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.     

ON THE EVOLUTION OF HARMING AND RECOGNITION IN FINITE PANMICTIC AND INFINITE STRUCTURED POPULATIONS

Natural selection may favor two very different types of social behaviors that have costs in vital rates (fecundity and/or survival) to the actor: helping behaviors, which increase the vital rates of recipients, and harming behaviors, which reduce the vital rates of recipients. Although social evolutionary theory has mainly dealt with helping behaviors, competition for limited resources creates ecological conditions in which an actor may benefit from expressing behaviors that reduce the vital rates of neighbors. This may occur if the reduction in vital rates decreases the intensity of competition experienced by the actor or that experienced by its offspring. Here, we explore the joint evolution of neutral recognition markers and marker-based costly conditional harming whereby actors express harming, conditional on actor and recipient bearing different conspicuous markers. We do so for two complementary demographic scenarios: finite panmictic and infinite structured populations. We find that marker-based conditional harming can evolve under a large range of recombination rates and group sizes under both finite panmictic and infinite structured populations. A direct comparison with results for the evolution of marker-based conditional helping reveals that, if everything else is equal, marker-based conditional harming is often more likely to evolve than marker-based conditional helping.     

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.     

Kin selection, local competition, and reproductive skew

In a spatially structured population, limited dispersal gives rise to local relatedness, potentially favoring indiscriminate helping behavior. However, it also leads to local competition, which reduces the benefits of helping local kin. This tension has become the focus for a growing body of theoretical work. Existing models, however, have focused chiefly on the net impact of limited dispersal on cooperative or competitive effort in a homogeneous population. Here, I extend existing models of kin selection in a group-structured population to allow for asymmetries in expected fecundity and reproductive success among group members. I explore the consequent impact of limited dispersal on the evolution of helping and harming behavior, and on the degree of reproductive inequality or skew. I show that when individuals in a group differ in their expected fecundity, limited dispersal gives rise to kin selection for harming behavior on the part of more fecund individuals, and for helping behavior on the part of less fecund individuals. As a result, philopatry tends to exaggerate differences in reproductive success, and so promotes greater reproductive skew.     

Characterizing selection in black‐throated blue warblers using a sexual network approach

Our understanding of trait evolution is built upon studies that examine the correlation between traits and fitness, most of which implicitly assume all individuals experience similar selective environments. However, accounting for differences in selective pressures, such as variation in the social environment, can advance our understanding of how selection shapes individual traits and subsequent fitness. In this study, we test whether variation in the social environment affects selection on individual phenotype. We apply a new sexual network framework to quantify each male's social environment as the mean body size of his primary competitors. We test for direct and social selection on male body size using a 10‐year data set on black‐throated blue warblers (Setophaga caerulescens), a territorial species for which body size is hypothesized to mediate competition for mates. We found that direct selection on body size was weak and nonsignificant, as was social selection via the body size of the males' competitors. Analysing both types of selection simultaneously allows us to firmly reject a role for body size in competitive interactions between males and subsequent male fitness in this population. We evaluate the application of the sexual network approach to empirical data and suggest that other phenotypic traits such as song characteristics and plumage may be more relevant than body size for male–male competition in this small passerine bird.     

Cultural transmission can inhibit the evolution of altruistic helping

The study of culturally inherited traits has led to the suggestion that the evolution of helping behaviors is more likely with cultural transmission than without. Here we evaluate this idea through a comparative analysis of selection on helping under both genetic and cultural inheritance. We develop two simple models for the evolution of helping through cultural group selection: one in which selection on the trait depends solely on Darwinian fitness effects and one in which selection is driven by nonreproductive factors, specifically imitation of strategies achieving higher payoffs. We show that when cultural variants affect Darwinian fitness, the selection pressure on helping can be markedly increased relative to that under genetic transmission. By contrast, when variants are driven by nonreproductive factors, the selection pressure on helping may be reduced relative to that under genetic inheritance. This occurs because, unlike biological offspring, the spread of cultural variants from one group to another through imitation does not reduce the number of these variants in the source group. As a consequence, there is increased within-group competition associated with traits increasing group productivity, which reduces the benefits of helping. In these cases, selection for harming behavior (decreasing the payoff to neighbors) may occur rather than selection for helping.     

