Social bond dynamics and the evolution of helping.

Empiricists often struggle to apply game theory models to real-life cases of animal cooperation. One reason is that many examples of cooperation occur in stable groups, where individuals form social bonds that influence exchanges of help in ways that are not well described by previous models, including the extent of reciprocity and how relationships are initiated. We present a game theory model exploring the conditions under which social bonds between group members promote cooperation. In the model, bonds build up from exchanges of help in a similar way as the strength of association increases in learning, as in the Rescorla-Wagner rule. The bonds in turn affect partner choice and influence helping amounts. The model has a mechanism of reciprocity for bonded pairs, which can evolve toward either loose or strict reciprocation. Several aspects of the model are inspired by observations of food sharing in vampire bats. We find that small social neighborhoods are required for the evolutionary stability of helping, either as small group sizes, or if bonded members of larger groups can form temporary (daily) smaller groupings. The costs of helping need to be fairly low, while the benefits can be substantial. The form of reciprocity that evolves is neither immediate nor very strict. Individuals in need request help based on bond strength, but there is also an evolved preference for initiating bonds with new group members. In contrast, if different groups come into temporary contact, the evolved tendency is to avoid forming bonds between groups.

Effects of local versus global competition on reproductive skew and sex differences in social dominance behaviour.

Social hierarchies are often found in group-living animals. The hierarchy position can influence reproductive success (RS), with a skew towards high-ranking individuals. The amount of aggression in social dominance varies greatly, both between species and between males and females within species. Using game theory we study this variation by taking into account the degree to which reproductive competition in a social group is mainly local to the group, emphasizing within-group relative RS, or global to a larger population, emphasizing an individual's absolute RS. Our model is similar to recent approaches in that reinforcement learning is used as a behavioural mechanism allowing social-hierarchy formation. We test two hypotheses. The first is that local competition should favour the evolution of mating or foraging interference, and thus of reproductive skew. Second, decreases in reproductive output caused by an individual's accumulated fighting damage, such as reduced parenting ability, will favour less intense aggression but should have little influence on reproductive skew. From individual-based simulations of the evolution of social dominance and interference, we find support for both hypotheses. We discuss to what extent our results can explain observed sex differences in reproductive skew and social dominance behaviour.

Behavioural specialization and learning in social networks.

Interactions in social groups can promote behavioural specialization. One way this can happen is when individuals engage in activities with two behavioural options and learn which option to choose. We analyse interactions in groups where individuals learn from playing games with two actions and negatively frequency-dependent payoffs, such as producer-scrounger, caller-satellite, or hawk-dove games. Group members are placed in social networks, characterized by the group size and the number of neighbours to interact with, ranging from just a few neighbours to interactions between all group members. The networks we analyse include ring lattices and the much-studied small-world networks. By implementing two basic reinforcement-learning approaches, action-value learning and actor-critic learning, in different games, we find that individuals often show behavioural specialization. Specialization develops more rapidly when there are few neighbours in a network and when learning rates are high. There can be learned specialization also with many neighbours, but we show that, for action-value learning, behavioural consistency over time is higher with a smaller number of neighbours. We conclude that frequency-dependent competition for resources is a main driver of specialization. We discuss our theoretical results in relation to experimental and field observations of behavioural specialization in social situations.

An evolutionary perspective on stress responses, damage and repair.

Variation in stress responses has been investigated in relation to environmental factors, species ecology, life history and fitness. Moreover, mechanistic studies have unravelled molecular mechanisms of how acute and chronic stress responses cause physiological impacts ('damage'), and how this damage can be repaired. However, it is not yet understood how the fitness effects of damage and repair influence stress response evolution. Here we study the evolution of hormone levels as a function of stressor occurrence, damage and the efficiency of repair. We hypothesise that the evolution of stress responses depends on the fitness consequences of damage and the ability to repair that damage. To obtain some general insights, we model a simplified scenario in which an organism repeatedly encounters a stressor with a certain frequency and predictability (temporal autocorrelation). The organism can defend itself by mounting a stress response (elevated hormone level), but this causes damage that takes time to repair. We identify optimal strategies in this scenario and then investigate how those strategies respond to acute and chronic exposures to the stressor. We find that for higher repair rates, baseline and peak hormone levels are higher. This typically means that the organism experiences higher levels of damage, which it can afford because that damage is repaired more quickly, but for very high repair rates the damage does not build up. With increasing predictability of the stressor, stress responses are sustained for longer, because the animal expects the stressor to persist, and thus damage builds up. This can result in very high (and potentially fatal) levels of damage when organisms are exposed to chronic stressors to which they are not evolutionarily adapted. Overall, our results highlight that at least three factors need to be considered jointly to advance our understanding of how stress physiology has evolved: (i) temporal dynamics of stressor occurrence; (ii) relative mortality risk imposed by the stressor itself versus damage caused by the stress response; and (iii) the efficiency of repair mechanisms.

