Nice natives and mean migrants: the evolution of dispersal-dependent social behaviour in viscous populations

There has been much interest in the evolution of social behaviour in viscous populations. While low dispersal increases the relatedness of neighbours, which tends to promote the evolution of indiscriminate helping behaviour, it can also increase competition between neighbours, which tends to inhibit the evolution of helping and may even favour harming behaviour. In the simplest scenario, these two effects exactly cancel, so that dispersal rate has no impact on the evolution of helping or harming. Here, we show that dispersal rate does matter when individuals can adjust their social behaviour conditional on whether they have dispersed or whether they have remained close to their place of origin. We find that nondispersing individuals are weakly favoured to indiscriminately help their neighbours, whereas dispersing individuals are more readily favoured to indiscriminately harm their neighbours.     

Siderophore-mediated cooperation and virulence in Pseudomonas aeruginosa

Why should organisms cooperate with each other? Helping close relatives that are likely to share the same genes (kin selection) is one important explanation that is likely to apply across taxa. The production of metabolically costly extracellular iron-scavenging molecules (siderophores) by microorganisms is a cooperative behaviour because it benefits nearby conspecifics. We review experiments focusing on the production of the primary siderophore (pyoverdin) of the opportunistic bacterial pathogen, Pseudomonas aeruginosa, which test kin selection theories that seek to explain the evolution of cooperation. First, cooperation is indeed favoured when individuals interact with their close relatives and when there is competition between groups of cooperators and noncooperators, such that the benefit of cooperation can be realized. Second, the relative success of cheats and cooperators is a function of their frequencies within populations. Third, elevated mutation rates can confer a selective disadvantage under conditions when cooperation is beneficial, because high mutation rates reduce how closely bacteria are related to each other. Fourth, cooperative pyoverdin production is also shown to be favoured by kin selection in vivo (caterpillars), and results in more virulent infections. Finally, we briefly outline ongoing and future work using this experimental system.     

Kin competition,natal dispersal and the moulding of senescence by natural selection

Most theoretical models for the evolution of senescence have assumed a very large, well mixed population. Here, we investigate how limited dispersal and kin competition might influence the evolution of ageing by deriving indicators of the force of selection, similar to Hamilton (Hamilton 1966 J. Theor. Biol. 12, 12–45). Our analytical model describes how the strength of selection on survival and fecundity changes with age in a patchy population, where adults are territorial and a fraction of juveniles disperse between territories. Both parent–offspring competition and sib competition then affect selection on age-specific life-history traits. Kin competition reduces the strength of selection on survival. Mutations increasing mortality in some age classes can even be favoured by selection, but only when fecundity deteriorates rapidly with age. Population structure arising from limited dispersal however selects for a broader distribution of reproduction over the lifetime, potentially slowing down reproductive senescence. The antagonistic effects of limited dispersal on age schedules of fecundity and mortality cast doubts on the generality of conditions allowing the evolution of ‘suicide genes’ that increase mortality rates without other direct pleiotropic effects. More generally, our model illustrates how limited dispersal and social interactions can indirectly produce patterns of antagonistic pleiotropy affecting vital rates at different ages.     

Simultaneous failure of two sex-allocation invariants: implications for sex-ratio variation within and between populations

Local mate competition (LMC) occurs when male relatives compete for mating opportunities, and this may favour the evolution of female-biased sex allocation. LMC theory is among the most well developed and empirically supported topics in behavioural ecology, clarifies links between kin selection, group selection and game theory, and provides among the best quantitative evidence for Darwinian adaptation in the natural world. Two striking invariants arise from this body of work: the number of sons produced by each female is independent of both female fecundity and also the rate of female dispersal. Both of these invariants have stimulated a great deal of theoretical and empirical research. Here, we show that both of these invariants break down when variation in female fecundity and limited female dispersal are considered in conjunction. Specifically, limited dispersal of females following mating leads to local resource competition (LRC) between female relatives for breeding opportunities, and the daughters of high-fecundity mothers experience such LRC more strongly than do those of low-fecundity mothers. Accordingly, high-fecundity mothers are favoured to invest relatively more in sons, while low-fecundity mothers are favoured to invest relatively more in daughters, and the overall sex ratio of the population sex ratio becomes more female biased as a result.     

