Table Of ContentOTHER TITLES IN THE SERIES ON PURE AND
APPLIED BIOLOGY
ZOOLOGY DIVISION
Vol. I. RAVEN -- An Outline of Developmental Physiology
Vol. 2. RAVEN -- Morphogenesis: The analysis of Molluscan
Development
Vol. 3· SAVORY -- Instinctive Living
Vol. 4· KERKUT -- Implications of Evolution
Vol. 5- TARTAR -- The Biology of Stentor
Vol. 6. JENKIN -- Animal Hormones—A Comparative Survey
Vol. 7· CORLISS -- The Ciliated Protozoa
Vol. 8. GEORGE -— The Brain as a Computer
Vol. 9· ARTHUR -— Ticks and Disease
Vol. II. MANN -— Leeches (Hirudinea)
BIOCHEMISTRY DIVISION
Vol. i. PITT-RIVERS and TATA — The Thyroid Hormones
Vol. 2. BUSH — The Chromatography of Steroids
Vol. 3. ENGEL — Physical Properties of Steroid Hormones
BOTANY DIVISION
Vol. 1. BOR — Grasses of Burma, Ceylon, India and Pakistan
Vol. 2. TURRILL — Vistas in Botany
Vol. 3. SCHULTES — Native Orchids of Trinidad and Tobago
Vol. 4. C00KE — Cork and the Cork Tree
MODERN TRENDS
IN PHYSIOLOGICAL SCIENCES DIVISION
Vol. 1. FLORKIN — Unity and Diversity in Biochemistry
Vol. 2. BRÄCHET — The Biochemistry of Development
Vol. 3. GEREBTZOFF — Cholinesterases
Vol. 4. BROUHA — Physiology in Industry
Vol. 5. BACQ and ALEXANDER — Fundamentals of Radiobiology
Vol. 6. FLORKIN (Ed.) — Aspects of the Origin of Life
Vol. 7. HOLLAENDER (Ed.) — Radiation Protection and Recovery
Vol. 8. KAYSER — The Physiology of Natural Hibernation
Vol. 9. FRANÇON — Progress in Microscopy
Vol. 10. CHARLIER — Coronary Vasodilators
Vol. 11. GROSS — Oncogenic Viruses
Vol. 12. MERCER — Keratin and Keratinization
Vol. 13. HEATH — Organophosphorus Poisons
Vol. 14. CHANTRENNE — The Biosynthesis of Proteins
Vol. 15. RIVERA — Cilia, Ciliated Epithelium and Ciliary Activity
Vol. 16. ENSELME — Unsaturated Fatty Acids in Atherosclerosis
PLANT PHYSIOLOGY DIVISION
Vol. 1. SUTCLIFFE — Mineral Salts Absorption in Plants
Vol. 2. SIEGEL — The Plant Cell Wall
OOGENESIS:
The storage of
developmental information
by
Chr. P. RAVEN
Professor of Zoology in the
University of Utrecht
PERGAMON PRESS
OXFORD · LONDON · NEW YORK · PARIS
1961
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1961
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CHAPTER I
EMBRYONIC DEVELOPMENT AS A
COMMUNICATION PROBLEM
1.1. Development and order
LIVING organisms can be characterized as systems in which the
elementary parts and processes are arranged in an orderly
temporospatial pattern. The adult animal forms a complicated
whole of organs and tissues, each of which has its own place in the
organism, and its own characteristic, orderly structure. Together
they form an integrated system of a very high degree of multi
plicity, which remains more or less constant in time notwith
standing continuous changes in material composition.
If we trace the history of the organism backwards through time,
however, we see that it has evolved, during embryonic develop
ment, from an initial stage, the fertilized egg, which has a most
simple shape, and exhibits hardly any visible structure. Apparently
the ordered spatial multiplicity of the adult organism has only
arisen during its ontogenetic development.
The question, "from what this order has sprung", lies at the
root of all speculations and investigations which have been
devoted to the problems of development.
It seems to me that all those who have speculated or experi
mented on embryonic development, from early times have been
guided by a deep-rooted prescientific intuitive conviction.
Apparently it is very difficult for the human mind to conceive of
ordered multiplicity arising "by itself " out of disorder, though the
reverse process, disorder arising out of order, seems a natural one.
This conception of the asymmetric relation between order and
disorder has led in the nineteenth century in physics to the various
formulations of the second law of thermodynamics. That it
existed as a more general and intuitive conviction long before that,
however, even without being clearly expressed as such, is shown
by the apparent role it has played in shaping the theories on
animal development.
1
2 EMBRYONIC DEVELOPMENT
One can consider the first general theory of development, the
preformation theory of the seventeenth and eighteenth centuries, as
a consistent application of this "asymmetry principle" to the
phenomena of development. The increase in ordered spatial
multiplicity during ontogenetic development, obvious as it may
seem to the unprejudiced eye, was flatly denied, because it was
incompatible with this principle. All considerations and arguments,
with which the theory was exemplified, were adduced secondarily
in vindication of this intuitive certainty. If no new-formation of
ordered spatial multiplicity during development is permitted, it
must have existed from the beginning. For those who pursued the
theory to its final consequences, the adherents to the doctrine of
emboîtement, this meant the beginning of all things, Creation.
