As part of our research on programmed self-decomposition, we formed the hypothesis that originally immortal terrestrial organisms evolve into ones that are programmed for autonomous death. We then conducted evolutionary simulation experiments in which we examined this hypothesis using an artificial ecosystem that we designed to resemble a terrestrial ecosystem endowed with artificial chemistry. Notable results corroborating our hypothesis were obtained, which showed that mortal organisms emerged from indigenous immortal organisms through mutation; such mortal organisms survived and left behind offspring, albeit very rarely, and, having survived, surpassed immortal organisms without exception. In this article, we report the details of the above findings and also discuss a background framework we previously constructed for approaching altruism.
We previously modeled autonomous death, which is one of the significant and universal attributes of terrestrial life, as programmed self-decomposition (PSD) [23, 25]. Our research has proceeded by means of a series of studies that look into the existence of autonomous death through experiments in the field of molecular cell biology with existing living organisms as subjects; concurrently, through evolutionary simulations of artificial life (ALife), we raise the possibility that mortal organisms having autonomous death are superior to immortal organisms [8–10, 18–25]. In doing so, we have meshed the following three approaches.
Model constitution: As typically shown in many studies in the field of evolution, including those by Charles R. Darwin and William D. Hamilton, the research model often predetermines both the possibility and limitation of the study in question. We have therefore attempted to construct a new model for autonomous death based on cutting-edge techniques and a perspective that draws on various fields, including ALife and molecular cell biology, so as to extend to areas beyond the scope of previous models.
Verification of a model throughcomparison with real-life phenomena: In carrying out a series of simple, straightforward experiments, we have deployed a concrete and sound approach drawing on the principles and methodology of molecular cell biology.
Simulation of evolution using artificial life as a critical tool: In order to verify our evolutionary model, we had to deal with an extremely complex ecosystem on a large spatiotemporal scale that far exceeds observations of and experiments on real-life individuals. It would be impracticable to perform anevolutionary experiment in the real world, because that would require an earth-scale space anda million-year time span. In view of our research objectives, artificial life has provided the optimum alternative to real life for scientific inquiry. To obtain conclusive research results, we have integrated various interdisciplinary approaches through evolutionary simulations making use of artificial life. Below we introduce certain key points in our studies to provide background for the current study.
1.1 Programmed Self-Decomposition Model
The essence of our PSD model derives from the fact that we have zeroed in on autolysis, which is universally observed in terrestrial lives, including unicellular organisms, as phenomena involving autonomous material recycling in a terrestrial ecosystem.
Since a terrestrial ecosystem has a finite material environment, terrestrial lives require material recycling to maintain their life activities. Eugene P. Odum listed four principal pathways responsible for material recycling in his Fundamentals of Ecology  as follows: (i) primary animal excretion; (ii) microbial decomposition of detritus; (iii) direct cycling from plant to plant through symbiotic microorganisms; and (iv) autolysis. Autolysis as treated by Odum has been conventionally regarded as uncontrollable, natural disintegration with increasing entropy. We have redefined autolysis as a kind of autonomous, altruistic phenomenon beneficial to an ecosystem, in part and as a whole . We thus regard autolysis as an active biochemical process built into cellular genetic programming by which a cell consumes its own metabolic energy. In accordance with this autolytic process, we posit that living individuals autonomously decompose themselves into components; in particular, cells hydrolyze biological polymers into biological monomers so that the materials that they used and the spaces wherethey existed can be optimally reutilized by all other living individuals, including adversaries and competitors, and by that means can return to the environment and thus contribute to the restoration of the entire ecosystem. Regarding the concept of altruism that we have utilized as a tool for these studies, we have partially revised the conventional concept, as discussed in Section 4.
We venture to posit that this phenomenon is built into each single cell, which is the fundamental unit of all terrestrial life, and that it takes place as the cell lives out its natural life span or whenever it encounters an inadaptable environment. Therefore this phenomenon is inseparable from programmed cell death. In unicellular organisms this phenomenon is nothing other than individual autonomous death. At the level of individuals, it corresponds to complete abandonment of self-preservation and self-reproduction, and is indicative of complete withdrawal from and total renunciation of a struggle for existence, or of competition as a survival strategy. We refer to such a phenomenon as programmed self-decomposition (PSD) [23, 25].
In the field of molecular biology, it has recently been reported that autolysis involves certain active processes, including synthesis of new proteins, and is now regarded as a programmed active process [7, 27]. Additionally, necrosis of multicellular organisms, which corresponds to autolysis of unicellular organisms, might involve the regulated genetic program for cell death [2, 11]. Those recent studies support the concept of PSD from the viewpoint of molecular cell biology, which we previously proposed.
To express this concept in the form of an abstract, logical model completely removed from any and all concrete aspects of actual life activities, we constructed a mathematical model of life activities exemplified by self-reproduction and self-decomposition, taking John von Neumann's self-reproductive automaton  as our prototype and naming it the PSD model . Details of this model are described elsewhere [23, 25].