Evolutionary dynamics of interlinked public goods traits: an experimental study of siderophore production in Pseudomonas aeruginosa

Public goods cooperation is common in microbes, and there is much interest in understanding how such traits evolve. Research in recent years has identified several important factors that shape the evolutionary dynamics of such systems, yet few studies have investigated scenarios involving interactions between multiple public goods. Here, we offer general predictions about the evolutionary trajectories of two public goods traits having positive, negative or neutral regulatory influence on one another's expression, and we report on a test of some of our predictions in the context of Pseudomonas aeruginosa's production of two interlinked iron‐scavenging siderophores. First, we confirmed that both pyoverdine and pyochelin siderophores do operate as public goods under appropriate environmental conditions. We then tracked their production in lines experimentally evolved under different iron‐limitation regimes known to favour different siderophore expression profiles. Under strong iron limitation, where pyoverdine represses pyochelin, we saw a decline in pyoverdine and a concomitant increase in pyochelin – consistent with expansion of pyoverdine‐defective cheats derepressed for pyochelin. Under moderate iron limitation, pyochelin declined – again consistent with an expected cheat invasion scenario – but there was no concomitant shift in pyoverdine because cross‐suppression between the traits is unidirectional only. Alternating exposure to strong and moderate iron limitation caused qualitatively similar though lesser shifts compared to the constant‐environment regimes. Our results confirm that the regulatory interconnections between public goods traits can significantly modulate the course of evolution, yet also suggest how we can start to predict the impacts such complexities will have on phenotypic divergence and community stability.     

The evolution of bacterial mutation rates under simultaneous selection by interspecific and social parasitism

Many bacterial populations harbour substantial numbers of hypermutable bacteria, in spite of hypermutation being associated with deleterious mutations. One reason for the persistence of hypermutators is the provision of novel mutations, enabling rapid adaptation to continually changing environments, for example coevolving virulent parasites. However, hypermutation also increases the rate at which intraspecific parasites (social cheats) are generated. Interspecific and intraspecific parasitism are therefore likely to impose conflicting selection pressure on mutation rate. Here, we combine theory and experiments to investigate how simultaneous selection from inter- and intraspecific parasitism affects the evolution of bacterial mutation rates in the plant-colonizing bacterium Pseudomonas fluorescens. Both our theoretical and experimental results suggest that phage presence increases and selection for public goods cooperation (the production of iron-scavenging siderophores) decreases selection for mutator bacteria. Moreover, phages imposed a much greater growth cost than social cheating, and when both selection pressures were imposed simultaneously, selection for cooperation did not affect mutation rate evolution. Given the ubiquity of infectious phages in the natural environment and clinical infections, our results suggest that phages are likely to be more important than social interactions in determining mutation rate evolution.     

Routes to indirect fitness in cooperatively breeding vertebrates: kin discrimination and limited dispersal

Hamilton demonstrated that the evolution of cooperative behaviour is favoured by high relatedness, which can arise through kin discrimination or limited dispersal (population viscosity). These two processes are likely to operate with limited overlap: kin discrimination is beneficial when variation in relatedness is higher, whereas limited dispersal results in less variable and higher average relatedness, reducing selection for kin discrimination. However, most empirical work on eukaryotes has focused on kin discrimination. To address this bias, we analysed how kin discrimination and limited dispersal interact to shape helping behaviour across cooperatively breeding vertebrates. We show that kin discrimination is greater in species where the: (i) average relatedness in groups is lower and more variable; (ii) effect of helpers on breeders reproductive success is greater; and (iii) probability of helping was measured, rather than the amount of help provided. There was also an interaction between these effects with the correlation between the benefits of helping and kin discrimination being stronger in species with higher variance in relatedness. Overall, our results suggest that kin discrimination provides a route to indirect benefits when relatedness is too variable within groups to favour indiscriminate cooperation.     

