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.     

Cooperative breeding in birds: a comparative test of the life history hypothesis

In approximately 3.2% of bird species individuals regularly forgo the opportunity to breed independently and instead breed cooperatively with other conspecifics, either as non-reproductive ''helpers'' or as co-breeders. The traditional explanation for cooperative breeding is that the opportunities for breeding independently are limited owing to peculiar features of the species'' breeding ecology. However, it has proved remarkably difficult to find any common ecological correlates of cooperative breeding in birds. This difficulty has led to the ''life history hypothesis'', which suggests that the common feature of cooperatively breeding birds is their great longevity, rather than any particular feature of their breeding ecology. Here, we use a comparative method to test the life history hypothesis by looking for correlations between life history variation and variation in the frequency of cooperative breeding. First, we find that cooperative breeding in birds is not randomly distributed, but concentrated in certain families, thus supporting the idea that there may be a common basis to cooperative breeding in birds. Second, increases in the level of cooperative breeding are strongly associated with decreases in annual adult mortality and modal clutch size. Third, the proportion of cooperatively breeding species per family is correlated with a low family-typical value of annual mortality, suggesting that low mortality predisposes cooperative breeding rather than vice versa. Finally, the low rate of mortality typically found in cooperatively breeding species is associated with increasing sedentariness, lower latitudes, and decreased environmental fluctuation. We suggest that low annual mortality is the key factor that predisposes avian lineages to cooperative breeding, then ecological changes, such as becoming sedentary, further slow population turnover and reduce opportunities for independent breeding. As the traditional explanation suggests, the breeding habitat of cooperatively breeding species is saturated, but this saturation is not owing to any peculiar feature of the breeding ecology of cooperative breeders. Rather, the saturation arises because the local population turnover in these species is unusually slow, as predicted by the life history hypothesis.     

Different axes of environmental variation explain the presence vs. extent of cooperative nest founding associations in Polistes paper wasps

Ecological constraints on independent breeding are recognised as major drivers of cooperative breeding across diverse lineages. How the prevalence and degree of cooperative breeding relates to ecological variation remains unresolved. Using a large data set of cooperative nesting in Polistes wasps we demonstrate that different aspects of cooperative breeding are likely to be driven by different aspects of climate. Whether or not a species forms cooperative groups is associated with greater short‐term temperature fluctuations. In contrast, the number of cooperative foundresses increases in more benign environments with warmer, wetter conditions. The same data set reveals that intraspecific responses to climate variation do not mirror genus‐wide trends and instead are highly heterogeneous among species. Collectively these data suggest that the ecological drivers that lead to the origin or loss of cooperation are different from those that influence the extent of its expression within populations.     

New phylogenetic information suggests both an increase and at least one loss of cooperative breeding during the evolutionary history of Aphelocoma jays

Efforts to identify ecological and life history factors associated with cooperative breeding have been largely unsuccessful, and interest is growing in the role of phylogenetic history in determining the distribution of this social system among lineages. In birds, cooperative breeding is distributed non-randomly among lineages, suggesting that phylogenetic inertia may play an important role in determining its distribution. The bird genus Aphelocoma has been particularly well studied because, although it is a relatively small genus, it shows broad among-lineage variation in level of cooperation. Previous analyses described an unusual unidirectional pattern of evolutionary loss of cooperation in Aphelocoma. Here, historical reconstructions based on new phylogenetic data suggest that evolutionary changes in cooperation have been bidirectional, with at least one gain and at least one loss over relatively recent timescales. This result emphasizes that, although history plays an important role in determining the incidence of cooperative breeding, cooperative behavior can switch relatively quickly in evolutionary time and may be influenced by the ecological context within which particular populations are distributed.     

Distinguishing ecological from evolutionary approaches to transposable elements

Considerable variation exists not only in the kinds of transposable elements (TEs) occurring within the genomes of different species, but also in their abundance and distribution. Noting a similarity to the assortment of organisms among ecosystems, some researchers have called for an ecological approach to the study of transposon dynamics. However, there are several ways to adopt such an approach, and it is sometimes unclear what an ecological perspective will add to the existing co‐evolutionary framework for explaining transposon‐host interactions. This review aims to clarify the conceptual foundations of transposon ecology in order to evaluate its explanatory prospects. We begin by identifying three unanswered questions regarding the abundance and distribution of TEs that potentially call for an ecological explanation. We then offer an operational distinction between evolutionary and ecological approaches to these questions. By determining the amount of variance in transposon abundance and distribution that is explained by ecological and evolutionary factors, respectively, it is possible empirically to assess the prospects for each of these explanatory frameworks. To illustrate how this methodology applies to a concrete example, we analyzed whole‐genome data for one set of distantly related mammals and another more closely related group of arthropods. Our expectation was that ecological factors are most informative for explaining differences among individual TE lineages, rather than TE families, and for explaining their distribution among closely related as opposed to distantly related host genomes. We found that, in these data sets, ecological factors do in fact explain most of the variation in TE abundance and distribution among TE lineages across less distantly related host organisms. Evolutionary factors were not significant at these levels. However, the explanatory roles of evolution and ecology become inverted at the level of TE families or among more distantly related genomes. Not only does this example demonstrate the utility of our distinction between ecological and evolutionary perspectives, it further suggests an appropriate explanatory domain for the burgeoning discipline of transposon ecology. The fact that ecological processes appear to be impacting TE lineages over relatively short time scales further raises the possibility that transposons might serve as useful model systems for testing more general hypotheses in ecology.     

