Maternal care leads to the evolution of long, slow lives.

Animals, and mammals in particular, vary widely in their "pace of life," with some species living long lives and reproducing infrequently (slow life histories) and others living short lives and reproducing often (fast life histories). These species also vary in the importance of maternal care in offspring fitness: In some species, offspring are fully independent of their mothers following a brief period of nutritional input, while others display a long period of continued dependence on mothers well after nutritional dependence. Here, we hypothesize that these two axes of variation are causally related to each other, such that extended dependence of offspring on maternal presence leads to the evolution of longer lives at the expense of reproduction. We use a combination of deterministic modeling and stochastic agent-based modeling to explore how empirically observed links between maternal survival and offspring fitness are likely to shape the evolution of mortality and fertility. Each of our modeling approaches leads to the same conclusion: When maternal survival has a strong impact on the survival of offspring and grandoffspring, populations evolve longer lives with less frequent reproduction. Our results suggest that the slow life histories of humans and other primates as well as other long-lived, highly social animals such as hyenas, whales, and elephants are partially the result of the strong maternal care that these animals display. We have designed our models to be readily parameterized with demographic data that are routinely collected by long-term researchers, which will facilitate more thorough testing of our hypothesis.

Coevolution of cognitive abilities and identity signals in individual recognition systems.

Social interactions are mediated by recognition systems, meaning that the cognitive abilities or phenotypic diversity that facilitate recognition may be common targets of social selection. Recognition occurs when a receiver compares the phenotypes produced by a sender with a template. Coevolution between sender and receiver traits has been empirically reported in multiple species and sensory modalities, though the dynamics and relative exaggeration of traits from senders versus receivers have received little attention. Here, we present a coevolutionary dynamic model that examines the conditions under which senders and receivers should invest effort in facilitating individual recognition. The model predicts coevolution of sender and receiver traits, with the equilibrium investment dependent on the relative costs of signal production versus cognition. In order for recognition to evolve, initial sender and receiver trait values must be above a threshold, suggesting that recognition requires some degree of pre-existing diversity and cognitive abilities. The analysis of selection gradients demonstrates that the strength of selection on sender signals and receiver cognition is strongest when the trait values are furthest from the optima. The model provides new insights into the expected strength and dynamics of selection during the origin and elaboration of individual recognition, an important feature of social cognition in many taxa. This article is part of the theme issue 'Signal detection theory in recognition systems: from evolving models to experimental tests'.

The evolution of conspecific acceptance threshold models.

How do organisms balance different types of recognition errors when cues associated with desirable and undesirable individuals or resources overlap? This is a fundamental question of signal detection theory (SDT). As applied in sociobiology, SDT is not limited to a single context or animal taxon, therefore its application can span what may be considered dissimilar systems. One of the applications of SDT is the suite of acceptance threshold models proposed by Reeve (1989), which analysed how individuals should balance acceptance and rejection errors in social discrimination decisions across a variety of recognition contexts, distinguished by how these costs and benefits relatively combine. We conducted a literature review to evaluate whether these models' specific predictions have been upheld. By examining over 350 research papers, we quantify how Reeve's models (Reeve 1989 Am. Nat.133, 407-435 (doi:10.1086/284926)) have influenced the field of ecological and behavioural recognition systems research. We found overall empirical support for the predictions of the specific models proposed by Reeve, and argue for further expansion of their applications into more diverse taxonomic and additional recognition contexts. This article is part of the theme issue 'Signal detection theory in recognition systems: from evolving models to experimental tests'.

Evolutionarily stable investments in recognition systems explain patterns of discrimination failure and success.

Many animals are able to perform recognition feats that astound us-such as a rodent recognizing kin it has never met. Yet in other contexts, animals appear clueless as when reed warblers rear cuckoo chicks that bear no resemblance to their own species. Failures of recognition when it would seem adaptive have been especially puzzling. Here, we present a simple tug-of-war game theory model examining how individuals should optimally invest in affecting the accuracy of discrimination between desirable and undesirable recipients. In the game, discriminating individuals (operators) and desirable and undesirable recipients (targets and mimics, respectively) can all invest effort into their own preferred outcome. We demonstrate that stable inaccurate recognition will arise when undesirable recipients have large fitness gains from inaccurate recognition relative to the pay-offs that the other two parties receive from accurate recognition. The probability of accurate recognition is often determined by just the relative pay-offs to the desirable and undesirable recipients, rather than to the discriminator. Our results provide a new lens on long-standing puzzles including a lack of nepotism in social insect colonies, tolerance of brood parasites and male birds caring for extra-pair young in their nests, which our model suggests should often lack accurate discrimination. This article is part of the theme issue 'Signal detection theory in recognition systems: from evolving models to experimental tests'.

