Self-organized fish schools: an examination of emergent properties

Heterogeneous, "aggregated" patterns in the spatial distributions of individuals are almost universal across living organisms, from bacteria to higher vertebrates. Whereas specific features of aggregations are often visually striking to human eyes, a heuristic analysis based on human vision is usually not sufficient to answer fundamental questions about how and why organisms aggregate. What are the individual-level behavioral traits that give rise to these features? When qualitatively similar spatial patterns arise from purely physical mechanisms, are these patterns in organisms biologically significant, or are they simply epiphenomena that are likely characteristics of any set of interacting autonomous individuals? If specific features of spatial aggregations do confer advantages or disadvantages in the fitness of group members, how has evolution operated to shape individual behavior in balancing costs and benefits at the individual and group levels? Mathematical models of social behaviors such as schooling in fishes provide a promising avenue to address some of these questions. However, the literature on schooling models has lacked a common framework to objectively and quantitatively characterize relationships between individual-level behaviors and group-level patterns. In this paper, we briefly survey similarities and differences in behavioral algorithms and aggregation statistics among existing schooling models. We present preliminary results of our efforts to develop a modeling framework that synthesizes much of this previous work, and to identify relationships between behavioral parameters and group-level statistics.     

How within-group behavioural variation and task efficiency enhance fitness in a social group

How task specialization, individual task performance and within-group behavioural variation affects fitness is a longstanding and unresolved problem in our understanding of animal societies. In the temperate social spider, Anelosimus studiosus, colony members exhibit a behavioural polymorphism; females either exhibit an aggressive 'asocial' or docile 'social' phenotype. We assessed individual prey-capture success for both phenotypes, and the role of phenotypic composition on group-level prey-capture success for three prey size classes. We then estimated the effect of group phenotypic composition on fitness in a common garden, as inferred from individual egg-case masses. On average, asocial females were more successful than social females at capturing large prey, and colony-level prey-capture success was positively associated with the frequency of the asocial phenotype. Asocial colony members were also more likely to engage in prey-capture behaviour in group-foraging situations. Interestingly, our fitness estimates indicate females of both phenotypes experience increased fitness when occupying colonies containing unlike individuals. These results imply a reciprocal fitness benefit of within-colony behavioural variation, and perhaps division of labour in a spider society.     

Variable valuations and voluntarism under group selection: An evolutionary public goods game

In biological systems, as in human society, competing social groups may depend heavily on a small number of volunteers to advance the group’s prospects. This phenomenon can be understood as the solution to an evolutionary public goods game, in which a beneficent individual or a small number of individuals may place the highest value on group success and contribute the most to achieving it while profiting very little. Here we demonstrate that this type of solution, recently recognized in the social sciences, is evolutionarily stable and evolves in evolutionary simulations sensitive to alternative ways of gaining fitness beyond the present social group. The public goods mechanism may help explain biological voluntarism in cases like predator inspection and foraging on behalf of non-relatives and may determine the extent of commitment to group welfare at different intensities of group selection.     

Fitness in stratified societies

When wealth or social status can be transmitted from parents to offspring and when fitness depends on wealth or social status, evolutionary consequences of individual transmission strategies can be described by a parameter, called long-term fitness by Rogers (1990), which is the expected relative contribution of an individual to the gene pool in the long-term future. We show how to measure and use this parameter in two models of general interest in sociobiology. First, we construct a system with social classes and hypergynous marriage. Our treatment includes a method for computing the fitnesses of the two sexes separately. As expected, upper-class males have the highest long-term fitness in this kind of social structure, followed by lower-class females, then lower-class males and upper-class females. Upper-class preference for sons would be favored by selection in this system, but not female unwillingness to marry down—in this sense such systems do not conform to a Darwinian model. We then study a system with one sex and three social classes, the poorest of which has very low single generation fitness. In this system, the class with the highest single generation fitness does not have the highest long-term fitness. We suggest that this system is a useful model for understanding the changes in reproductive behavior that occured during the demographic transition in Europe. We suggest that the absence of a destitute lower class in Africa may help explain the failure, so far, for signs of demographic transition to appear in Africa.     

