestral structure, but a relationship inherited by parts
of organisms. Taxa are relationships and have homologies for their parts (Nelson,
1989: 279). Nelson’s view is much closer to the spirit of Geoffroy Saint-Hilaire.
Homology is not the conservation of material structures among descendant lineages,
but rather the conservation of positional relationships within the developmental
process: ‘… systematics and comparative anatomy … are possible only to the extent
that ontogeny is orderly … the concept of evolution is an extrapolation, or
interpretation, of the orderliness of ontogeny.’ (Nelson, 1978: 336).
The four laws of von Baer affirm the orderliness of the developmental process (von
Baer, 1828: 224; modified from the translation in Gould, 1977: 56):
1. The general features of a broad animal type appear earlier in the embryo than
the special features.