Reproductive skew, fighting costs and winner-loser effects in social dominance evolution.

Social hierarchies are often found in group-living animals and can be formed through pairwise aggressive interactions. The dominance rank can influence reproductive success (RS) with a skew towards high-ranking individuals. Using game theory, we investigate how the opportunity for differently ranked individuals to achieve RS influences the costs of hierarchy formation and the strength of winner and loser effects. In our model, individuals adjust their aggressive and submissive behaviour towards others through reinforcement learning. The learning is based on rewards and penalties, which depend on relative fighting ability. From individual-based simulations, we determine evolutionary equilibria of traits such as learning rates. We examine situations that differ in the extent of monopolisation of contested RS by dominants and in the proportion of total RS that is contested. The model implements two kinds of fighting costs: a decrease in effective fighting ability from damage (loss of condition) and a risk of mortality that increases with the total accumulated damage. Either of these costs can limit the amount of fighting. We find that individuals form stable dominance hierarchies, with a positive correlation between dominance position and fighting ability. The accumulated costs differ between dominance positions, with the highest costs paid by low or intermediately ranked individuals. Costs tend to be higher in high-skew situations. We identify a 'stay-in, opt-out' syndrome, comprising a range from weaker (stay-in) to stronger (opt-out) winner-loser effects. We interpret the opt-out phenotype to be favoured by selection on lower ranked individuals to opt out of contests over social dominance, because it is more pronounced when more of the total RS is uncontested. We discuss our results in relation to field and experimental observations and argue that there is a need for empirical investigation of the behaviour and reproductive success of lower ranked individuals.

The Evolution of Social Dominance through Reinforcement Learning.

AbstractGroups of social animals are often organized into dominance hierarchies that are formed through pairwise interactions. There is much experimental data on hierarchies, examining such things as winner, loser, and bystander effects, as well as the linearity and replicability of hierarchies, but there is a lack evolutionary analyses of these basic observations. Here I present a game theory model of hierarchy formation in which individuals adjust their aggressive behavior toward other group members through reinforcement learning. Individual traits such as the tendency to generalize learning between interactions with different individuals, the rate of learning, and the initial tendency to be aggressive are genetically determined and can be tuned by evolution. I find that evolution favors individuals with high social competence, making use of individual recognition, bystander observational learning, and, to a limited extent, generalizing learned behavior between opponents when adjusting their behavior toward other group members. The results are in qualitative agreement with experimental data, for instance, in finding weaker winner effects compared to loser effects.

Reinforcement Learning Theory Reveals the Cognitive Requirements for Solving the Cleaner Fish Market Task.

Learning is an adaptation that allows individuals to respond to environmental stimuli in ways that improve their reproductive outcomes. The degree of sophistication in learning mechanisms potentially explains variation in behavioral responses. Here, we present a model of learning that is inspired by documented intra- and interspecific variation in the performance of a simultaneous two-choice task, the biological market task. The task presents a problem that cleaner fish often face in nature: choosing between two client types, one that is willing to wait for inspection and one that may leave if ignored. The cleaner's choice hence influences the future availability of clients (i.e., it influences food availability). We show that learning the preference that maximizes food intake requires subjects to represent in their memory different combinations of pairs of client types rather than just individual client types. In addition, subjects need to account for future consequences of actions, either by estimating expected long-term reward or by experiencing a client leaving as a penalty (negative reward). Finally, learning is influenced by the absolute and relative abundance of client types. Thus, cognitive mechanisms and ecological conditions jointly explain intra- and interspecific variation in the ability to learn the adaptive response.

Ecological Genetic Conflict: Genetic Architecture Can Shift the Balance between Local Adaptation and Plasticity.