Value of species and the evolution of conservation ethics.

The theory of evolution by natural selection can help explain why people care about other species. Building upon recent insights that morality evolves to secure fitness advantages of cooperation, we propose that conservation ethics (moral beliefs, attitudes, intuitions and norms regarding other species) could be adaptations that support cooperation between humans and non-humans. We present eco-evolutionary cost-benefit models of conservation behaviours as interspecific cooperation (altruism towards members of other species). We find that an evolutionary rule identical in structure to Hamilton's rule (which explains altruistic behaviour towards related conspecifics) can explain altruistic behaviour towards members of other species. Natural selection will favour traits for selectively altering the success of members of other species (e.g. conserving them) in ways that maximize inclusive fitness return benefits. Conservation behaviours and the ethics that evolve to reinforce them will be sensitive to local ecological and socio-cultural conditions, so will assume different contours in different places. Difficulties accurately assessing costs and benefits provided by other species, time required to adapt to ecological and socio-cultural change and barriers to collective action could explain the apparent contradiction between the widespread existence of conservation ethics and patterns of biodiversity decline globally.

Modeling strategic sperm allocation: Tailoring the predictions to the species.

Two major challenges exist when empirically testing the predictions of sperm allocation theory. First, the study species must adhere to the assumptions of the model being tested. Unfortunately, the common assumption of sperm allocation models that females mate a maximum of once or twice does not hold for many, if not most, multiply and sequentially mating animals. Second, a model's parameters, which dictate its predictions, must be measured in the study species. Common examples of such parameters, female mating frequency and sperm precedence patterns, are unknown for many species used in empirical tests. Here, we present a broadly applicable model, appropriate for multiply, sequentially mating animals, and test it in three species for which data on all the relevant parameter values are available. The model predicts that relative allocation to virgin females, compared to nonvirgins, depends on the interaction between female mating rate and the sperm precedence pattern: relative allocation to virgins increases with female mating rate under first-male precedence, while the opposite is true under later-male precedence. Our model is moderately successful in predicting actual allocation patterns in the three species, including a cricket in which we measured the parameter values and performed an empirical test of allocation.

Identity Signaling and Patterns of Cooperative Behavior.

Recognition systems play a central role in mediating cooperative behavior among individuals in a population. Despite the importance of discriminating among potential recipients of cooperation, the evolutionary forces that maintain diversity in traits used for kin recognition are poorly understood. Greenbeard-based models of kin recognition in which alleles for cooperative behavior also control recognition of those alleles in potential cooperators suggest that discrimination based on a greenbeard locus leads to positive frequency dependence, eroding diversity at the very genes responsible for recognition. As a result, the phenotypic diversity used for kin recognition has been widely assumed to be cues rather than signals of genetic identity. Diversity in identity cues is maintained by selection on other traits for reasons unrelated to recognition. A major problem with greenbeard-based models is that greenbeard recognition systems are uncommon among animals, which tend to learn kin phenotypes. We develop a simple model showing that learning a kin recognition template is sufficient to increase and maintain diversity in genetic traits used for kin recognition. Thus, our results suggest that phenotypes used for recognition may be true signals of genetic identity. As such, phenotypes are expected to evolve to facilitate recognition. Increased diversity in genetically-based recognition signals is also predicted to initiate a positive feedback loop between recognition efficiency and levels of cooperation. Finally, we discuss how the genetic architecture of recognition traits may influence kin discrimination abilities.

Synthesizing perspectives on the evolution of cooperation within and between species.

