Biosemiotics (2008) 1:361377

DOI 10.1007/s12304-008-9027-z

Understanding the Emergence of Cellular Organization

Walter Riofrio

Received: 20 November 2007 / Accepted: 04 July 2008 /

Published online: 10 September 2008
# Springer Science + Business Media B.V. 2008

Abstract More than one researcher is currently proposing that the notion of
information become an important element for defining living systems as well as for
explaining conditions that make their origins possible. During the pre-biotic era, the
type of compounds encountered would mainly have been very simple in nature and
might have been immersed in the natural dynamic of the physical world and in
processes of self-organization. It is furthermore quite possible that they formed a
relationship between and among certain types of processes that here we are
specifically proposing as central for the emergence of cell organization. Consequently, an important initial step towards constructing a theory of biological information is
to ask ourselves the question: how do biological systems process information? In this
way, we will be contributing to the proposals of this paper where we seek to identify
general principles that govern biological computing and that deal with biosemiotic
approaches as they are defended in naturalistic normative terms.
Keywords Biological computing . Bio-meaning information . Evolvability .
Informational dynamic systems . Naturalistic normative emergence .
Small-world phenomenon

The study of the twin processes of communication and signification can be

regarded as ultimately a branch of the life science, or as belonging in large part
to nature, in some part to culture, which is, of course, also a part of nature.
(Sebeok 1991, p. 22)
W. Riofrio
Complex Thought Institute Edgar Morin, University Ricardo Palma, Lima, Peru
W. Riofrio (*)
Peruvian University Cayetano Heredia, Lima, Peru
e-mail: walter.riofrio@iscpif.fr
W. Riofrio
Complex Systems Institute (ISC-PIF), Paris, France

362

W. Riofrio

The life science and the sign science thus mutually imply one another.
(Sebeok 1994, p. 114)

Introduction
How does one approach the causes that produced the initial stages of cellular
organization? For such a purpose, in this paper we will be following a line of
reasoning which has begun to receive recognition as a new means of shedding light
on this issue: the nature of signs and information in living systems. There is a
growing conviction concerning the emerging role of information as a fundamental
building block in physics and other sciences, and leading researches in these fields
claim that information it is not just a construct of the mind but a fundamental
element of the physical world (Lloyd 2000, 2006; Seife 2006; von Baeyer 2005).
It is our line of reasoning that the nature of biological information does not stop at
the mere idea of genetic information but is rooted in the foundations of biological
phenomena; thus, we need to look into the question of how living systems gather
information about their environment and respond adequately to it.
We shall organize the article as follows:

Preliminaries shall present some conceptual aspects about autonomous agents

and the difficulties in explaining their emergence by means of the dynamics of
classical self-organizing systems.
Signs, Molecular Networks and Information shall demonstrate the need to
improve biosemiotic studies from a naturalistic point of view. Doing thus, we
may reach an adequate understanding of the existing relationships between
signs, information, meaning, and a network of molecular compounds.
The Dynamics of Bio-information shall discuss the nature and dynamics of
biological information viewed from a theoretical proposal that we have
developed to study the origins of the pre-biotic world, connected with the
emergence of certain properties related to evolution at that period.
Lastly, Biosemiotics and Biological Computation shall be a brief overview of
some of the implications derived from studies discussed in the preceding
sections and our proposal for future research that connects biosemiotics with the
evolution of biological systems from the perspective of the theory of
computation.

Preliminaries
In the past few decades, the debate regarding the origin of life has focused on the
controversy between which came first: RNA or metabolism. The most well-known
proposals, in terms of the origin of life, have to do with behaviours (and properties)
of nucleic acids, proteins, and lipids (Eigen and Schuster 1979; Gilbert 1986; Segr
et al. 2001; Szathmry and Demeter 1987).
Wchtershuser proposed an alternative to one of these scenarios. His surface
metabolism theory contains two main axioms: (1) the energy source for life is a

Understanding the emergence of cellular organization

363

pyrite formation of H2S and FeS and (2) an archaic reductive citric acid cycle is put
into the centre of a metabolic network (Wchtershauser 1988). Nevertheless, there
are shortcomings in this concept; for instance, it fails to explain how raw materials
are supplied to the reductive citric acid cycle.
We can visualize the dilemma between the RNA first or metabolism first
scenario from Eigens (1971) proposal, which identifies the relationship between
biological information and biological function as a sort of chickenegg quandary.
We now understand that this question moves beyond a mere historical problem. Yet,
before we inquire which came first, it is more important that we ask ourselves which
one of them could have given rise to pre-biotic evolutionary processes. At present,
we recognize that the solution for the aforementioned dilemma must necessarily pass
through the stage of understanding the notion of biological information (Wills 1994)
and of designing a definition of functions in naturalistic terms (Collier 2000).
There are still other interesting approaches to the dilemma of the origin of life,
like the chemoton concept, which searches for the minimum components that
encompass the most basic forms of life. This chemical supersystem comprises three
subsystems: a metabolic network, template replication, and a boundary system
(Szathmry et al. 2005). Gnti (2003) introduced the chemoton model in 1971 as a
fundamental unit model of living systems.
It is our contention, though, that the passage from the inanimate world to the
animate world needs a transition phase: the dynamics of the pre-biotic world. As a
consequence, we should ask ourselves what the essential properties are for
determining and characterizing the organizational dynamic of living systems.
We know that biological systems are self-organized and self-reproducing, and, in
this context, we also understand that the self-organizational dynamic of these
systems is composed of many levels and types of processes that are interconnected
and interdependent (Fontana and Buss 1994; Furusawa and Kaneko 2002). One of
the most characteristic global properties of biological systems is that which enables
the behaviour of an autonomous agent with respect to its environment (Kauffman
2000, pp. 4979).
An autonomous agent, as defined by Kauffman, is a system capable of
reproducing itself and carrying out one or more thermodynamic work cycles
(Kauffman 2000, p. 53). This relational definition connects the notion of work with
the concept of constraint (Kauffman 2000, p. 97). In another paper, Kauffman further
develops the notion of autonomous agent. In this definition, we see the autonomous
component as well as the agent component such that the capacity to reproduce itself is
connected with both aspects. According to Kauffman, in this hypothetical autonomous
agent, the DNA hexamer is able to behave as an enzyme that links the two trimers, thus
forming a copy of the initial hexamer. This reaction is coupled to the exergonic
breakdown of pyrophosphate (PP) to two monophosphates, P+P. The characteristic ratio
at equilibrium between hexamers and trimers is not achievable because of this kind of
chemical motor, the PP P + P reaction cycle; this exergonic breakdown is used to
drive endergonic excess synthesis of the hexamer (Kauffman 2003).
As Kauffman says, ...The system eats trimers and photons, and...Pumps that
energy into the excess synthesis of hexamer... The system only works if displaced
from chemical equilibrium...towards an excess of trimers and photons. Agency only
exists in systems displaced from equilibrium... (Kauffman 2003, p. 1093).