1.2 Molecular Cell Biology Studies
It is of critical importance that our PSD model be applicable to actual terrestrial lives. We therefore adopted a eukaryotic unicellular organism, the protozoan Tetrahymena, as our experimental material, since it is highly conducive to mathematical modeling [23, 25]. For our impulse shock experimental model [25, 36]: First of all, we activated, for a short period of time, a genetic program with an external signal indicative of a fatal environment. Next, the culture condition was immediately restored to one appropriate for life, so that the physiological processes responsible for self-decomposition could proceed smoothly. To actualize our impulse shock model in a flask, we created concrete experimental conditions to induce the self-decomposition process. The success of this experiment corroborated evidence of the existence of the PSD mechanism (Figure 1) . In three other experiments, the decomposition of cells was significantly suppressed due to the inhibition of any of three processes that occurred directly after the impulse shock treatment: transcription from DNA to mRNA, energy-requiring metabolic processes, or lysosomal hydrolytic enzyme activities. Such experiments supported our model  by which the PSD mechanism constitutes endergonic, genetically regulated hydrolysis that decomposes a biological polymer into biological monomers. Details are described elsewhere .
1.3 Artificial Life Studies
We have also developed a series of simulators of evolution using artificial life, SIVA (simulator for individuals of virtual automata), which provide a basic tool for examining the PSD model. Since 1996, when we constructed SIVA-III , a pioneering prototype for an AChem [3, 31] system, we have continued to make enhancements of SIVA [8–10, 18–22, 25], the most current one being the SIVA-T group [10, 25].
SIVA is configured with virtual life individuals (VLIs) installed in a virtual ecosystem in a two-dimensional space. Two different kinds of VLIs are designed for SIVA, based on AChem. One is a VLI of a mortal organism that exerts an altruistic effect through autonomous death accompanied by the PSD mechanism. The other kind is a VLI of an immortal organism having the same structure and functioning as the mortal organism but without autonomous death in the PSD mechanism and thus lacking any altruistic characteristics. Details of the simulator design are described elsewhere .
When the two types of VLIs proliferate within the same virtual ecosystem whose environmental conditions are identical throughout the entire ecosystem and are programmed so as to fit both mortal and immortal VLIs, the immortal VLIs prosperously proliferate while, as expected, they exterminate the mortal VLIs, which decrease in number, due to death, during the simulation. This finding well supports the Darwinian principle of survival of the fittest. Actual environmental conditions on Earth, however, are heterogeneous. We therefore designed a virtual environment whose conditions were suitable for VLIs in the initial habitation area, but gradually diverged from the optimal conditions for VLIs. In contradistinction to the above-mentioned results, the immortal VLIs ceased proliferation after occupying the initial areas whose environmental conditions were amenable to their survival, whereas the mortal VLIs succeeded in expanding their habitation area and overwhelmingly surpassed the immortal VLIs [8, 19, 20]. Thus it can be paradoxically stated that a genealogy of living individuals that renounce their self-preservation and self-reproduction prospers to a greater extent than those continuing this pursuit.
The context for such a seemingly contradictory finding is as follows. Mortal VLIs with an altruistic PSD mechanism can endlessly self-reproduce by reusing materials and space restored to the ecosystem due to death and self-decomposition of others and thus cause an increase in the frequency of mutation. Evolutionary adaptation to the environment is accelerated by diversity of species, that is, mutant VLIs evolve one after the other with characteristics that allow them to survive in environmental conditions under which the initial VLIs are unable to survive and thus are able to greatly expand their territory. On the other hand, since immortal VLIs irreversibly fill their habitable area and never reuse it, the available space for existence becomes circumscribed so reproduction becomes increasingly difficult over time. This factor leads to a decrease of emergent mutant VLIs and the blockage of proliferation and evolutionary adaptation. As a result, their inhabitable territory hits a ceiling. We can understand this situation as evidence that autonomous, altruistic self-decomposition accelerates evolutionary adaptation to the environment through the diversification of species.
Moreover, we examined how differences in the degree of altruism affected offspring prosperity using a SIVA simulator endowed with a terrestrial-type finite, heterogeneous environment . In that experiment, we considered the degree of ease for other VLIs to reutilize decomposed parts, which had returned to the environment as a result of self-decomposition, as a hypothetical index of altruism. That is, we designed three different types of mortal VLIs, each of which returned differing types of decomposed parts to the environment. The amount of energy required for reutilization by other organisms differed among the three. Namely, the more energy required for reutilization by others, the less altruistic the decomposing organism. We then conducted simulations in which those three types of mortal VLIs and the immortal VLIs proliferated within the same ecosystem. The results showed that the immortal VLIs hit a ceiling at a certain stage, as in the previous experiment, while mortal VLIs with relatively low degrees of altruism on the hypothetical index, hence requiring others to expend a greater amount of energy to reutilize their parts, became extinct. By contrast, mortal VLIs that were decomposed into parts requiring the least amount of energy for reutilization rendered the maximum altruistic contribution to all the other organisms, and thus the whole ecosystem overwhelmingly prospered. The point of such an outcome is that the genealogy of organisms contributing a higher degree of altruism to other organisms allows for greater diversification of the species and accelerates their evolutionary adaptation to the environment. Such findings further support our PSD model and suggest the effectiveness of self-decomposition in the evolution of terrestrial lives.