Endocrine mechanisms,behavioral phenotypes and plasticity: known relationships and open questions

Behavior of wild vertebrate individuals can vary in response to environmental or social factors. Such within-individual behavioral variation is often mediated by hormonal mechanisms. Hormones also serve as a basis for among-individual variations in behavior including animal personalities and the degree of responsiveness to environmental and social stimuli. How do relationships between hormones and behavioral traits evolve to produce such behavioral diversity within and among individuals? Answering questions about evolutionary processes generating among-individual variation requires characterizing how specific hormones are related to variation in specific behavioral traits, whether observed hormonal variation is related to individual fitness and, whether hormonal traits are consistent (repeatable) aspects of an individual's phenotype. With respect to within-individual variation, we need to improve our insight into the nature of the quantitative relationships between hormones and the traits they regulate, which in turn will determine how they may mediate behavioral plasticity of individuals. To address these questions, we review the actions of two steroid hormones, corticosterone and testosterone, in mediating changes in vertebrate behavior, focusing primarily on birds. In the first part, we concentrate on among-individual variation and present examples for how variation in corticosterone concentrations can relate to behaviors such as exploration of novel environments and parental care. We then review studies on correlations between corticosterone variation and fitness, and on the repeatability over time of corticosterone concentrations. At the end of this section, we suggest that further progress in our understanding of evolutionary patterns in the hormonal regulation of behavior may require, as one major tool, reaction norm approaches to characterize hormonal phenotypes as well as their responses to environments.In the second part, we discuss types of quantitative relationships between hormones and behavioral traits within individuals, using testosterone as an example. We review conceptual models for testosterone-behavior relationships and discuss the relevance of these models for within-individual plasticity in behavior. Next, we discuss approaches for testing the nature of quantitative relationships between testosterone and behavior, concluding that again reaction norm approaches might be a fruitful way forward.We propose that an integration of new tools, especially of reaction norm approaches into the field of behavioral endocrinology will allow us to make significant progress in our understanding of the mechanisms, the functional implications and the evolution of hormone–behavior relationships that mediate variation both within and among individuals. This knowledge will be crucial in light of already ongoing habitat alterations due to global change, as it will allow us to evaluate the mechanisms as well as the capacity of wild populations to adjust hormonally-mediated behaviors to altered environmental conditions.     

Population viscosity can promote the evolution of altruistic sterile helpers and eusociality

Because it increases relatedness between interacting individuals, population viscosity has been proposed to favour the evolution of altruistic helping. However, because it increases local competition between relatives, population viscosity may also act as a brake for the evolution of helping behaviours. In simple models, the kin selected fecundity benefits of helping are exactly cancelled out by the cost of increased competition between relatives when helping occurs after dispersal. This result has lead to the widespread view, especially among people working with social organisms, that special conditions are required for the evolution of altruism. Here, we re-examine this result by constructing a simple population genetic model where we analyse whether the evolution of a sterile worker caste (i.e. an extreme case of altruism) can be selected for by limited dispersal. We show that a sterile worker caste can be selected for even under the simplest life-cycle assumptions. This has relevant consequences for our understanding of the evolution of altruism in social organisms, as many social insects are characterized by limited dispersal and significant genetic population structure.     

Social competition as a driver of phenotype–environment correlations: implications for ecology and evolution

While it is universally recognised that environmental factors can cause phenotypic trait variation via phenotypic plasticity, the extent to which causal processes operate in the reverse direction has received less consideration. In fact individuals are often active agents in determining the environments, and hence the selective regimes, they experience. There are several important mechanisms by which this can occur, including habitat selection and niche construction, that are expected to result in phenotype–environment correlations (i.e. non-random assortment of phenotypes across heterogeneous environments). Here we highlight an additional mechanism – intraspecific competition for preferred environments – that may be widespread, and has implications for phenotypic evolution that are currently underappreciated. Under this mechanism, variation among individuals in traits determining their competitive ability leads to phenotype–environment correlation; more competitive phenotypes are able to acquire better patches. Based on a concise review of the empirical evidence we argue that competition-induced phenotype–environment correlations are likely to be common in natural populations before highlighting the major implications of this for studies of natural selection and microevolution. We focus particularly on two central issues. First, competition-induced phenotype–environment correlation leads to the expectation that positive feedback loops will amplify phenotypic and fitness variation among competing individuals. As a result of being able to acquire a better environment, winners gain more resources and even better phenotypes – at the expense of losers. The distinction between individual quality and environmental quality that is commonly made by researchers in evolutionary ecology thus becomes untenable. Second, if differences among individuals in competitive ability are underpinned by heritable traits, competition results in both genotype–environment correlations and an expectation of indirect genetic effects (IGEs) on resource-dependent life-history traits. Theory tells us that these IGEs will act as (partial) constraints, reducing the amount of genetic variance available to facilitate evolutionary adaptation. Failure to recognise this will lead to systematic overestimation of the adaptive potential of populations. To understand the importance of these issues for ecological and evolutionary processes in natural populations we therefore need to identify and quantify competition-induced phenotype–environment correlations in our study systems. We conclude that both fundamental and applied research will benefit from an improved understanding of when and how social competition causes non-random distribution of phenotypes, and genotypes, across heterogeneous environments.     