364

W. Riofrio

We now accept that autonomy is one of the most important global properties in
living systems. Nevertheless, the question about how it emerges from the dynamics
of self-organization of simple molecular compounds still remains unanswered.
From the thermodynamic point of view, the dissipative structures are open
systems (they exchange energy and/or matter with their environment), and the selforganization phenomena are produced due to the continuous changes in the local
interactions of the components that form the dynamic system (Nicolis and Prigogine
1977). But if we take, for example, the BelouzovZhabotinskii (BZ) reaction,
which is an oscillating, autocatalytic chemical reaction (Strogatz 1994), we are
unable to see in it similarities to the kind of self-organizing dynamics that we
encounter in living systems. In other words, living systems are self-organizing
systems with properties that go far beyond the common phenomena of selforganization. We propose that these properties could have been formedcould have
emergedat the beginning of the transition from the inanimate to the animate.

Signs, Molecular Networks and Information

One of the major and most interesting problems in this issue is the move from the
inanimate to the animate, the mechanics of which we must ask ourselves about. It
continues to be a question which confronts and puzzles the different approximations
(Barabsi and Oltvai 2004; Maturana and Varela 1973; Quastler 1964). At this point
of the discussion, the claim coming from new researches (the growing community of
biosemioticians) looks valid, when they state, with Pattee, that life is distinguished
from the nonliving world by its dependence on signs. (Pattee 2005, p. 299)
Biosemiotics is a new discipline which combines approaches from such diverse
fields as semiotics, linguistics, biology, philosophy, systems theory, theory of
science, physics and information theory with the ultimate goal of successfully
investigating the rule-governed, sign-mediated interactions within and between cells,
tissues, organs, and organisms (Barbieri 2007; Hoffmeyer 1997; Krampen 1981; von
Uexkll et al. 1993).
If, in the realm of the living, different kinds of interactions are mediated by signs,
which are themselves governed by certain rules, then we need to find out how the
production of codes, signals, or signs is related to the emergence of the rules that
govern that production, explained in natural terms.
The naturalizing aspects of biosemiotic approaches must be clearly stated. It
follows, then, that the intent to deal with the aforementioned problem within this
framework would only use a naturalistic account. In other words, we need to avoid
extrapolations coming from the human world, like ascriptional interpretations or
epiphenomenal ones.
In agreement with Bickhards (2004) proposals, we are confident that normative
emergence is necessary for any naturalistic account of biology. We have a working
hypothesis framed in a process metaphysics which is a naturalized normative
account of the basic emerging properties of life, and, at the same time, it is also a
proposal in biosemiotics. In our hypothesis, we defend the emergent nature of
normative information and normative function and, with these, the emergent
normative nature of autonomy (Riofrio 2007, pp. 241244). In the following

Understanding the emergence of cellular organization

365

sections, we will discuss certain consequences of our working hypothesis applied to

some problems in biosemiotics that are connected with studies on the appearance of
cellular organization.
Signs and Information
What is the nature of a sign? There are many challenges that we must surmount in
order to develop an account of the nature of signs that could be seen from a
naturalized perspective (Hoffmeyer 1996; Pattee 1995; Sebeok 1991, 1994). In order
to do so, we will study this problem within a process metaphysics, and our guiding
principles shall be 1) natural existence is best understood in terms of processes
rather than things and 2) time and change are among the fundamental features of
our physical reality.
Consequently, we accept neither the existence of something like signs as things nor
the existence of signs in and of themselves. If there are such things as signs in reality,
then they would have much to do with the existence of certain processes; they would be
connected with natural relationships developed inside certain spatialtemporal
dynamic interactions; such a proposal is very similar to the approach of Peirce (1868).
What we are putting forward is not just the relationships between living systems
and their environments, but also the relationships that exist inside a living system. In
the physical world, certain matterenergy variations, for instance electromagnetic
fluctuations, do not convey a sign of any kind that would have meaning for, say, a
rock. Notwithstanding, the same electromagnetic fluctuation produces some type of
response in living systemsit conveys some signsand it is the carrier of some
potential type of information to them. But still we must ask ourselves why?
It seems appropriate, in a naturalistic approach, to connect the matterenergy
variations with the possible emergence of signs. If a sign is not a thing but a product
of certain relationships, then its nature will depend on the type of relationship in which
it is involved. In other words, signs will be formedwill emerge, so to speakwhen
certain relationships take place. We propose, therefore, that the emergence of signs is
linked to the emergence of a kind of phenomenon which has, within itself, an
interconnected network of molecular processes that are mainly made up of chemical
compounds. We wish to say that signs, signals, and codes essentially belong to the
world of the living, not only to the world of the human.
In the case of information, we propose the following: information emerges in
the biological world as information with meaning or meaningful information. To
be exact, it emerges as information with biological meaning or what we like to call
bio-meaning.
Like signs, information is also a relational notion, and as such it will depend on
processes, specifically biological processes. Information will always be meaningful
information for biological systems.
Our line of reasoning follows from the fact that whatever kind of energy variation
may occur in a biological system, it will only turn into a sign (it will become
potential information for the system) when the system has the capability to react
accordingly. And this happens when the energy variation impacts something in the
system and is incorporated into the systemas a variationwith the capacity of
becoming part of the systems processes.