One of the most critical questions remaining for this hypothesis to stand is a reasonable explanation as to how such an effective gene of altruistic death has emerged in the evolution of terrestrial life. Using our evolutionary model, in which the most primitive form of living individuals is immortal and in which mortal lives emerged by the acquisition of an altruistic death gene as a property highly suitable to the terrestrial environment through the process of evolutionary sophistication , we conducted a preliminary investigation using an artificial ecosystem SIVA-III  of our previous design and obtained results that would suggest the robustness of the above hypothesis [9, 19]. Thereafter, we constructed a more sophisticated model for a more detailed investigation making use of an AChem ecosystem SIVA-T05 . The essential questions we sought to answer were as follows: Would an individual mortal organism, overwhelmed by immortal organisms, become extinct, or could such an individual survive and produce offspring? If it survived and produced offspring, what kind of power relationships would be established between such mortal organisms and the immortal ones?
Our findings suggest that a mortal mutant individual, born in an ecosystem where only indigenous immortal organisms exist, cannot repeat self-reproduction steadily and thus becomes extinct in most cases. Nonetheless, some mortal mutant individuals in our study did manage to survive at an extremely small but not negligible rate. Moreover, the offspring of these mortal mutant individuals that survived extended their habitation area, surpassed immortal organisms, and prospered without exception. This article discusses the above findings in detail.
2.1 Design of the SIVA Virtual Environment
In the present study, we again used SIVA-T05 as an evolution simulator. Its construction and functions are the same as those utilized in an earlier report . In short, the virtual environment of SIVA-T05 consists of a lattice of spatial blocks on a two-dimensional plane (Figure 2). Environmental conditions regarding temperature, energy, and four kinds of virtual inorganic biomaterials were independently defined for each spatial block. The initial configuration was identical to that in the previous report .
2.2 Structure and Behavior of Artificial Life in SIVA
2.2.1 Structure of a Virtual-Life Individual
As in the earlier report , we designed a virtual-life individual (VLI) based on Oohashi's self-reproductive, self-decomposable (SRSD) automaton model (Figure 3), which took von Neumann's self-reproductive automaton model  as its prototype. Oohashi's automaton G is described as G = D + FZ + ID+FZ, where D = A + B + C. Here, automaton A produces automata according to instructions on data tape I (that is, a virtual genome). Automaton B reads and replicates data tape I. Automaton C sets the copy of data tape I replicated by automaton B into new automata produced by automaton A and separates these as automaton D. Automaton FZ, which is a modular subsystem plugged into automaton D, decomposes the whole automaton G into components suitable for reutilization when automaton G encounters serious environmental conditions in which it is unable to live or has reached the end of its life span. Data tape ID+FZ carries an instruction describing automaton D + FZ. Thus, automaton G, which corresponds to D + FZ + ID+FZ, can reproduce an identical automaton G as well as decompose itself.
We designed artificial life based on AChem so as to actualize the above-mentioned logical actions and, as faithfully as possible, to reflect the principles of terrestrial life and its subsequent reproduction (Figure 4). That is, a VLI is constructed from four classes of virtual biomolecules: virtual inorganic biomaterials (VI), virtual organic biomaterials (VO), virtual biological monomers (VM), and virtual biological polymers (VP). There are four kinds of VI; moreover, any molecules in the latter three classes consist of combinations of the four kinds of VI. A virtual genome in the VP class consists of virtual nucleotides belonging to the VM class. The virtual protein in the VP class is produced according to a sequence of virtual nucleotides that determines the primary sequence of virtual amino acids belonging to the VM class. We developed a SIVA language that actualizes virtual-life activities by recognizing the sequence of the virtual amino acids contained in the virtual protein as coded program sentences and executing therewith. According to given conditions, this SIVA language reproduces, divides, and decomposes a VLI.
2.2.2 Behavior of Virtual-Life Individuals
A VLI executes its life activities by consuming materials and energy from the virtual environment . Activities of each VLI are so designed as to depend on the amount of material and energy available as well as the temperature in the inhabited spatial block. Namely, optimum environmental conditions are defined for each VLI a priori. Activities of a VLI decrease when environmental conditions of the habitation point move away from VLI optimum points. A VLI cannot express its life activities when environmental conditions markedly deviate from the optimum, and, in the case of a mortal organism, it decomposes itself just as it does when it has lived out its life span. Materials and energy released by the decomposition of a VLI are restored to the environment and become utilizable by other individuals within the same space as that occupied by the VLI.
When VLI reproduce, point mutation can occur at a predefined probability during replication of the virtual genome. Mutations may alter the optimum environmental conditions of a VLI. This enables the VLI to live in an environment where it originally could not live. That is to say, evolutionary adaptation to the environment can occur.
2.3 Experimental Setting
We constructed an experimental model to examine our hypothesis  on the evolutionary emergence of an altruistic gene using ALife: namely, that primitive immortal organisms through evolution have acquired death accompanied by altruistic self-decomposition.
