Spite and the scale of competition in Pseudomonas aeruginosa

Scale of competition has been shown to be an important factor in shaping the evolution of social interactions. Although many theoretical and experimental studies have examined its effect on altruistic cooperation, relatively little research effort has been focused on spiteful behaviors--actions that harm both the actor and the recipient. In this study, we expand on existing theory by investigating the importance of the global frequency of spiteful alleles, and we determine experimentally how the scale of competition affects selection for spite in the bacterial pathogen Pseudomonas aeruginosa under high and intermediate spatial relatedness. Consistent with our theoretical results, we found in our experiments that spiteful genotypes are more favored under local (rather than global) competition and intermediate (rather than high) spatial relatedness, conditions that have been shown to select against indiscriminate altruism.     

Pairwise competition and the replicator equation

Spite in Hamilton’s sense is defined as the willingness to harm oneself in order to harm another more. The standard replicator dynamic predicts that evolutionarily stable strategies are payoff-maximizing equilibria of the underlying game, and hence rules out the evolution of spiteful behavior. We propose a modified replicator dynamic, where selection is based on local outcomes, rather than on the population ’state’, as in standard models. We show that under this new model spite can evolve readily. The new dynamic suggests conditions under which spite in animals might be found.     

Effect of the presence of empty sites on the evolution of cooperation by costly punishment in spatial games

Cooperation and spiteful behavior are still evolutionary puzzles. Costly punishment, for which the game payoff is the same as that of spiteful behavior, is one mechanism for promoting the evolution of cooperation. A spatially structured population facilitates the evolution of either cooperation or spite/punishment if cooperation is linked explicitly or implicitly with spite/punishment; a cooperator cooperates with another cooperator and punishes/spites the other type of player. Different updating rules in the evolutionary game produce different evolutionary outcomes: with one updating rule—the score-dependent viability model, in which a player dies with a probability inversely proportional to the game score and the resulting unoccupied site is colonized by one player chosen randomly—the evolution of spite/punishment is promoted more than with the other updating rule—the score-dependent fertility model, in which, after a player dies randomly, the site is colonized by a player with a higher game score. If the population has empty sites, spiteful players or punishers should have less chance to interact with others and then spite/punish others. Thus the presence of empty sites would affect the evolutionary dynamics of spite/punishment. Here, we investigated whether the presence of empty sites discourages the evolution of spite/punishment in both a lattice-structured population and a completely mixing population where players interact with others randomly, especially when the score-dependent viability model is adopted. In the lattice-structured population adopting this viability model, the presence of empty sites promoted the evolution of cooperation and did not reduce the effect of spite/punishment. In the completely mixing population, the presence of empty sites did not promote evolution of cooperation by punishment. The evolutionary dynamics of the score-dependent viability model with empty sites were close to those of the score-dependent fertility model.     

Could sex be maintained through harmful males?

All else being equal, parthenogenetic females should produce as many surviving daughters as sexual couples produce daughters plus sons. Hence the resources spent on producing sons are a cost of sex and parthenogenetic females economize on sons. It has recently been shown that a small competitive advantage of sexual individuals can recoup this large reproductive disadvantage, while the adaptation behind the competitive advantage might differ from case to case. One hypothesis that has not yet been considered as a potential competitive advantage is that males could differentially harm parthenogenetic females, for example, through harassment, toxic seminal fluids, or infanticide. Harmful male functions result from the selection for males that maximise their fitness at the expense of females in the context of sexual conflict. Unless parthenogenetic lineages can maintain their resistance against harmful male functions, a competitive advantage for sex should be a by-product benefit of sexual conflict.
Mutations that make males harm parthenogenetic females worse than sexual ones, however, can be seen as evolutionary spite. The spiteful trait is not the production of costly sons, but the production of males that discriminate against parthenogenetic females. Spiteful behaviour can be positively selected, if it acts against negatively related victims. Sexual and parthenogenetic individuals within a population should usually be negatively related, because the genomes of the sexual individuals are bound together by recombination while those of parthenogenetic individuals will be identical except for divergence through mutation.
Some unusual cases of parthenogenesis are discussed in the light of this new hypothesis and an experimental approach for testing it is suggested.     