Cooperation is widespread both within and between species, but are intraspecific and interspecific cooperation fundamentally similar or qualitatively different phenomena? This review evaluates this question, necessary for a general understanding of the evolution of cooperation. First, we outline three advantages of cooperation relative to noncooperation (acquisition of otherwise inaccessible goods and services, more efficient acquisition of resources, and buffering against variability), and predict when individuals should cooperate with a conspecific versus a heterospecific partner to obtain these advantages. Second, we highlight five axes along which heterospecific and conspecific partners may differ: relatedness and fitness feedbacks, competition and resource use, resource-generation abilities, relative evolutionary rates, and asymmetric strategy sets and outside options. Along all of these axes, certain asymmetries between partners are more common in, but not exclusive to, cooperation between species, especially complementary resource use and production. We conclude that cooperation within and between species share many fundamental qualities, and that differences between the two systems are explained by the various asymmetries between partners. Consideration of the parallels between intra- and interspecific cooperation facilitates application of well-studied topics in one system to the other, such as direct benefits within species and kin-selected cooperation between species, generating promising directions for future research.

Polyandrous females provide sons with more competitive sperm: Support for the sexy-sperm hypothesis in the rattlebox moth (Utetheisa ornatrix).

Given the costs of multiple mating, why has female polyandry evolved? Utetheisa ornatrix moths are well suited for studying multiple mating in females because females are highly polyandrous over their life span, with each male mate transferring a substantial spermatophore with both genetic and nongenetic material. The accumulation of resources might explain the prevalence of polyandry in this species, but another, not mutually exclusive, possibility is that females mate multiply to increase the probability that their sons will inherit more-competitive sperm. This latter "sexy-sperm" hypothesis posits that female multiple mating and male sperm competitiveness coevolve via a Fisherian runaway process. We tested the sexy-sperm hypothesis by using competitive double matings to compare the sperm competition success of sons of polyandrous versus monandrous females. In accordance with sexy-sperm theory, we found that in 511 offspring across 17 families, the male whose polyandrous mother mated once with each of three different males sired significantly more of all total offspring (81%) than did the male whose monandrous mother was mated thrice to a single male. Interestingly, sons of polyandrous mothers had a significantly biased sex ratio of their brood toward sons, also in support of the hypothesis.

The puzzle of partial resource use by a parasitoid wasp.

When there is conspicuous underexploitation of a limited resource, it is worth asking, what mechanisms allow presumably valuable resources to be left unused? Evolutionary biologists have generated a wide variety of hypotheses to explain this, ranging from interdemic group selection to selfishly prudent individual restraint. We consider a situation in which, despite high intraspecific competition, individuals leave most of a key resource unexploited. The parasitic wasp that does this finds virtually all host egg clusters in a landscape but parasitizes only about a third of the eggs in each and then leaves a deterrent mark around the cluster. We first test-and reject-a series of system-specific simple constraints that might limit full host exploitation, such as asynchronous maturation of host eggs. We then consider classical hypotheses for the evolution of restraint. Prudent predation and bet-hedging fail as explanations because the wasp lives as a large, well-mixed population. Additionally, we find no individual benefits to the parasitoid of developing in a sparsely parasitized host nest. However, an optimal foraging model, including empirically measured costs of superparasitism and hyperparasitism, can explain through individual selection both the consistently low rate of parasitism and deterrent marking.

Partial ovary development is widespread in honey bees and comparable to other eusocial bees and wasps.

Honey bee workers have few opportunities for direct reproduction because their ovary development is chemically suppressed by queens and worker-laid eggs are destroyed by workers. While workers with fully developed ovaries are rare in honey bee colonies, we show that partial ovary development is common. Across nine studies, an average of 6% to 43% of workers had partially developed ovaries in queenright colonies with naturally mated queens. This shift by workers toward potential future reproduction is linked to lower productivity, which suggests that even small investments in reproductive physiology by selfish workers reduce cooperation below a theoretical maximum. Furthermore, comparisons across 26 species of bees and wasps revealed that the level of partial ovary development in honey bees is similar to that of other eusocial Hymenoptera where there is reproductive conflict among colony members. Natural variation in the extent of partial ovary development in honey bee colonies calls for an exploration of the genetic and ecological factors that modulate shifts in cooperation within animal societies.

Can evolutionary design of social networks make it easier to be 'green'?

The social Web is swiftly becoming a living laboratory for understanding human cooperation on massive scales. It has changed how we organize, socialize, and tackle problems that benefit from the efforts of a large crowd. A new, applied, behavioral ecology has begun to build on theoretical and empirical studies of cooperation, integrating research in the fields of evolutionary biology, social psychology, social networking, and citizen science. Here, we review the ways in which these disciplines inform the design of Internet environments to support collective pro-environmental behavior, tapping into proximate prosocial mechanisms and models of social evolution, as well as generating opportunities for 'field studies' to discover how we can support massive collective action and shift environmental social norms.

