Guppies in large groups cooperate more frequently in an experimental test of the group size paradox.

The volunteer's dilemma, in which a single individual is required to produce a public good, predicts that individuals in larger groups will cooperate less frequently. Mechanistically, this could result from trade-offs between costs associated with volunteering and costs incurred if the public good is not produced (nobody volunteers). During predator inspection, one major contributor to the cost of volunteering is likely increased probability of predation; however, a predator also poses a risk to all individuals if nobody inspects. We tested the prediction that guppies in larger groups will inspect a predator less than those in smaller groups. We also predicted that individuals in larger groups would perceive less threat from the predator stimulus because of the protective benefits of larger groups (e.g. dilution). Contrary to prediction, we found that individuals in large groups inspected more frequently than those in smaller groups, but (as predicted) spent less time in refuges. There was evidence that individuals in intermediate-sized groups made fewest inspections and spent most time in refuges, suggesting that any link between group size, risk and cooperation is not driven by simple dilution. Extensions of theoretical models that capture these dynamics will likely be broadly applicable to risky cooperative behaviour.

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.

Learning is negatively associated with strength of left/right paw preference in wild grey squirrels (Sciurus carolinensis).

Cerebral laterality, via hemispheric specialisation, has been evidenced across the animal kingdom and linked to cognitive performance in a number of species. Previously it has been suggested that cognitive processing is more efficient in brains with stronger hemispheric differences in processing, which may be the key fitness benefit driving the evolution of laterality. However, evidence supporting a positive association between cognitive performance and lateralization is mixed: data from studies of fish and birds show a positive relationship whereas more limited data from studies of mammals suggest a weak or even negative relationship, suggesting the intriguing possibility of a mammal/non-mammal divide in the nature of this relationship. Here, we report an empirical test examining the relationship between lateralization and cognitive performance in wild grey squirrels (Sciurus carolinensis) by measuring left/right paw preference as a behavioural assay of cerebral lateralization and learning speed as an assay of cognitive efficiency. We carried out a motor-based laterality test using a reaching paradigm and measured learning speed on a problem-solving task. In accordance with the suggestion of a mammal/non-mammal divide, we found a negative relationship between strength of paw preference and performance on the learning task. We discuss this finding in light of niche-specific adaptations, task-specific demands and cognitive flexibility.

Between-group attack and defence in an ecological setting: Insights from nonhuman animals.

Attempts to understand the fundamental forces shaping conflict between attacking and defending groups can be hampered by a narrow focus on humans and reductionist, oversimplified modelling. Further progress depends on recognising the striking parallels in between-group conflict across the animal kingdom, harnessing the power of experimental tests in nonhuman species and modelling the eco-evolutionary feedbacks that drive attack and defence.

Trust your gut: using physiological states as a source of information is almost as effective as optimal Bayesian learning.

Approaches to understanding adaptive behaviour often assume that animals have perfect information about environmental conditions or are capable of sophisticated learning. If such learning abilities are costly, however, natural selection will favour simpler mechanisms for controlling behaviour when faced with uncertain conditions. Here, we show that, in a foraging context, a strategy based only on current energy reserves often performs almost as well as a Bayesian learning strategy that integrates all previous experiences to form an optimal estimate of environmental conditions. We find that Bayesian learning gives a strong advantage only if fluctuations in the food supply are very strong and reasonably frequent. The performance of both the Bayesian and the reserve-based strategy are more robust to inaccurate knowledge of the temporal pattern of environmental conditions than a strategy that has perfect knowledge about current conditions. Studies assuming Bayesian learning are often accused of being unrealistic; our results suggest that animals can achieve a similar level of performance to Bayesians using much simpler mechanisms based on their physiological state. More broadly, our work suggests that the ability to use internal states as a source of information about recent environmental conditions will have weakened selection for sophisticated learning and decision-making systems.

Adaptive Use of Information during Growth Can Explain Long-Term Effects of Early Life Experiences.

Development is a continuous process during which individuals gain information about their environment and adjust their phenotype accordingly. In many natural systems, individuals are particularly sensitive to early life experiences, even in the absence of later constraints on plasticity. Recent models have highlighted how the adaptive use of information can explain age-dependent plasticity. These models assume that information gain and phenotypic adjustments either cannot occur simultaneously or are completely independent. This assumption is not valid in the context of growth, where finding food results both in a size increase and learning about food availability. Here, we describe a simple model of growth to provide proof of principle that long-term effects of early life experiences can arise through the coupled dynamics of information acquisition and phenotypic change in the absence of direct constraints on plasticity. The increase in reproductive value from gaining information and sensitivity of behavior to experiences declines across development. Early life experiences have long-term impacts on age of maturity, yet-due to compensatory changes in behavior-our model predicts no substantial effects on reproductive success. We discuss how the evolution of sensitive windows can be explained by experiences having short-term effects on informational and phenotypic states, which generate long-term effects on life-history decisions.