Reproduction and production in a social context: Group size,reproductive skew and increasing returns

Evolutionary success requires both production (acquisition of food, protection and warmth) and reproduction. We suggest that both may increase disproportionately as group size grows, reflecting ‘increasing returns’ or ‘group augmentation benefits’, raising fitness in groups that cooperate in production and limit reproduction to one or a few high fertility females supported by non-reproductives, with high reproductive skew. In our optimisation theory both Allee effects (when individual fitness increases with group size or density) and reproductive skew arise when increasing returns determine optimal group size and proportion of reproductive females. Depending on which of food or maternal time is more important for reproduction, evolutionary trajectories of lineages may (1) reach a boundary constraint where only one female reproduces in a period (as with African wild dogs) or (2) reach a boundary where all females reproduce during their lifetimes but only during an early life stage (human menopause) or a late life stage (birds with non-dispersing helpers), where stage length optimises the proportion of females that is reproductive at any time or (3) reach the intersection of these boundary constraints where a single reproductive female is fully specialised in reproduction (as with eusocial insects). We end with some testable hypotheses.     

Why do Hymenopteran workers drift to non-natal groups? Generalized reciprocity and the maximization of group and parental success

Eusocial Hymenoptera are often characterized by having facultatively or obligately sterile worker castes. However, findings across an increasing number of species are that some workers are non-natal—they have ‘drifted’ away from where they were born and raised. Moreover, drifters are often indistinguishable from natal workers in the work and benefits provided to joined groups. This seems an evolutionary paradox of providing benefits to potentially unrelated individuals over close kin. Rather than being mistakes, drifting is proposed to be adaptive if joiners either gain inclusive fitness by preferentially moving to other kin groups or through generalized reciprocity in which exchanging workers across groups raises group-level genetic diversity and creates social heterosis. It is unclear, however, if reciprocity is unlikely because of a susceptibility to cheating. In resolving this question, a series of evolutionary simulations show: (1) Reciprocity can persist under a range of genetic assumptions and scenarios of cheating, (2) cheating almost always evolves, but can be expressed in a variety of ways that are not always predictable, (3) the inclusive fitness hypothesis is equally or more susceptible to cheating. Moreover, existing data in Hymenoptera (although not extensive) are more consistent with generalized reciprocity. This supports a hypothesis that drifting, as a phenomenon, may more often reflect maximization of group and parental fitness rather than fitness gains for the individual drifters.     

Geometry of the ideal free distribution: individual behavioural variation and annual reproductive success in aggregations of a social ungulate

Variation in social environment can mitigate risks and rewards associated with occupying a particular patch. We aim to integrate Ideal Free Distribution (IFD) and Geometry of the Selfish Herd (GSH) to address an apparent conflict in their predictions of equal mean fitness between patches (IFD) and declining fitness benefits within a patch (GSH). We tested these hypotheses in a socio‐spatial context using individual caribou that were aggregated or disaggregated during calving and varied in their annual reproductive success (ARS). We then tested individual consistency of these spatial tactics. We reveal that two socio‐spatial tactics accorded similar mean ARS (IFD); however, ARS for aggregated individuals declined near the periphery (GSH). Individuals near the aggregation periphery exhibited flexibility, whereas others were consistent. The integration of classical theories through a contemporary lens of consistent individual differences provides evidence for an integrated GSH and IFD strategy that may represent an evolutionary stable state.     

Levels of selection, altruism, and primate behavior.

Altruistic behaviors seem anomalous from a traditional view of Darwinian natural selection, and evolutionary explanations for them have generated much discussion. The debate centers around four major explanations: classic individual-level selection, reciprocity and game theory, kin selection, and trait-group selection. The historical context and defining criteria of each model must be reviewed before its validity can be assessed. Of these proposed mechanisms, group selection historically has been the most controversial. Although the extent to which empirical data support group selection hypotheses is uncertain, there is evidence for group-level selection among avirulent virus strains and foraging ant queens. Researchers studying mammalian behavior, particularly primatologists, have largely dismissed models of group-level selection. Most discussion of altruism among primates has focused on differences in fitness among individuals within a single group, but students of altruistic behaviors exhibited by primates also need to investigate intergroup variation with respect to these behaviors. Various altruistic behaviors are likely to have evolved through different forms of selection, and each example of apparent altruism therefore needs to be evaluated separately.     

