Not only states but traits — Humans can identify permanent altruistic dispositions in 20 s

Humans behave altruistically in one-shot interactions under total anonymity. In search of explanations for such behavior, it has been argued that at least some individuals have a general tendency to behave altruistically independent of profitability. In fact, a stable altruistic trait would be adaptive if it were recognizable. Then, altruists could choose each other in order to retain benefits through mutual cooperation. Previous research has shown that individuals can predict the degree of altruistic behavior of strangers by reading signs of emotions evoked in significant social decisions. However, the identification of benevolent emotional states is no guarantee of the existence of permanent altruistic traits, though permanent traits are the preferable criterion for selection of good interaction partners. In this study, we tested whether individuals are able to identify altruistic traits. Judges watched 20-s silent video clips of unacquainted target persons and were asked to estimate the behavior of these target persons in a money-sharing task. As the videotapes of the target persons had been recorded in a setting unrelated to altruistic behavior, the judges could not base their estimates on situational cues related to the money-sharing task but instead had to draw on stable signals of altruism. Estimates were significantly better than chance, indicating that individuals can identify permanent altruistic traits in others. As this mechanism raises opportunities for selective interactions between altruists, our findings are discussed with respect to their relevance for explaining the evolution of altruism through assortment.     

Inertia: the discrepancy between individual and common good in dispersal and prospecting behaviour

The group selection debate of the 1960s made it clear that evolution does not necessarily increase population performance. Individuals can be selected to have traits that diminish a common good and make population persistence difficult. At the extreme, the discrepancy between levels of selection is predicted to make traits evolve towards values at which a population can no longer persist (evolutionary suicide). Dispersal and prospecting are prime examples of traits that have a strong influence on population persistence under environmental and demographic stochasticity. Theory predicts that an ‘optimal’ dispersal strategy from a population point of view can differ considerably from that produced by individual‐level selection. Because dispersal is frequently risky or otherwise costly, individuals are often predicted to disperse less than would be ideal for population performance (persistence or size). We define this discrepancy as ‘inertia’ and examine current knowledge of its occurrence and effects on population dynamics in nature. We argue that inertia is potentially widespread but that a framework is currently lacking for predicting precisely the extent to which it has a real influence on population persistence. The opposite of inertia, ‘hypermobility’ (more dispersal by individuals than would maximize population performance) remains a possibility: it is known that highest dispersal rates do not lead to best expected population performance, and examples of such high dispersal evolving exist at least in the theoretical literature. We also show, by considering prospecting behaviour, that similar issues arise in species with advanced cognitive and learning abilities. Individual prospecting strategies and the information acquired during dispersal are known to influence the decisions and therefore the fate of individuals and, as a corollary, populations. Again, the willingness of individuals to sample environments might evolve to levels that are not optimal for populations. This conflict can take intriguing forms. For example, better cognitive abilities of individuals may not always lead to better population‐level performance. Simulation studies have found that ‘blind’ dispersal can lead to better connected metapopulations than cognitively more advanced habitat choice rules: the latter can lead to too many individuals sticking to nearby safe habitat. The study of the mismatch between individual and population fitness should not be a mere intellectual exercise. Population managers typically need to take a population‐level view of performance, which may necessitate human intervention if it differs from what is selected for. We conclude that our knowledge of inertia and hypermobility would advance faster if theoretical studies—without much additional effort—quantified the population consequences of the evolving traits and compared this with hypothetical (not selectively favoured) dispersal rules, and if empirical studies were similarly conducted with the differing levels of selection in mind.     

Group selection in plant populations

Summary Several mechanisms have been proposed for group selection, to account for the evolution of altruistic traits. One type, Neighbourhood models, suggests that individuals react with those immediately around them, but with no recognition mechanism. The organization of plant populations seems especially favorable for this type of selection. The possibility of Neighbourhood selection was investigated by simulating a plant population. It was possible for an altruistic trait to evolve, though only under restricted conditions. The main requirement was gene flow only by very restricted pollen dispersal, and a high benefit : cost ratio in the altruistic relationship. Under conditions favourable for such evolution, the starting frequency of the allele, the initial pattern, and the population size, had little effect. Inbreeding tended to prevent the increase of the altruism allele, though this depended on the mechanism of selfing. Known ecological features of plants are discussed that could be considered altruistic and hence require some form of group selection for their evolution, and whether the benefit : cost requirements are likely to be met. Neighbourhood models of group selection are a possibility in plant populations, and we therefore cannot exclude the possibility of altruism in plants. However, Neighbourhood selection is weak force, unlikely to be effective in the face of opposing individual selection. It may be more important as reinforcement of individual selection.     