Co‐evolutionary dynamics between public good producers and cheats in the bacterium Pseudomonas aeruginosa

The production of beneficial public goods is common in the microbial world, and so is cheating – the exploitation of public goods by nonproducing mutants. Here, we examine co‐evolutionary dynamics between cooperators and cheats and ask whether cooperators can evolve strategies to reduce the burden of exploitation, and whether cheats in turn can improve their exploitation abilities. We evolved cooperators of the bacterium Pseudomonas aeruginosa, producing the shareable iron‐scavenging siderophore pyoverdine, together with cheats, defective in pyoverdine production but proficient in uptake. We found that cooperators managed to co‐exist with cheats in 56% of all replicates over approximately 150 generations of experimental evolution. Growth and competition assays revealed that co‐existence was fostered by a combination of general adaptions to the media and specific adaptions to the co‐evolving opponent. Phenotypic screening and whole‐genome resequencing of evolved clones confirmed this pattern, and suggest that cooperators became less exploitable by cheats because they significantly reduced their pyoverdine investment. Cheats, meanwhile, improved exploitation efficiency through mutations blocking the costly pyoverdine‐signalling pathway. Moreover, cooperators and cheats evolved reduced motility, a pattern that likely represents adaptation to laboratory conditions, but at the same time also affects social interactions by reducing strain mixing and pyoverdine sharing. Overall, we observed parallel evolution, where co‐existence of cooperators and cheats was enabled by a combination of adaptations to the abiotic and social environment and their interactions.     

Stable public goods cooperation and dynamic social interactions in yeast

Despite long-standing theoretical interest in the evolution of cooperation, empirical data on the evolutionary dynamics of cooperative traits remain limited. Here, we investigate the evolutionary dynamics of a simple public goods cooperative trait, invertase secretion, using a long-term selection experiment in Saccharomyces cerevisiae. We show that average investment in cooperation remains essentially constant over a period of hundreds of generations in viscous populations with high relatedness. Average cooperation remains constant despite transient local selection for high and low levels of cooperation that generate dynamic social interactions. Natural populations of yeast show similar variation in social strategies, which is consistent with the existence of similar selective pressures on public goods cooperation in nature.     

Evolution of helping and harming in heterogeneous populations

There has been much interest in understanding how demographic factors can mediate social evolution in viscous populations. Here, we examine the impact of heterogeneity in patch quality--that is, the availability of reproductive resources for each breeder--upon the evolution of helping and harming behaviors. We find that, owing to a cancellation of relatedness and kin competition effects, the evolution of obligate and facultative helping and harming is not influenced by the degree of viscosity in populations characterized by either spatial or temporal heterogeneity in patch quality. However, facultative helping and harming may be favored when there is both spatial and temporal heterogeneity in patch quality, with helping and harming being favored in both high-quality and low-quality patches. We highlight the prospect for using kin selection theory to explain within-population variation in social behavior, and point to the need for further theoretical and empirical investigation of this topic.     

Selection on non-social traits limits the invasion of social cheats

While the conditions that favour the maintenance of cooperation have been extensively investigated, the significance of non-social selection pressures on social behaviours has received little attention. In the absence of non-social selection pressures, patches of cooperators are vulnerable to invasion by cheats. However, we show both theoretically, and experimentally with the bacterium Pseudomonas fluorescens, that cheats may be unable to invade patches of cooperators under strong non-social selection (both a novel abiotic environment and to a lesser extent, the presence of a virulent parasite). This is because beneficial mutations are most likely to arise in the numerically dominant cooperator population. Given the ubiquity of novel selection pressures on microbes, these results may help to explain why cooperation is the norm in natural populations of microbes.     

Crystal toxins and the volunteer's dilemma in bacteria

The growth and virulence of the bacteria Bacillus thuringiensis depend on the production of Cry toxins, which are used to perforate the gut of its host. Successful invasion of the host relies on producing a threshold amount of toxin, after which there is no benefit from producing more toxin. Consequently, the production of Cry toxin appears to be a different type of social problem compared with the public goods scenarios that bacteria usually encounter. We show that selection for toxin production is a volunteer's dilemma. We make specific predictions that (a) selection for toxin production depends upon an interplay between the number of bacterial cells that each host ingests and the genetic relatedness between those cells; (b) cheats that do not produce toxin gain an advantage when at low frequencies, and at high bacterial density, allowing them to be maintained in a population alongside toxin‐producing cells. More generally, our results emphasize the diversity of the social games that bacteria play.     