Cannibalism as an interacting phenotype: precannibalistic aggression is influenced by social partners in the endangered Socorro Isopod (Thermosphaeroma thermophilum)

Models for the evolution of cannibalism highlight the importance of asymmetries between individuals in initiating cannibalistic attacks. Studies may include measures of body size but typically group individuals into size/age classes or compare populations. Such broad comparisons may obscure the details of interactions that ultimately determine how socially contingent characteristics evolve. We propose that understanding cannibalism is facilitated by using an interacting phenotypes perspective that includes the influences of the phenotype of a social partner on the behaviour of a focal individual and focuses on variation in individual pairwise interactions. We investigated how relative body size, a composite trait between a focal individual and its social partner, and the sex of the partners influenced precannibalistic aggression in the endangered Socorro isopod, Thermosphaeroma thermophilum. We also investigated whether differences in mating interest among males and females influenced cannibalism in mixed sex pairs. We studied these questions in three populations that differ markedly in range of body size and opportunities for interactions among individuals. We found that relative body size influences the probability of and latency to attack. We observed differences in the likelihood of and latency to attack based on both an individual's sex and the sex of its partner but found no evidence of sexual conflict. The instigation of precannibalistic aggression in these isopods is therefore a property of both an individual and its social partner. Our results suggest that interacting phenotype models would be improved by incorporating a new conditional ψ, which describes the strength of a social partner's influence on focal behaviour.     

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.     

Variation in habitat choice and delayed reproduction: adaptive queuing strategies or individual quality differences?

In most species, some individuals delay reproduction or occupy inferior breeding positions. The queue hypothesis tries to explain both patterns by proposing that individuals strategically delay breeding (queue) to acquire better breeding or social positions. In 1995, Ens, Weissing, and Drent addressed evolutionarily stable queuing strategies in situations with habitat heterogeneity. However, their model did not consider the non-mutually exclusive individual quality hypothesis, which suggests that some individuals delay breeding or occupy inferior breeding positions because they are poor competitors. Here we extend their model with individual differences in competitive abilities, which are probably plentiful in nature. We show that including even the smallest competitive asymmetries will result in individuals using queuing strategies completely different from those in models that assume equal competitors. Subsequently, we investigate how well our models can explain settlement patterns in the wild, using a long-term study on oystercatchers. This long-lived shorebird exhibits strong variation in age of first reproduction and territory quality. We show that only models that include competitive asymmetries can explain why oystercatchers' settlement patterns depend on natal origin. We conclude that predictions from queuing models are very sensitive to assumptions about competitive asymmetries, while detecting such differences in the wild is often problematic.     

Evolutionary causes and consequences of consistent individual variation in cooperative behaviour

Behaviour is typically regarded as among the most flexible of animal phenotypic traits. In particular, expression of cooperative behaviour is often assumed to be conditional upon the behaviours of others. This flexibility is a key component of many hypothesized mechanisms favouring the evolution of cooperative behaviour. However, evidence shows that cooperative behaviours are often less flexible than expected and that, in many species, individuals show consistent differences in the amount and type of cooperative and non-cooperative behaviours displayed. This phenomenon is known as ‘animal personality’ or a ‘behavioural syndrome’. Animal personality is evolutionarily relevant, as it typically shows heritable variation and can entail fitness consequences, and hence, is subject to evolutionary change. Here, we review the empirical evidence for individual variation in cooperative behaviour across taxa, we examine the evolutionary processes that have been invoked to explain the existence of individual variation in cooperative behaviour and we discuss the consequences of consistent individual differences on the evolutionary stability of cooperation. We highlight that consistent individual variation in cooperativeness can both stabilize or disrupt cooperation in populations. We conclude that recognizing the existence of consistent individual differences in cooperativeness is essential for an understanding of the evolution and prevalence of cooperation.     