Selection for altruism through random drift in variable size populations

ABSTRACT: BACKGROUND: Altruistic behavior is defined as helping others at a cost to oneself and a lowered fitness. The lower fitness implies that altruists should be selected against, which is in contradiction with their widespread presence is nature. Present models of selection for altruism (kin or multilevel) show that altruistic behaviors can have 'hidden' advantages if the 'common good' produced by altruists is restricted to some related or unrelated groups. These models are mostly deterministic, or assume a frequency dependent fitness. RESULTS: Evolutionary dynamics is a competition between deterministic selection pressure and stochastic events due to random sampling from one generation to the next. We show here that an altruistic allele extending the carrying capacity of the habitat can win by increasing the random drift of "selfish" alleles. In other terms, the fixation probability of altruistic genes can be higher than those of a selfish ones, even though altruists have a smaller fitness. Moreover when populations are geographically structured, the altruists advantage can be highly amplified and the fixation probability of selfish genes can tend toward zero. The above results are obtained both by numerical and analytical calculations. Analytical results are obtained in the limit of large populations. CONCLUSIONS: The theory we present does not involve kin or multilevel selection, but is based on the existence of random drift in variable size populations. The model is a generalization of the original Fisher-Wright and Moran models where the carrying capacity depends on the number of altruists.     

Local adaptation at the range peripheries of Sitka spruce

High‐dispersal rates in heterogeneous environments and historical rapid range expansion can hamper local adaptation; however, we often see clinal variation in high‐dispersal tree species. To understand the mechanisms of the species’ distribution, we investigated local adaptation and adaptive plasticity in a range‐wide context in Sitka spruce, a wind‐pollinated tree species that has recently expanded its range after glaciations. Phenotypic traits were observed using growth chamber experiments that mimicked temperature and photoperiodic regimes from the limits of the species realized niche. Bud phenology exhibited parallel reaction norms among populations; however, putatively adaptive plasticity and strong divergent selection were seen in bud burst and bud set timing respectively. Natural selection appears to have favoured genotypes that maximize growth rate during available frost‐free periods in each environment. We conclude that Sitka spruce has developed local adaptation and adaptive plasticity throughout its range in response to current climatic conditions despite generally high pollen flow and recent range expansion.     

When is dispersal for dispersal? Unifying marine and terrestrial perspectives

Recent syntheses on the evolutionary causes of dispersal have focused on dispersal as a direct adaptation, but many traits that influence dispersal have other functions, raising the question: when is dispersal ‘for’ dispersal? We review and critically evaluate the ecological causes of selection on traits that give rise to dispersal in marine and terrestrial organisms. In the sea, passive dispersal is relatively easy and specific morphological, behavioural, and physiological adaptations for dispersal are rare. Instead, there may often be selection to limit dispersal. On land, dispersal is relatively difficult without specific adaptations, which are relatively common. Although selection for dispersal is expected in both systems and traits leading to dispersal are often linked to fitness, systems may differ in the extent to which dispersal in nature arises from direct selection for dispersal or as a by‐product of selection on traits with other functions. Our analysis highlights incompleteness of theories that assume a simple and direct relationship between dispersal and fitness, not just insofar as they ignore a vast array of taxa in the marine realm, but also because they may be missing critically important effects of traits influencing dispersal in all realms.     

