The evolution of cooperative breeding in birds: kinship,dispersal and life history

The evolution of cooperation among animals has posed a major problem for evolutionary biologists, and despite decades of research into avian cooperative breeding systems, many questions about the evolution of their societies remain unresolved. A review of the kin structure of avian societies shows that a large majority live in kin-based groups. This is consistent with the proposed evolutionary routes to cooperative breeding via delayed dispersal leading to family formation, or limited dispersal leading to kin neighbourhoods. Hypotheses proposed to explain the evolution of cooperative breeding systems have focused on the role of population viscosity, induced by ecological/demographic constraints or benefits of philopatry, in generating this kin structure. However, comparative analyses have failed to generate robust predictions about the nature of those constraints, nor differentiated between the viscosity of social and non-social populations, except at a coarse level. I consider deficiencies in our understanding of how avian dispersal strategies differ between social and non-social species, and suggest that research has focused too narrowly on population viscosity and that a broader perspective that encompasses life history and demographic processes may provide fresh insights into the evolution of avian societies.     

Dispersal costs set the scene for helping in an atypical avian cooperative breeder

The ecological constraints hypothesis is suggested to explain the evolution of cooperative breeding in birds. This hypothesis predicts that the scene for cooperative breeding is set when ecological factors constrain offspring from dispersal. This prediction was tested in the atypical cooperative breeding system of the long-tailed tit, Aegithalos caudatus, by comparing the degree of philopatry and cooperation in an isolated and a contiguous site whilst experimentally controlling for confounding aspects of reproduction. No difference was found between the two sites in the survival of offspring but a greater proportion were found to remain philopatric in the isolated site. This difference was caused by greater philopatry of normally dispersive females suggesting, as predicted, that dispersal costs were greater from this site. Furthermore, a greater proportion of males and females cooperated following breeding failure in the isolated site than in the contiguous site. Thus, as has been suggested for typical avian cooperative breeders, dispersal costs, relative to philopatric benefits, appear to set the scene for cooperative breeding in long-tailed tits.     

Cooperation‐mediated plasticity in dispersal and colonization

Kin selection theory predicts that costly cooperative behaviors evolve most readily when directed toward kin. Dispersal plays a controversial role in the evolution of cooperation: dispersal decreases local population relatedness and thus opposes the evolution of cooperation, but limited dispersal increases kin competition and can negate the benefits of cooperation. Theoretical work has suggested that plasticity of dispersal, where individuals can adjust their dispersal decisions according to the social context, might help resolve this paradox and promote the evolution of cooperation. Here, we experimentally tested the hypothesis that conditional dispersal decisions are mediated by a cooperative strategy: we quantified the density‐dependent dispersal decisions and subsequent colonization efficiency from single cells or groups of cells among six genetic strains of the unicellular Tetrahymena thermophila that differ in their aggregation level (high, medium, and low), a behavior associated with cooperation strategy. We found that the plastic reaction norms of dispersal rate relative to density differed according to aggregation level: highly aggregative genotypes showed negative density‐dependent dispersal, whereas low‐aggregation genotypes showed maximum dispersal rates at intermediate density, and medium‐aggregation genotypes showed density‐independent dispersal with intermediate dispersal rate. Dispersers from highly aggregative genotypes had specialized long‐distance dispersal phenotypes, contrary to low‐aggregation genotypes; medium‐aggregation genotypes showing intermediate dispersal phenotype. Moreover, highly aggregation genotypes showed evidence for beneficial kin‐cooperation during dispersal. Our experimental results should help to resolve the evolutionary conflict between cooperation and dispersal: cooperative individuals are expected to avoid kin‐competition by dispersing long distances, but maintain the benefits of cooperation by dispersing in small groups.     