Social Selection and Indirect Genetic Effects in Structured populations

Social selection and indirect genetic effects (IGEs) are established concepts in both behavioural ecology and evolutionary genetics. While IGEs describe effects of an individual’s genotype on phenotypes of social partners (and may thus affect their fitness indirectly), the concept of social selection assumes that a given phenotype in one individual affects the fitness of other individuals directly. Although different frameworks, both have been used to investigate the evolution of social traits, such as cooperative behaviour. Despite their similarities (both concepts consider interactions among individuals), they differ in the type of interaction. It remains unclear whether the two concepts make the same predictions about evolutionary trajectories or not. To address this question, we investigate four possible scenarios of social interactions and compare the effects of IGEs and social selection for trait evolution in a multi-trait multi-member model. We show that the two mechanisms can yield similar evolutionary outcomes and that both can create selection pressure at the group level. However, the effect of IGEs can be stronger due to the possibility of feedback loops. Finally, we demonstrate that IGEs, but not social selection gradients, may lead to differences in the direction of evolutionary response between genotypes and phenotypes.     

THE EVOLUTION OF SOCIAL SIGNALS: MORPHOLOGICAL,FUNCTIONAL, AND GENETIC INTEGRATION OF THE SEX PHEROMONE IN NAUPHOETA CINEREA

Social signals that mediate intraspecific interactions can be complex, conveying considerable information concerning the probable behavior of individuals and minimizing overt aggression and wasted energy. In the cockroach Nauphoeta cinerea, male-male competition and female mate choice are mediated by a multicomponent male-produced sex pheromone. In this study, I examine variation in this pheromone. First I measure differences among males in both individual pheromone compounds and the overall composition of the pheromone. Principal component analysis is used to quantify and describe pheromone composition. Next, I explore some of the causes and consequences of this variation by examining the pheromone of males with different social experiences. Compared to subordinate males, dominant males have significantly less variable quantities of the individual pheromone compounds and are significantly less variable in the composition of their pheromone. Because of an association between status and mating success, male-male competition can result in stabilizing sexual selection on the sex pheromone. Finally, I test the hypothesis that the pheromone compounds evolve in a manner consistent with their function. As predicted for morphologically integrated characters, the patterns of phenotypic, genetic, and environmental correlations among my measures of pheromone compounds and composition match functional patterns suggested by this study and the developmental patterns demonstrated in my previous studies. Based on these studies of the N. cinerea sex pheromone, I argue that stabilizing sexual selection shapes the evolution of pheromonal communication involved in social interactions among male N. cinerea. Further, I argue that coordinated evolution of social signals may be possible due to the morphological integration of their multiple compounds.     

Phenotypic and Evolutionary Consequences of Social Behaviours: Interactions among Individuals Affect Direct Genetic Effects

Traditional quantitative genetics assumes that an individual''s phenotype is determined by both genetic and environmental factors. For many animals, part of the environment is social and provided by parents and other interacting partners. When expression of genes in social partners affects trait expression in a focal individual, indirect genetic effects occur. In this study, we explore the effects of indirect genetic effects on the magnitude and range of phenotypic values in a focal individual in a multi-member model analyzing three possible classes of interactions between individuals. We show that social interactions may not only cause indirect genetic effects but can also modify direct genetic effects. Furthermore, we demonstrate that both direct and indirect genetic effects substantially alter the range of phenotypic values, particularly when a focal trait can influence its own expression via interactions with traits in other individuals. We derive a function predicting the relative importance of direct versus indirect genetic effects. Our model reveals that both direct and indirect genetic effects can depend to a large extent on both group size and interaction strength, altering group mean phenotype and variance. This may lead to scenarios where between group variation is much higher than within group variation despite similar underlying genetic properties, potentially affecting the level of selection. Our analysis highlights key properties of indirect genetic effects with important consequences for trait evolution, the level of selection and potentially speciation.     