Genome‐wide differentiation in closely related populations: the roles of selection and geographic isolation

Population divergence in geographic isolation is due to a combination of factors. Natural and sexual selection may be important in shaping patterns of population differentiation, a pattern referred to as ‘isolation by adaptation’ (IBA). IBA can be complementary to the well‐known pattern of ‘isolation by distance’ (IBD), in which the divergence of closely related populations (via any evolutionary process) is associated with geographic isolation. The barn swallow Hirundo rustica complex comprises six closely related subspecies, where divergent sexual selection is associated with phenotypic differentiation among allopatric populations. To investigate the relative contributions of selection and geographic distance to genome‐wide differentiation, we compared genotypic and phenotypic variation from 350 barn swallows sampled across eight populations (28 pairwise comparisons) from four different subspecies. We report a draft whole‐genome sequence for H. rustica, to which we aligned a set of 9493 single nucleotide polymorphisms (SNPs). Using statistical approaches to control for spatial autocorrelation of phenotypic variables and geographic distance, we find that divergence in traits related to migratory behaviour and sexual signalling, as well as geographic distance, together explain over 70% of genome‐wide divergence among populations. Controlling for IBD, we find 42% of genomewide divergence is attributable to IBA through pairwise differences in traits related to migratory behaviour and sexual signalling alone. By (i) combining these results with prior studies of how selection shapes morphological differentiation and (ii) accounting for spatial autocorrelation, we infer that morphological adaptation plays a large role in shaping population‐level differentiation in this group of closely related populations.     

Effect of group selection on the evolution of altruistic behavior

By using a Monte Carlo simulation, we studied the effect of group selection on the altruistic trait that is controlled by a single locus. The altruistic trait is disadvantageous to the bearer but advantageous to the others. Group selection is defined as the differential reproductive rate among demes caused by genotypic difference among demes. We found that the simulation reproduced many results of former studies. Additionally, when the mutation rate and the migration rate are small enough, we observed two new phenomena: (1) When the effect of the group selection is as large as that of the individual selection, the gene frequency is quite unstable. We found two local stable states, the A- and the S-state. When the metapopulation is in the A-state, altruists are nearly fixed. When in the S-state, on the contrary, altruists are almost lost. The metapopulation shifted quickly from one state to another. We call this phenomenon as the S-A transition. (2) When the mutation rate and migration rate are small enough we found an extremely strong mechanism to stop the non-altruists from expanding no matter how strong the individual selection coefficient is. This is caused by a phenomenon, which we call SA splitting, in which most demes are fixed either by altruists or non-altruists; thus, the relatedness of the metapopulation becomes nearly equal to one. We show SA splitting plays an important role in S-A transition. We define a parameter d to see the degree of SA splitting. We found that d is roughly proportional to mutation rate and deme size.     

"Runaway" social evolution: reinforcing selection for inbreeding and altruism.

Kin selection theory predicts that altruistic behaviors, those that decrease the fitness of the individual performing the behavior but increase the fitness of the recipient, can increase in frequency if the individuals interacting are closely related. Several studies have shown that inbreeding therefore generally increases the effectiveness of kin selection when fitnesses are linear, additive functions of the number of altruists in the family, although with extreme forms of altruism, inbreeding can actually retard the evolution of altruism. These models assume that a constant proportion of the population mates at random and a constant proportion practices some form of inbreeding. In order to investigate the effect of inbreeding on the evolution of altruistic behavior when the mating structure is allowed to evolve, we examined a two-locus model by computer simulation of a diploid case and illustrated the important qualitative features by mathematical analysis of a haploid case. One locus determines an individual's propensity to perform altruistic social behavior and the second locus determines the probability that an individual will mate within its sibship. We assumed positive selection for altruism and no direct selection at the inbreeding locus. We observed that the altruistic allele and the inbreeding allele become positively associated, even when the initial conditions of the model assume independence between these loci. This linkage disequilibrium becomes established, because the altruistic allele increases more rapidly in the inbreeding segment of the population. This association subsequently results in indirect selection on the inbreeding locus. However, the dynamics of this model go beyond a simple "hitch-hiking" effect, because high levels of altruism lead to increased inbreeding, and high degrees of inbreeding accelerate the rate of change of the altruistic allele in the entire population. Thus, the dynamics of this model are similar to those of "runaway" sexual selection, with gene frequency change at the two loci interactively causing rapid evolutionary change.     