There is no fitness but fitness,and the lineage is its bearer

Inclusive fitness has been the cornerstone of social evolution theory for more than a half-century and has matured as a mathematical theory in the past 20 years. Yet surprisingly for a theory so central to an entire field, some of its connections to evolutionary theory more broadly remain contentious or underappreciated. In this paper, we aim to emphasize the connection between inclusive fitness and modern evolutionary theory through the following fact: inclusive fitness is simply classical Darwinian fitness, averaged over social, environmental and demographic states that members of a gene lineage experience. Therefore, inclusive fitness is neither a generalization of classical fitness, nor does it belong exclusively to the individual. Rather, the lineage perspective emphasizes that evolutionary success is determined by the effect of selection on all biological and environmental contexts that a lineage may experience. We argue that this understanding of inclusive fitness based on gene lineages provides the most illuminating and accurate picture and avoids pitfalls in interpretation and empirical applications of inclusive fitness theory.     

A popular misapplication of evolutionary modeling to the study of human cooperation

To examine the evolutionary basis of a behavior, an established approach (known as the phenotypic gambit) is to assume that the behavior is controlled by a single allele, the fitness effects of which are derived from a consideration of how the behavior interacts, via life-history, with other ecological factors. Here we contrast successful applications of this approach with several examples of an influential and superficially similar line of research on the evolutionary basis of human cooperation. A key difference is identified: in the latter line of research the focal behavior, cooperation, is abstractly defined in terms of immediate fitness costs and benefits. Selection is then assumed to act on strategies in an iterated social context for which fitness effects can be derived by aggregation of the abstractly defined immediate fitness effects over a lifetime. This approach creates a closed theoretical loop, rendering models incapable of making predictions or providing insight into the origin of human cooperation. We conclude with a discussion of how evolutionary approaches might be appropriately used in the study of human social behavior.     

Insect Stage-Specific Adenylate Cyclases Regulate Social Motility in African Trypanosomes

Sophisticated systems for cell-cell communication enable unicellular microbes to act as multicellular entities capable of group-level behaviors that are not evident in individuals. These group behaviors influence microbe physiology, and the underlying signaling pathways are considered potential drug targets in microbial pathogens. Trypanosoma brucei is a protozoan parasite that causes substantial human suffering and economic hardship in some of the most impoverished regions of the world. T. brucei lives on host tissue surfaces during transmission through its tsetse fly vector, and cultivation on surfaces causes the parasites to assemble into multicellular communities in which individual cells coordinate their movements in response to external signals. This behavior is termed “social motility,” based on its similarities with surface-induced social motility in bacteria, and it demonstrates that trypanosomes are capable of group-level behavior. Mechanisms governing T. brucei social motility are unknown. Here we report that a subset of receptor-type adenylate cyclases (ACs) in the trypanosome flagellum regulate social motility. RNA interference-mediated knockdown of adenylate cyclase 6 (AC6), or dual knockdown of AC1 and AC2, causes a hypersocial phenotype but has no discernible effect on individual cells in suspension culture. Mutation of the AC6 catalytic domain phenocopies AC6 knockdown, demonstrating that loss of adenylate cyclase activity is responsible for the phenotype. Notably, knockdown of other ACs did not affect social motility, indicating segregation of AC functions. These studies reveal interesting parallels in systems that control social behavior in trypanosomes and bacteria and provide insight into a feature of parasite biology that may be exploited for novel intervention strategies.     

Phenotypic assortment mediates the effect of social selection in a wild beetle population

Social interactions often have major fitness consequences, but little is known about how specific interacting phenotypes affect the strength of natural selection. Social influences on the evolutionary process can be assessed using a multilevel selection approach that partitions the effects of social partner phenotypes on fitness (referred to as social or group selection) from those of the traits of a focal individual (nonsocial or individual selection). To quantify the contribution of social selection to total selection affecting a trait, the patterns of phenotypic association among interactants must also be considered. We estimated selection gradients on male body size in a wild population of forked fungus beetles (Bolitotherus cornutus). We detected positive nonsocial selection and negative social selection on body size operating through differences in copulation success, indicating that large males with small social partners had highest fitness. In addition, we found that, in low-density demes, the phenotypes of focal individuals were negatively correlated with those of their social partners. This pattern reversed the negative effect of group selection on body size and led to stronger positive selection for body size. Our results demonstrate multilevel selection in nature and stress the importance of considering social selection whenever conspecific interactions occur nonrandomly.     

Does the match between individual and group behavior matter in shoaling sticklebacks?