Competition over personal resources favors contribution to shared resources in human groups.

Members of social groups face a trade-off between investing selfish effort for themselves and investing cooperative effort to produce a shared group resource. Many group resources are shared equitably: they may be intrinsically non-excludable public goods, such as vigilance against predators, or so large that there is little cost to sharing, such as cooperatively hunted big game. However, group members' personal resources, such as food hunted individually, may be monopolizable. In such cases, an individual may benefit by investing effort in taking others' personal resources, and in defending one's own resources against others. We use a game theoretic "tug-of-war" model to predict that when such competition over personal resources is possible, players will contribute more towards a group resource, and also obtain higher payoffs from doing so. We test and find support for these predictions in two laboratory economic games with humans, comparing people's investment decisions in games with and without the options to compete over personal resources or invest in a group resource. Our results help explain why people cooperatively contribute to group resources, suggest how a tragedy of the commons may be avoided, and highlight unifying features in the evolution of cooperation and competition in human and non-human societies.

Promiscuous honey bee queens increase colony productivity by suppressing worker selfishness.

Queen monogamy is ancestral among bees, ants, and wasps (Order Hymenoptera), and the close relatedness that it generates within colonies is considered key for the evolution of eusociality in these lineages. Paradoxically, queens of several eusocial species are extremely promiscuous, a derived behavior that decreases relatedness among workers and fitness gained from rearing siblings but benefits queens by enhancing colony productivity and inducing workers to rear queens' sons instead of less related worker-derived males. Selection for promiscuity would be especially strong if productivity in a singly inseminated queen's colony declined because selfish workers invested in personal reproduction at the expense of performing tasks that contribute to colony productivity. We show in honey bees that workers' ovaries are more developed when queens are singly rather than multiply inseminated and that increasing ovary activation is coupled with reductions in task performance by workers and colony-wide rates of foraging and waggle-dance recruitment. Increased investment in reproductive physiology by selfish workers might result from greater incentive for them to favor worker-derived males or because low mating frequency signals a queen's diminished quality or future fecundity. Either possibility fosters selection for queen promiscuity, revealing a novel benefit of it for eusocial insects.

Parental care, cost of reproduction and reproductive skew: a general costly young model.

Understanding the mechanisms by which animals resolve conflicts of interest is the key to understanding the basis of cooperation in social species. Conflict over reproductive portioning is the critical type of conflict among cooperative breeders. The costly young model represents an important, but underappreciated, idea about how an individual's intrinsic condition and cost of reproduction should affect the resolution of conflict over the distribution of reproduction within a cooperatively breeding group. However, dominant control in various forms and fixed parental care (offspring fitness dependent solely on total brood size) are assumed in previous versions of costly young models. Here, we develop a general costly young model by relaxing the restrictive assumptions of existing models. Our results show that (1) when the complete-control assumption is relaxed, the costly young model behaves very differently from the original model, and (2) when the fixed parental care assumption is relaxed, the costly young-costly care model displays similar predictions to the tug-of-war model, although the underlying mechanisms causing these similar patterns are different. These results, we believe, help simplify the seemingly divergent predictions of different reproductive skew models and highlight the importance of studying the group members' intrinsic conditions, costs of producing young, and costs of parental care for understanding breeding conflict resolution in cooperatively breeding animals.

The brave leader game and the timing of altruism among nonkin.

The evolution of cooperation among nonkin remains a puzzle, and almost no theoretical work has examined the timing of altruism, that is, when a behavior that benefits others at one's own fitness expense should be expressed in time. We present an evolutionary dynamic-game model to address the question of when, if ever, an altruist would voluntarily emerge in time in groups of nonrelatives. Our model shows that when the benefit of having an altruistic leader decays with time, leaders will eventually emerge and will emerge later (i) in larger groups, (ii) when the cost of leadership increases, and (iii) when the assessment interval increases. The model applies to diverse situations in which time-decaying group benefits are obtained only after a group member assumes a leadership role at some cost to itself, including leader roles in foraging flocks and migration groups in birds and spiny lobsters and in high-risk foraging in desert ants.

The emergence of a superorganism through intergroup competition.