Feedback between Population and Evolutionary Dynamics Determines the Fate of Social Microbial Populations

The evolutionary spread of cheater strategies can destabilize populations engaging in social cooperative behaviors, thus demonstrating that evolutionary changes can have profound implications for population dynamics. At the same time, the relative fitness of cooperative traits often depends upon population density, thus leading to the potential for bi-directional coupling between population density and the evolution of a cooperative trait. Despite the potential importance of these eco-evolutionary feedback loops in social species, they have not yet been demonstrated experimentally and their ecological implications are poorly understood. Here, we demonstrate the presence of a strong feedback loop between population dynamics and the evolutionary dynamics of a social microbial gene, SUC2, in laboratory yeast populations whose cooperative growth is mediated by the SUC2 gene. We directly visualize eco-evolutionary trajectories of hundreds of populations over 50–100 generations, allowing us to characterize the phase space describing the interplay of evolution and ecology in this system. Small populations collapse despite continual evolution towards increased cooperative allele frequencies; large populations with a sufficient number of cooperators “spiral” to a stable state of coexistence between cooperator and cheater strategies. The presence of cheaters does not significantly affect the equilibrium population density, but it does reduce the resilience of the population as well as its ability to adapt to a rapidly deteriorating environment. Our results demonstrate the potential ecological importance of coupling between evolutionary dynamics and the population dynamics of cooperatively growing organisms, particularly in microbes. Our study suggests that this interaction may need to be considered in order to explain intraspecific variability in cooperative behaviors, and also that this feedback between evolution and ecology can critically affect the demographic fate of those species that rely on cooperation for their survival.     

How life history and demography promote or inhibit the evolution of helping behaviours

In natural populations, dispersal tends to be limited so that individuals are in local competition with their neighbours. As a consequence, most behaviours tend to have a social component, e.g. they can be selfish, spiteful, cooperative or altruistic as usually considered in social evolutionary theory. How social behaviours translate into fitness costs and benefits depends considerably on life-history features, as well as on local demographic and ecological conditions. Over the last four decades, evolutionists have been able to explore many of the consequences of these factors for the evolution of social behaviours. In this paper, we first recall the main theoretical concepts required to understand social evolution. We then discuss how life history, demography and ecology promote or inhibit the evolution of helping behaviours, but the arguments developed for helping can be extended to essentially any social trait. The analysis suggests that, on a theoretical level, it is possible to contrast three critical benefit-to-cost ratios beyond which costly helping is selected for (three quantitative rules for the evolution of altruism). But comparison between theoretical results and empirical data has always been difficult in the literature, partly because of the perennial question of the scale at which relatedness should be measured under localized dispersal. We then provide three answers to this question.     

Cooperation can promote rescue or lead to evolutionary suicide during environmental change

The adaptation of populations to changing conditions may be affected by interactions between individuals. For example, when cooperative interactions increase fecundity, they may allow populations to maintain high densities and thus keep track of moving environmental optima. Simultaneously, changes in population density alter the marginal benefits of cooperative investments, creating a feedback loop between population dynamics and the evolution of cooperation. Here we model how the evolution of cooperation interacts with adaptation to changing environments. We hypothesize that environmental change lowers population size and thus promotes the evolution of cooperation, and that this, in turn, helps the population keep up with the moving optimum. However, we find that the evolution of cooperation can have qualitatively different effects, depending on which fitness component is reduced by the costs of cooperation. If the costs decrease fecundity, cooperation indeed speeds adaptation by increasing population density; if, in contrast, the costs decrease viability, cooperation may instead slow adaptation by lowering the effective population size, leading to evolutionary suicide. Thus, cooperation can either promote or—counterintuitively—hinder adaptation to a changing environment. Finally, we show that our model can also be generalized to other social interactions by discussing the evolution of competition during environmental change.     

LIMITED DISPERSAL, BUDDING DISPERSAL, AND COOPERATION: AN EXPERIMENTAL STUDY

Numerous theoretical studies have investigated how limited dispersal may provide an explanation for the evolution of cooperation, by leading to interactions between relatives. However, despite considerable theoretical attention, there has been a lack of empirical tests. In this article, we test how patterns of dispersal influence the evolution of cooperation, using iron-scavenging in the bacterium Pseudomonas aeruginosa as our cooperative trait. We found that relatively limited dispersal does not favor cooperation. The reason for this is that although limited dispersal increases the relatedness between interacting individuals, it also leads to increased local competition for resources between relatives. This result supports Taylor's prediction that in the simplest possible scenario, the effects of increased relatedness and local competition exactly cancel out. In contrast, we show that one way for cooperation to be favored is if individuals disperse in groups (budding dispersal), because this maintains high relatedness while reducing local competition between relatives (relatively global competition).     