366

W. Riofrio

If an energy variation does not have the capacity to be incorporated in the form of
a variation (any kind of variation) in the system, then it is not a sign for the system,
and, as a consequence, the system cannot develop a response. This is the form in
which signs emerge from physical reality.
Biological Information and Meaning
At this point in the paper, it is important that we relate our ideas to certain recent
developments that are taking place within the discussion on biological information.
In order to establish the main features of our contribution to the debate, we will do a
brief comparisoncontrast with other works (Jablonka 2002; Kauffman et al. 2008;
Maynard 2000).
One important common aspect is expressed by Jablonka: ...There is nothing
necessary in a particular aspect of the environment acting as information...
(Jablonka 2002, p. 586). First, we agree that signs and biological information are
relational notions. Secondly, it is necessary to identify the connection involving
information, evolution, and living systems.
Other authors address this last point from an evolutionary perspective, with
arguments stating that information is strongly connected to natural selection.
Maynard Smith, for instance, contends that the most important characteristic of
biological information is that it is designed by natural selection and, in this sense,
is intentional (Maynard 2000, pp. 189190). It should be noted that this proposal is
a function-related notion of biological information, mainly focused on genetic
information. For Maynard Smith, the notion of biological information is intimately
linked to the idea that the signal carrying the information and the response to it are
both products of natural selection. Moreover, his claim for the notion of design
makes a connection between natural selection, information, and function that is very
similar to Millikans (1984) proper function.
Jablonka also uses the notions of design and intentionality (Jablonka 2002,
p. 588). Her goal was to widen the notion of biological information developed by
Maynard Smith, by not limiting it to just genetic information but also addressing
other types of biological information (e.g., epigenetic information). She maintains
that the system receiving the information must be an interpretive system (Jablonka
2002, p. 602). The notion of function in Jablonkas work is similar to Kitchers
(1993) general design-based notion.
Kauffman et al. (2008) have recently published a paper on this topic. First, they
have proposed that the Shannon theory is powerful but limited in scope; in particular,
Shannons information cannot describe the information contained in a living organism.
So they introduced the notion of the relativity of information and showed that the
concept of information depends on the context of where and how it is being used.
Finally, they examined the link between information and organization, showing that
these two are intimately associated in biotic systems (Kauffman et al. 2008).
Compared to the interesting proposals outlined above, our approach to biological
information through an evolutionary perspective need not be related to any specific
ontology which involves design or intentional notions, or to any kind of interpretive
sub-system inside the receiver system. We are interested in the basic properties of
life and the way they initially emerged, generating the conditions that allow a kind of

Understanding the emergence of cellular organization

367

dynamic self-organizationthose that contain simple chemical components, as well

as a minimal set of processes that is sufficiently robust to suggest that it could be the
direct ancestor of biological systems.
If we accept the statement that ...more than 3 billion years ago, there were no genes at
all... a lot of evolution must have happened between the protocellular and the bacterial
phases of evolutionary history... (Szathmry et al. 2005, pp.169170), then we can
choose from among different reasonable alternatives in order to attempt an explanation
of the great amount of evolutionary activity that took place in those times.
Focusing our quest on the initial systems in pre-biotic times, we ask ourselves
what kind of necessity imposed natural selection and precluded the use of other
reliable mechanisms of evolutionary change. We need to be aware that there have
been times when we would hardly be able to find a molecule remotely resembling
DNA, RNA, or even proteins. It is not fitting, therefore, to claim that evolution by
natural selection was the evolutionary form involved in the adaptive changes of the
different systems that appeared in those early times. Thus, it is feasible to propose
that in the dawn of the pre-biotic epoch there would have been a different type of
evolution that subsequently introduced evolution by natural selection. We may look
at those times as being the first step in the transition from the inanimate to the
animate (more on this in The Dynamics of Bio-information).
Now, if it is true that evolution at the beginnings of pre-biotic times did not
involve natural selection, then the initial emergence of biological information and
biological function was not connected with that mechanism. We could understand
the ways these systems evolved and adapted in their environments without the need
to use the notions of design and intentionality, even in ascriptional terms.
The more we identify the mechanisms of evolutionary change in the first forms of
pre-biotic systems, the greater our understanding would be of the elements that are
necessary for expanding the evolutionary theory. We agree with Kauffman and with
Jablonka about the powerful but limited scope of the Shannon theory for adequately
addressing all the different kinds of information existing in living systems. Now, let
us examine some of the approaches taken by other contributors to this issue,
approaches that are important for us because they focus on the relations between
biological information and meaning.
Information-with-Meaning
So, we come to the problem of trying to perform a conceptual analysis that will
allow us to understand how bio-meaning emerged in the physical reality, yet in
naturalistic normative terms.
To start with, we shall discuss the ideas proposed by Menant (2003) and El-Hani
et al. (2006). We agree with these researchers and assert that information in
biological systems is information with meaning.
In his work, Menant provides us a systemic approach to the generation of
meaning. Meaningful information is defined as the connection that exists between
the information received by a system and the constraints of that system (Menant
2003, p. 197). Here we see that Menant is concerned with understanding the
definition of meaning; his proposal, like ours, is that there is no way of removing the
notion of meaning from meaningful information.