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).     

Demography, altruism, and the benefits of budding

It is now widely appreciated that competition between kin inhibits the evolution of altruism. In standard population genetics models, it is difficult for indiscriminate altruism towards social partners to be favoured at all. The reason is that while limited dispersal increases the kinship of social partners it also intensifies local competition. One solution that has received very little attention is if individuals disperse as groups (budding dispersal), as this relaxes local competition without reducing kinship. Budding behaviour is widespread through all levels of biological organization, from early protocellular life to cooperatively breeding vertebrates. We model the effects of individual dispersal, budding dispersal, soft selection and hard selection to examine the conditions under which altruism is favoured. More generally, we examine how these various demographic details feed into relatedness and scale of competition parameters that can be included into Hamilton's rule.     

ASYMMETRIC PATCH SIZE DISTRIBUTION LEADS TO DISRUPTIVE SELECTION ON DISPERSAL

Numerous models have been designed to understand how dispersal ability evolves when organisms live in a fragmented landscape. Most of them predict a single dispersal rate at evolutionary equilibrium, and when diversification of dispersal rates has been predicted, it occurs as a response to perturbation or environmental fluctuation regimes. Yet abundant variation in dispersal ability is observed in natural populations and communities, even in relatively stable environments. We show that this diversification can operate in a simple island model without temporal variability: disruptive selection on dispersal occurs when the environment consists of many small and few large patches, a common feature in natural spatial systems. This heterogeneity in patch size results in a high variability in the number of related patch mates by individual, which, in turn, triggers disruptive selection through a high per capita variance of inclusive fitness. Our study provides a likely, parsimonious and testable explanation for the diversity of dispersal rates encountered in nature. It also suggests that biological conservation policies aiming at preserving ecological communities should strive to keep the distribution of patch size sufficiently asymmetric and variable.     

Kin selection and natal dispersal in an age-structured population

We examine the effect of iteroparity on the evolution of dispersal for a species living in a stable but fragmented habitat. We use a kin selection model that incorporates the effects of demographic stochasticity on the local age structure and age-specific genetic identities. We consider two cases: when the juvenile dispersal rate is allowed to change with maternal age and when it is not. In the latter case, we find that the unconditional evolutionarily stable dispersal rate increases when the adult survival rate increases. Two antagonistic forces act upon the evolution of age-specific dispersal rates. First, when the local age structure varies between patches of habitat, the intensity of competition between adults and juveniles in the natal patch is, on average, lower for offspring born to older senescent mothers. This selects for decreasing dispersal with maternal age. Second, offspring born to older parents are on average more related to other juveniles in the same patch and they experience a higher intensity of kin competition, which selects for increasing dispersal with maternal age. We show that the evolutionary outcome results from a balance between these two opposing forces, which depends on the amount of variance in age structure among sub-populations.     

Ecological succession,patch age and the evolution of social behaviour and terminal investment

Recent years have witnessed a growing interest in understanding the evolution of social behaviour in heterogeneous spatially structured populations. These studies, however, have neglected the impact of extinction–colonisation dynamics and ecological succession on the dynamical expression of social behaviour over time. Here, I present a kin‐selection model in which patches are structured into age‐classes. I show that ecological succession and patch age lead to highly plastic social phenotypes that vary dramatically as societies age since their initial establishment until their ultimate collapse. I find that the mode of colonisation following dispersal strongly influences the patch age‐dependent trajectories of social phenotypes. When patches are colonised by a random collection of immigrants, aggression is favoured during the build‐up of a society, but it slowly subsides until it eventually gives place to cooperation throughout the later stages of a society's lifespan. When newly established societies are formed by collectives of close relatives, cooperation is favoured during the build‐up of the society as well as when the society nears its eventual collapse. At intermediate societal ages, the genetic structure of the society is sufficiently resilient to the influx of immigrants such that cooperation remains relatively high. Moreover, I report a novel form of social terminal investment, whereby cooperative effort rises when patches approach their collapse. When dispersal is allowed to co‐evolve with cooperation, we observe a sudden rise in dispersal phenotypes before a patch's collapse, and the surprising result that clonal colonisation does not yield significantly higher levels of cooperation than the individual mode of colonisation. More generally, my results show that ecological succession strongly determines the dynamics of kin selection after colonisation, and therefore I expect that these findings will be valuable for understanding behavioural syndromes during range expansion or biological invasions.     