Selective feedback between dispersal distance and the stability of mutualism

The evolution and maintenance of mutually beneficial interactions has been one of the oldest problems for evolutionary theory. For cooperation to be stable, mechanisms such as spatial population structure must exist that prevent non‐cooperative individuals from invading cooperative groups. Selection for certain traits like increased dispersal can erode that structure. Here, I used a spatially explicit individual based dual lattice computer simulation to investigate how the evolution of dispersal interacts with the evolution of mutualism and how this interaction affects the stability of mutualism in the face of non‐mutualists. I ran simulations manipulating the self‐structuring phenotype, dispersal distance, over a range of environmental conditions, as well as letting both dispersal and mutualism evolve independently, with and without a cost of dispersal. I found that environmental productivity is negatively correlated with the stability of mutualism, and that the stability of mutualism relied on the ability of mutualists to evolve shorter dispersal distances than non‐mutualists. The inclusion of a dispersal cost essentially fixed the upper limit of dispersal, and therefore limits the ability of non‐mutualists to evolve higher average dispersal than mutualists, but as costs are relaxed, the differences are recovered. These results show how selection on seemingly unrelated traits can align suites of traits into holistic life history strategies.     

The evolution of delayed dispersal in cooperative breeders.

Why do the young of cooperative breeders--species in which more than two individuals help raise offspring at a single nest--delay dispersal and live in groups? Answering this deceptively simple question involves examining the costs and benefits of three alternative strategies: (1) dispersal and attempting to breed, (2) dispersal and floating, and (3) delayed dispersal and helping. If, all other things being equal, the fitness of individuals that delay dispersal is greater than the fitness of individuals that disperse and breed on their own, intrinsic benefits are paramount to the current maintenance of delayed dispersal. Intrinsic benefits are directly due to living with others and may include enhanced foraging efficiency and reduced susceptibility to predation. However, if individuals that disperse and attempt to breed in high-quality habitat achieve the highest fitness, extrinsic constraints on the ability of offspring to obtain such high-quality breeding opportunities force offspring to either delay dispersal or float. The relevant constraint to independent reproduction has frequently been termed habitat saturation. This concept, of itself, fails to explain the evolution of delayed dispersal. Instead, we propose the delayed-dispersal threshold model as a guide for organizing and evaluating the ecological factors potentially responsible for this phenomenon. We identify five parameters critical to the probability of delayed dispersal: relative population density, the fitness differential between early dispersal/breeding and delayed dispersal, the observed or hypothetical fitness of floaters, the distribution of territory quality, and spatiotemporal environmental variability. A key conclusion from the model is that no one factor by itself causes delayed dispersal and cooperative breeding. However, a difference in the dispersal patterns between two closely related species or populations (or between individuals in the same population in different years) may be attributable to one or a small set of factors. Much remains to be done to pinpoint the relative importance of different ecological factors in promoting delayed dispersal. This is underscored by our current inability to explain satisfactorily several patterns including the relative significance of floating, geographic biases in the incidence of cooperative breeding, sexual asymmetries in delayed dispersal, the relationship between delayed dispersal leading to helping behavior and cooperative polygamy, and the rarity of the co-occurrence of helpers and floaters within the same population. Advances in this field remain to be made along several fronts.(ABSTRACT TRUNCATED AT 400 WORDS)     