368

W. Riofrio

A simple organism (like a paramecium) has the capacity to do certain things to

face environmental changes. When confronted with an acid environment, for
example, the paramecium triggers different kinds of internal mechanisms that put a
distance between itself and the environment (Menant 2003, p. 196).
In such a systemic approach, the generation of meaning by a system is directly
linked to maintaining its nature within its environment by satisfying the constraints.
Meaning is therefore meaningful relative to the constraints of the system. We quite
agree with this understanding on the connection that links information, meaning, and
system. Nevertheless, we do consider other points, like proposing the nature of the
vital constraint, the specific dynamics between the system and its environment
such that the incident information could be recognized and transmitted to some
degree inside the system. Also, there are ways in which we could understand the
exact forms that meaningful information could participate in the response developed
by the system. Some of the most important aspects of these questions are addressed
in this paper.
In the case of El-Hani et al., there is a connection between the emergence of
semiosis, a Peircean approach in which they perceive that gene expression is
regulated by processes that involve signalling, and the communicative processes that
take place between cells or entities at a higher level in organisms. In this work, the
researchers attempt to describe the exact nature of genetic information as a result of a
biosemiotic process of interpretation (El-Hani et al. 2006, p. 46).
We aim to move further and seek answers to questions like: could this special
semiotic interrelationship between processes have emerged in naturalistic terms, and,
if so, what would the driving forces have been? As well, could this model explain
the transmission-failure of genetic information, and does there exist (at least in
principle) an explanation of genetic diseases?
El-Hani et al. do not say much about the evolution of semiosis up to this point.
But their thesis is that the establishment of surfaces that distinguish external from
internal media in cell-like systems was the main driving force, at the origins of life, for
cells to become semiotic systems. We can see in these inquiries a new understanding of
the role played by information in living systems and, overall, the recognition of the
importance of taking into account the semantic nature of organisms.
What is Bio-meaning?
Now that we have reviewed a few of the other pertinent theories on the matter, let us
focus on our proposal. In our approach, we claim that information is one of the three
fundamental properties of living systems, the other two being function and
autonomy. Rather, biological information reveals itself physically as information
with meaning or, as we describe it, information with biological meaning. Such
meaning does not depend on human adscription or interpretations, and is referred to
as bio-meaning.
We propose to introduce the notion of Informational Dynamic System (IDS).
This type of system would constitute the ancestor system that opened the door to the
pre-biotic world. So, Informational Dynamic Systems already have in their
organization those basic properties that are present in all living systems and are
expressed at increasing levels of complexity as we move forward in evolution.

Understanding the emergence of cellular organization

369

We see IDS as a type of Complex Dynamic Adaptive System. Thus, since we

propose that information emerges simultaneously with function in an integrated and
interrelated network of molecular processes, we now have a related mechanism that
enables us to detect information flow (Riofrio 2007, p. 241 and 243).
Our conceptual model is likewise a biosemiotic proposal, where bio-meaning
would emerge somewhere inside the system to the same degree in which it has some
type of impact on the system cohesion as a whole (Riofrio 2007, p. 244). Therefore,
the kind of self-organization in our IDS is a sustained and robust Informational and
Functional Dynamic Organization (Riofrio 2007, p. 243).
Before finishing this section, we would like to point out our approach on functions. As
we are adopting a systemic approach to functions, our proposals are in agreement with
most of the arguments proposed by Cummins (1975) and Christensen and Bickhard
(2002). Moreover, we could say that the normative nature of functions can be
successfully treated by different perspectives other than design. We believe that the
causal properties that identify a system in naturalistic terms can be found in connection
with Colliers notion of cohesion (Christensen and Bickhard 2002, p. 16).
It must be made clear that our IDS is made up of simple molecular compounds
related to each other by interconnected processes. The relationships between them
produce dynamic processes of transformation and maintenance, given that they are
interdependent. If cohesion is a concept that integrates the totality of these processes
and their interrelationships, then there is no reason against adopting this notion to
address the underlying causes that characterize the identity of the IDS.
In this way, we could claim that something is a function when a certain group of
molecular actions manage to maintain the most basic state of the IDS, i.e., the far
from thermodynamic equilibrium state. If this does not happen and there is a
reduction of the far-from-equilibrium state, then we can consistently affirm that that
something is dysfunctional. As we can see, the normative nature of functions is a
relational concept because the collection of actions produced by a process is a
function only when these actions have their raison dtre in the concert of
interdependent connections that make up the system.
Molecular Networks and Information
This special type of self-organization could have come into existence only because
there were three pre-existing sets of processes, two of which act as different system
constrictions (Kauffman 2000; Pattee 1972).
The first constriction is the spontaneous self-organization of a simple, amphiphilic
protoplasmic membrane, which mimics, at least qualitatively, some of the basic
processes displayed by the current plasma membranes (Segr et al. 2001). This set of
processes permits a dynamic interaction with its external and internal environment: a
semi-selective membrane that contains the compounds that would generate the
processes to give the system the capacity to manage both external and internal
conditions. In it we can see the emergence of an agential behaviour with respect to
its external and internal milieu (energy capture, control of concentration gradients by
active transport, among others).
The second constriction we shall call the basic constriction as it directly
maintains the IDS in the far from thermodynamic equilibrium state. It is a cycle

370

W. Riofrio

between the endergonic processes linked with the exergonic ones and with the added
capacity of generating work, a necessary and sufficient condition to produce the
organizational dynamic phenomena (Kauffman 2000). It is important to highlight
that both types of constrictions are so interrelated that a very basic, direct
communication exists between them.
Finally, there is one more set of processes that makes up the dynamic identity of
an IDS system. This third group is a network of reactions involved in regeneration,
maintenance, and reproduction processes and is, in one way or another, connected to
the constrictions. An IDS is therefore organized by the interdependence of the above
three sets of processes, and we know that a correlation among processes is to be
expected whenever a system is in a far from thermodynamic equilibrium state
(Kosztin and Schulten 2004; Levine 2005).
The basic constriction in our conceptual model is the most important step towards
the origins of the pre-biotic world. The correlation between endergonic and
exergonic processes could have significantly benefited from the existence of
compounds with high energy bonds, forming in this way a micro-cycle that is
capable of generating work (chemical work). Inorganic pyrophosphate and/or a
simple thioester could have been the ancestral energy currency molecules of these
types of chemical bonds. It was de Duve who proposed the thioester world, which
represents a ...hypothetical early stage in the development of life that could have
provided the energetic and catalytic framework of the protometabolic set of primitive
chemical reactions that led from the first building blocks of life to the RNA world
and subsequently sustained the RNA world until metabolism took over... (de Duve
1995, p. 436 and further developed in his last book, de Duve 2005, pp. 5465).
The interesting point here is that the thioester bond is what biochemists call a
high-energy bond, equivalent to the phosphate bonds in adenosine triphosphate
(ATP). In current cells, we find that thioesters are bound up with the esters
formation, including those that exist in complex lipids. We also find them actively
participating in the synthesis of peptides, fatty acids, sterols, terpenes, porphyrins,
and others. This underlines the feasibility of maintaining an adequate exchange of
energy between the exergonicendergonic cycle and the production of compounds
(doing chemical work) that have much to do with the formation (and regeneration)
of a proto-membrane.
We now see how signs turn into meaningful information (bio-meaning). If a
matterenergy variation becomes incorporated in the form of a variation somewhere
inside the system, then it will turn into a sign for the system. Once inside the system,
if this sign has an effect on its cohesion, in one way or another, then it will become
meaningful information for the system. Cohesion is the idea that gives the IDS its
identity in all its transformations through time (Collier 1986, 2004).