Spiteful soldiers and sex ratio conflict in polyembryonic parasitoid wasps

The existence of spiteful behaviors remains controversial. Spiteful behaviors are those that are harmful to both the actor and the recipient, and they represent one of the four fundamental types of social behavior (alongside selfishness, altruism, and mutual benefit). It has generally been assumed that the conditions required for spite to evolve are too restrictive, and so spite is unlikely to be important. This idea has been challenged in recent years, with the realization that localized competition can relax the conditions required for spite to evolve. Here we develop a theoretical model for a prime candidate for a spiteful behavior, the production of the sterile soldier caste in polyembryonic wasps. Our results show that (a) the biology of these soldiers is consistent with their main role being to mediate conflict over the sex ratio and not to defend against competitors and (b) greater conflict will occur in more outbred populations. We also show that the production of the sterile soldier caste can be classed as a spiteful behavior but that, to an extent, this is merely a semantic choice, and other interpretations such as altruism or indirect altruism are valid. However, the spite interpretation is useful in that it can lead to a more natural interpretation of relatedness and facilitate the classification of behaviors in a way that emphasizes biologically interesting differences that can be empirically tested.     

Evolution of spite through indirect reciprocity

How can cooperation persist in the face of a temptation to ''cheat''? Several recent papers have suggested that the answer may lie in indirect reciprocity. Altruistic individuals may benefit by eliciting altruism from observers, rather than (as in direct reciprocity) from the recipient of the aid they provide. Here, we point out that indirect reciprocity need not always favour cooperation; by contrast, it may support spiteful behaviour, which is costly for the both actor and recipient. Existing theory suggests spite is unlikely to persist, but we demonstrate that it may do so when spiteful individuals are less likely to incur aggression from observers (a negative form of indirect reciprocity).     

An evolutionary analysis of the relationship between spite and altruism

We investigate the selective pressures on a social trait when evolution occurs in a population of constant size. We show that any social trait that is spiteful simultaneously qualifies as altruistic. In other words, any trait that reduces the fitness of less related individuals necessarily increases that of related ones. Our analysis demonstrates that the distinction between "Hamiltonian spite" and "Wilsonian spite" is not justified on the basis of fitness effects. We illustrate this general result with an explicit model for the evolution of a social act that reduces the recipient's survival ("harming trait"). This model shows that the evolution of harming is favoured if local demes are of small size and migration is low (philopatry). Further, deme size and migration rate determine whether harming evolves as a selfish strategy by increasing the fitness of the actor, or as a spiteful/altruistic strategy through its positive effect on the fitness of close kin.     

THE EVOLUTIONARY DYNAMICS OF SPITE IN FINITE POPULATIONS

Spite, the shady relative of altruism, involves paying a fitness cost to inflict a cost on some recipient. Here, we investigate a density dependent dynamic model for the evolution of spite in populations of changing size. We extend the model by introducing a dynamic carrying capacity. Our analysis shows that it is possible for unconditionally spiteful behavior to evolve without population structure in any finite population. In some circumstances spiteful behavior can contribute to its own stability by limiting population growth. We use the model to show that there are differences between spite and altruism, and to refine Hamilton’s original argument about the insignificance of spite in the wild. We also discuss the importance of fixing the measure of fitness to classify behaviors as selfish or spiteful.     

Spiteful interactions between sympatric natural isolates of Xenorhabdus bovienii benefit kin and reduce virulence

Spite occurs when an individual harms itself in the act of harming others. Spiteful behaviour may be more pervasive in nature than commonly thought. One of the clearest examples of spite is the costly production and release of bacteriocins, antimicrobial toxins noted for their ability to kill conspecifics. A key question is to what extent these toxins provide a fitness advantage to kin of the producer cell, especially in natural communities. Additionally, when bacteria are involved in parasitic relationships, spiteful interactions are predicted to lower bacterial densities within a host, causing a reduction in parasite-induced virulence. Using five sympatric, field-collected genotypes of the insect pathogen Xenorhabdus bovienii, we experimentally demonstrate that bacteriocin production benefits kin within the host, and that it slows the mortality rate of the host. These results confirm that spite among naturally coexisting bacterial clones can be a successful kin-selected strategy that has emergent effects on virulence.     