Joint evolution of differential seed dispersal and self‐fertilization

Differential seed dispersal, in which selfed and outcrossed seeds possess different dispersal propensities, represents a potentially important individual‐level association. A variety of traits can mediate differential seed dispersal, including inflorescence and seed size variation. However, how natural selection shapes such associations is poorly known. Here, we developed theoretical models for the evolution of mating system and differential seed dispersal in metapopulations, incorporating heterogeneous pollination, dispersal cost, cost of outcrossing and environment‐dependent inbreeding depression. We considered three models. In the ‘fixed dispersal model’, only selfing rate is allowed to evolve. In the ‘fixed selfing model’, in which selfing is fixed but differential seed dispersal can evolve, we showed that natural selection favours a higher, equal or lower dispersal rate for selfed seeds to that for outcrossed seeds. However, in the ‘joint evolution model’, in which selfing and dispersal can evolve together, evolution necessarily leads to higher or equal dispersal rate for selfed seeds compared to that for outcrossed. Further comparison revealed that outcrossed seed dispersal is selected against by the evolution of mixed mating or selfing, whereas the evolution of selfed seed dispersal undergoes independent processes. We discuss the adaptive significance and constraints for mating system/dispersal association.     

Sensory trait variation contributes to biased dispersal of threespine stickleback in flowing water

Gene flow is widely thought to homogenize spatially separate populations, eroding effects of divergent selection. The resulting theory of ‘migration–selection balance’ is predicated on a common assumption that all genotypes are equally prone to dispersal. If instead certain genotypes are disproportionately likely to disperse, then migration can actually promote population divergence. For example, previous work has shown that threespine stickleback (Gasterosteus aculeatus) differ in their propensity to move up‐ or downstream (‘rheotactic response’), which may facilitate genetic divergence between adjoining lake and stream populations of stickleback. Here, we demonstrate that intraspecific variation in a sensory system (superficial neuromast lines) contributes to this variation in swimming behaviour in stickleback. First, we show that intact neuromasts are necessary for a typical rheotactic response. Next, we showed that there is heritable variation in the number of neuromasts and that stickleback with more neuromasts are more likely to move downstream. Variation in pectoral fin shape contributes to additional variation in rheotactic response. These results illustrate how within‐population quantitative variation in sensory and locomotor traits can influence dispersal behaviour, thereby biasing dispersal between habitats and favouring population divergence.     

Paradoxes of tumour complexity: somatic selection,vulnerability by design,or infectious aetiology?

The aetiology of cancer involves intricate cellular and molecular mechanisms that apparently emerge on the short timescale of a single lifetime. Some of these traits are remarkable not only for their complexity, but also because it is hard to conceive selection pressures that would favour their evolution within the local competitive microenvironment of the tumour. Examples include ‘niche construction’ (re‐programming of tumour‐specific target sites) to create permissive conditions for distant metastases; long‐range feedback loops of tumour growth; and remarkably ‘plastic’ phenotypes (e.g. density‐dependent dispersal) associated with metastatic cancer. These traits, which we term ‘paradoxical tumour traits’, facilitate the long‐range spread or long‐term persistence of the tumours, but offer no apparent benefit, and might even incur costs in the competition of clones within the tumour. We discuss three possible scenarios for the origin of these characters: somatic selection driven by specific selection regimes; non‐adaptive emergence due to inherent vulnerabilities in the organism; and manipulation by putative transmissible agents that contribute to and benefit from these traits. Our work highlights a lack of understanding of some aspects of tumour development, and offers alternative hypotheses that might guide further research.     

Interpreting the 'selection effect' of biodiversity on ecosystem function

Experimental ecosystems often function differently than expected under the null hypothesis that intra‐ and interspecific interactions are identical. Recent theory attributes this to the ‘selection effect’ (dominance by species with particular traits), and the ‘complementarity effect’ (niche differentiation and/or facilitative interactions). Using the Price Equation, I show that the ‘selection effect’ only partially reflects dominance by species with particular traits at the expense of other species, and therefore is only partially analogous to natural selection. I then derive a new, tripartite partition of the difference between observed and expected ecosystem function. The ‘dominance effect’ is analogous to natural selection. ‘Trait‐independent complementarity’ occurs when species function better than expected, independent of their traits and not at the expense of other species. ‘Trait‐dependent complementarity’ occurs when species with particular traits function better than expected, but not at the expense of other species. I illustrate the application of this new partition using experimental data.     