As mentioned above, our SRSD VLI is described as G = D + FZ + ID+FZ. Its prototype is von Neumann's automaton, described as E = D + ID, which reproduces without autonomous death. With the added function module FZ for self-decomposition along with its genetic program IFZ, our automaton can achieve autonomous death accompanied by altruistic self-decomposition. Consequently, mortal organisms are more complex than immortal organisms in terms of structure and function. Von Neumann stated as a matter of principle that “when an automaton performs certain operations, they must be expected to be of a lower degree of complication than the automaton itself ”; furthermore, he described living organisms as follows : “They produce new organisms with no decrease in complexity. In addition, there are long periods of evolution during which the complexity is even increasing.” Our self-decomposable mortal automaton, having greater complexity, achieves prosperity of its offspring exceeding that of its immortal prototype. Consequently, we hypothesized that mortal organisms with altruistic self-decomposition emerge evolutionarily from immortal organisms [19, 23].
We constructed our experimental simulation model using SIVA configured with a terrestrial-type finite, heterogeneous environment. First, we designed an immortal organism as a precursor at an evolutionary stage just prior to its becoming a mortal organism, and configured a virtual ecosystem inhabited by that precursor organism as its only indigenous species. Then we considered what might become of a mortal individual with altruistic self-decomposition that had emerged evolutionarily from an indigenous immortal organism through mutation. As shown in Figures 3 and 4, the mortal VLIs consist of automata A, B, C, and FZ, each of which is a virtual protein with a specific function, as well as a data tape ID+FZ, that is, a virtual genome that stores the data for each automaton. Automaton FZ, which has decomposed VLI itself, was activated whenever either of the following conditions was determined to be true: (1) the VLI encountered an environment incompatible with its survival, or (2) the VLI's life span had ended. For immortal VLIs, therefore, we assumed such conditions to be false so as not to make FZ execute self-decomposition. If this mechanism became the target of a mutation that canceled the “false” setting, it would correctly determine the above conditions to be true. Consequently, the mutant VLI could activate FZ and execute its own self-decomposition, resulting in the evolutionary emergence of a mortal organism with altruistic self-decomposition. We seeded an immortal VLI possessing this precursor of a genetic program for death at the very center habitation point of an ecosystem whose environmental conditions were deemed most suitable for a VLI.
The mutation rate was determined as follows. Existing terrestrial lives tend to have a higher mutation rate, as the length of their genome is shorter. For example, an organism with a genome of 104 molecules has a mutation rate 10−4. Since the virtual genomes of VLIs in the present simulation consisted of 1,275 VM molecules, we used three mutation rates: 0.005, 0.002, and 0.001.
For each of the three mutation rates, we conducted 200 to 800 simulations of 800 passage durations each and observed changes in size of habitation area, number of VLIs, and frequency of mutation. Here one passage duration corresponded to five time counts (TCs, the unit of virtual time in SIVA-T05), because it took at least five TCs for a newborn individual to reproduce itself in our current simulation experiments. We have used the passage duration as the time unit in this report.
Simulations of whether mortal VLIs emerging from immortal VLIs through mutation survived and proliferated obtained the following results.
Table 1 shows the proportions of the simulations in which mortal VLIs emerged and then survived at each mutation rate. Not so many mortal mutants emerged evolutionarily within the passage duration of 800, and, even when emerging, most of them were surpassed by native immortal VLIs and did not survive. The survival rates of emerging mortal mutants, however, were not negligible: 3.5%, 1.4%, and 0.25%, respectively, of the total number of simulations at mutation rates of 0.005, 0.002, and 0.001. Namely, the mortal mutants and their offspring that evolutionarily acquired altruistic self-decomposition were mostly but not altogether exterminated, with some surviving in extremely low proportions.
|Total number of simulations|
|Proportion of emergence (number of simulations)|
|Proportion of survival (number of simulations)|
|Survival proportion of simulations with emergence|
|0.005||200||29% (58)||3.5% (7)||12%|
|0.002||500||11% (56)||1.4% (7)||13%|
|0.001||800||5.3% (42)||0.25% (2)||4.8%|
|Total number of simulations|
|Proportion of emergence (number of simulations)|
|Proportion of survival (number of simulations)|
|Survival proportion of simulations with emergence|
|0.005||200||29% (58)||3.5% (7)||12%|
|0.002||500||11% (56)||1.4% (7)||13%|
|0.001||800||5.3% (42)||0.25% (2)||4.8%|
It was noteworthy that once the emerging mortal mutants survived and left offspring, these invariably surpassed immortal VLIs and increasingly proliferated as the passage duration became longer. Figure 5 shows changes in habitation area, number of VLIs, and frequency of mutation in a typical example for each of the three mutation rates, and indicates that the numbers of individuals and the frequency of mutation of mortal VLIs were quite low as they began to emerge, but, as their activity gradually increased, they began to surpass immortal VLIs between passage durations of 300 and 400, and afterward proliferated exponentially.
4.1 Emergence and Prosperity of Mortal Organisms
We carried out an evolutionary simulation experiment using our artificial ecosystem SIVA-T05, modeled for a finite, heterogeneous terrestrial environment and arranged in a biomolecular hierarchy. When a mortal mutant individual endowed with an evolutionarily acquired genetic program for death was born in a place in which immortal organisms already existed as indigenous ones, although such mortal individuals had difficulty in surviving, yet they did survive and produced offspring, albeit at a very low reproductive rate. We also showed that, once these living individuals survived, they invariably prospered and surpassed existing immortal organisms.