THE EVOLUTION OF SPITE: POPULATION STRUCTURE AND BACTERIOCIN‐MEDIATED ANTAGONISM IN TWO NATURAL POPULATIONS OF XENORHABDUS BACTERIA

Spite occurs when an individual harms itself in the act of harming other individuals. Such behaviors were once assumed to be of limited evolutionary importance, as the conditions for the evolution of spite were thought to be too restrictive. Recent theoretical work, however, suggests that spatial population structure, which allows local competition among genotypes, could favor the evolution of spite. One of the clearest examples of spite is the costly production and release by bacteria of toxins (called bacteriocins) that can kill unrelated strains of the same species. Here, we establish the existence of spatial structure in two natural populations of bacteriocin‐producing bacteria. Specifically, relatedness decreased with increasing spatial distance between the field isolates. In addition, toxin‐mediated inhibitions were found only between isolates that were collected more than 1 m apart and that were generally less than 80% similar in their genomic fingerprints. Taken together, the results suggest that the bacteria are spatially structured, with mixing of genotypes and spiteful interactions at the boundaries between demes.     

Spite and the scale of competition

In recent years there has been a large body of theoretical work examining how local competition can reduce and even remove selection for altruism between relatives. However, it is less well appreciated that local competition favours selection for spite, the relatively neglected ugly sister of altruism. Here, we use extensions of social evolution theory that were formulated to deal with the consequences for altruism of competition between social partners, to illustrate several points on the evolution of spite. Specifically, we show that: (i) the conditions for the evolution of spite are less restrictive than previously assumed; (ii) previous models which have demonstrated selection for spite often implicitly assumed local competition; (iii) the scale of competition must be allowed for when distinguishing different forms of spite (Hamiltonian vs. Wilsonian); (iv) local competition can enhance the spread of spiteful greenbeards; and (v) the theory makes testable predictions for how the extent of spite should vary dependent upon population structure and average relatedness.     

What's in it for me? Self-regard precludes altruism and spite in chimpanzees

Sensitivity to fairness may influence whether individuals choose to engage in acts that are mutually beneficial, selfish, altruistic, or spiteful. In a series of three experiments, chimpanzees (Pan troglodytes) could pull a rope to access out-of-reach food while concomitantly pulling another piece of food further away. In the first study, they could make a choice that solely benefited themselves (selfishness), or both themselves and another chimpanzee (mutualism). In the next two experiments, they could choose between providing food solely for another chimpanzee (altruism), or for neither while preventing the other chimpanzee from receiving a benefit (spite). The main result across all studies was that chimpanzees made their choices based solely on personal gain, with no regard for the outcomes of a conspecific. These results raise questions about the origins of human cooperative behaviour.     

SPITE VERSUS CHEATS: COMPETITION AMONG SOCIAL STRATEGIES SHAPES VIRULENCE IN PSEUDOMONAS AERUGINOSA

Social interactions have been shown to play an important role in bacterial evolution and virulence. The majority of empirical studies conducted have only considered social traits in isolation, yet numerous social traits, such as the production of spiteful bacteriocins (anticompetitor toxins) and iron‐scavenging siderophores (a public good) by the opportunistic pathogen Pseudomonas aeruginosa, are frequently expressed simultaneously. Crucially, both bacteriocin production and siderophore cheating can be favored under the same competitive conditions, and we develop theory and carry out experiments to determine how the success of a bacteriocin‐producing genotype is influenced by social cheating of susceptible competitors and the resultant impact on disease severity (virulence). Consistent with our theoretical predictions, we find that the spiteful genotype is favored at higher local frequencies when competing against public good cheats. Furthermore, the relationship between spite frequency and virulence is significantly altered when the spiteful genotype is competed against cheats compared with cooperators. These results confirm the ecological and evolutionary importance of considering multiple social traits simultaneously. Moreover, our results are consistent with recent theory regarding the invasion conditions for strong reciprocity (helping cooperators and harming noncooperators).     