Adaptive explanations for sensitive windows in development.

Development in many organisms appears to show evidence of sensitive windows-periods or stages in ontogeny in which individual experience has a particularly strong influence on the phenotype (compared to other periods or stages). Despite great interest in sensitive windows from both fundamental and applied perspectives, the functional (adaptive) reasons why they have evolved are unclear. Here we outline a conceptual framework for understanding when natural selection should favour changes in plasticity across development. Our approach builds on previous theory on the evolution of phenotypic plasticity, which relates individual and population differences in plasticity to two factors: the degree of uncertainty about the environmental conditions and the extent to which experiences during development ('cues') provide information about those conditions. We argue that systematic variation in these two factors often occurs within the lifetime of a single individual, which will select for developmental changes in plasticity. Of central importance is how informational properties of the environment interact with the life history of the organism. Phenotypes may be more or less sensitive to environmental cues at different points in development because of systematic changes in (i) the frequency of cues, (ii) the informativeness of cues, (iii) the fitness benefits of information and/or (iv) the constraints on plasticity. In relatively stable environments, a sensible null expectation is that plasticity will gradually decline with age as the developing individual gathers information. We review recent models on the evolution of developmental changes in plasticity and explain how they fit into our conceptual framework. Our aim is to encourage an adaptive perspective on sensitive windows in development.

Heavy use of equations impedes communication among biologists.

Most research in biology is empirical, yet empirical studies rely fundamentally on theoretical work for generating testable predictions and interpreting observations. Despite this interdependence, many empirical studies build largely on other empirical studies with little direct reference to relevant theory, suggesting a failure of communication that may hinder scientific progress. To investigate the extent of this problem, we analyzed how the use of mathematical equations affects the scientific impact of studies in ecology and evolution. The density of equations in an article has a significant negative impact on citation rates, with papers receiving 28% fewer citations overall for each additional equation per page in the main text. Long, equation-dense papers tend to be more frequently cited by other theoretical papers, but this increase is outweighed by a sharp drop in citations from nontheoretical papers (35% fewer citations for each additional equation per page in the main text). In contrast, equations presented in an accompanying appendix do not lessen a paper's impact. Our analysis suggests possible strategies for enhancing the presentation of mathematical models to facilitate progress in disciplines that rely on the tight integration of theoretical and empirical work.

Sex-ratio control erodes sexual selection, revealing evolutionary feedback from adaptive plasticity.

Female choice is a powerful selective force, driving the elaboration of conspicuous male ornaments. This process of sexual selection has profound implications for many life-history decisions, including sex allocation. For example, females with attractive partners should produce more sons, because these sons will inherit their father's attractiveness and enjoy high mating success, thereby yielding greater fitness returns than daughters. However, previous research has overlooked the fact that there is a reciprocal feedback from life-history strategies to sexual selection. Here, using a simple mathematical model, we show that if mothers adaptively control offspring sex in relation to their partner's attractiveness, sexual selection is weakened and male ornamentation declines. This weakening occurs because the ability to determine offspring sex reduces the fitness difference between females with attractive and unattractive partners. We use individual-based, evolutionary simulations to show that this result holds under more biologically realistic conditions. Sexual selection and sex allocation thus interact in a dynamic fashion: The evolution of conspicuous male ornaments favors sex-ratio adjustment, but this conditional strategy then undermines the very same process that generated it, eroding sexual selection. We predict that, all else being equal, the most elaborate sexual displays should be seen in species with little or no control over offspring sex. The feedback process we have described points to a more general evolutionary principle, in which a conditional strategy weakens directional selection on another trait by reducing fitness differences.

Generalized optimal risk allocation: foraging and antipredator behavior in a fluctuating environment.

Animals live in complex environments in which predation risk and food availability change over time. To deal with this variability and maximize their survival, animals should take into account how long current conditions may persist and the possible future conditions they may encounter. This should affect their foraging activity, and with it their vulnerability to predation across periods of good and bad conditions. Here we develop a comprehensive theory of optimal risk allocation that allows for environmental persistence and for fluctuations in food availability as well as predation risk. We show that it is the duration of good and bad periods, independent of each other, rather than the overall proportion of time exposed to each that is the most important factor affecting behavior. Risk allocation is most pronounced when conditions change frequently, and optimal foraging activity can either increase or decrease with increasing exposure to bad conditions. When food availability fluctuates rapidly, animals should forage more when food is abundant, whereas when food availability fluctuates slowly, they should forage more when food is scarce. We also show that survival can increase as variability in predation risk increases. Our work reveals that environmental persistence should profoundly influence behavior. Empirical studies of risk allocation should therefore carefully control the duration of both good and bad periods and consider manipulating food availability as well as predation risk.