The Dynamics of Bio-information

Our proposal rests upon the naturalistic supposition that the IDS is different from
other self-organizing systems because it is able to develop and maintain a capacity
for remaining in, or even for increasing, the far from thermodynamic equilibrium
state, an essential condition for its existence.

Understanding the emergence of cellular organization

371

It is because of the basic constriction that we postulate the emergence of information and function in the local interactions among the processes in the integrated
molecular network that makes up the IDS. As we said above, information and function
emerge at the same time in the IDS, and the physical emergence of both characteristics
takes place in such an interrelated way that it has two aspects: an informational
function aspect and a functional information aspect (Riofrio 2007, p. 241).
This is the reason why we said that, from the beginning of the emergence of the IDS,
the information flow could be detected by the occurrences of mechanisms that are related
to the execution of some function inside the dynamic organization of these systems.
It is reasonable to postulate that the compounds encountered during the pre-biotic
era would have mostly been very simple in nature, and might have been immersed in
the natural dynamic of the physical world and in phenomena of self-organization.
Therefore, it is quite possible that they would have formed a relationship among the
three types of processes that we have proposed, and the IDS allows us to understand
the emergence of the global property known as autonomy.
First, the basic constriction is fundamental for providing the system with a certain
degree of independence with respect to its environment since it generates the
conditions for being in the far from thermodynamic equilibrium state, that is, the
endergonicexergonic cycle capable of producingin each cyclequantities of free
energy in the system that are appropriate to generate work (of a fundamentally
chemical type). In other words, being a system in the far from thermodynamic
equilibrium state is an intrinsic priority to the system, and, because of that, it is the
basic, most fundamental aspect of the IDS.
The second constriction gives another important contribution to the dynamic
organization of these systems, since it is involved in the making up of the
protoplasmic membrane. This structure creates a separation, a physical barrier,
between the system and its environment, thus producing a different distribution of
compounds, a different dynamic, and a different interaction among the processes.
The protoplasmic membrane is the place where we are objectively able to observe
the emergence of autonomy. It is the part of the system that regulates the interaction
with its environment in conditions compatible with its survival. And it is this kind of
protoplasmic membrane that made it possible for systems from their very beginning
in pre-biotic times to be evolvable.
We talk about evolvability when we can observe a phenotypic variation that is
susceptible to being a target of natural selection or, in other words, when an
organism has the capacity to generate an inheritable phenotypic variation (Altenberg
1994; Conrad 1990; Dawkins 1989; Kirschner and Gerhart 1998). Notwithstanding,
the term evolvability has been defined and used in different ways; it is a
sophisticated, new concept that is solidly grounded in empirical data (Colegrave
and Collins 2008).
It is believed that evolvability depends on biological phenomena, such as the
degree of modularity of developmental systems (Callebaut and Rasskin-Gutman
2005), as well as on their robustness vis--vis perturbation (Lenski et al. 2006;
Wagner 2005). Perhaps the most profound usage of evolvability is related with the
ability to generate novel variation or to acquire novel functions (Wagner 2005).
In order to be able to grasp the most important connections between evolvability
and evolutionary innovations that occurred at the beginnings of the pre-biotic era, we

372

W. Riofrio

should ask if a pre-biotic system could be evolvable in terms of generating novel

variations through the acquisition of new functions.
The ability to innovate (and then to evolve) in the IDS is due to its sustained
and robust intrinsic dynamic self-organization. Because this system has the capacity
to stay in a far from thermodynamic equilibrium state by itself, within its dynamic
self-organization, we could hypothesize that its innovative potential cannot be
governed other than by its cohesive dynamic way of existing.
Once these systems are confronted by a specific, environmentally-generated
problem, the different possible solutions (strategies), produced in the systems
protoplasmic membrane as a product of the reproduction of these systems, are
nothing more than the maintenance of the integrity of their dynamic organization,
i.e., the maintenance of the close interrelation between the three kinds of processes
that would result in the physical expression of information, function, and autonomy
at every moment and in each type of pre-biotic system. In other words, the system
evolved by overcoming environmentally-generated problems through different ways
of preserving the basic properties which characterized it.
The components of a system could be changed but, as a whole, the systems
descendants would tend to preserve their most fundamental properties that are
compatible with their survival in conditions, and their far from the thermodynamic
equilibrium state. This sort of pre-biotic inheritance must have been associated
with evolvability rather than with a Darwinian type of evolution.
As a result of these arguments, it seems feasible to propose the idea that the basis
of hereditary similarity in pre-biotic evolution depended on the way cell-like
systems were embedded in their environments rather than on internal gene-like
mechanisms. We also suggest that evolution is happening at small-time scales, i.e.,
that it is virtually continuous, since it is the membrane that makes the cell evolvable.
As we are proposing a dynamic adaptive system, it is important to discover whether
or not the IDS is sufficiently robust to be capable of adaptive reproductive behaviours.
In other words, the origins of heredity could be better understood if we consider a prebiotic origin of heredity, a kind of heredity without DNA or any similar molecule.
It was Waddington who, in the 1940s, coined the term epigenetics mainly
related to the study of genes and the dynamics involved in the production of
phenotypes (Waddington 1968). Today, epigenetics had grown into a widely
recognized subdiscipline of biology (Holliday 1994; Lederberg 2001; Mller
2007). Although many problems remain in this field, its great practical significance
has been acknowledged (Jablonka and Lamb 2002). One of the interesting results is
that the epigenetic approach probes the influences of the environment on
development, demonstrating that the same genotype can produce strikingly different
phenotypes in response to altered external conditions (West-Eberhard 2003).
In the first stages of pre-biotic times, systems increased their robustness in the
presence of perturbations to perpetuate their self-organization in each reproductive
cycle. This is the resultant picture of our conceptual construct because we consider
that each time the system passed through reproductive cycles, the components
produced were not exactly the same as the original ones, but properties and
processes remained unchanged.
With a perspective on heredity other than that which causes the statistical
correlation in phenotype between ancestor and offspring, we could say that heredity