The evolution of cytoplasmic incompatibility or when spite can be successful

It is proposed that the phenomena of cytoplasmic incompatibility is explicable in terms of the selfish interests of the prokaryotic symbionts associated with the phenomena. It is hypothesized that in males the symbionts produce a product, termed wolbachin, which is carried in sperm and has the capability of inhibiting zygotic development if not neutralized. Symbionts are capable of neutralizing wolbachin. If this is the correct mechanism then the symbionts by killing eggs incapable of neutralizing wolbachin are acting spitefully. A simple model demonstrates that spiteful symbionts can invade a population of non-spiteful symbionts. The resulting population of spiteful symbionts is capable of resisting invasion by other spiteful symbionts even if the invaders have more efficient vertical transmission. Spite is successful in this system because all of the costs of being spiteful are inflicted on the host and not on the symbionts. This is in contrast to other systems of spite.     

Impact of Psychopathy on Moral Judgments about Causing Fear and Physical Harm

Psychopathy is a personality variable associated with persistent immoral behaviors. Despite this, attempts to link moral reasoning deficits to psychopathic traits have yielded mixed results with many findings supporting intact moral reasoning in individuals with psychopathic traits. Abundant evidence shows that psychopathy impairs responses to others’ emotional distress. However, most studies of morality and psychopathy focus on judgments about causing others physical harm. Results of such studies may be inconsistent because physical harm is an imperfect proxy for emotional distress. No previous paradigm has explicitly separated judgments about physical harm and emotional distress and assessed how psychopathy affects each type of judgment. In three studies we found that psychopathy impairs judgments about causing others emotional distress (specifically fear) but minimally affects judgments about causing physical harm and that judgments about causing fear predict instrumental aggression in psychopathy. These findings are consistent with reports linking psychopathy to insensitivity to others’ fear, and suggest that sensitivity to others’ fear may play a fundamental role in the types of moral decision-making impaired by psychopathy.     

KIN-MEDIATED MORPHOGENESIS IN FACULTATIVELY CANNIBALISTIC TADPOLES

Inclusive fitness theory predicts that organisms can increase their fitness by helping or not harming relatives, and many animals modify their behavior toward kin in a manner consistent with this prediction. Morphogenesis also may be sensitive to kinship environment, particularly in species where certain individuals facultatively develop structures that can be used against conspecifics as weaponry. We tested this hypothesis by examining whether and how consanguinity affected the probability that a structurally distinctive carnivore phenotype, which is opportunistically cannibalistic, would be produced in plains spadefoot toad tadpoles (Spea bombifrons) and southern spadefoot toad tadpoles (S. multiplicata). For tadpoles of S. multiplicata, individuals were significantly more likely to express the carnivore phenotype in mixed sibship groups than in pure sibship groups. For tadpoles of S. bombifrons, individuals were significantly more likely to express the carnivore phenotype when reared alone than in pure sibship groups. Both outcomes were independent of food availability or sibship specific differences in size or growth rate, and waterborne chemical signals from nonkin were sufficient to trigger expression of the carnivore phenotype. Our results suggest that morphogenesis may be responsive to kinship environment in any species or population that occurs as multiple, environmentally induced forms (polyphenism) that differ in their ability to help or to harm others.     

The harm principle as a mid-level principle?: three problems from the context of infectious disease control