Genetics of dispersal

Dispersal is a process of central importance for the ecological and evolutionary dynamics of populations and communities, because of its diverse consequences for gene flow and demography. It is subject to evolutionary change, which begs the question, what is the genetic basis of this potentially complex trait? To address this question, we (i) review the empirical literature on the genetic basis of dispersal, (ii) explore how theoretical investigations of the evolution of dispersal have represented the genetics of dispersal, and (iii) discuss how the genetic basis of dispersal influences theoretical predictions of the evolution of dispersal and potential consequences. Dispersal has a detectable genetic basis in many organisms, from bacteria to plants and animals. Generally, there is evidence for significant genetic variation for dispersal or dispersal‐related phenotypes or evidence for the micro‐evolution of dispersal in natural populations. Dispersal is typically the outcome of several interacting traits, and this complexity is reflected in its genetic architecture: while some genes of moderate to large effect can influence certain aspects of dispersal, dispersal traits are typically polygenic. Correlations among dispersal traits as well as between dispersal traits and other traits under selection are common, and the genetic basis of dispersal can be highly environment‐dependent. By contrast, models have historically considered a highly simplified genetic architecture of dispersal. It is only recently that models have started to consider multiple loci influencing dispersal, as well as non‐additive effects such as dominance and epistasis, showing that the genetic basis of dispersal can influence evolutionary rates and outcomes, especially under non‐equilibrium conditions. For example, the number of loci controlling dispersal can influence projected rates of dispersal evolution during range shifts and corresponding demographic impacts. Incorporating more realism in the genetic architecture of dispersal is thus necessary to enable models to move beyond the purely theoretical towards making more useful predictions of evolutionary and ecological dynamics under current and future environmental conditions. To inform these advances, empirical studies need to answer outstanding questions concerning whether specific genes underlie dispersal variation, the genetic architecture of context‐dependent dispersal phenotypes and behaviours, and correlations among dispersal and other traits.     

Ecological constraints, life history traits and the evolution of cooperative breeding

The ecological constraints hypothesis is widely accepted as an explanation for the evolution of delayed dispersal in cooperatively breeding birds. Intraspecific studies offer the strongest support. Observational studies have demonstrated a positive association between the severity of ecological constraints and the prevalence of cooperation, and experimental studies in which constraints on independent breeding were relaxed resulted in helpers moving to adopt the vacant breeding opportunities. However, this hypothesis has proved less successful in explaining why cooperative breeding has evolved in some species or lineages but not in others. Comparative studies have failed to identify ecological factors that differ consistently between cooperative and noncooperative species. The life history hypothesis, which emphasizes the role of life history traits in the evolution of cooperative breeding, offers a solution to this difficulty. A recent analysis showed that low adult mortality and low dispersal predisposed certain lineages to show cooperative behaviour, given the right ecological conditions. This represents an important advance, not least by offering an explanation for the patchy phylogenetic distribution of cooperative breeding. We discuss the complementary nature of these two hypotheses and suggest that rather than regarding life history traits as predisposing and ecological factors as facilitating cooperation, they are more likely to act in concert. While acknowledging that different cooperative systems may be a consequence of different selective pressures, we suggest that to identify the key differences between cooperative and noncooperative species, a broad constraints hypothesis that incorporates ecological and life history traits in a single measure of 'turnover of breeding opportunities' may provide the most promising avenue for future comparative studies. Copyright 2000 The Association for the Study of Animal Behaviour.     

Evolutionary causes and consequences of consistent individual variation in cooperative behaviour

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

Joint evolution of altruistic cooperation and dispersal in a metapopulation of small local populations

We investigate the joint evolution of public goods cooperation and dispersal in a metapopulation model with small local populations. Altruistic cooperation can evolve due to assortment and kin selection, and dispersal can evolve because of demographic stochasticity, catastrophes and kin selection. Metapopulation structures resulting in assortment have been shown to make selection for cooperation possible. But how does dispersal affect cooperation and vice versa, when both are allowed to evolve as continuous traits? We found four qualitatively different evolutionary outcomes. (1) Monomorphic evolution to full defection with positive dispersal. (2) Monomorphic evolution to an evolutionarily stable state with positive cooperation and dispersal. In this case, parameter changes selecting for increased cooperation typically also select for increased dispersal. (3) Evolutionary branching can result in the evolutionarily stable coexistence of defectors and cooperators. Although defectors could be expected to disperse more than cooperators, here we show that the opposite case is also possible: Defectors tend to disperse less than cooperators when the total amount of cooperation in the dimorphic population is low enough. (4) Selection for too low cooperation can cause the extinction of the evolving population. For moderate catastrophe rates dispersal needs to be initially very frequent for evolutionary suicide to occur. Although selection for less dispersal in principle could prevent such evolutionary suicide, in most cases this rescuing effect is not sufficient, because selection in the cooperation trait is typically much stronger. If the catastrophe rate is large enough, a part of the boundary of viability can be evolutionarily attracting with respect to both strategy components, in which case evolutionary suicide is expected from all initial conditions.     

