Life as a process of open-ended becoming: Analysis of a minimal model

We argue that the phenomenon of life is best understood as a process of open-ended becoming and that this potentiality for continuous change is expressed over a variety of timescales, in particular in the form of metabolism, behavior, development, and evolution. We make use of a minimal synthetic approach that attempts to model this potentiality of life in terms of simpler dissipative structures, using reaction-diffusion systems to produce models that exhibit these characteristics. An analysis of the models shows that its structures exhibit some instances of relevant changes, but we do not consider them open-ended enough to be called alive. Still, the models shed light on current debates about the origins of life, especially by highlighting the potential role of motility in metabolism-first evolution. Introduction – The standard view In the field of synthetic biology there is a widespread optimism that the creation of an entire living cell from scratch is imminent (e.g. Zimmer, 2009; Deamer, 2005; Szostak, et al. 2001). It is hoped that this bio-engineering approach will help to resolve one of the outstanding mysteries of science, namely the origin of life on earth. The mainstream consensus is that the crucial element in the transition from non-living to living matter is the appearance of evolution. Many of the researchers in the field of artificial life, who are studying the origin of life, also share this guiding idea. Their work is thus focused on the question of how best to simulate or chemically engineer the emergence of self-replicating structures (e.g. Rasmussen, et al. 2004; Solé, 2009). Within this general direction of research we can distinguish two relatively distinct traditions in terms of whether they assume the replication of information or the replication of metabolism to be the first factor in evolution. The information-first (a.k.a. ‘replicator-first’) view of life claims that there was genetic evolution right at the start of life itself. An extreme version of this view is known as the “RNA world”, which holds that “the first stage of evolution proceeds [...] by RNA molecules performing the catalytic activities necessary to assemble themselves from a nucleotide soup” (Gilbert, 1986, p. 618). However, it is now recognized that this RNA-only view is incomplete, and that the appearance of 1 We call the ‘replicator-first’ tradition ‘information-first’ here in to avoid the misleading impression that the ‘metabolism-first’ tradition does not involve replication. The core of the dispute is not about replication versus emergence as such, but rather about what kind of replication was primary, namely informational versus metabolic or compositional. Darwinian evolution also requires the compartmentalization of replicating nucleic acids to ensure the segregation of genomes from one another. The field has therefore turned toward the task of incorporating suitable information-carrying molecules into the right kind of vesicle in a way that ensures the reproduction of both (e.g. Hanzcyc, et al. 2003), and in a way that allows for competition and differential success (e.g. Chen, et al. 2004). On this updated information-first view, the role of metabolism in the origin of the first living cell is at most a secondary aspect, and perhaps even completely absent. Rather, the essence of life consists of only two components: “fundamentally, a cell consists of a genome, which carries information, and a membrane, which separates the genome from the external environment” (Chen, 2006: 1558). The metabolism-first view of life, on the other hand, claims that the main driving force at the origin of life was epigenetic evolution. A radical version of this view holds that the origin of life coincided with the emergence of autocatalytic systems (e.g. Kauffman, 1986), and that under certain conditions some selective pressures could have already been effective at this chemical level (e.g. Fernando and Rowe, 2007; MeléndezHevia, et al. 2008). It has also been claimed that “Darwinian competitive exclusion is rooted in the chemical competitive exclusion of metabolism” (Morowitz and Smith, 2007: 58), and that metabolism has played a bigger role than replication in making novelties appear in evolution (Pulselli, et al. 2009). Similar to the updated information-first view, many of the metabolism-first researchers also argue for the essential role of some kind of spatial separation. It is said that autocatalysis by itself is not sufficient for life, and that these processes must necessarily be part of the constitution of a spatially localized individual (Maturana and Varela, 1980). Some researchers have gone further in claiming that the network of autocatalytic processes must necessarily be enclosed within a bounding membrane (e.g. Luisi and Varela, 1989). Modeling studies along these lines have tended to assume that a physical membrane is essential, because it prevents the autocatalytic processes