Understanding the emergence of cellular organization

373

has two main features: (1) a control property and (2) a preservation property
(Kaneko and Yomo 2002).
The control property is distributed in the interdependence between the networks
of processes so that the systems cohesion towards the far from the thermodynamic
equilibrium is maintained by the intertwined correlation between biological
functions and bio-meaning. The preservation property, on the other hand, is about
preserving not so much the chemical structure of the molecules as the interrelation
between the three kinds of processes that make up the dynamic self-organization of
the IDS.
It is the environment that created conditions that were influencingbut not
determiningthe specific self-organization of the protocells. Faced with an
environment filled with materials that could be used to build systems from scratch,
the IDS would have developed ways to construct a network of processes that were
maintaining the characteristic self-organization of Informational Dynamic Systems
and their offspring.
This ancient epigenetic form of heredity was the origin of heredity as we know it
and has more in common with Lamarckian evolution than any other type (Jablonka
and Lamb 1995). In a more recent work on Lamarckian evolution, the researchers
argue that there is more to heredity than genes; for instance, some hereditary
variations are nonrandom in origin, while some acquired information is inherited
(Jablonka and Lamb 2005). Moreover, Jablonka and her co-author have pointed out
ideas that extend heritable, adaptive changes beyond natural selection to include the
action of evolved internal systems that generate nonrandom alternatives in
response to environmental challenges (Jablonka and Lamb 2005, p. 361).
All in all, this sets the stage for our next working hypothesis, which is a new
interpretation of Lamarckian evolution that could shed light on the transition from
random to nonrandom processes in biology.

Biosemiotics and Biological Computation

In this last part of our proposal, we briefly present certain implications that our
argument has on biosemiotics and on the evolution of biological systems from the
perspective of the theory of computation. Also, we would like to propose some
possible future areas of research as a consequence of it.
Some years ago, famous evolutionary researchers pointed out that several major
transitions occurred during evolution in the way that genetic information is
organized and transmitted from one generation to the next, and went as far as to
propose that if there were entities with the capacity to replicate independently before
any of these great transitions, afterwards they would be able to replicate only as part
of a larger whole (Maynard and Szathmry 1998).
Likewise, we state that the way in which bio-meaning was organized and
transmitted in hierarchically structured networks during pre-biotic and biological
evolution is on the list of the major evolutionary transitions that occurred from the
dawn of pre-biotic times onwards.
As Lloyd says: ...the amount of information that a physical system can store and
process is related to the number of distinct physical states that are accessible to the

374

W. Riofrio

system (Lloyd 2000, p. 1049). In the same spirit, we ask the following questions: 1)
exactly how much meaningful information, or bio-meaning, can a living system
store? 2) to what extent it is possible to know this? 3) what kind of states could be
related with the amount of meaningful information or bio-meaning? These are
difficult questions to answer, and further research is needed to determine if there is a
causal relationship or correlation between the possible variables/states and the
amount of bio-meaning.
Moving to another theme, we often find that biological systems function through
decentralized control mechanisms in which the systems numerous subunitsthe
molecules of a cell, the cells of an organism, or the organisms of a groupadjust
their activities by themselves on the basis of limited, local information. It happens
without guidance from an external controller or even from an internal control centre.
The way in which biological systems behave, grasping a hold of any information
close at hand, compels us to hypothesize that a situation like meaningful biological
computation could exist.
Put in a different way, suppose that biological systems possess computational
abilities (Badre and Wagner 2006; Hopfield 1982). Then we would be required to
ask the following question: are there general principles governing natural-biological
computing? As we know, small-world structures have emerged spontaneously in the
biological realm. An important associated research topic, then, is how this could
have happened (Gong and van Leeuwen 2003, 2004). Small-world networks have
interesting potential as models for interacting structures in complex systems (Amaral
et al. 2000; Strogatz 2001; Watts and Strogatz 1998).
Our conceptual modeltranslated into a formal onemay be used to help us
understand the formation of the structured networks in some real systems with
dynamic units. One of our future research objectives is to find certain criteria that
will help us clarify the possible ways in which meaningful biological computation
may emerge in the physical universe. In this way, we will be contributing to the
discussion that seeks to reveal general principles governing biological computing.
Another objective is to uncover a possible way of explaining the emergence of
small world phenomena (Duchon et al. 2006; Kleinberg 2000)containing, among
other elements, scale-free characteristics and evolutionary capacitieswithin the
dynamic of simple physical phenomena (simple molecular compounds
interconnected to the three types of processes of our IDS conceptual model). It
would also be interesting to find out how could have emerged a sort of relative
reference point that enabled the development of something to be greedy about on
the routing paths of the biological small-world (Fraigniaud 2005). It seems to us that
our input to this discussion might point us in a new direction, aside from DNA
computation, for understanding emergence, robustness, resilience, scalability, and
evolution of living systems from the perspective of the theory of computation.