Is it possible to apply such a finding to the actual evolutionary history of the terrestrial ecosystem? For example, since the evolution and prosperity of mortal organisms were only observed twice out of eight hundred simulations with a mutation rate of 0.001, such a result might be deemed merely an extremely rare phenomenon. However, in consideration of the enormously long evolutionary period of 3.8 billion years since most ancestors of life emerged, the boundless expanse of the terrestrial environment relative to a unicellular organism as minute as a few microns, for which even a cubic meter of water environment would be greatly expansive, and the immeasurable diversity and heterogeneity of matter and energy, we suggest that evolution from immortal to mortal life might well occur even if the probability might be lower than what we employed in the simulations.
4.2 Background to the Superiority of Mortal Organisms
As shown in our research, including the current experiment, the superiority of mortal organisms to immortal organisms pertains to the following background. Immortal organisms dominate space and materials, once secured, while the volume of resources in the ecosystem to sustain life activities monotonically decreases. With less chance of reproduction in association with a decrease of resources, the chances for mutation and evolutionary adaptation are reduced. By contrast, mortal organisms through self-decomposition release space and return their parts to the environment for other organisms to reutilize. As a result, accumulated mutations through the continuous alternation of generations accelerate evolutionary adaptation to the environment.
Death is the non-reversible termination of two definitive attributes of living individuals, namely, self-preservation and self-reproduction. In terrestrial lives, these attributes are associated with autolysis, which we have modeled as programmed death accompanied by altruistic self-decomposition, that is, the restoration of biomaterials and habitation space to the environment. In terrestrial lives, moreover, death is triggered not only by external forces such as predation, injury, or infection, but also by overwhelming environmental unconformity and the normal life span of that species. Consequently, death is essentially inevitable for terrestrial lives.
From the viewpoint of the individual-centric umwelt1 considering the life principles of self-preservation and self-reproduction, such death of a terrestrial life form can be understood as the last defect of life, which should be essentially flawless, and as the epitome of the incompleteness of life, which could be overcome through evolution. Nonetheless, in our previous evolutionary simulation studies based on the ecosystem-dominant umwelt model, we found that living individuals endowed with a mortal genetic program that includes altruistic self-decomposition prospered and surpassed flawless living individuals with perfect self-preservation and self-reproduction in a heterogeneous, complex, terrestrial-type virtual environment.
The current experiment revealed that offspring of indigenous immortal organisms prospered more significantly than did their parents because of the autonomous, altruistic mortal genetic program newly installed in the immortal organisms that converted them into mortal organisms; that is, they evolutionarily acquired a paradoxical survival strategy. This finding encourages us to create a model for the acquisition of autonomous, altruistic death as the fruit of evolution.
Independent of the studies that we have undertaken since 1987 [8–10, 17–25], Peter M. Todd implemented artificial death in his ALife system [33, 34], and those experiments supported the recognition shared with us that death affords another entity its space in which to exist, and that death, accordingly, is essential throughout the ongoing evolutionary process. Nevertheless, the model of death constructed by Todd differs from ours in two obvious respects. First, death in Todd's model affords no process by which the organism might decompose itself into constituent parts for the efficient and collective reutilization of other organisms, which is an essential feature of our model. Second, the death of an individual in Todd's model appears as a probabilistic phenomenon, or as a given event controlled by the simulation system, in sharp contrast to the activation of death in our model, which is an independent and autonomous process genetically regulated in the individual that starts from detection either of the end of its life span or of excess unconformity with the environment. Consequently, it would be difficult to rely on the ALife system as constructed by Todd to investigate the evolutionary emergence of death in a terrestrial ecosystem.
4.3 Reorganization of the Altruistic Concept
In this section, we describe the concept of altruism that informs our research, including the current study. In conventional zoology, altruism is defined, for example, as “a self-jeopardizing, self-exposing or self-sacrificing behaviour of animals, i.e. any unselfish behaviour pattern which increases the fitness of the object at expense of the altruistic individual” (Elsevier'sDictionary of Biology ). Thus, in the field of zoology, both a negative effect on a self-individual (i.e., sacrifice) and a positive effect on other individuals (i.e., contribution) are usually regarded as an intrinsic attribute of altruism. Yet there remains the need to measure the degree of altruism in terms of the magnitude of sacrifice. On the other hand, when we look at how altruism is described as a more general concept, we find that the Oxford English Dictionary  calls it “Devotion to the welfare of others, regard for others, as a principle of action.” This notion offers a slightly different slant on altruism by referring to the target of altruistic behaviors as not likely limited to an individual and with greater attention paid to the contribution per se rather than to the sacrifice itself. There seems to be an inconsistency between the zoological concept and the general concept of altruism as to whether the following two conditions should be regarded as essential attributes of altruism: targeting only individuals and always accompanying sacrifice. This semantic deviation, for example, poses a challenging question: Which is more altruistic, a tremendous contribution with negligible sacrifice or an tremendous sacrifice with negligible contribution?