Genetic polymorphism can contribute to local adaptation in heterogeneous habitats, for instance, as a single locus with alleles adapted to different habitats. Phenotypic plasticity can also contribute to trait variation across habitats, through developmental responses to habitat-specific cues. We show that the genetic architecture of genetically polymorphic and plasticity loci may influence the balance between local adaptation and phenotypic plasticity. These effects of genetic architecture are instances of ecological genetic conflict. A reduced effective migration rate for genes tightly linked to a genetic polymorphism provides an explanation for the effects, and they can occur both for a single trait and for a syndrome of coadapted traits. Using individual-based simulations and numerical analysis, we investigate how among-habitat genetic polymorphism and phenotypic plasticity depend on genetic architecture. We also study the evolution of genetic architecture itself, in the form of rates of recombination between genetically polymorphic loci and plasticity loci. Our main result is that for plasticity genes that are unlinked to loci with between-habitat genetic polymorphism, the slope of a reaction norm is steeper in comparison with the slope favored by plasticity genes that are tightly linked to genes for local adaptation.

Biased generalization of salient traits drives the evolution of warning signals.

The importance of receiver biases in shaping the evolution of many signalling systems is widely acknowledged. Here, we show that receiver bias can explain which traits evolve to become warning signals. For warning coloration, a generalization bias for a signalling trait can result from predators learning to discriminate unprofitable from profitable prey. However, because the colour patterns of prey are complex traits with multiple components, it is crucial to understand which of the many aspects of prey appearance evolve into signals. We provide experimental evidence that the more salient differences in prey traits give rise to greater generalization bias, corresponding to stronger selection towards trait exaggeration. Our results are based on experiments with domestic chickens as predators in a Skinner-box-like setting, and imply that the difference in appearance between profitable and unprofitable prey that is most rapidly learnt produces the greatest generalization bias. As a consequence, certain salient traits of unprofitable prey are selected towards exaggeration to even higher salience, driving the evolution of warning coloration. This general idea may also help to explain the evolution of many other striking signalling traits found in nature.

Genes as Cues of Relatedness and Social Evolution in Heterogeneous Environments.

There are many situations where relatives interact while at the same time there is genetic polymorphism in traits influencing survival and reproduction. Examples include cheater-cooperator polymorphism and polymorphic microbial pathogens. Environmental heterogeneity, favoring different traits in nearby habitats, with dispersal between them, is one general reason to expect polymorphism. Currently, there is no formal framework of social evolution that encompasses genetic polymorphism. We develop such a framework, thus integrating theories of social evolution into the evolutionary ecology of heterogeneous environments. We allow for adaptively maintained genetic polymorphism by applying the concept of genetic cues. We analyze a model of social evolution in a two-habitat situation with limited dispersal between habitats, in which the average relatedness at the time of helping and other benefits of helping can differ between habitats. An important result from the analysis is that alleles at a polymorphic locus play the role of genetic cues, in the sense that the presence of a cue allele contains statistical information for an organism about its current environment, including information about relatedness. We show that epistatic modifiers of the cue polymorphism can evolve to make optimal use of the information in the genetic cue, in analogy with a Bayesian decision maker. Another important result is that the genetic linkage between a cue locus and modifier loci influences the evolutionary interest of modifiers, with tighter linkage leading to greater divergence between social traits induced by different cue alleles, and this can be understood in terms of genetic conflict.

Winter chilling speeds spring development of temperate butterflies.

Understanding and predicting phenology has become more important with ongoing climate change and has brought about great research efforts in the recent decades. The majority of studies examining spring phenology of insects have focussed on the effects of spring temperatures alone. Here we use citizen-collected observation data to show that winter cold duration, in addition to spring temperature, can affect the spring emergence of butterflies. Using spatial mixed models, we disentangle the effects of climate variables and reveal impacts of both spring and winter conditions for five butterfly species that overwinter as pupae across the UK, with data from 1976 to 2013 and one butterfly species in Sweden, with data from 2001 to 2013. Warmer springs lead to earlier emergence in all species and milder winters lead to statistically significant delays in three of the five investigated species. We also find that the delaying effect of winter warmth has become more pronounced in the last decade, during which time winter durations have become shorter. For one of the studied species, Anthocharis cardamines (orange tip butterfly), we also make use of parameters determined from previous experiments on pupal development to model the spring phenology. Using daily temperatures in the UK and Sweden, we show that recent variation in spring temperature corresponds to 10-15 day changes in emergence time over UK and Sweden, whereas variation in winter duration corresponds to 20 days variation in the south of the UK versus only 3 days in the south of Sweden. In summary, we show that short winters delay phenology. The effect is most prominent in areas with particularly mild winters, emphasising the importance of winter for the response of ectothermic animals to climate change. With climate change, these effects may become even stronger and apply also at higher latitudes.