Prudent males,group adaptation,and the tragedy of the commons

For almost five decades three threads have coexisted in the evolutionary and ecological literature, with their links only recently becoming visible and some of them still not properly addressed. These are the levels of selection debate, the metaphor of the tragedy of the commons, and the evolutionary study of sexual conflict. We analyze the eco‐evolutionary dynamics of a curious system where an asexual all‐female fish species (the Amazon molly Poecilia formosa) requires sperm from other species as a developmental trigger, without utilizing the genes from sperm. The dynamics of such a system bear strong resemblance to host–parasite dynamics, and populations of the sexual ‘host’ species persist much better if males avoid mating with Amazons. However, such avoidance may compromise their current mating success, and if this is the case, prudent mating becomes an altruistic trait that helps to keep an accumulating problem of a competing species at bay, and Amazon‐free space can be seen to form a common good that a population should maintain for future generations. A model shows that the evolution of altruistic mating restraint is possible but selection for short‐term gains means that it will remain less than perfect. This helps to explain why the anomalous gynogenetic system can persist, but it also raises questions about what kinds of traits can be classified as adaptations when optimization is not perfect and traits evolve to achieve short‐term goals better than long‐term performance. Contributing to the levels of selection debate, we encourage researchers to study the implications of the different timescales involved in the eco‐evolutionary process.     

More on the genetical theory of multilevel selection

In my article The genetical theory of multilevel selection, I provided a synthesis of the theory of multilevel selection (MLS) and the theory of natural selection in class‐structured populations. I framed this synthesis within Fisher's genetical paradigm, taking a strictly genetical approach to traits and fitness. I showed that this resolves a number of long‐standing conceptual problems that have plagued the MLS literature, including the issues of ‘aggregate’ vs. ‘emergent’ group traits, ‘collective fitness₁’ vs. ‘collective fitness₂’ and ‘MLS1’ vs. ‘MLS2 ‘. In his commentary, Goodnight suggests this theoretical and conceptual synthesis is flawed in several respects. Here, I show this is incorrect, by: reiterating the theoretical and conceptual goals of my synthesis; clarifying that my genetical approach to traits is necessary for a proper analysis of the action of MLS independently of non‐Darwinian factors; emphasizing that the Price–Hamilton approach to MLS provides a consistent, useful and conceptually superior theoretical framework; and explaining the role of reproductive value in the study of natural selection in class‐structured populations. I also show that Goodnight's contextual analysis treatment of MLS in a class‐structured population is mathematically, biologically and conceptually inadequate.     

Conditions for the evolution of altruism under darwinian selection

A model of population structure is discussed which under certain circumstances allows for evolution of altruistic traits, beyond the classical restrictions imposed by kin selection theory and related concepts such as reciprocal altruism. Essentially, the model sees a large population as socially subdivided into small groups without any barriers, however, to free random mating. An altruistic trait is defined as lowering, locally, the fitness of a carrier below that of noncarriers within the same group; but the local fitness of an individual randomly chosen in a group increases with the number of altruists. It is shown that altruism can evolve even if the groups are randomly formed. The conditions for such evolution are contrasted with those prevailing when the groups are formed either with some phenotypic assortment between the members or on the basis of kinship. It is shown that any possibility of evolution tends to rapidly disappear as groups become large, unless there is complete positive assortment or individuals in the groups are kin. The example of alarm calls is also considered, and the two extremes of random and sib-groups are contrasted, using a model by Maynard Smith. It is shown that alarm calls can evolve in small groups of unrelated individuals under conditions qualitatively similar but quantitatively more rigorous than those prevailing for sib-groups.     

Spotting altruistic dictator game players and mingling with them: the elective assortation of classmates

Altruism can evolve through assortation if the selfish advantage of egoistic individuals is outcompeted by the benefits of mutual cooperation between altruists. This selection process is possible if (a) individuals can distinguish altruists from egoists and (b) altruists cooperate electively with other altruists, leaving egoists no chance but to mingle with each other. This study investigates whether these two conditions are fulfilled in a natural setting. One hundred twenty-two students of six secondary school classes (age 10 to 19 years) played an anonymous dictator game, which functioned as a measure of altruism. Afterwards and unannounced, the students had to estimate their classmates' decisions and did so better than chance. Sociometry revealed that the accuracy of predictions depended on social closeness. Friends and disliked classmates were judged more accurately than liked classmates or those met with indifference. Moreover, altruists were friends with more altruistic persons than were egoists. The results confirm the existence of the two prerequisites for the evolution of altruism through assortation: the predictability of altruistic behavior and the association of altruists.     