Investment in the public good through conditional phenotypes of large effect

We investigate the evolution of an individual's willingness to invest in a public good (what we call, helping) in a patch‐structured population with limited natal dispersal. We assume that an individual's decision to invest is informed by its dispersal status: an individual makes one decision given it is native to the patch on which it breeds, and is free to make a different decision given that it is not native to the patch on which it breeds. Unlike previous work, we assume that investment in the public good, and the public good, itself, both have a large effect on individual fecundity. Kin selection analysis reveals that only extreme investment decisions (i.e. ‘always invest’ or ‘never invest’) can be evolutionarily stable. Numerical results suggest that the evolutionary instability of the ‘never invest’ phenotype (what we call, complete nonhelping) implies the evolutionary stability of ‘always invest’ (what we call, complete helping). In addition, numerical results show that bistability of extreme phenotypes is possible, indicating that the adaptive significance of altruism, in this context, is greater than has been previously recognized. Numerical results are supported by computer simulation, and results, themselves, are briefly discussed in a concluding section.     

Individual and social discounting in a viscous population

Social discounting in economics involves applying a diminishing weight to community-wide benefits or costs into the future. It impacts on public policy decisions involving future positive or negative effects, but there is no consensus on the correct basis for determining the social discount rate. This study presents an evolutionary biological framework for social discounting. How an organism should value future benefits to its local community is governed by the extent to which members of the community in the future are likely to be its kin. Trade-offs between immediate and delayed benefits to an individual or to its community are analysed for a modelled patch-structured iteroparous population with limited dispersal. It is shown that the social discount rate is generally lower than the individual (private) discount rate. The difference in the two rates is most pronounced, in ratio terms, when the dispersal level is low and the hazard rate for patch destruction is much smaller than the individual mortality rate. When decisions involve enforced collective action rather than individuals acting independently, social investment increases but the social discount rate remains the same.     

Cooperation‐mediated plasticity in dispersal and colonization

Kin selection theory predicts that costly cooperative behaviors evolve most readily when directed toward kin. Dispersal plays a controversial role in the evolution of cooperation: dispersal decreases local population relatedness and thus opposes the evolution of cooperation, but limited dispersal increases kin competition and can negate the benefits of cooperation. Theoretical work has suggested that plasticity of dispersal, where individuals can adjust their dispersal decisions according to the social context, might help resolve this paradox and promote the evolution of cooperation. Here, we experimentally tested the hypothesis that conditional dispersal decisions are mediated by a cooperative strategy: we quantified the density‐dependent dispersal decisions and subsequent colonization efficiency from single cells or groups of cells among six genetic strains of the unicellular Tetrahymena thermophila that differ in their aggregation level (high, medium, and low), a behavior associated with cooperation strategy. We found that the plastic reaction norms of dispersal rate relative to density differed according to aggregation level: highly aggregative genotypes showed negative density‐dependent dispersal, whereas low‐aggregation genotypes showed maximum dispersal rates at intermediate density, and medium‐aggregation genotypes showed density‐independent dispersal with intermediate dispersal rate. Dispersers from highly aggregative genotypes had specialized long‐distance dispersal phenotypes, contrary to low‐aggregation genotypes; medium‐aggregation genotypes showing intermediate dispersal phenotype. Moreover, highly aggregation genotypes showed evidence for beneficial kin‐cooperation during dispersal. Our experimental results should help to resolve the evolutionary conflict between cooperation and dispersal: cooperative individuals are expected to avoid kin‐competition by dispersing long distances, but maintain the benefits of cooperation by dispersing in small groups.