ON THE PARADIGM OF ALTRUISTIC SUICIDE IN THE UNICELLULAR WORLD

Altruistic suicide is best known in the context of programmed cell death (PCD) in multicellular individuals, which is understood as an adaptive process that contributes to the development and functionality of the organism. After the realization that PCD‐like processes can also be induced in single‐celled lineages, the paradigm of altruistic cell death has been extended to include these active cell death processes in unicellular organisms. Here, we critically evaluate the current conceptual framework and the experimental data used to support the notion of altruistic suicide in unicellular lineages, and propose new perspectives. We argue that importing the paradigm of altruistic cell death from multicellular organisms to explain active death in unicellular lineages has the potential to limit the types of questions we ask, thus biasing our understanding of the nature, origin, and maintenance of this trait. We also emphasize the need to distinguish between the benefits and the adaptive role of a trait. Lastly, we provide an alternative framework that allows for the possibility that active death in single‐celled organisms is a maladaptive trait maintained as a byproduct of selection on pro‐survival functions, but that could—under conditions in which kin/group selection can act—be co‐opted into an altruistic trait.     

Maintainence of parasitaemia – is it to die for?

One of the major differences between protozoan differentiation and metazoan differentiation is that protozoan cells normally retain potency during differentiation, which need not, therefore, be considered altruistic. Altruism does, however, arise at the level of the organism and consequently, protozoons have the potential to evolve altruistic traits. This is particularly true when, as with Trypanosoma brucei parasitaemias, populations are genetically homogeneous. This essay argues that whilst reports of altruistic phenomena during the trypanosome life cycle remain controversial, the prospect of reagents able to instigate pathways of cell death or differentiation bears further investigation.     

Maintainence of parasitaemia - is it to die for?

One of the major differences between protozoan differentiation and metazoan differentiation is that protozoan cells normally retain potency during differentiation, which need not, therefore, be considered altruistic. Altruism does, however, arise at the level of the organism and consequently, protozoons have the potential to evolve altruistic traits. This is particularly true when, as with Trypanosoma brucei parasitaemias, populations are genetically homogeneous. This essay argues that whilst reports of altruistic phenomena during the trypanosome life cycle remain controversial, the prospect of reagents able to instigate pathways of cell death or differentiation bears further investigation.     

Altruistic cell suicide in relation to radiation hormesis

The high radiosensitivity to killing of undifferentiated primordial cells (Bergonié and Tribondeau 1906) can be described as a manifestation of the suicide of injured cells for the benefit of an organism as a whole if their suicide stimulates proliferation of healthy cells to replace them, resulting in complete elimination of injury. This process is called cell-replacement repair, to distinguish it from DNA repair which is rarely complete. 'Cell suicide', 'programmed death' and 'apoptosis' are terms used for the same type of active cell death. Cell suicide is not always altruistic. Altruistic suicide in Drosophila, mice, humans, plants, and E. coli is reviewed in this paper to illustrate its widely different facets. The hypothesis that in animals, radiation hormesis results from altruistic cell suicide is proposed. This hypothesis can explain the hormetic effect of low doses of radiation on the immune system in mice. In contrast, in plants, radiation hormesis seems to be mainly due to non-altruistic cell death. HORMESIS--'the stimulating effect of small doses of substances which in larger doses are inhibitory' (British Medical Dictionary, Caxton Publ. Co., 1961).     

Death of a trypanosome: a selfish altruism

African trypanosomes and some related parasitic protozoa are affected by a form of programmed cell death (PCD) that shows typical hallmarks of apoptosis. Although it has been speculated that PCD has a function in life-cycle progression and the struggle for survival of these parasites, no satisfactory model has yet been proposed for the molecular mechanism(s) of PCD in protozoa, raising questions about its physiological relevance in these organisms. As we discuss here, the most important point that needs to be addressed is whether a single-celled organism can undertake a process that is considered altruistic.     