Conclusion
How can meaning be related to information? Are they two separate things? What
kind of things are they? Are they, after all, even remotely like things? In this
paper, we proposein a context of process metaphysicsthat information arises in

Understanding the emergence of cellular organization

375

the physical world as information-with-biological-meaning or bio-meaning. In

this way, information is always meaningful information for the biological system.
Our approach considers the underlining features that separate biological and prebiotic systems from other kinds of dynamic systems that make sense of information
in function and function of information and, with these, attempts to understand the
emergence of autonomy as a global system property.
An interesting contribution of our study is the proposal that functions in a system
are such that they cause the system to maintain the far from equilibrium state
(informational function), and a physical sign is expressed in agreement (or
disagreement) with maintaining the far from equilibrium state.
Our approach is an evolutionary theory of semantics. In the growing field of
biosemiotics, researchers are attempting to use semiotic concepts (mainly in the
tradition of Pierce) to answer questions on the production and the interpretation of
signs that are hardly answered in a purely mechanistic and physicalistic framework.
In such a approach, semiotics embraces semantics as this is concerned with the
meaning of signs.
Accordingly, we propose that biosemiotics embraces biosemantics since this is
concerned with the evolutionary emergence of meaning in life. Our proposal is
an evolutionary theory of semantics where meaning first emerged in the form of
bio-meaning.
We claim that signs in biological systems (and in pre-biotic systems as well) are
related to matterenergy transformations as they are incorporated into the system as
variations. In turn, these variations become biological informationalways with
bio-meaningbecause they impact cohesion, maintaining, increasing or even
decreasing the far from thermodynamic equilibrium state. And finally, bio-meaning
is followed by a response from the specific type of biotic or pre-biotic system.
From its initial emergence in the physical world, we can hypothesize that biomeaning has the ability of increasing its levels of complexity and sophistication all
the way up to the human world. Meaning and biological information were connected
at their very beginning, and this bond conditioned the evolution of both notions well
into the abstract levels of human culture.
We also propose that the inheritance mechanisms of the primitive systems were
distributed in the informationalfunctional networks of the processes that made up
their organization. This ancient epigenetic heredity is closer to certain aspects of
Lamarckian evolution than others, and we suspect that the transition from random to
nonrandom processes in biology is better understood within a more profound
comprehension of Lamarckian-like evolutionary implications on the transmission of
biological information. Finally, our proposal could give us a naturalistic account of
biosemiotics and explain its connections with biological computing.

References
Altenberg, L. (1994). The evolution of evolvability in genetic programming. In K. Kinnear (Ed.) Advances
in genetic programming (pp. 4774). MIT.
Amaral, L. A. N., Scala, A., Barthlmy, M., & Stanley, H. E. (2000). Classes of small-world networks.
Proceedings of the National Academy of Science of the United States of America, 97, 11149.

376

W. Riofrio

Badre, D., & Wagner, A. D. (2006). Computational and neurobiological mechanisms underlying cognitive
flexibility. Proceedings of the National Academy of Science of the United States of America, 103(18),
71867191.
Barabsi, A. L., & Oltvai, Z. N. (2004). Network biology: understanding the cells functional organization.
Nature Reviews Genetics, 5, 101113.
Barbieri, M. (Ed.) (2007). Introduction to biosemiotics. The new biological synthesis. Dordrecht: Springer.
Bickhard, M. H. (2004). Part II: applications of process-based theories: process and emergence: normative
function and representation. AxiomathesAn International Journal in Ontology and Cognitive
Systems, 14(1), 121155.
Callebaut, W. & Rasskin-Gutman, D. (Eds.) (2005). Modularity: Understanding the development and
evolution of natural complex systems. Cambridge, MA: MIT.
Christensen, W. D., & Bickhard, M. H. (2002). The process dynamics of normative function. Monist, 85(1), 328.
Colegrave, N., & Collins, S. (2008). Experimental evolution: experimental evolution and evolvability.
Heredity. doi:10.1038/sj.hdy.6801095.
Collier, J. (1986). Entropy in evolution. Biology and Philosophy, 1, 524.
Collier, J. (2000). Autonomy and process closure as the basis for functionality. In J. L. R., Chandler, & G.
van de Vijver (Eds.), Closure: Emergent organizations and their dynamics. Annals of the New York
Academy of Science, 901, pp. 280290.
Collier, J. (2004). Self-organization, individuation and identity. Revue Internationale de Philosophie, 59,
151172.
Conrad, M. (1990). The geometry of evolution. Biosystems, 24, 6181.
Cummins, R. (1975). Functional analysis. Journal of Philosophy, 72, 741765.
Dawkins, R. (1989). The evolution of evolvability. In C. Langton (Ed.) Artificial life. Addison Wesley.
de Duve, C. (1995). The beginnings of life on earth. American Scientist, SeptemberOctober, 428437.
de Duve, C. (2005). Singularities: Landmarks on the Pathways of Life. Cambridge University Press.
Duchon, Ph., Hanusse, N., Lebhar, E., & Schabanel, N. (2006). Towards small world emergence. Proceedings
of SPAA, 18th ACM Symposium on Parallelism in Algorithms and Architectures, pp 225232.
Eigen, M., & Schuster, P. (1979). The hypercycle: A principle of natural self-organization. Berlin:
Springer-Verlag.
Eigen, M. (1971). Self organization of matter and the evolution of biological macro molecules.
Naturwissenschaften, 58, 465523.
El-Hani, C. N., Queiroz, J., & Emmeche, C. (2006). A semiotic analysis of the genetic information system.
Semiotica, 160, 168.
Fontana, W., & Buss, L. W. (1994). The arrival of the fittest: toward a theory of biological organization.
Bulletin of Mathematical Biology, 56, 164.
Fraigniaud, P. (2005). Greedy routing in tree-decomposed graphs: a new perspective on the small-world
phenomenon. Proceedings of the 13th European Symposium on Algorithms, pp. 791802.
Furusawa, C., & Kaneko, K. (2002). Origin of multicellular organisms as an inevitable consequence of
dynamical systems. Anatomical Record, 268, 327342.
Gnti, T. (2003). Chemoton theory. Berlin: Springer.
Gilbert, W. (1986). The RNA world. Nature, 319, 618.
Gong, P., & van Leeuwen, C. (2003). Emergence of scale-free network with chaotic units. Physica A, 321,
679688.
Gong, P., & van Leeuwen, C. (2004). Evolution to a small-world network with chaotic units. Europhysics
Letters, 67(2), 328333.
Hoffmeyer, J. (1996). Signs of meaning in the universe. Bloomington: Indiana University Press.
Hoffmeyer, J. (1997). Biosemiotics: towards a new synthesis in biology. European Journal for Semiotic
Studies, 9(2), 355376.
Holliday, R. (1994). Epigenetics: an overview. Developmental genetics, 15, 453457.
Hopfield, J. J. (1982). Neural networks and physical systems with emergent collective computational abilities.
Proceedings of the National Academy of Science of the United States of America, 79(8), 25542558.
Jablonka, E., & Lamb, M. J. (2002). The changing concept of epigenetics. Annals of the New York
Academy of Sciences, 981, 8296.
Jablonka, E., & Lamb, M. J. (1995). Epigenetic inheritance and evolution: The Lamarckian dimension.
Oxford: Oxford University Press.
Jablonka, E., & Lamb, M. J. (2005). Evolution in four dimensions: Genetic, epigenetic, behavioral, and
symbolic variation in the history of life. Cambridge, MA: MIT.
Jablonka, E. (2002). Information: its interpretation, its inheritance, and its sharing. Philosophy of Science,
69, 578605.