The evolution of density-dependent dispersal in a noisy spatial population model

It is well-known that dispersal is advantageous in many different ecological situations, e.g. to survive local catastrophes where populations live in spatially and temporally heterogeneous habitats. However, the key question, what kind of dispersal strategy is optimal in a particular situation, has remained unanswered. We studied the evolution of density-dependent dispersal in a coupled map lattice model, where the population dynamics are perturbed by external environmental noise. We used a very flexible dispersal function to enable evolution to select from practically all possible types of monotonous density-dependent dispersal functions. We treated the parameters of the dispersal function as continuously changing phenotypic traits. The evolutionary stable dispersal strategies were investigated by numerical simulations. We pointed out that irrespective of the cost of dispersal and the strength of environmental noise, this strategy leads to a very weak dispersal below a threshold density, and dispersal rate increases in an accelerating manner above this threshold. Decreasing the cost of dispersal increases the skewness of the population density distribution, while increasing the environmental noise causes more pronounced bimodality in this distribution. In case of positive temporal autocorrelation of the environmental noise, there is no dispersal below the threshold, and only low dispersal below it, on the other hand with negative autocorrelation practically all individual disperses above the threshold. We found our results to be in good concordance with empirical observations.     

Evolution of complex dynamics in spatially structured populations

Dynamics of populations depend on demographic parameters which may change during evolution. In simple ecological models given by one-dimensional difference equations, the evolution of demographic parameters generally leads to equilibrium population dynamics. Here we show that this is not true in spatially structured ecological models. Using a multi-patch metapopulation model, we study the evolutionary dynamics of phenotypes that differ both in their response to local crowding, i.e. in their competitive behaviour within a habitat, and in their rate of dispersal between habitats. Our simulation results show that evolution can favour phenotypes that have the intrinsic potential for very complex dynamics provided that the environment is spatially structured and temporally variable. These phenotypes owe their evolutionary persistence to their large dispersal rates. They typically coexist with phenotypes that have low dispersal rates and that exhibit equilibrium dynamics when alone. This coexistence is brought about through the phenomenon of evolutionary branching, during which an initially uniform population splits into the two phenotypic classes.     

Temporal Structure in Cooperative Interactions: What Does the Timing of Exploitation Tell Us about Its Cost?

Exploitation in cooperative interactions both within and between species is widespread. Although it is assumed to be costly to be exploited, mechanisms to control exploitation are surprisingly rare, making the persistence of cooperation a fundamental paradox in evolutionary biology and ecology. Focusing on between-species cooperation (mutualism), we hypothesize that the temporal sequence in which exploitation occurs relative to cooperation affects its net costs and argue that this can help explain when and where control mechanisms are observed in nature. Our principal prediction is that when exploitation occurs late relative to cooperation, there should be little selection to limit its effects (analogous to “tolerated theft” in human cooperative groups). Although we focus on cases in which mutualists and exploiters are different individuals (of the same or different species), our inferences can readily be extended to cases in which individuals exhibit mixed cooperative-exploitative strategies. We demonstrate that temporal structure should be considered alongside spatial structure as an important process affecting the evolution of cooperation. We also provide testable predictions to guide future empirical research on interspecific as well as intraspecific cooperation.     

How is dispersal integrated in life histories: a quantitative analysis using butterflies

As dispersal plays a key role in gene flow among populations, its evolutionary dynamics under environmental changes is particularly important. The inter-dependency of dispersal with other life history traits may constrain dispersal evolution, and lead to the indirect selection of other traits as a by-product of this inter-dependency. Identifying the dispersal's relationships to other life-history traits will help to better understand the evolutionary dynamics of dispersal, and the consequences for species persistence and ecosystem functioning under global changes. Dispersal may be linked to other life-history traits as their respective evolutionary dynamics may be inter-dependent, or, because they are mechanistically related to each other. We identify traits that are predicted to co-vary with dispersal, and investigated the correlations that may constrain dispersal using published information on butterflies. Our quantitative analysis revealed that (1) dispersal directly correlated with demographic traits, mostly fecundity, whereas phylogenetic relationships among species had a negligible influence on this pattern, (2) gene flow and individual movements are correlated with ecological specialisation and body size, respectively and (3) routine movements only affected short-distance dispersal. Together, these results provide important insights into evolutionary dynamics under global environmental changes, and are directly applicable to biodiversity conservation.     