The theory of preformation in its original form, with its denial
of all actual development, in the eighteenth and early nineteenth
century did not hold out against the ever-increasing load of
conflicting evidence, and gradually had to give way to the opposite
theory of epigenesis. The evidence of direct observation, made
possible by the gradual improvement of optical equipment, clearly
pointed to an actual increase in ordered structure during develop
ment, starting from the structureless egg and ending in the
complicated pattern of the adult organism. But the supporters of
the theory of epigenesis immediately found themselves confronted
with the asymmetry principle. If order arises during development
in an originally unordered system, where does it come from?
Only one answer seemed possible: when order cannot arise "by
itself" out of disorder, it has to be created by an ordering agent.
This explains why the rise of the epigenesis theory went hand in
hand with a revival of vitalistic thinking in biology, and all
adherents to this theory were at the same time vitalists (cf. Driesch,
1905). It is the vis essentialis (C. Fr. Wolff), the Bildungstrieb
(Blumenbach), equipped with a prescience of the end to be
reached, which moulds the unformed matter of the germ into the
ordered structure of the adult organism.
The old controversy springs up again towards the end of the
nineteenth century. Again, the adherents of mechanicism in
biology, on the strength of the asymmetry principle, were com
pelled to deny the possibility of an actual increase in ordered
multiplicity. In W. Roux' theory of neo-evolution, the "mosaic
DEVELOPMENT AND ORDER 3
theory" of development, it is no more the embryo as such which is
present in the egg, but each part of the future animal is repre
sented by a corresponding part of the egg, and each part of the egg
can only give rise to a certain part of the animal, so that there is a
one-one relation between the parts of egg and adult, and both have
the same degree of ordered multiplicity. In Aug. Weismann's
Keimplasma theory, it is the three-dimensional architecture of the
id, contained in the nucleus of the fertilized egg, which adumbrates
the adult animal's ordered multiplicity.
The refutation of the Roux-Weismann doctrine by Driesch's
experiments on sea urchins led this author to the acceptance of the
opposite theory of (neo-)epigenesis. It is hardly surprising, but, in
the light of the above, can rather be seen as a historical necessity,
that this was attended with his conversion to vitalism.
Since the days of Roux and Driesch, research in experimental
embryology has yielded a rich harvest of facts. It may be said that
it has decided substantially in favour of an epigenetic view of
development. It is generally conceded now that the structure of
the fertilized egg, at least in by far most groups of animals, is very
simple, that it contains no counterpart of the complicated structure
of the adult animal, and that this structure therefore is only
gradually built up during development. Hence, a real increase in
spatial multiplicity during ontogenetic development seems irre
futable.
On the other hand, the number of those biologists who have
followed Driesch in his theoretical deductions leading to the
doctrine of vitalism, and are willing to accept the introduction of
a more or less metaphysical "vital force", intervening as an
ordering agent in the processes of development, is only very small.
In consequence of this situation, theoretical biology sees itself
placed before a dilemma which at first sight appears unsolvable.
On the one hand, a real increase in ordered spatial multiplicity
during development seems undeniable; on the other hand, the
existence of an ordering agent, creating order out of disorder, is
rejected. On the strength of the intuitive certainty which lies at
the base of the asymmetry principle, science is once more con
fronted with the age-old question: where does the order come
from?
A new approach to the solution of this problem might be gained
4 EMBRYONIC DEVELOPMENT
by the application of the concepts of information theory to the
problems of development.
1. 2. Information
Information theory has proceeded from communication en
gineering. It is based on the conception that information is
measurable. The term information is not used here in its meaning
of everyday language, but as a measure of the amount of know
ledge which a message of some sort ideally can convey.
A good introduction to information theory is given by Quastler
(1958a). I will mention here only some points which are im
portant in connexion with our further considerations.
In a communication system, messages are transmitted, as
signals through a communication channel, from a transmitter to a
receiver. The signals are not identical with the message they carry,
but they represent it symbolically. To this end, the message must
be translated into the system of signals {encoded) at the side of the
transmitter, and translated back {decoded) at the side of the re
ceiver. The clearest example of this is found in telegraphy, where
the letters, in which the message is written, are encoded in the
dots and dashes of the Morse code, transmitted by alternating
closing and breaking of the electric circuit, and decoded at the
receiver end. In telephony, the encoding and decoding is done by
the apparatus itself which translates the sound vibrations into
variations of the electric current, and inversely. Similar relation
ships can be shown to hold in all cases, where messages are trans
mitted from a source to a destination.
In these translations of messages from one system of represen
tation into another, in the ideal case, certain properties of the
message are truly preserved throughout all transformations, quite
independently of the actual content of the message. These general
properties are indicated by the term "information". Information
is a measurable abstract quantity. Its value does not depend on
what the message is about.
Every message consists of an ordered system of signs. If it is
transmitted without loss from a transmitter to a receiver, the order
(or pattern) which existed among the elements at the transmitter
will be represented in the arrangement of elements on the side of
the receiver. Hence, it is the pattern as such which is transmitted.