Understanding the emergence of cellular organization

377

Kaneko, K., & Yomo, T. (2002). On a kinetic origin of heredity: minority control in a replicating system
with mutually catalytic molecules. Journal of theoretical biology, 214, 563576.
Kauffman, S. (2000). Investigations. Oxford University Press.
Kauffman, S. (2003). Molecular autonomous agents. Philos T Roy Soc A, 361, 10891099.
Kauffman, S., Logan, R. K., Este, R., Goebel, R., Hobill, D., & Shmulevich, I. (2008). Propagating
organization: an enquiry. Biology and Philosophy, 23(1), 2745.
Kirschner, M., & Gerhart, J. (1998). Evolvability. Proceedings of the National Academy of Science of the
United States of America, 95, 84208427.
Kitcher, P. S. (1993). Function and design. Midwest Studies in Philosophy, 18, 379397.
Kleinberg, J. M. (2000). Navigation in a small world. Nature, 406, 845.
Kosztin, I., & Schulten, K. (2004). Fluctuation-driven molecular transport through an asymmetric
membrane channel. Physical Review Letters, 93, 238102.
Krampen, M. (1981). Phytosemiotics. Semiotica, 36(3/4), 187209.
Lederberg, J. (2001). The meaning of epigenetics. The Scientist, Sept. 17, 6.
Lenski, R. E., Barrick, J. E., & Ofria, C. (2006). Balancing robustness and evolvability. PLoS Biol, 4,
21902192.
Levine, R. D. (2005). Molecular reaction dynamics. Cambridge University Press.
Lloyd, S. (2000). Ultimate physical limits to computation. Nature, 406, 10471054.
Lloyd, S. (2006). Programming the universe. Knopf.
Maturana, H., & Varela, F. (1973). Autopoiesis: The organization of the living. Reidel.
Maynard Smith, J., & Szathmry, E. (1998). The major transitions in evolution. Oxford University Press.
Maynard Smith, J. (2000). The concept of information in biology. Philosophy of Science, 67, 177194.
Menant, C. (2003). Information and meaning. Entropy, 5(2), 193204.
Millikan, R. G. (1984). Language, thought and other biological categories. Cambridge, MA: MIT.
Mller, G. B. (2007). Evodevo: extending the evolutionary synthesis. Nature Reviews Genetics, 8, 943
949.
Nicolis, G., & Prigogine, I. (1977). Self-organization in non-equilibrium systems. New York: Wiley.
Pattee, H. H. (1972). Laws and constraints, symbols and languages. In C. H. Waddington (Ed.) Towards a
theoretical Biology 4, Essays. Edinburgh University Press, pp. 248258.
Pattee, H. H. (1995). Evolving self-reference: matter, symbols, and semantic closure. Communication and
CognitionArtificial Intelligence, 12(12), 928.
Pattee, H. H. (2005). The physics and metaphysics of biosemiotics. Journal of Biosemiotics, 1, 281301.
Peirce, C. S. (1868). On a new list of categories. Proceedings of the American Academy of Arts and
Sciences, 7, 287298 Eprint: http://www.cspeirce.com/menu/library/bycsp/newlist/nl-frame.htm.
Quastler, H. (1964). The emergence of biological organization. Yale University Press.
Riofrio, W. (2007). Informational dynamic systems: Autonomy, information, function. In C. Gershenson,
D. Aerts, & B. Edmonds (Eds.), Worldviews, science, and us: Philosophy and complexity (pp. 232
249). Singapore: World Scientific.
Sebeok, T. A. (1991). A sign is just a sign. Bloomington: Indiana University Press.
Sebeok, T. A. (1994). Signs: An introduction to semiotics. Toronto: University of Toronto Press.
Segr, D., Ben-Eli, D., Deamer, D. W., & Lancet, D. (2001). The lipid world. Origins of Life and
Evolution of the Biosphere, 31, 119145.
Seife, C. (2006). Decoding the universe. Penguin Books.
Strogatz, S. H. (1994). Nonlinear dynamics and chaos. Westview.
Strogatz, S. H. (2001). Exploring complex networks. Nature, 410, 268.
Szathmry, E., & Demeter, L. (1987). Group selection of early replicators and the origin of life. Journal of
Theoretical Biology, 128, 463486.
Szathmry, E., Santos, M., & Fernando, C. (2005). Evolutionary potential and requirements for minimal
protocells. Topics in Current Chemistry, 259, 167211.
von Baeyer, H. C. (2005). Information: The new language of science. Harvard University Press.
von Uexkll, T., & Geigges, H. J. M. (1993). Endosemiosis. Semiotica, 96(1/2), 551.
Wchtershauser, G. (1988). Before enzymes and templates: theory of surface metabolism. Microbiological
Reviews, 52, 452484.
Waddington, C. H. (1968). The basic ideas of biology. In C. H. Waddington (Ed.), Towards a theoretical
biology, vol. 1, Prolegomena, 132. Edinburgh: Edinburgh University Press.
Wagner, A. (2005). Robustness, evolvability, and neutrality. FEBS letters, 579, 17721778.
Watts, D. J., & Strogatz, S. H. (1998). Collective dynamics of small-world networks. Nature, 393, 440.
West-Eberhard, M. J. (2003). Developmental plasticity and evolution. Oxford: Oxford University Press.
Wills, P. R. (1994). Does information acquire meaning naturally. Ber Bunsen Phys Chem, 98, 11291134.