Detection vs. selection: integration of genetic, epigenetic and environmental cues in fluctuating environments.

There are many inputs during development that influence an organism's fit to current or upcoming environments. These include genetic effects, transgenerational epigenetic influences, environmental cues and developmental noise, which are rarely investigated in the same formal framework. We study an analytically tractable evolutionary model, in which cues are integrated to determine mature phenotypes in fluctuating environments. Environmental cues received during development and by the mother as an adult act as detection-based (individually observed) cues. The mother's phenotype and a quantitative genetic effect act as selection-based cues (they correlate with environmental states after selection). We specify when such cues are complementary and tend to be used together, and when using the most informative cue will predominate. Thus, we extend recent analyses of the evolutionary implications of subsets of these effects by providing a general diagnosis of the conditions under which detection and selection-based influences on development are likely to evolve and coexist.

The evolution of transgenerational integration of information in heterogeneous environments.

An organism's phenotype can be influenced by maternal cues and directly perceived environmental cues, as well as by its genotype at polymorphic loci, which can be interpreted as a genetic cue. In fluctuating environments, natural selection favors organisms that efficiently integrate different sources of information about the likely success of phenotypic alternatives. In such situations, it can be beneficial to pass on maternal cues that offspring can respond to. A maternal cue could be based on environmental cues directly perceived by the mother but also partly on cues that were passed on by the grandmother. We have used a mathematical model to investigate how the passing of maternal cues and the integration of different sources of information evolve in response to qualitatively different kinds of temporal and spatial environmental fluctuations. The model shows that the passing of maternal cues and the transgenerational integration of sources of information readily evolve. Factors such as the degree of temporal autocorrelation, the predictive accuracy of different environmental cues, and the level of gene flow strongly influence the expression of adaptive maternal cues and the relative weights given to different sources of information. We outline the main features of the relation between the characteristics of environmental fluctuations and the adaptive systems of phenotype determination and compare these predictions with empirical studies on cue integration.

Multi-trait mimicry and the relative salience of individual traits.

Mimicry occurs when one species gains protection from predators by resembling an unprofitable model species. The degree of mimic-model similarity is variable in nature and is closely related to the number of traits that the mimic shares with its model. Here, we experimentally test the hypothesis that the relative salience of traits, as perceived by a predator, is an important determinant of the degree of mimic-model similarity required for successful mimicry. We manipulated the relative salience of the traits of a two-trait artificial model prey, and subsequently tested the survival of mimics of the different traits. The unrewarded model prey had two colour traits, black and blue, and the rewarded prey had two combinations of green, brown and grey shades. Blue tits were used as predators. We found that the birds perceived the black and blue traits to be similarly salient in one treatment, and mimic-model similarity in both traits was then required for high mimic success. In a second treatment, the blue trait was the most salient trait, and mimic-model similarity in this trait alone achieved high success. Our results thus support the idea that similar salience of model traits can explain the occurrence of multi-trait mimicry.

Social status and personality: stability in social state can promote consistency of behavioural responses.

Stability of 'state' has been suggested as an underlying factor explaining behavioural stability and animal personality (i.e. variation among, and consistency within individuals in behavioural responses), but the possibility that stable social relationships represent such states remains unexplored. Here, we investigated the influence of social status on the expression and consistency of behaviours by experimentally changing social status between repeated personality assays. We used male domestic fowl (Gallus gallus domesticus), a social species that forms relatively stable dominance hierarchies, and showed that behavioural responses were strongly affected by social status, but also by individual characteristics. The level of vigilance, activity and exploration changed with social status, whereas boldness appeared as a stable individual property, independent of status. Furthermore, variation in vocalization predicted future social status, indicating that individual behaviours can both be a predictor and a consequence of social status, depending on the aspect in focus. Our results illustrate that social states contribute to both variation and stability in behavioural responses, and should therefore be taken into account when investigating and interpreting variation in personality.