Men with elevated testosterone levels show more affiliative behaviours during interactions with women.

Testosterone (T) is thought to play a key role in male-male competition and courtship in many vertebrates, but its precise effects are unclear. We explored whether courtship behaviour in humans is modulated and preceded by changes in T. Pairs of healthy male students first competed in a non-physical contest in which their T levels became elevated. Each participant then had a short, informal interaction with either an unfamiliar man or woman. The sex of the stimulus person did not affect the participants' behaviour overall. However, in interactions with women, those men who had experienced a greater T increase during the contest subsequently showed more interest in the woman, engaged in more self-presentation, smiled more and made more eye contact. No such effects were seen in interactions with other men. This is the first study to provide direct evidence that elevating T during male-male competition is followed by increased affiliative behaviour towards women.

Individual variation and the resolution of conflict over parental care in penduline tits.

Eurasian penduline tits (Remiz pendulinus) have an unusually diverse breeding system consisting of frequent male and female polygamy, and uniparental care by the male or the female. Intriguingly, 30 to 40 per cent of all nests are deserted by both parents. To understand the evolution of this diverse breeding system and frequent clutch desertion, we use 6 years of field data to derive fitness expectations for males and females depending on whether or not they care for their offspring. The resulting payoff matrix corresponds to an asymmetric Snowdrift Game with two alternative evolutionarily stable strategies (ESSs): female-only and male-only care. This, however, does not explain the polymorphism in care strategies and frequent biparental desertion, because theory predicts that one of the two ESSs should have spread to fixation. Using a bootstrapping approach, we demonstrate that taking account of individual variation in payoffs explains the patterns of care better than a model based on the average population payoff matrix. In particular, a model incorporating differences in male attractiveness closely predicts the observed frequencies of male and female desertion. Our work highlights the need for a new generation of individual-based evolutionary game-theoretic models.

Hot-headed peckers: thermographic changes during aggression among juvenile pheasants (Phasianus colchicus).

In group-living vertebrates, dominance status often covaries with physiological measurements (e.g. glucocorticoid levels), but it is unclear how dominance is linked to dynamic changes in physiological state over a shorter, behavioural timescale. In this observational study, we recorded spontaneous aggression among captive juvenile pheasants (Phasianus colchicus) alongside infrared thermographic measurements of their external temperature, a non-invasive technique previously used to examine stress responses in non-social contexts, where peripheral blood is redirected towards the body core. We found low but highly significant repeatability in maximum head temperature, suggesting individually consistent thermal profiles, and some indication of lower head temperatures in more active behavioural states (e.g. walking compared to resting). These individual differences were partly associated with sex, females being cooler on average than males, but unrelated to body size. During pairwise aggressive encounters, we observed a non-monotonic temperature change, with head temperature dropping rapidly immediately prior to an attack and increasing rapidly afterwards, before returning to baseline levels. This nonlinear pattern was similar for birds in aggressor and recipient roles, but aggressors were slightly hotter on average. Our findings show that aggressive interactions induce rapid temperature changes in dominants and subordinates alike, and highlight infrared thermography as a promising tool for investigating the physiological basis of pecking orders in galliforms. This article is part of the theme issue 'The centennial of the pecking order: current state and future prospects for the study of dominance hierarchies'.

Towards an Evolutionary Theory of Stress Responses.

All organisms have a stress response system to cope with environmental threats, yet its precise form varies hugely within and across individuals, populations, and species. While the physiological mechanisms are increasingly understood, how stress responses have evolved remains elusive. Here, we show that important insights can be gained from models that incorporate physiological mechanisms within an evolutionary optimality analysis (the 'evo-mecho' approach). Our approach reveals environmental predictability and physiological constraints as key factors shaping stress response evolution, generating testable predictions about variation across species and contexts. We call for an integrated research programme combining theory, experimental evolution, and comparative analysis to advance scientific understanding of how this core physiological system has evolved.

Learning your own strength: winner and loser effects should change with age and experience.