INFORMATION 5
This order in the arrangement of the elements is essential for
its information content. The information carried by an event is
only positive when the arrangement of its elements deviates from
a random distribution. The more it deviates, hence the more
improbable the system is and the greater its "orderliness", the
more information it carries. Hence, information is a measure for
the degree of orderliness of a system. There is a close relationship
between the concepts of information and entropy ; if one chooses
the right units, the two are equal in amount, but have opposite
signs. Therefore, information may also be called negentropy. It
follows that the amount of information in a closed system cannot
increase ; it can at best be preserved, and it is likely to diminish.
The order, hence the information of a system, is always endangered
by the prevailing unrest or disorder. For instance, in the trans
mission of a message information may be lost by random dis
turbances in the communication channel. The effects of such
random disturbances are indicated by the general term noise.
In order to counteract the loss of information in a noisy channel,
and to increase the reliability in the transmission of a message,
one may give extra or redundant information, e.g. when an S.O.S.
message is broadcasted repeatedly. In general, the greater the
noise, the more redundant information must be given, in order to
obtain the same degree of reliability. Thereby the total information
transmitted increases, but nothing new is added to the contents of
the message. The total information diminished by the redundant
information will be called the effective information transmitted.
Information is measured in binary units or bits. A bit may
somewhat roughly be defined as the information contained in the
answer to a question that can only be answered by "yes" or "no"
(or, positive-negative, black-white, etc.). If x is a system with
categories i and the associated probabilities p(i)> then the informa
tion content of x> H{x) expressed in bits, is given by
y
H(x) = -E/>(t)lo />(*).
ga
ί
In the simple case, where all probabilities p(i) are equal, this
reduces to
H(x) = -\og p
2
6 EMBRYONIC DEVELOPMENT
or, if there are r equiprobable categories, since p = -,
H(x) = log r.
2
It has been shown that the concept of information, outside the
domain of communication engineering, can be applied fruitfully
in various other branches of science, where the representation and
transmission of order forms a critical problem. Especially in
biology, where the idea of order lies at the root of all teleology,
the application of information theory may become very important
(cf. Raven, 1960).
1. 3. Developmental information
If one considers the relationship between the generations of
living organisms, connected by sexual reproduction, in which the
ordered structure of the parents is repeated in their offspring, it
is clear that we have to do with a typical example of transmission
of information. In such a communication system the sex cells,
and the fertilized egg cell produced by their union, are parts of
the communication channel; the parents are the source, the
individual arising from the egg is the destination of the informa
tion transmitted.
Quite generally, it can be stated that the germ at the beginning
of development, in order to be able to realize its inherent pattern
of development, must be provided with the necessary information
to do so. In other words : the ordered structure, the pattern of the
fertilized egg cell, must be such that it faithfully "represents" the
pattern of the organism which develops from the egg.
This statement needs some qualification, however. It is clear
that not all particulars of the adult organism need be represented
in the egg from which it develops ; this holds especially for those
which are acquired by individual experience. In general terms, it
can be said that all animals are able, at least during part of their
period of development, to take up information from the environ
ment. This is most evident in those animals in which the egg
develops rapidly into a free-living larva, which is adapted to a
particular environment, in which it lives and from which it derives
its food. But the same holds e.g. in mammals, where the developing
DEVELOPMENTAL INFORMATION 7
embryo is provided with matter and energy by the maternal
organism. The nearest approach to a "closed" communication
system is formed by those cases, where the developing animal is
surrounded by a tight shell, which permits hardly any exchanges
with the environment, as for example in the development of the
bird's egg from laying till hatching. But even here the uptake of
information, e.g. by the perception of the direction of gravity, is
not entirely excluded.
On the other hand, it must be taken into account that those
particulars of the structure of the adult organism which are mainly
due to influences of the environment, are in general not the ones
in which developmental biology is most interested. This science
deals mainly with the complex of structural details which may be
considered as species-specific, or, more generally, as "hereditary".
Though it is evident that the development of these hereditary
characters is only possible in a special environment and, moreover,
that there is no sharp distinction between "hereditary" and "non-
hereditary" characters, so that the environmental factors have
always to be taken into account for a full understanding of
development, on the other hand experimental embryology has
taught us that these factors hardly ever play a decisive role in the
determination of the essential traits of the structural pattern of the
embryo.
All information measures are, by their very nature, relative ones ;
in their application, one has to decide as to what features of the
events studied are to be considered as relevant (cf. Quastler,
1958a,b). When applying information theory to animal develop
ment it seems advisable, at least at a first approach, to leave the
acquired individual characters of the organisms out of considera
tion, and to concentrate upon the problem of the realization of
their species-specific patterns. Moreover, the problem may perhaps
be further restricted by excluding growth in its purely quantitative
aspects, hence as a mere augmentation of living matter. Since,
however, certain elements of the pattern are dependent for their
realization upon a sufficient size of the system as a whole, and,
moreover, differential (allometric) growth may be a factor in the
establishment of species-specific and organ-specific shapes, it will
not be easy here to draw a sharp line. On the other hand, in so
doing one has the advantage that, under these conditions, a great