In order to adequately address such a question in setting up a reliable framework for our own research, we examined the conventional concept of altruism, which is constrained by individuals and sacrifice. In doing so, we reconstructed a more flexible concept of altruism [17, 18], which need not restrict its target to an individual and need not regard sacrifice as an indispensable requirement.
We redefined an altruistic phenomenon as a phenomenon by which a living individual renders certain biological benefits to a part of the ecosystem including individuals as well as to that ecosystem as a whole, regardless of any biological benefit or disadvantage to itself [17, 18], and we have deployed this construction as a conceptual apparatus in our research. The key point is not to regard sacrifice as an indispensable requirement and not to restrict recipients of contribution to individuals, while extending the notion of recipient to the system level, that is, the ecosystem itself. The biological benefits for the ecosystem may cover various aspects, including the restoration of the environment to its original state, regeneration of reproductive potential, mutation increase, biodiversity, and so forth.
The problem of deciding whether to focus on sacrifice or contribution in altruism or whether to restrict altruism to an individual or extend it to a system is similar to deciding whether to consider light as a wave or a particle in physics. It is well known that a feature of light is easier to understand as a wave in some cases, and as a particle in other cases, and those two aspects are practically selected depending on the circumstances. Such a relationship between two standpoints may correspond to the interrelationship of paradigms, or independent axiomatic systems not mutually constraining, as proposed by Thomas Kuhn .
4.4 Evolutionary Mechanism of Altruistic Phenomena
Many theories and principles have been proposed and examined with regard to the evolution of altruism. Kin selection mechanisms based on inclusive fitness, first proposed by John B. S. Haldane and refined by William D. Hamilton and George R. Price [4, 5, 26], elegantly explains the evolution of various altruistic behaviors in animals. In addition, related studies by Tom Lenaerts, Francisco C. Santos, and Jorge M. Pacheco [28, 29] suggest that heterogeneity and complexity, which are essential attributes of the real world, have led to the evolutionary emergence and sustainability of cooperation, a concept closely related to that of altruism. Such studies are compatible and complementary with our finding that mortal organisms endowed with altruism overwhelmingly proliferate in a complex heterogeneous terrestrial-type environment.
In addition, Martin A. Nowak has provided a useful framework to explain the evolution of cooperation—which is closely related to the concept of altruism—on the basis of the principle of natural selection [12–15, 35]. Although Nowak's idea appears to be mainly based on an interest in the origin and evolution of cooperative behaviors in humans and therefore may not precisely correspond to our concept of altruism, his framework indeed effectively explains the PSD mechanism.
According to Nowak, mechanisms for the evolution of cooperation can be classified according to five rules according to the state of the interaction among components, as follows: (i) kin selection, (ii) direct reciprocity, (iii) indirect reciprocity, (iv) network reciprocity, and (v) group selection . In summary, the evolution of cooperation may occur in the following manner: (i) Kin selection operates when the donor and the recipient of an altruistic act are genetic relatives. (ii) Direct reciprocity operates when there are repeated encounters between the same two individuals and both remember their history of cooperation. (iii) Indirect reciprocity is based on reputation, that is, a helpful individual is more likely to receive help. (iv) Network reciprocity operates when cooperators form a close network in which reciprocity develops. (v) Group selection involves the recognition that competition is not only between individuals but also among groups. Group selection sometimes has priority over individual selection, and pure cooperator groups prevail over groups laden with defectors.
Nowak examined this taxonomy while referring to a large number of previous studies, pointing out that emerging cooperation evolves from natural selection as appropriate conditions are satisfied, whereas it becomes extinct when such conditions are not satisfied. He also formulated five simple rules, dependent mainly on the parameters of cost and benefit, by which to discriminate whether or not cooperation will be naturally selected . Based on this framework, he insightfully suggested natural cooperation as a third principle of evolution apart from mutation and natural selection.
Nowak's insight with regard to the mechanisms for the evolution of cooperation throws light on our findings of a paradoxical phenomenon in which individuals actualizing altruistic death by means of self-decomposition, though seemingly withdrawing from the struggle for survival, actually prevail over immortal individuals. Needless to say, the kin selection mechanism at least partly explains our seemingly contradictory finding that a species endowed with altruistic death is superior to one without it. Moreover, network reciprocity may also work because the environmental conditions of our simulation space were heterogeneously determined and the virtual individuals were set so that they could not migrate outside their habitation area. Therefore, each group of virtual individuals adapted evolutionarily to environmental conditions specific to the habitat spatial block, and the individuals were spatially separated from other individuals existing under other environmental conditions. Since these circumstances can be interpreted as indicating that virtual individuals within each spatial block form a close network, the superiority of PSD may include a mechanism categorized as network reciprocity. In addition, because a network constructed only by mortal lives reuses materials and space more efficiently than does that inclusive of immortal lives, it likely accelerates evolutionary adaptation to the environment. Thus group selection is also of importance. Moreover, multiple evolutionary mechanisms interacting with one another could be involved.
Thus Nowak's five rules for the evolution of cooperation convincingly account for at least a part of the PSD mechanism. Yet there is one more point that should be considered. That is, is Nowak's model sufficiently robust that we can exclude an examination of unknown factors possibly missing from his model?