Winner and loser effects, in which the outcome of an aggressive encounter influences the tendency to escalate future conflicts, have been documented in many taxa, but we have limited understanding of why they have evolved. One possibility is that individuals use previous victories and defeats to assess their fighting ability relative to others. We explored this idea by modelling a population of strong and weak individuals that do not know their own strength, but keep track of how many fights they have won. Under these conditions, adaptive behaviour generates clear winner and loser effects: individuals who win fights should escalate subsequent conflicts, whereas those who lose should retreat from aggressive opponents. But these effects depend strongly on age and experience. Young, naive individuals should show highly aggressive behaviour and pronounced loser effects. For these inexperienced individuals, fighting is especially profitable because it yields valuable information about their strength. Aggression should then decline as an individual ages and gains experience, with those who lose fights becoming more submissive. Older individuals, who have a better idea of their own strength, should be more strongly influenced by victories than losses. In conclusion, we predict that both aggressiveness and the relative magnitude of winner and loser effects should change with age, owing to changes in how individuals perceive their own strength.

Sex-ratio biasing towards daughters among lower-ranking co-wives in Rwanda.

There is considerable debate as to whether human females bias the sex ratio of their offspring as a function of their own condition. We apply the Trivers-Willard prediction-that mothers in poor condition will overproduce daughters-to a novel measure of condition, namely wife rank within a polygynous marriage. Using a large-scale sample of over 95 000 Rwandan mothers, we show that lower-ranking polygynous wives do indeed have significantly more daughters than higher-ranking polygynous wives and monogamously married women. This effect remains when controlling for potential confounds such as maternal age. We discuss these results in reference to previous work on sex-ratio adjustment in humans.

Sexual selection: copycat mating in birds.

Female zebra finches may be influenced by the choices of other females when selecting mates, challenging the view that mate-choice copying should not occur in species with biparental care.

Adaptive and non-adaptive models of depression: A comparison using register data on antidepressant medication during divorce.

Divorce is associated with an increased probability of a depressive episode, but the causation of events remains unclear. Adaptive models of depression propose that depression is a social strategy in part, whereas non-adaptive models tend to propose a diathesis-stress mechanism. We compare an adaptive evolutionary model of depression to three alternative non-adaptive models with respect to their ability to explain the temporal pattern of depression around the time of divorce. Register-based data (304,112 individuals drawn from a random sample of 11% of Finnish people) on antidepressant purchases is used as a proxy for depression. This proxy affords an unprecedented temporal resolution (a 3-monthly prevalence estimates over 10 years) without any bias from non-compliance, and it can be linked with underlying episodes via a statistical model. The evolutionary-adaptation model (all time periods with risk of divorce are depressogenic) was the best quantitative description of the data. The non-adaptive stress-relief model (period before divorce is depressogenic and period afterwards is not) provided the second best quantitative description of the data. The peak-stress model (periods before and after divorce can be depressogenic) fit the data less well, and the stress-induction model (period following divorce is depressogenic and the preceding period is not) did not fit the data at all. The evolutionary model was the most detailed mechanistic description of the divorce-depression link among the models, and the best fit in terms of predicted curvature; thus, it offers most rigorous hypotheses for further study. The stress-relief model also fit very well and was the best model in a sensitivity analysis, encouraging development of more mechanistic models for that hypothesis.

Adaptive learning can result in a failure to profit from good conditions: implications for understanding depression.

BACKGROUND AND OBJECTIVES: Depression is a major medical problem diagnosed in an increasing proportion of people and for which commonly prescribed psychoactive drugs are frequently ineffective. Development of treatment options may be facilitated by an evolutionary perspective; several adaptive reasons for proneness to depression have been proposed. A common feature of many explanations is that depressive behaviour is a way to avoid costly effort where benefits are small and/or unlikely. However, this viewpoint fails to explain why low mood persists when the situation improves. We investigate whether a behavioural rule that is adapted to a stochastically changing world can cause inactivity which appears similar to the effect of depression, in that it persists after the situation has improved. METHODOLOGY: We develop an adaptive learning model in which an individual has repeated choices of whether to invest costly effort that may result in a net benefit. Investing effort also provides information about the current conditions and rates of change of the conditions. RESULTS: An individual following the optimal behavioural strategy may sometimes remain inactive when conditions are favourable (i.e. when it would be better to invest effort) when it is poorly informed about the current environmental state. Initially benign conditions can predispose an individual to inactivity after a relatively brief period of negative experiences. CONCLUSIONS AND IMPLICATIONS: Our approach suggests that the antecedent factors causing depressed behaviour could go much further back in an individual s history than is currently appreciated. The insights from our approach have implications for the ongoing debate about best treatment options for patients with depressive symptoms.