In animals living in groups, the social environment is fundamental to shaping the behaviors and life histories of an individual. A mismatch between individual and group behavior patterns may have disadvantages if the individual is incapable of flexibly changing its state in response to the social environment that influences its energy gain and expenditure. We used different social groups of juvenile three‐spined sticklebacks (Gasterosteus aculeatus) with experimentally manipulated compositions of individual sociability to study the feedback between individual and group behaviors and to test how the social environment shapes behavior, metabolic rate, and growth. Experimentally created unsociable groups, containing a high proportion of less sociable fish, showed bolder collective behaviors during feeding than did corresponding sociable groups. Fish within groups where the majority of members had a level of sociability similar to their own gained more mass than did those within mismatched groups. Less sociable individuals within sociable groups tended to have a relatively low mass but a high standard metabolic rate. A mismatch between the sociability of an individual and that of the majority of the group in which it is living confers a growth disadvantage probably due to the expression of nonadaptive behaviors that increase energetic costs.     

MULTI‐LEVEL SEXUAL SELECTION: INDIVIDUAL AND FAMILY‐LEVEL SELECTION FOR MATING SUCCESS IN A HISTORICAL HUMAN POPULATION

Precopulatory sexual selection is the association between fitness and traits associated with mate acquisition. Although sexual selection is generally recognized to be a powerful evolutionary force, most investigations are limited to characters belonging to individuals. A broader multilevel perspective acknowledges that individual fitness can be affected by aspects of mating success that are characters of groups, such as families. Parental mating success in polygynous or polyandrous human societies may exemplify traits under group‐level sexual selection. Using fitness measures that account for age‐structure, I measure multilevel selection for mate number over 55 years in a human population with declining rates of polygyny. Sexual selection had three components: individual‐level selection for ever‐mating (whether an individual mated) and individual‐ and family‐level selection for polyandry and polygyny. Family‐ and individual‐level selection for polygyny was equally strong, three times stronger than family‐level selection for polyandry and more than an order of magnitude stronger than individual‐level selection for polyandry. However, individual‐level selection for polyandry and polygyny was more effective at explaining relative fitness variance than family‐level selection. Selection for ever‐mating was the most important source of sexual selection for fitness; variation for ever‐mating explained 23% of relative fitness variance.     

ASSORTATIVE SOCIAL LEARNING AND ITS IMPLICATIONS FOR HUMAN (AND ANIMAL?) SOCIETIES

Choosing from whom to learn is an important element of social learning. It affects learner success and the profile of behaviors in the population. Because individuals often differ in their traits and capabilities, their benefits from different behaviors may also vary. Homophily, or assortment, the tendency of individuals to interact with other individuals with similar traits, is known to affect the spread of behaviors in humans. We introduce models to study the evolution of assortative social learning (ASL), where assorting on a trait acts as an individual‐specific mechanism for filtering relevant models from which to learn when that trait varies. We show that when the trait is polymorphic, ASL may maintain a stable behavioral polymorphism within a population (independently of coexistence with individual learning in a population). We explore the evolution of ASL when assortment is based on a nonheritable or partially heritable trait, and when ASL competes with different non‐ASL strategies: oblique (learning from the parental generation) and vertical (learning from the parent). We suggest that the tendency to assort may be advantageous in the context of social learning, and that ASL might be an important concept for the evolutionary theory of social learning.     

Sociality and health: impacts of sociality on disease susceptibility and transmission in animal and human societies

This paper introduces a theme issue presenting the latest developments in research on the impacts of sociality on health and fitness. The articles that follow cover research on societies ranging from insects to humans. Variation in measures of fitness (i.e. survival and reproduction) has been linked to various aspects of sociality in humans and animals alike, and variability in individual health and condition has been recognized as a key mediator of these relationships. Viewed from a broad evolutionary perspective, the evolutionary transitions from a solitary lifestyle to group living have resulted in several new health-related costs and benefits of sociality. Social transmission of parasites within groups represents a major cost of group living, but some behavioural mechanisms, such as grooming, have evolved repeatedly to reduce this cost. Group living also has created novel costs in terms of altered susceptibility to infectious and non-infectious disease as a result of the unavoidable physiological consequences of social competition and integration, which are partly alleviated by social buffering in some vertebrates. Here, we define the relevant aspects of sociality, summarize their health-related costs and benefits, and discuss possible fitness measures in different study systems. Given the pervasive effects of social factors on health and fitness, we propose a synthesis of existing conceptual approaches in disease ecology, ecological immunology and behavioural neurosciences by adding sociality as a key factor, with the goal to generate a broader framework for organismal integration of health-related research.     