First, we need to mention that, in our experimental system, all VLIs in the ecosystem are offspring of one initially seeded VLI, which means that all VLIs participating in one simulation are genetic relatives. In particular, since the initial mortal VLI was born from an immortal VLI through a point mutation, these two VLIs share the same genes to a significant degree. At the same time, mortal VLIs have advanced through evolution to other spatial blocks having remarkably different environmental conditions from those of the spatial block in which the initial VLIs existed. This suggests that the genotypes of mortal VLIs distant from the initial habitat point should differ markedly from that of the initial mortal VLI, due to repeated mutations. Thus the commonality of genotypes between different VLIs, that is, the degree of kin relationship, would continuously decrease. It follows that an evolutionary force driven by kin selection cannot be strengthened, although it can be weakened, as time passes. In our simulation experiments, however, the number of mutations kept increasing and evolutionary adaptation to the environment continuously accelerated. It is necessary to examine whether the kin selection mechanism, basically resting its claim on the commonality between genotypes, can be independently verified as a determinant force for evolution in such situations.
Second, in our simulations it was noteworthy that a VLI contributing to others through altruistic self-decomposition disappeared in tandem with the self-decomposition process and thus no longer existed as a target for reciprocity or retribution nor as a subject of recognition and decision. Therefore, it is difficult to compare the degree of risk or sacrifice with the degree of benefit at the individual level according to Nowak's model. We should carefully consider how altruistic phenomena might be actively selected under such a condition.
Third, in order to delve into potential activities within our ecosystem-dominant umwelt model, the SIVA simulator used in our research was designed to eliminate direct interactions between particular individuals such as bestowal, partnership, predation, and competition as well as sexual reproduction. In our experimental system, each VLI is designed to interact only with its environment through utilizing materials for self-reproduction, releasing its decomposed parts at self-decomposition, and occupying and releasing habitat space, as shown in Figure 3. By assumption, mutual direct interaction between or among plural VLIs cannot occur. Instead, all interaction between VLIs always occurs indirectly through the ecosystem as a change in environmental conditions. No decomposed parts produced by the PSD mechanism belong to any particular individuals, but they do exist as a group of environmental materials that can be utilized by any VLI in the ecosystem. Decomposed parts are utilized by any VLI, and direct descendants are not accorded any special favoritism. In other words, the recipients of decomposed biomaterial contributed by self-decomposition are not restricted to any particular individual or group of individuals. In order to actualize such a concept, we did not install any mechanisms into the VLIs by which to recognize and discriminate other individuals. Thus, using SIVA, we can perform a simulation experiment in which particular individuals do not become targets for cooperation or antagonism based on individual discrimination. All our past simulations were conducted in this manner. Our experimental setting attempts to draw a distinction counter to the conventional meaning of “selection” implied by individual discrimination, which can be regarded as a selection function regulated by internal factors. Selections by individual discrimination should be kept distinct from natural selections induced by an external factor of environmental conditions.
Given these considerations, we implemented for the SIVA simulator a most primitive theoretical model for life in which the fundamental principle of terrestrial life is ultimately simplified and abstracted, taking von Neumann's self-reproductive automaton  as our prototype, that is, it reproduces and decomposes itself solely according to genetic information. All biological information possessed by a VLI is remembered as a sequence of virtual genomes while precluding any other method by which to remember information. In other words, in our experimental system, a VLI does not make use of any method by which to remember experiences during its life span or to discriminate between individuals, and all its life activities are regulated solely according to genetic information in read-only memory (that is, a genome), and can be changed only by mutation in the event of self-reproduction of VLIs.
Taking into account the above-mentioned points raised by our experimental system, we reexamined Nowak's five rules from the viewpoint of evolutionary biology, especially focusing on evolutional development of a biological control system, and discussed their bearing on our studies.
First of all, we focused on the most developed biological control system of interest to Nowak, the central nervous system in vertebrates (including humans), in which plasticity of efficiency of information transmission at the synaptic junction and its extensive accumulation effectively function to remember experiences . Functions of individual discrimination and behavior selection based on such a flexible memory function are not only essential for indirect reciprocity requiring communication regarding others' reputation, but are also important for direct reciprocity requiring contribution to specific individuals that have contributed to oneself, as well as for network reciprocity requiring clustering with specific individuals. The distributed neural network connecting neural ganglia, which corresponds to the biological control system evolutionarily preceding the central nervous system, is fundamental to direct reciprocity and network reciprocity based on individual discrimination of, for example, social insects. Of course, such functions of the nervous system can enable organisms to actualize group selection and kin selection.
Next, the biological control system evolutionarily preceding the nervous systems is a chemical messenger, typically observed as the endocrine system of animals, hormones of multicellular plants, pheromones of insects, and so forth. In the case of organisms without a nervous system, selective expression of life activities based on individual discrimination by means of a certain chemical messenger system is indispensable for group selection, in which cooperative behaviors should be exerted on discriminating individuals within a group from those outside the group, and for kin selection, in which cooperative behaviors should follow according to the degree of kinship. Nowak's five rules essentially require reference to remembered information to discriminate whether other individuals are appropriate recipients of cooperation, and to selectively express a cooperative behavior toward a specific individual or a group of individuals (including the species) under the commitment of a relatively developed biological control system, as mentioned above.