Plasticity in reproductive phenotypes reveals status-specific correlations between behavioral, morphological, and physiological sexual traits

Reproductive success is determined by a complex interplay between multiple sexual traits that promote mate acquisition and, following copulation, provide control over paternity. The intensity of sexual competition that individuals experience often fluctuates, and here we investigate how this influences the expression of reproductive traits and their relationships. We show in the fowl, Gallus gallus, that males of different social status, which experience different intensities of sexual competition, before and after copulation, have different reproductive phenotypes. Dominant males are more vigilant, feed less, and have larger sexual ornaments than subordinate males. Experimentally manipulating social status revealed that these differences were phenotypically plastic, indicating multiple sexual traits were dependent on the social environment. We integrated these data with previous published findings on changes in sperm numbers and velocity to show that relationships between traits were different for males when they were dominant and when they were subordinate. Furthermore, when males switched status a complex array of negative and positive correlations between the degree traits changed was observed. Our results suggest that variation in the intensity of sexual competition generates reversible plasticity in reproductive phenotypes and that relationships between sexual traits may be variable and influence the evolution of reproductive strategies.     

Density-dependent cooperation as a mechanism for persistence and coexistence

To overcome stress, such as resource limitation, an organism often needs to successfully mediate competition with other members of its own species. This may favor the evolution of defective traits that are harmful to the species population as a whole, and that may lead to its dilution or even to its extinction (the tragedy of the commons). Here, we show that this phenomenon can be circumvented by cooperation plasticity, in which an individual decides, based on environmental conditions, whether to cooperate or to defect. Specifically, we analyze the evolution of density-dependent cooperation. In our model, the population is spatially subdivided, periodically remixed, and comprises several species. We find that evolution pushes individuals to be more cooperative when their own species is at lower densities, and we show that not only could this cooperation prevent the tragedy of the commons, but it could also facilitate coexistence between many species that compete for the same resource.     

Maternal effects of egg size in brown trout (Salmo trutta): norms of reaction to environmental quality

The magnitude of fitness variation caused by maternal effects and, thus, the adaptive significance of maternal traits may depend on environmental quality, generating crossing reaction norms among offspring phenotypes that shape life-history evolution. By manipulating intraclutch variation in egg size and comparing siblings we examined the maternal effects of egg size on offspring performance and tested for the existence of reaction norms to environmental quality using the brown trout Salmo trutta. When sibling groups of small and large eggs were reared separately in a hatchery environment initial size differences disappeared rapidly. However, in semi-natural environments and under direct competition, juveniles from large eggs experienced growth and survival advantages over siblings from small eggs. Moreover, distinct reaction norms existed, with the differences in performance of juveniles from small and large eggs being most pronounced in the poorer growth environments. Our results provide the first direct evidence, to our knowledge, for a causal relationship between egg size and fitness-related traits in fishes, independent of potentially confounding genetic effects. Moreover, they indicate that previous studies have been biased by experimental conditions that excluded competitive asymmetries and environmental variability. The existence of reaction norms indicates a shift in optimal egg size across gradients of environmental quality that probably shapes the evolution of this trait.     

Quantitative genetics of natural variation of behavior in Drosophila melanogaster: the possible role of the social environment on creating persistent patterns of group activity

Using a set of nine effectively isogenic lines collected from nature in 1998, we observed unperturbed behaviors of mixed-sex groups of Drosophila melanogaster. We repeatedly scanned replicated groups of genetically identical individuals, five females and five males, and recorded the behavior of each individual (i.e., walking, feeding, grooming, flying, courting, mating, fighting, or resting). From these behaviors, we made a composite variable of activity for our quantitative genetic analysis. Genotypes differed in activity, explaining 14.41% of the variation in activity; 8.60% of the variation was explained by a significant genotype x sex interaction, which signifies genetic variation for sexual dimorphism in behavior. Phenotypic plasticity explained 11.13% of the variation in activity. Different genotypes and sexes within genotypes had different rank orders of the component behaviors that contribute to activity. We found no effect of common rearing environment. Instead, differences between replicate groups within genotype accounted for 19.47% variation in activity, and activity was significantly repeatable across scans. This emergent group behavior is likely caused by differences between groups of interacting individuals, even though individuals were genetically identical across groups. Thus, emergent group behavior explained almost as much variation in activity as the combined sources of genetic variation (23.01%), and this is an additional level on which selection could operate: individuals and groups. We discuss how differences among groups could change patterns of additive genetic variation available for evolution. Furthermore, because the behavior of an individual is influenced by conspecifics, genotype interactions between individuals could contribute to indirect selection. Finally, if we consider activity as a syndrome governing all component behaviors with strong genetic correlations among behaviors within an individual, then these component behaviors cannot evolve independently. These results suggest that reductionist approaches of molecular behavior genetics may be incomplete and/or misleading when considering similar phenotypes at the population level or when trying to understand how behaviors evolve.