Effective infectious disease control may require states to restrict the liberty of individuals. Since preventing harm to others is almost universally accepted as a legitimate (prima facie) reason for restricting the liberty of individuals, it seems plausible to employ a mid-level harm principle in infectious disease control. Moral practices like infectious disease control support - or even require - a certain level of theory-modesty. However, employing a mid-level harm principle in infectious disease control faces at least three problems. First, it is unclear what we gain by attaining convergence on a specific formulation of the harm principle. Likely candidates for convergence, a harm principle aimed at preventing harmful conduct, supplemented by considerations of effectiveness and always choosing the least intrusive means still leave ample room for normative disagreement. Second, while mid-level principles are sometimes put forward in response to the problem of normative theories attaching different weight to moral principles, employing a mid-level harm principle completely leaves open how to determine what weight to attach to it in application. Third, there appears to be a trade-off between attaining convergence and finding a formulation of the harm principle that can justify liberty-restrictions in all situations of contagion, including interventions that are commonly allowed. These are not reasons to abandon mid-level theorizing altogether. But there is no reason to be too theory-modest in applied ethics. Morally justifying e.g. if a liberty-restriction in infectious disease control is proportional to the aim of harm-prevention, promptly requires moving beyond the mid-level harm principle.     

Diel vertical migration of zooplankton: optimum migrating schedule based on energy accumulation

Zooplankton perform diel vertical migration (DVM) to avoid predators at the upper water layer, but often stay in the upper water layer throughout the day seeking food in spite of the presence of predators. This difference in migrating behavior has been explained by differences in environmental conditions or genetic differences. We examined theoretically how nutritious conditions of zooplankton individuals relate to determining different migrating behavior. A simple optimization model, maximizing the population growth rate, demonstrates that zooplankton individuals change their migrating behavior depending on the amount of accumulated energy. Such energy accumulation and its investment in reproduction are repeated every reproductive cycle. Therefore, unless the reproductive cycle is synchronized among individuals, different migrating behaviors will be observed within a population even if no genetic differences exist. Our model demonstrates that such coexistence of the two migrating behaviors is possible in natural Daphnia populations, and suggests that internal conditions of zooplankton individuals may be important as a factor for determining migrating behavior of zooplankton. This revised version was published online in July 2006 with corrections to the Cover Date.     

Reproductive skew can provide a net advantage in both conditional and unconditional social interactions

We revisit a model for the evolution of costly social behaviour in the presence of reproductive skew. The model population is structured into groups, and reproductive skew is captured by assuming individuals adopt one of two social roles (dominant/subordinate). Unlike previous work, we adopt an ultimate perspective by tracking a mutant allele over the entire course of an invasion. Our main analysis applies the theory of branching processes, but a parallel analysis using the inclusive-fitness approach is also provided. Our first two results are modifications of known inequalities describing selective advantages for behaviours expressed conditional upon social status. We find that altruistic subordinate individuals are favoured more readily than previously thought; spiteful dominant individuals, however, are favoured less readily. Secondly, we identify the condition under which unconditional altruism (performed by both dominant and subordinate) will be adaptive. Our third main result shows that increasing the strength of selection can also change the range of parameters over which costly social behaviours are favoured. We find that stronger selection makes it relatively easier for subordinate altruism to emerge, but more difficult for dominant spite and unconditional altruism to occur. We discuss the possible implications of our results for human social evolution.     

The Harm of Bioethics: A Critique of Singer and Callahan on Obesity

Debate concerning the social impact of obesity has been ongoing since at least the 1980s. Bioethicists, however, have been relatively silent. If obesity is addressed it tends to be in the context of resource allocation or clinical procedures such as bariatric surgery. However, prominent bioethicists Peter Singer and Dan Callahan have recently entered the obesity debate to argue that obesity is not simply a clinical or personal issue but an ethical issue with social and political consequences. This article critically examines two problematic aspects of Singer and Callahan's respective approaches. First, there is an uncritical assumption that individuals are autonomous agents responsible for health‐related effects associated with food choices. In their view, individuals are obese because they choose certain foods or refrain from physical activity. However, this view alone does not justify intervention. Both Singer and Callahan recognize that individuals are free to make foolish choices so long as they do not harm others. It is at this point that the second problematic aspect arises. To interfere legitimately in the liberty of individuals, they invoke the harm principle. I contend, however, that in making this move both Singer and Callahan rely on superficial readings of public health research to amplify the harm caused by obese individuals and ignore pertinent epidemiological research on the social determinants of obesity. I argue that the mobilization of the harm principle and corresponding focus on individual behaviours without careful consideration of the empirical research is itself a form of harm that needs to be taken seriously.