The Role of Compassion in Altruistic Helping and Punishment Behavior

Compassion, the emotional response of caring for another who is suffering and that results in motivation to relieve suffering, is thought to be an emotional antecedent to altruistic behavior. However, it remains unclear whether compassion enhances altruistic behavior in a uniform way or is specific to sub-types of behavior such as altruistic helping of a victim or altruistic punishment of a transgressor. We investigated the relationship between compassion and subtypes of altruistic behavior using third-party paradigms where participants 1) witnessed an unfair economic exchange between a transgressor and a victim, and 2) had the opportunity to either spend personal funds to either economically a) help the victim or b) punish the transgressor. In Study 1, we examined whether individual differences in self-reported empathic concern (the emotional component of compassion) was associated with greater altruistic helping or punishment behavior in two independent samples. For participants who witnessed an unfair transaction, trait empathic concern was associated with greater helping of a victim and had no relationship to punishment. However, in those who decided to punish the transgressor, participants who reported greater empathic concern decided to punish less. In Study 2, we directly enhanced compassion using short-term online compassion meditation training to examine whether altruistic helping and punishment were increased after two weeks of training. Compared to an active reappraisal training control group, the compassion training group gave more to help the victim and did not differ in punishment of the transgressor. Together, these two studies suggest that compassion is related to greater altruistic helping of victims and is not associated with or may mitigate altruistic punishment of transgressors.     

Multilevel selection and human altruism

Views on the evolution of altruism based upon multilevel selection on structured populations pay little attention to the difference between fortuitous and deliberate processes leading to assortative grouping. Altruism may evolve when assortative grouping is fortuitously produced by forces external to the organism. But when it is deliberately produced by the same proximate mechanism that controls altruistic responses, as in humans, exploitation of altruists by selfish individuals is unlikely and altruism evolves as an individually advantageous trait. Groups formed with altruists of this sort are special, because they are not affected by subversion from within. A synergistic process where altruism is selected both at the individual and at the group level can take place.     

Altruism and organism: disentangling the themes of multilevel selection theory

The evolution of groups into adaptive units, similar to single organisms in the coordination of their parts, is one major theme of multilevel selection theory. Another major theme is the evolution of altruistic behaviors that benefit others at the expense of self. These themes are often assumed to be strongly linked, such that altruism is required for group-level adaptation. Multilevel selection theory reveals a more complex relationship between the themes of altruism and organism. Adaptation at every level of the biological hierarchy requires a corresponding process of natural selection, which includes the fundamental ingredients of phenotypic variation, heritability, and fitness consequences. These ingredients can exist for many kinds of groups and do not require the extreme genetic variation among groups that is usually associated with the evolution of altruism. Thus, it is reasonable to expect higher-level units to evolve into adaptive units with respect to specific traits, even when their members are not genealogically related and do not behave in ways that are obviously altruistic. As one example, the concept of a group mind, which has been well documented in the social insects, may be applicable to other species.     

The co-evolution of culturally inherited altruistic helping and cultural transmission under random group formation

Limited migration results in kin selective pressure on helping behaviors under a wide range of ecological, demographic and life-history situations. However, such genetically determined altruistic helping can evolve only when migration is not too strong and group size is not too large. Cultural inheritance of helping behaviors may allow altruistic helping to evolve in groups of larger size because cultural transmission has the potential to markedly decrease the variance within groups and augment the variance between groups. Here, we study the co-evolution of culturally inherited altruistic helping behaviors and two alternative cultural transmission rules for such behaviors. We find that conformist transmission, where individuals within groups tend to copy prevalent cultural variants (e.g., beliefs or values), has a strong adverse effect on the evolution of culturally inherited helping traits. This finding is at variance with the commonly held view that conformist transmission is a crucial factor favoring the evolution of altruistic helping in humans. By contrast, we find that under one-to-many transmission, where individuals within groups tend to copy a “leader” (or teacher), altruistic helping can evolve in groups of any size, although the cultural transmission rule itself hitchhikes rather weakly with a selected helping trait. Our results suggest that culturally determined helping behaviors are more likely to be driven by “leaders” than by popularity, but the emergence and stability of the cultural transmission rules themselves should be driven by some extrinsic factors.     