Altruists Proliferate Even at a Selective Disadvantage within Their Own Niche

The evolutionary origin of altruism is a long-standing puzzle. Numerous explanations have been proposed, most prominently based on inclusive fitness or group selection. One possibility that has not yet been considered is that new niches will be created disproportionately often when altruism appears, perhaps by chance, causing altruists to be over-represented in such new niches. This effect is a novel variant of group selection in which altruistic groups benefit by discovering unoccupied niches instead of by competing for the limited resources within a single niche. Both an analytical population genetics model and computational simulations support that altruism systematically arises due to this side effect of increased carrying capacity even when it is strongly selected against within any given niche. In fact, even when selection is very strongly negative and altruism does not develop in most populations, it can still be expected to be observed in a consistent fraction of species. The ecological structure provided by niches thereby may be sufficient for altruists to proliferate even if they are always at a disadvantage within each niche considered individually.     

The concepts of asymmetric and symmetric power can help resolve the puzzle of altruistic and cooperative behaviour

Evolutionary theory predicts competition in nature yet altruistic and cooperative behaviour appears to reduce the ability to compete in order to help others compete better. This evolutionary puzzle is usually explained by kin selection where close relatives perform altruistic and cooperative acts to help each other and by reciprocity theory (i.e. direct, indirect and generalized reciprocity) among non‐kin. Here, it is proposed that the concepts of asymmetry and symmetry in power and dominance are critical if we are ever to resolve the puzzle of altruism and cooperation towards non‐kin. Asymmetry in power and dominance is likely to emerge under competition in nature as individuals strive to gain greater access to the scarce resources needed to survive and reproduce successfully. Yet asymmetric power presents serious problems for reciprocity theory in that a dominant individual faces a temptation to cheat in interactions with subordinates that is likely to far outweigh any individual selective benefits gained through reciprocal mechanisms. Furthermore, action taken by subordinates to deter non‐reciprocation by dominants is likely to prove prohibitively costly to their fitness, making successful enforcement of reciprocal mechanisms unlikely. It is also argued here that many apparently puzzling forms of cooperation observed in nature (e.g. cooperative breeding in which unrelated subordinates help dominants to breed) might be best explained by asymmetry in power and dominance. Once it is recognized that individuals in these cooperative interactions are subject to the constraints and opportunities imposed on them by asymmetric power then they can be seen as pursuing a ‘least bad’ strategy to promote individual fitness – one that is nevertheless consistent with evolutionary theory. The concept of symmetric power also provides important insights. It can inhibit reciprocal mechanisms in the sense that symmetric power makes it easier for a cheat to appropriate common resources while incurring fewer penalties. Nevertheless under certain restrictive conditions, symmetric power is seen as likely to promote direct reciprocity through ‘tit for tat’.     

The role of environment and core‐margin effects on range‐wide phenotypic variation in a montane grasshopper

The integration of genetic information with ecological and phenotypic data constitutes an effective approach to gain insight into the mechanisms determining interpopulation variability and the evolutionary processes underlying local adaptation and incipient speciation. Here, we use the Pyrenean Morales grasshopper (Chorthippus saulcyi moralesi) as study system to (i) analyse the relative role of genetic drift and selection in range‐wide patterns of phenotypic differentiation and (ii) identify the potential selective agents (environment, elevation) responsible for variation. We also test the hypothesis that (iii) the development of dispersal‐related traits is associated with different parameters related to population persistence/turnover, including habitat suitability stability over the last 120 000 years, distance to the species distribution core and population genetic variability. Our results indicate that selection shaped phenotypic differentiation across all the studied morphological traits (body size, forewing length and shape). Subsequent analyses revealed that among‐population differentiation in forewing length was significantly explained by a temperature gradient, suggesting an adaptive response to thermoregulation or flight performance under contrasting temperature regimes. We found support for our hypothesis predicting a positive association between the distance to the species distribution core and the development of dispersal‐related morphology, which suggests an increased dispersal capability in populations located at range edges that, in turn, exhibit lower levels of genetic variability. Overall, our results indicate that range‐wide patterns of phenotypic variation are partially explained by adaptation in response to local environmental conditions and differences in habitat persistence between core and peripheral populations.