Pairs of cooperating cleaner fish provide better service quality than singletons.

Service providers may vary service quality depending on whether they work alone or provide the service simultaneously with a partner. The latter case resembles a prisoner's dilemma, in which one provider may try to reap the benefits of the interaction without providing the service. Here we present a game-theory model based on the marginal value theorem, which predicts that as long as the client determines the duration, and the providers cooperate towards mutual gain, service quality will increase in the pair situation. This prediction is consistent with field observations and with an experiment on cleaning mutualism, in which stable male-female pairs of the cleaner wrasse Labroides dimidiatus repeatedly inspect client fish jointly. Cleaners cooperate by eating ectoparasites off clients but actually prefer to cheat and eat client mucus. Because clients often leave in response to such cheating, the benefits of cheating can be gained by only one cleaner during a pair inspection. In both data sets, the increased service quality during pair inspection was mainly due to the smaller females behaving significantly more cooperatively than their larger male partners. In contrast, during solitary inspections, cleaning behaviour was very similar between the sexes. Our study highlights the importance of incorporating interactions between service providers to make more quantitative predictions about cooperation between species.

Flexible learning in complex worlds.

Cognitive flexibility can enhance the ability to adjust to changing environments. Here, we use learning simulations to investigate the possible advantages of flexible learning in volatile (changing) environments. We compare two established learning mechanisms, one with constant learning rates and one with rates that adjust to volatility. We study an ecologically relevant case of volatility, based on observations of developing cleaner fish Labroides dimidiatus that experience a transition from a simpler to a more complex foraging environment. There are other similar transitions in nature, such as migrating to a new and different habitat. We also examine two traditional approaches to volatile environments in experimental psychology and behavioral ecology: reversal learning, and learning set formation (consisting of a sequence of different discrimination tasks). These provide experimental measures of cognitive flexibility. Concerning transitions to a complex world, we show that both constant and flexible learning rates perform well, losing only a small proportion of available rewards in the period after a transition, but flexible rates perform better than constant rates. For reversal learning, flexible rates improve the performance with each successive reversal because of increasing learning rates, but this does not happen for constant rates. For learning set formation, we find no improvement in performance with successive shifts to new stimuli to discriminate for either flexible or constant learning rates. Flexible learning rates might thus explain increasing performance in reversal learning but not in learning set formation, and this can shed light on the nature of cognitive flexibility in a given system.

Limiting similarity, species packing, and the shape of competition kernels.

A traditional question in community ecology is whether species' traits are distributed as more-or-less regularly spaced clusters. Interspecific competition has been suggested to play a role in such structuring of communities. The seminal theoretical work on limiting similarity and species packing, presented four decades ago by Robert MacArthur, Richard Levins and Robert May, has recently been extended. There is now a deeper understanding of how competitive interactions influence community structure, for instance, how the shape of competition kernels can determine the clustering of species' traits. Competition is typically weaker for greater phenotypic difference, and the shape of the dependence defines a competition kernel. The clustering tendencies of kernels interact with other effects, such as variation in resource availability along a niche axis, but the kernel shape can have a decisive influence on community structure. Here we review and further extend the recent developments and evaluate their importance.

Transgenerational effects and the cost of ant tending in aphids.

In mutualistic interactions, partners obtain a net benefit, but there may also be costs associated with the provision of benefits for a partner. The question of whether aphids suffer such costs when attended by ants has been raised in previous work. Transgenerational effects, where offspring phenotypes are adjusted based on maternal influences, could be important in the mutualistic interaction between aphids and ants, in particular because aphids have telescoping generations where two offspring generations can be present in a mature aphid. We investigated the immediate and transgenerational influence of ant tending on aphid life history and reproduction by observing the interaction between the facultative myrmecophile Aphis fabae and the ant Lasius niger over 13 aphid generations in the laboratory. We found that the effect of ant tending changes dynamically over successive aphid generations after the start of tending. Initially, total aphid colony weight, aphid adult weight and aphid embryo size decreased compared with untended aphids, consistent with a cost of ant association, but these differences disappeared within four generations of interaction. We conclude that transgenerational effects are important in the aphid-ant interactions and that the costs for aphids of being tended by ants can vary over generations.