The economics of altruistic punishment and the maintenance of cooperation

Explaining the evolution and maintenance of cooperation among unrelated individuals is one of the fundamental problems in biology and the social sciences. Recent findings suggest that altruistic punishment is an important mechanism maintaining cooperation among humans. We experimentally explore the boundaries of altruistic punishment to maintain cooperation by varying both the cost and the impact of punishment, using an exceptionally extensive subject pool. Our results show that cooperation is only maintained if conditions for altruistic punishment are relatively favourable: low cost for the punisher and high impact on the punished. Our results indicate that punishment is strongly governed by its cost-to-impact ratio and that its effect on cooperation can be pinned down to one single variable: the threshold level of free-riding that goes unpunished. Additionally, actual pay-offs are the lowest when altruistic punishment maintains cooperation, because the pay-off destroyed through punishment exceeds the gains from increased cooperation. Our results are consistent with the interpretation that punishment decisions come from an amalgam of emotional response and cognitive cost-impact analysis and suggest that altruistic punishment alone can hardly maintain cooperation under multi-level natural selection. Uncovering the workings of altruistic punishment as has been done here is important because it helps predicting under which conditions altruistic punishment is expected to maintain cooperation.     

The remarkable discreteness of being

Life is a discrete, stochastic phenomenon: for a biological organism, the time of the two most important events of its life (reproduction and death) is random and these events change the number of individuals of the species by single units. These facts can have surprising, counterintuitive consequences. I review here three examples where these facts play, or could play, important roles: the spatial distribution of species, the structuring of biodiversity and the (Darwinian) evolution of altruistic behaviour.     

Altruism and mental disorders

Data suggest that the theories of kin selection and reciprocal altruism are viable working models to explain altruistic behavior. It remains to be demonstrated if these models can explain the behavior of persons with mentaL disorders for whom altruistic behavior is reported to be reduced. This paper addresses this issue. Part I reviews proximate factors that are thought to influence both altruistic decision making and interindividual variation in altruistic behavior. The focus is on trait signaling by potential beneficiaries and the evaluation of signals and altruistic decision making by potential altruists. In Part II, points developed in Part I are combined with clinical and empirical findings to analyze data on personality disorders and dysthymic disorder. The analysis leads to three causal hypotheses: Reduced altruistic behavior may be an evolved strategy, a consequence of dysfunctional recognition systems or algorithms, and/or a secondary response to an increase in symptoms. Different disorders and features of disorders are explained by each hypothesis.     

Archaeal DNA uracil repair via direct strand incision: A minimal system reconstituted from purified components

Hydrolytic deamination of DNA cytosine residues results in U/G mispairs, pre-mutagenic lesions threatening long-term genetic stability. Hence, DNA uracil repair is ubiquitous throughout all extant life forms and base excision repair, triggered by a uracil DNA glycosylase (UDG), is the mechanistic paradigm adopted, as it seems, by all bacteria and eukaryotes and a large fraction of archaea. However, members of the UDG superfamily of enzymes are absent from the extremely thermophilic archaeon Methanothermobacter thermautotrophicus ΔH. This organism, as a hitherto unique case, initiates repair by direct strand incision next to the DNA-U residue, a reaction catalyzed by the DNA uridine endonuclease Mth212, an ExoIII homologue. To elucidate the detailed mechanism, in particular to identify the molecular partners contributing to this repair process, we reconstituted DNA uracil repair in vitro from only four purified enzymes of M. thermautotrophicus ΔH. After incision at the 5′-side of a 2′-d-uridine residue by Mth212 DNA polymerase B (mthPolB) is able to take over the 3′-OH terminus and carry out repair synthesis generating a 5′-flap structure that is resolved by mthFEN, a 5′-flap endonuclease. Finally, DNA ligase seals the resulting nick. This defines mechanism and minimal enzymatic requirements of DNA-U repair in this organism.     

Sociobiology and the structural stability of behavior patterns

A structural stability approach to population-genetic systems and to dynamic evolutionary games is attempted in order to examine the theoretical significance of sociobiological selection models. A criterion of weak selection is derived that is not restricted to differential reproduction in polymorphic systems but describes possible directions of evolutionary change in time scales governed by genetic mutation rates. The criterion applies to the problems of how the initial mutational basis of an adaptive trait may be established and how this may happen, for analogous traits, independently in different species. Two basic sociobiological concepts are reconsidered with reference to the criterion. It is shown that W. D. Hamilton's condition of increases in inclusive fitness due to altruistic interactions among kin expresses the structural instability of populations against the evolution of altruistic behavior. Using the dynamic approach to evolutionary game theory, it is demonstrated that if a behavioral phenotype is an evolutionarily stable strategy, it is structurally stable against perturbations of the fitness payoffs, provided selection is weak. These results are applied to material problems of the evolution of animal social behavior.     