Mutability as an altruistic trait in finite asexual populations

Mutation rate (MR) is a crucial determinant of the evolutionary process. Optimal MR may enable efficient evolutionary searching and therefore increase the fitness of the population over time. Nevertheless, individuals may favor MRs that are far from being optimal for the whole population. Instead, each individual may tend to mutate at rates that selfishly increase its own relative fitness. We show that in some cases, undergoing a mutation is altruistic, i.e., it increases the expected fitness of the population, but decreases the expected fitness of the mutated individual itself. In this case, if the population is uniform (completely mixed, undivided), immutability is evolutionary stable and is probably selected for. However, our examination of a segregated population, which is divided into several groups (or patches), shows that the optimal, altruistic MR may out-compete the selfish MR if the coupling between the groups is neither too strong nor too weak. This demonstrates that the population structure is crucial for the succession of the evolutionary process itself. For example, in a uniform population, the evolutionary process may be stopped before the highest fitness is reached, as demonstrated in a one-pick fitness landscape. In addition, we show that the dichotomy between evolutionary stable and optimal MRs can be seen as a special case of a more general phenomenon in which optimal behaviors may be destabilized in finite populations, since optimal sub-populations may become extinct before the benefit of their behavior is expressed.     

Fitness costs of worker specialization for ant societies

Division of labour is of fundamental importance for the success of societies, yet little is known about how individual specialization affects the fitness of the group as a whole. While specialized workers may be more efficient in the tasks they perform than generalists, they may also lack the flexibility to respond to rapid shifts in task needs. Such rigidity could impose fitness costs when societies face dynamic and unpredictable events, such as an attack by socially parasitic slavemakers. Here, we experimentally assess the colony-level fitness consequences of behavioural specialization in Temnothorax longispinosus ants that are attacked by the slavemaker ant T. americanus. We manipulated the social organization of 102 T. longispinosus colonies, based on the behavioural responses of all 3842 workers. We find that strict specialization is disadvantageous for a colony''s annual reproduction and growth during slave raids. These fitness costs may favour generalist strategies in dynamic environments, as we also demonstrate that societies exposed to slavemakers in the field show a lower degree of specialization than those originating from slavemaker-free populations. Our findings provide an explanation for the ubiquity of generalists and highlight their importance for the flexibility and functional robustness of entire societies.     

Is tibetan polyandry adaptive?

This paper addresses methodological and metatheoretical aspects of the ongoing debate over the adaptive significance of Tibetan polyandry. Methodological contributions include a means of estimating relatedness of fraternal co-husbands given multigenerational polyandry, and use of Hamilton’s rule and a member-joiner model to specify how inclusive fitness gains of co-husbands may vary according to seniority, opportunity costs, and group size. These methods are applied to various data sets, particularly that of Crook and Crook (1988). The metatheoretical discussion pivots on the critique by evolutionary psychologists of adaptationist accounts of polyandry. Contrary to this critique, I argue that valid adaptationist explanations of such practices do not necessitate cognitive mechanisms evolved specifically to produce polyandry, nor that there must have been exact equivalents of Tibetan agricultural estates and social institutions in human evolutionary history. Specific issues raised when one posits either kin selection or cultural evolution to explain the adaptive features of Tibetan polyandry are also discussed.     

Sexually antagonistic evolution caused by male–male competition in the pistil

Although sexual selection and sexual conflict are important evolutionary forces in animals, their significance in plants is uncertain. In hermaphroditic organisms, such as many plants, sexual conflict may occur both between mating partners (interlocus conflict) and between male and female sex roles within an individual (intralocus conflict). We performed experimental evolution, involving lines that were crossed with either one or two pollen donors (monogamous or polyandrous lines), in the hermaphroditic plant (Collinsia heterophylla) where early fertilizations are associated with female fitness costs (reduced seed set). Artificial polyandry for four generations resulted in enhanced pollen performance and increased female fitness costs compared to the monogamous and source (starting material) lines. Female fitness was also reduced in the monogamous line, indicating a possible trade‐off between sex roles, resulting from early pollination. We performed a second experiment to investigate a potential harming effect of pollen performance on seed set. We found that high siring success of early arriving pollen competing with later‐arriving pollen was associated with high female fitness costs, consistent with an interlocus sexual conflict. Our study provides evidence for the importance of sexual selection in shaping evolution of plant reproductive strategies, but also pinpoints the complexity of sexual conflict in hermaphroditic species.