Abstract
In this paper we review and argue for the relevance of the concept of open-ended evolution in biological theory. Defining it as a process in which a set of chemical systems bring about an unlimited variety of equivalent systems that are not subject to any pre-determined upper bound of organizational complexity, we explain why only a special type of self-constructing, autonomous systems can actually implement it. We further argue that this capacity derives from the ‘dynamic decoupling’ (in its minimal or most basic sense: the phenotype–genotype decoupling) by means of which a radically new way of material organization (minimal living organization) is achieved, allowing for the long-term sustenance of systems whose individual-metabolic and collective-historical pathways become thereafter deeply intertwined.
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Notes
In the case of development, understood as «a process whereby a relatively unspecified system comprised of loosely connected lower level parts becomes organized into a coherent, higher-level agency» (Coffman 2006), one could interpret that there is also some sort of ‘evolutionary pathway’, with an overall increase in the complexity of the system, but this would be restricted to an individual organism and its lifetime. The problem is really much more complicated, because development is, in fact, tightly linked to evolution, in that wider and more common, biological sense of the term. Nevertheless, here we will not deal with it: we will focus on the actual conditions for the origin of evolution as a long-term process of change (that takes place in a population of historically related systems), before proper developmental systems appeared.
The terms ‘full-fledged living being’ and ‘infrabiological system’ are here used to make the distinction between living systems as we know them and certain (hypothetical) ones with a significantly lower degree of complexity (see also (Szathmary et al. 2005)). Some of us have discussed more extensively the criteria to define life elsewhere (Ruiz-Mirazo et al. 2004), which would mainly cover metabolic (‘autonomous’) and Darwinian (‘open-ended’) evolution capacities. These are very demanding conditions, so in the process of origins of life (or any artificial reconstruction of it) there must necessarily be systems below the threshold. In our account open-ended evolution will be the last condition for prebiotic systems to become proper living ones, so the beginning of open-ended evolution would be equivalent to the end of the process of origins of life.
Our use of the term ‘mechanism’ (following (Bechtel 2005)) is not reductionist: i.e., it is not restricted to local and deterministic molecular devices, but includes more global and emergent organizational principles.
The term ‘functional’ will be used in this paper in a very broad sense, to describe an action of a part of a system/organization (or a relation between different parts of that system/organization) that contributes to its global self-maintenance (Moreno et al. 1994).
We will distinguish the terms ‘replication’ and ‘reproduction’ following Dyson (1985), Fleischaker (1994) and Luisi (1994): i.e., restricting the use of replication for the ‘copying’ of a specific molecular structure in which sequence is conserved, and taking ‘reproduction’ as a more general term (close to the idea of multiplication) that can be applied to global organizations. This distinction is not widely spread yet, although more and more researchers are becoming aware of its importance (see, e.g.: (Szathmáry and Maynard Smith 1997; Griesemer 2000; Szathmáry 2006)).
In other words, we hold the view that, even if sex or conscious intelligence had never arisen (given different circumstances from the ones life has endured on Earth), the type of evolutionary pathway followed by living organisms (also assuming that these remained unicellular) would still be fully open-ended.
So our approach does not exclude the possibility that, previous to the appearance of a process of open-ended evolution, there were other types of ‘selective dynamics’ among the members of a population of reproducing and interacting systems. On the contrary, it demands that there actually were. However, we do not agree with authors that tend to consider all of these dynamics as ground for natural selection processes ((Maynard Smith 1986; Szathmáry 2000)). If the mechanism of diversification is just the arbitrary variation of any component/set of components of the system, if multiplication simply takes place by autocatalytic growth and statistical division, if heredity can only be understood as a kind of ‘compositional invariance’ through generations (Segré et al. 2000), or if the fitness function (selection criterion) is defined as a mere physical parameter of each system (e.g., energetic efficiency), without including somehow the relationship/interactions with other systems in the population and with the environment, we consider that such ‘selective dynamics’ is quite far from Darwin’s original idea of evolution by natural selection.
In the context of this article we have in mind complex chemical systems, like self-bounded reaction networks, but a more illustrative example to grasp this idea (that more constraints do not always involve a more reduced dynamic space) consists in the following: a comparison between the complexity of the pieces (components) and rules (dynamic constraints) of chess and draughts, with regard to the richness of the game they can respectively generate on the same board (general physico-chemical scenario).
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Acknowledgements
Kepa Ruiz-Mirazo carried out this research work thanks to a post-doctoral fellowship from the Basque Government and became a Ramon y Cajal fellow in the course of it. Jon Umerez was also a Ramon y Cajal fellow during most of the time required for the elaboration of the article. We thank the editor, Kim Sterelny, and an anonymous reviewer for useful criticism on previous versions of this manuscript. We would also like to acknowledge financial help from research grants 9/UPV 00003.230-15840/2004, HUM2005-02449 and BMC2003-06957.
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Glossary (of specific chemical terms)
Glossary (of specific chemical terms)
Work (thermodynamic definition): any form of energy that, unlike heat, can be kept and used by a system without dispersion.
Exergonic process: A process defined by a decrease in the system’s Gibbs free energy (ΔG < 0, at constant pressure and temperature), so it is thermodynamically spontaneous. This involves the release of energy, originally in the form of work, to the surroundings.
Endergonic process: A process defined by an increase in the system’s Gibbs free energy (ΔG > 0, at constant pressure and temperature), so it is thermodynamically non-spontaneous. This involves the absorption of energy, in the form of work, from the surroundings.
Endergonic–exergonic coupling: the coming together (in time and space) of two processes, one endergonic and one exergonic, so that the former (non-spontaneous in normal circumstances) takes place at the expense of the latter. The release of energy associated to the exergonic process is, thus, constrained, so that it is absorbed by the endergonic one, leading to an overall production of work.
Supramolecular chemistry: term that refers to the area of chemistry which focuses on the non-covalent bonding interactions of molecules (hydrogen bonds, metal coordination, hydrophobic forces, van der Waals forces, pi–pi interactions, electrostatic effects to assemble molecules into multimolecular complexes,…).
Multimers/Oligomers: molecular chains that consist of a finite number of monomer units (a few—up to 10/more than a few—up to 100)
Polymers: molecular chains that consist of a large (unbounded) number of monomer units (more than 100)
Stereochemistry: a sub-discipline of chemistry that involves the study of the relative spatial arrangement of atoms within molecules, including the case of chiral molecules (particularly relevant in biochemistry).
Active site: small pocket on the surface of an enzyme where catalysis actually occurs. The structure and chemical properties of the active site allow the recognition and binding of the substrate(s).
Chemical affinity: tendency of an atom or compound to combine by chemical reaction with atoms or compounds of unlike composition.
Energetic degeneracy: situation in which the different arrangements of the parts within a system are equi-probable, due to the fact that their corresponding energy levels are the same.
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Ruiz-Mirazo, K., Umerez, J. & Moreno, A. Enabling conditions for ‘open-ended evolution’. Biol Philos 23, 67–85 (2008). https://doi.org/10.1007/s10539-007-9076-8
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DOI: https://doi.org/10.1007/s10539-007-9076-8