Kin selection,kin avoidance and correlated strategies

Summary Kin selection of correlated strategies is examined for both weak and strong altruism under simple haploid inheritance. While kin assortment enhances the range of evolutionary stability for (strongly altruistic) correlated strategies (defined herein), kin avoidance is possible under a weakly altruistic correlated strategy. When social competition induces role assignments of variable fitness, group mates may prefer association with non-relatives. Even when group life is mandatory, an individual may accept the risk of abandonment (and reproductive death) rather then associate with kin: a competitive superior may behave altruistically by permitting competitively inferior kin to emigrate. Thus, kin selection and social competition are not necessarily mutually supportive processes within groups. I conclude by interpreting dominance as a strongly altruistic correlated strategy in two social hymenopteran contexts.     

The evolution of cell death programs as prerequisites of multicellularity

One of the hallmarks of multicellularity is that the individual cellular fate is sacrificed for the benefit of a higher order of life-the organism. The accidental death of cells in a multicellular organism results in swelling and membrane-rupture and inevitably spills cell contents into the surrounding tissue with deleterious effects for the organism. To avoid this form of necrotic death the cells of metazoans have developed complex self-destruction mechanisms, collectively called programmed cell death, which see to an orderly removal of superfluous cells. Since evolution never invents new genes but plays variations on old themes by DNA mutations, it is not surprising, that some of the genes involved in metazoan death pathways apparently have evolved from homologues in unicellular organisms, where they originally had different functions. Interestingly some unicellular protozoans have developed a primitive form of non-necrotic cell death themselves, which could mean that the idea of an altruistic death for the benefit of genetically identical cells predated the invention of multicellularity. The cell death pathways of protozoans, however, show no homology to those in metazoans, where several death pathways seem to have evolved in parallel. Mitochondria stands at the beginning of several death pathways and also determines, whether a cell has sufficient energy to complete a death program. However, the endosymbiotic bacterial ancestors of mitochondria are unlikely to have contributed to the recent mitochondrial death machinery and therefore, these components may derive from mutated eukaryotic precursors and might have invaded the respective mitochondrial compartments. Although there is no direct evidence, it seems that the prokaryotic-eukaryotic symbiosis created the space necessary for sophisticated death mechanisms on command, which in their distinct forms are major factors for the evolution of multicellular organisms.     

Sudden Oak Death: Interactions of the Exotic Oomycete Phytophthora ramorum with Na?ve North American Hosts

Ten years after a threatening and previously unknown disease of oaks and tanoaks appeared in coastal California, a significant amount of progress has been made toward the understanding of its causal agent Phytophthora ramorum and of the novel pathosystems associated with this exotic organism. However, a complete understanding of the ecology and epidemiology of this species still eludes us. In part, our inability to fully understand this organism is due to its phylogenetic, phylogeographic, phenotypic, and epidemiological complexities, all reviewed in this paper. Most lines of evidence suggest that the high degree of disease severity reported in California is not simply due to a generalized lack of resistance or tolerance in naïve hosts but also to an innate ability of the pathogen to survive in unfavorable climatic conditions and to reproduce rapidly when conditions become once again favorable.     

Does dishonesty really invite third-party punishment? Results of a more stringent test

Many experiments have demonstrated that people are willing to incur cost to punish norm violators even when they are not directly harmed by the violation. Such altruistic third-party punishment is often considered an evolutionary underpinning of large-scale human cooperation. However, some scholars argue that previously demonstrated altruistic third-party punishment against fairness-norm violations may be an experimental artefact. For example, envy-driven retaliatory behaviour (i.e. spite) towards better-off unfair game players may be misidentified as altruistic punishment. Indeed, a recent experiment demonstrated that participants ceased to inflict third-party punishment against an unfair player once a series of key methodological problems were systematically controlled for. Noticing that a previous finding regarding apparently altruistic third-party punishment against honesty-norm violations may have been subject to methodological issues, we used a different and what we consider to be a more sound design to evaluate these findings. Third-party punishment against dishonest players withstood this more stringent test.