from diffusing into the environment (e.g. Bourgine and Stewart, 2004; Varela, et al. 1974), and allows the regulation of molecular intake (e.g. Bitbol and Luisi, 2004). Research in prebiotic chemistry has shown that it is possible to engineer the emergence of membrane-bounded micelles that provide the autocatalysis for their own replication (e.g. Walde, et al. 1994; Bachmann, et al. 1992; see also the model by Ono and Ikegami, 2000). In addition, recent models have demonstrated that under some conditions the growth and division of membrane-bounded autocatalytic systems can lead to differential replicative success (e.g. Ono, 2005; Ono, et al. 2008). On this view, which is sometimes identified with the “autopoietic” approach (e.g. Maturana and Varela, 1980; Varela, et al. 1974), the essence of life consists in a membrane-bounded, self-producing system. It is important to notice that, although the two mainstream traditions may differ in emphasis, they do not hold mutually exclusive theories about the essence of life. In fact, they both accept the general claim that a biological individual is defined by the physical boundary that is imposed by its membrane, although they have different primary reasons for doing so (i.e. unit of selection versus unit of self-production). And they also both accept that life is essentially about stability and survival, and that the driving force of instability and biological change is primarily located outside of the individual, in the external environment and in evolutionary changes. They only disagree on the details of this account (i.e. is survival primarily about other generation or self re-generation, and is the beginning of evolution genetic or epigenetic). In general, the underlying assumption of the mainstream view is that the first form of life is essentially structurally isolated and behaviorally passive. In this paper we will challenge this assumption. We follow Virgo (2011) in arguing that dissipative structures whose selfproduction is spatiotemporally localized, but not necessarily membrane-bound, have much in common with living beings. Even very simple examples of these structures are capable of motility, adaptive behavior, structural change, and epigenetic evolution. Consequently we regard such systems as worthy of study in the context of the origins of life. Living without doing? An alternative view Despite some outstanding disagreements, the two mainstream traditions are united by a theoretical view of life that is centered on a combination of the spatiotemporal conservation of the individual with an evolutionary realization of biological change. Accordingly, there are promising attempts to bring these two traditions together, such that life is viewed as essentially consisting of three distinct and yet functionally interrelated components: an informational system, a metabolic system, and a compartment (e.g. Rasmussen, et al. 2003; Ganti, 1975). And given this convergence of the two main traditions, and considering the recent experimental successes in realizing this view via synthetic biology, it seems that the optimism pervading the field is well founded. The creation of all kinds of useful artificial life forms appears to be within our grasp, and the final mysteries of the origin and evolution of life on earth seem tantalizingly close to being resolved. However, the confident promises of synthetic biology will sound all too familiar to those of us who know the history of synthetic psychology – an approach better known as artificial intelligence. Indeed, around half a century ago there was a similar optimism prevalent in the scientific community that the creation of artificial minds and conscious robots was just around the corner. The driving force of that optimism, which in hindsight looks hopelessly naïve and deeply misguided, was a digital-information-centered science of the mind that resonated with advances in engineering and technology. Today the view that cognitive science can be reduced to computer science is no longer in fashion, although the alternative still remains to be properly worked out (Froese 2010). How ironic it is, then, that at the moment in which cognitive science is undergoing a major theoretical makeover, namely toward a view of the mind as essentially embodied, embedded, and enactive (e.g. Gallagher 2005; Clark 2008; Thompson 2007), the science of life is at the same time extoling the virtues of trying to reduce the complexities of cellular biology to the abstract linearity of “logic circuits” (Nurse 2008) and “computer programming” (Balazs & Epstein 2009). History, it seems, is repeating itself. But the purported reduction of life to logic is not as straightforward as the recent advances in biotechnology may seem to indicate. In particular, we note that, in a crucial sense, the life of the individual organism is completely absent from the mainstream framework outlined above. On the one hand we have structural self-maintenance, and on other hand we have informational self-re