On the other hand, there is a biological control mechanism evolutionarily preceding the chemical messenger system, namely, metabolic regulation on the basis of genetic information remembered in DNA a priori. This mechanism can be actualized by a single cell alone, which is a basic unit of terrestrial life, and therefore it is fundamental to all kinds of biological control systems of terrestrial lives. Our SIVA simulator is designed to focus on evolutionary phenomena that can be actualized solely by means of this biological control system. Thus the PSD mechanism corresponds to the most primitive class of terrestrial lives, namely, cells controlled only by metabolic regulation, and does not reach any level of the five mechanisms as proposed by Nowak. Terrestrial lives in this class not only control themselves, but also support those belonging to higher-developed classes, of which Nowak took note, possibly as an indispensable infrastructure. It is noteworthy that PSD, which is an altruistic phenomenon specific to metabolic regulation or autolysis, may exist universally in terrestrial lives, as suggested by the universal extent of lysosomes (i.e., organelles executing PSD) in every eukaryote cell.
Various findings from our experiments support Nowak's idea that “we might add natural cooperation as a third fundamental principle of evolution beside mutation and natural selection.” Nowak incorporated evolutionary mechanisms of cooperative behavior in higher organisms, which are dependent on interaction between particular living individuals. Such mechanisms require biological control systems, such as chemical messengers and, ideally, a central nervous system, that enable the remembering of experience and the ability to discriminate between individuals. In other words, functions to discriminate and select other individuals, partly through referring to remembered information, are inseparable from cooperative behaviors. Consequently, Nowak's framework quite adequately accounts for cooperative behaviors, which can be regarded as a certain type of altruistic phenomena that target only specific individuals or groups.
By contrast, our research has suggested that the involvement of altruism promotes evolutionary adaptation even in very primitive life forms equipped with only the fundamental principle of terrestrial life, namely, self-reproduction and self-decomposition regulated solely by a genetic program, and without any functions by which to discriminate between individuals. This means that altruistic phenomena can be an evolutionary force even without requiring discrimination and selection of other living individuals, that is, interaction including cooperation among specific individuals.
An individual-oriented evolutionary mechanism is conventionally accepted in which a living individual or the population to which it belongs actively retains its specific properties based on interaction between individuals, that is, discrimination and selection of other individuals, as is the case with higher animals. On the other hand, in our experimental conditions it was difficult for such individual-oriented discrimination and selection to occur. Nevertheless, the altruistic gene contributed to either a part of or the entire system through the restoration of the ecosystem to its original state in a way that rendered neither advantage nor disadvantage to individuals. As a result, the altruistic gene was naturally selected as a trait suitable for such an environment. Our findings suggest the possibility of the existence of an ecosystem-oriented evolutionary mechanism. Yet it seems premature to conclude that no mechanism promoting evolution other than an individual-oriented mechanism exists. We therefore wish to pay increased attention to the possibility that a more fundamental ecosystem-oriented evolutionary mechanism of programmed death accompanied by altruistic self-decomposition could exist as the infrastructure of individual-oriented altruistic mechanisms.
As described above, our research has focused on a lacuna in previous research on altruism by paying keen attention to death with altruistic self-decomposition, which seemingly contradicts our understanding of the survival of the fittest and the struggle for existence. We have identified a mechanism by which mortal organisms through altruistic activity overcome immortal organisms deprived of altruism and prosper. We also suggest that such activity might promote evolution in a finite, heterogeneous terrestrial-type environment. In showing that the altruistic mortal gene endowed with self-decomposition can be acquired through the evolution of immortal lives, our findings thus offer new insight into the overwhelming evolutionary superiority of lives with the altruistic mortal gene over immortal lives. We believe that such results might augur the opening of a new field of inquiry not only in the study of altruism, but also, more broadly, in the realm of evolutionary biology.
In addition, our present study advocates the study of artificial life based on artificial chemistry to simulate existent terrestrial life, as a promising research tool in the field of interdisciplinary life science including evolutionary biology. We believe in the potential of artificial chemistry in this regard and expect that the concepts, insights, and cutting-edge techniques of artificial life research will henceforward become ever more widely disseminated in all fields of inquiry related to life phenomena.
We wish to thank Dr. Katsunori Shimohara, Doshisha University, and Dr. Hideaki Suzuki, National Institute of Information and Communications Technology, for their valuable comments on our study; Dr. Hiroki Sayama, Binghamton University, for his contribution to the development of the earlier version of the SIVA series; Dr. Michael E. Workman and Ms. Jane S. Workman at BEST Ltd., Tokyo, for their patient editing; and members of Yamashiro Institute of Science and Culture for much appreciated technical support.
These authors have contributed equally to this article.
Faculty of Environmental and Information Sciences, Yokkaichi University, 1200 Kayou-cho, Yokkaichi, Mie 512-8512, Japan. E-mail: firstname.lastname@example.org
Center of ICT and Distance Education, The Open University of Japan and School of Cultural and Social Studies, The Graduate University for Advanced Studies, 2-11 Wakaba, Mihama-ku, Chiba 261-8586 Japan. E-mail: email@example.com