Human uniqueness-self-interest and social cooperation

Humans are unique among all species of terrestrial history in both ecological dominance and individual properties. Many, or perhaps all, of the unique elements of this nonpareil status can be plausibly interpreted as evolutionary and strategic elements and consequences of the unprecedented intensity and scale of our social cooperation. Convincing explanation of this unique human social adaptation remains a central, unmet challenge to the scientific enterprise.We develop a hypothesis for the ancestral origin of expanded cooperative social behavior. Specifically, we present a game theoretic analysis demonstrating that a specific pattern of expanded social cooperation between conspecific individuals with conflicts of interest (including non-kin) can be strategically viable, but only in animals that possess a highly unusual capacity for conspecific violence (credible threat) having very specific properties that dramatically reduce the costs of coercive violence. The resulting reduced costs allow preemptive or compensated coercion to be an instantaneously self-interested behavior under diverse circumstances rather than in rare, idiosyncratic circumstances as in actors (animals) who do not have access to inexpensive coercive threat.Humans are apparently unique among terrestrial organisms in having evolved conspecific coercive capabilities that fulfill these stringent requirements. Thus, our results support the proposal that access to a novel capacity for projection of coercive threat might represent the essential initiating event for the evolution of a human-like pattern of social cooperation and the subsequent evolution of the diverse features of human uniqueness. Empirical evidence indicates that these constraints were, in fact, met only in our evolutionary lineage. The logic for the emergence of uniquely human cooperation suggested by our analysis apparently accounts simply for the human fossil record.     

Speciation and the evolution of dispersal along environmental gradients

We analyze the joint evolution of an ecological character and of dispersal distance in asexual and sexual populations inhabiting an environmental gradient. Several interesting phenomena resulting from the evolutionary interplay of these characters are revealed. First, asexual and sexual populations exhibit two analogous evolutionary regimes, in which either speciation in the ecological character occurs in conjunction with evolution of short-range dispersal, or dispersal distance remains high and speciation does not occur. Second, transitions between these two regimes qualitatively differ between asexual and sexual populations, with the former showing speciation with long-range dispersal and the latter showing no speciation with short-range dispersal. Third, a phenotypic gradient following the environmental gradient occurs only in the last case, i.e., for non-speciating sexual populations evolving towards short-range dispersal. Fourth, the transition between the evolutionary regimes of long-range dispersal with no speciation and short-range dispersal with speciation is typically abrupt, mediated by a positive feedback between incipient speciation and the evolution of short-range dispersal. Fifth, even though the model of sexual evolution analyzed here does not permit assortative mating preferences, speciation occurs for a surprisingly wide range of conditions. This illustrates that dispersal evolution is a powerful alternative to preference evolution in enabling spatially distributed sexual populations to respond to frequency-dependent disruptive selection.     

Why What Juveniles Do Matters in the Evolution of Cooperative Breeding

The evolution of cooperative breeding is complex, and particularly so in humans because many other life history traits likely evolved at the same time. While cooperative childrearing is often presumed ancient, the transition from maternal self-reliance to dependence on allocare leaves no known empirical record. In this paper, an exploratory model is developed that incorporates probable evolutionary changes in birth intervals, juvenile dependence, and dispersal age to predict under what life history conditions mothers are unable to raise children without adult cooperation. The model’s outcome variable (net balance) integrates dependent children’s production and consumption as a function of varying life history parameters to estimate the investment mothers or others have to spend subsidizing children. Results suggest that maternal-juvenile cooperation can support the early transition toward a reduction in birth intervals, a longer period of juvenile dependence, and having overlapping young. The need for adult cooperation is most evident when birth intervals are short and age at net production is late. Findings suggest that the needs of juveniles would not have been an early selective force for adult cooperation. Rather, an age-graded division of labor and the mutual benefits of maternal-juvenile cooperation could be an important, but overlooked step in the evolution of cooperative breeding.