Surveys of insect societies have revealed four key, recurring organizational trends: (i) The most elaborated cooperation occurs in groups of relatives. (ii) Cooperation is typically more elaborate in species with large colony sizes than in species with small colony sizes, the latter exhibiting greater internal reproductive conflict and lesser morphological and behavioral specialization. (iii) Within a species, per capita brood output typically declines as colony size increases. (iv). The ecological factors of resource patchiness and intergroup competition are associated with the most elaborated cooperation. Predictions of all four patterns emerge elegantly from a game-theoretic model in which within-group tug-of-wars are nested within a between-group tug-of-war. In this individual selection model, individuals are faced with the problem of how to partition their energy between investment in intercolony competition versus investment in intracolony competition, i.e., internal tugs-of-war over shares of the resources gained through intergroup competition. An individual's evolutionarily stable investment in between-group competition (i.e., within-group cooperation) versus within-group competition is shown to increase as within-group relatedness increases, to decrease as group size increases (for a fixed number of competing groups), to increase as the number of competing groups in a patch increases, and to decrease as between-group relatedness increases. Moreover, if increasing patch richness increases both the number of individuals within a group and the number of competing groups, greater overall cooperation within larger groups will be observed. The model presents a simple way of determining quantitatively how intergroup conflict will propel a society forward along a "superorganism continuum."

Why animals lie: how dishonesty and belief can coexist in a signaling system.

We develop and apply a simple model for animal communication in which signalers can use a nontrivial frequency of deception without causing listeners to completely lose belief. This common feature of animal communication has been difficult to explain as a stable adaptive outcome of the options and payoffs intrinsic to signaling interactions. Our theory is based on two realistic assumptions. (1) Signals are "overheard" by several listeners or listener types with different payoffs. The signaler may then benefit from using incomplete honesty to elicit different responses from different listener types, such as attracting potential mates while simultaneously deterring competitors. (2) Signaler and listener strategies change dynamically in response to current payoffs for different behaviors. The dynamic equations can be interpreted as describing learning and behavior change by individuals or evolution across generations. We explain how our dynamic model differs from other solution concepts from classical and evolutionary game theory and how it relates to general models for frequency-dependent phenotype dynamics. We illustrate the theory with several applications where deceptive signaling occurs readily in our framework, including bluffing competitors for potential mates or territories. We suggest future theoretical directions to make the models more general and propose some possible experimental tests.

Putting competition strategies into ideal free distribution models: habitat selection as a tug of war.

When resources are patchily distributed in an environment, behavioral ecologists frequently turn to ideal free distribution (IFD) models to predict the spatial distribution of organisms. In these models, predictions about distributions depend upon two key factors: the quality of habitat patches and the nature of competition between consumers. Surprisingly, however, no IFD models have explored the possibility that consumers modulate their competitive efforts in an evolutionarily stable manner. Instead, previous models assume that resource acquisition ability and competition are fixed within species or within phenotypes. We explored the consequences of adaptive modulation of competitive effort by incorporating tug-of-war theory into payoff equations from the two main classes of IFD models (continuous input (CI) and interference). In the models we develop, individuals can increase their share of the resources available in a patch, but do so at the costs of increased resource expenditures and increased negative interactions with conspecifics. We show how such models can provide new hypotheses to explain what are thought to be deviations from IFDs (e.g., the frequent observation of fewer animals than predicted in "good" patches of habitat). We also detail straightforward predictions made uniquely by the models we develop, and we outline experimental tests that will distinguish among alternatives.

Optimal reproductive-skew models fail to predict aggression in wasps.

Optimal-skew models (OSMs) predict that cooperative breeding occurs as a result of dominants conceding reproductive benefits to subordinates, and that division of reproduction within groups reflects each cooperator's willingness and ability to contest aggressively for dominance. Polistine paper wasps are a leading model system for testing OSMs, and data on reproduction and aggression appear to support OSMs. These studies, however, measure aggression as a single rate rather than by the activity patterns of individuals. This leads to a potential error: if individuals are more likely to receive aggression when active than when inactive, differences in aggression across samples can reflect changes in activity rather than hostility. This study replicates a field manipulation cited as strongly supporting OSMs. We show that fundamentally different conclusions arise when controlling for individual activity states. Our analyses strongly suggest that behaviours classified as 'aggression' in paper wasps are unlikely to function in establishing, maintaining or responding to changes in reproductive skew. This illustrates that OSM tests using aggression or other non-reproductive behaviour as a metric for reproductive partitioning must demonstrate those links rather than assume them.