Variation in mating system among birds: ecological basis revealed by hierarchical comparative analysis of mate desertion

Since most bird species are socially monogamous, variation among species in social mating systems is determined largely by variation in the frequency of mate desertion. Mate desertion is expected to occur when the benefits, in terms of additional reproductive opportunities, outweigh the costs, in terms of reduced reproductive success from the present brood. However, despite much research, the relative importance of costs and benefits in explaining mating system variation is not well understood. Here, we investigate this problem using a comparative method. We analyse changes in the frequency of mate desertion at different phylogenetic levels. Differences between orders and families in the frequency of desertion are negatively associated with changes in the potential costs of desertion, but are not associated with changes in the potential benefits of desertion. Conversely, differences among genera and species in the frequency of desertion are positively associated with increases in the potential benefits of desertion, but not with changes in the potential costs of desertion. Hence, we suggest that mate desertion in birds originates through a combination of evolutionary predisposition and ecological facilitation. In particular, ancient changes in life-history strategy determine the costs of desertion and predispose certain lineages to polygamy, while contemporary changes in the distribution of resources determine the benefits of desertion and thereby the likelihood that polygamy will be viable within these lineages. Thus, monogamy can arise via two very different evolutionary pathways. Groups such as albatrosses (Procellariidae) are constrained to social monogamy by the high cost to desertion, irrespective of the potential benefits. However, in groups such as the accentors (Prunellidae), which are predisposed to desertion, monogamy occurs only when the benefits of desertion are very limited. These conclusions emphasise the additional power which a hierarchical approach contributes to the modern comparative method.     

Life histories and the evolution of cooperative breeding in mammals

While the evolution of cooperative breeding systems (where non-breeding helpers participate in rearing young produced by dominant females) has been restricted to lineages with socially monogamous mating systems where coefficients of relatedness between group members are usually high, not all monogamous lineages have produced species with cooperative breeding systems, suggesting that other factors constrain the evolution of cooperative breeding. Previous studies have suggested that life-history parameters, including longevity, may constrain the evolution of cooperative breeding. Here, we show that transitions to cooperative breeding across the mammalian phylogeny have been restricted to lineages where females produce multiple offspring per birth. We find no support for effects of longevity or of other life-history parameters. We suggest that the evolution of cooperative breeding has been restricted to monogamous lineages where helpers have the potential to increase the reproductive output of breeders.     

Cooperative breeding in mammals

Cooperative breeding in mammals covers a diversity of breeding systems. In all cases, however, Individuals assist in the rearing of offspring other than their own. Recent research has highlighted some of the factors responsible for variation both within and between species. While it is possible to generalize about the selective pressures leading to cooperative breeding, doing so may obscure important contrasts between taxa. Of course, inclusive-fitness models explain the generalities of cooperative breeding, but differences in ecology, physiology and life history may result in distinctive processes operating in different taxa-data only likely to emerge from long-term field studies.     

Active and resting metabolism in birds: allometry, phylogeny and ecology

Variation in resting metabolic rate is strongly correlated with differences in body weight among birds. The lowest taxonomic level at which most of the variance in resting metabolic rate and body weight is evident for the sample is among families within orders. The allometric exponent across family points is 0.67. This exponent accords with the surface area interpretation of metabolic scaling based on considerations of heat loss. Deviations of family points from this allometric line are used to examine how resting metabolic rates differ among taxa, and whether variation in resting metabolic rate is correlated with broad differences in ecology and behaviour. Despite the strong correlation between resting metabolic rate and body weight, there is evidence for adaptive departures from the allometric line, and possible selective forces are discussed.
The allometric scaling of active metabolic rate is compared with that of resting metabolic rate. The allometric exponents for the two levels of energy expenditure differ, demonstrating that active small-bodied birds require proportionately more energy per unit time above resting levels than do active large-bodied birds. No consistent evidence was found to indicate that the different methods used to estimate active metabolic rate result in systematic bias. Birds require more energy relative to body size when undertaking breeding activities than at other stages of the annual cycle.     

Sociality,ecology and developmental constraints predict variation in brain size across birds

Conflicting theories have been proposed to explain variation in relative brain size across the animal kingdom. Ecological theories argue that the cognitive demands of seasonal or unpredictable environments have selected for increases in relative brain size, whereas the ‘social brain hypothesis’ argues that social complexity is the primary driver of brain size evolution. Here, we use a comparative approach to test the relative importance of ecology (diet, foraging niche and migration), sociality (social bond, cooperative breeding and territoriality) and developmental mode in shaping brain size across 1886 bird species. Across all birds, we find a highly significant effect of developmental mode and foraging niche on brain size, suggesting that developmental constraints and selection for complex motor skills whilst foraging generally imposes important selection on brain size in birds. We also find effects of social bonding and territoriality on brain size, but the direction of these effects do not support the social brain hypothesis. At the same time, we find extensive heterogeneity among major avian clades in the relative importance of different variables, implying that the significance of particular ecological and social factors for driving brain size evolution is often clade- and context-specific. Overall, our results reveal the important and complex ways in which ecological and social selection pressures and developmental constraints shape brain size evolution across birds.     

RAPID SYMPATRY EXPLAINS GREATER COLOR PATTERN DIVERGENCE IN HIGH LATITUDE BIRDS

Latitudinal variation in patterns of evolution has fascinated biologists for over a century, but our understanding of latitudinal differences in evolutionary processes—such as selection and drift—remains limited. Here, we test for, and find, accelerated evolution of color patterns in bird taxa that breed at higher latitudes compared with those breeding in the tropics, analyzing data from seven diverse avian families. Most important, we show that the extent of overlap of species' breeding ranges (degree of sympatry) explains the elevated rate of color pattern evolution at higher latitudes. We suggest that the dynamic shifts in breeding ranges that accompanied climatic changes during the last 3 million years (Milankovitch Oscillations) resulted in more rapid and more frequent secondary contact at high latitudes. We argue that sympatry among diverging clades causes greater divergence of color traits in birds at higher latitudes through sexual, social, or ecological character displacement that accelerate rates of evolution, and through the selective elimination of weakly differentiated lineages that hybridize and fuse in sympatry (differential fusion).     

Molecular phylogenetics at the population/species interface in cave spiders of the southern Appalachians (Araneae:Nesticidae:Nesticus)

This paper focuses on the relationship between population genetic structure and speciation mechanisms in a monophyletic species group of Appalachian cave spiders (Nesticus). Using mtDNA sequence data gathered from 256 individuals, I analyzed patterns of genetic variation within and between populations for three pairs of closely related sister species. Each sister-pair comparison involves taxa with differing distributional and ecological attributes; if these ecological attributes are reflected in basic demographic differences, then speciation might proceed differently across these sister taxa comparisons. Both frequency-based and gene tree analyses reveal that the genetic structure of the Nesticus species studied is characterized by similar and essentially complete population subdivision, regardless of differences in general ecology. These findings contrast with results of prior genetic studies of cave-dwelling arthropods that have typically revealed variation in population structure corresponding to differences in general ecology. Species fragmentation through both extrinsic and intrinsic evolutionary forces has resulted in discrete, perhaps independent, populations within morphologically defined species. Large sequence divergence values observed between populations suggest that this independence may extend well into the past. These patterns of mtDNA genealogical structure and divergence imply that species as morphological lineages are currently more inclusive than basal evolutionary or phylogenetic units, a suggestion that has important implications for the study of speciation mechanisms.      

Reproductive mode and population genetic structure of the cereal aphid Sitobion avenae studied using phenotypic and microsatellite markers

As French populations of the aphid Sitobion avenae exhibit a range of reproductive modes, this species provides a good opportunity for studying the evolution of breeding system variation. The present analysis combined ecological and genetic investigations into the spatial distribution of variation in reproductive mode. Reproductive mode was characterized in 277 lineages of S. avenae from France, and these aphids were scored for five microsatellite loci. The analyses revealed strong geographical partitioning of breeding systems, with obligate asexuals mostly restricted to the south of France, while lineages producing sexual forms were more common in the north. Contrary to what might be anticipated for organisms with frequent parthenogenesis, there was substantial genic and genotypic diversity, even in the obligately asexual lineages. More than 120 different genotypes were detected among the 277 aphid lineages, with an average of 5.9 alleles per locus (range four to 16) and heterozygosity of 56.7%. As with previous studies of allozyme variation in aphids, most loci showed heterozygote deficits, and disequilibrium was common among allelic variants at different loci, even after removal of replicate copies of genotypes that might have been derived through clonal reproduction. Our results suggest that selection is important in structuring reproductive systems and genetic variation in French S. avenae. Canonical correspondence analysis was employed to examine the associations between genotypic and phenotypic variables, enabling the identification of alleles correlated with life-history traits.     

First evidence for heritable variation in cooperative breeding behaviour

Understanding the evolution of complex social behaviours, such as cooperative breeding, is a fundamental problem in evolutionary biology, which has attracted much theoretical and empirical interest. Variation within and between species in the frequency of helping behaviour has been typically associated with variation in direct costs and benefits due to ecological constraints, or with indirect fitness payoffs (i.e. kin selection). Here, we provide the first evidence that individual variation in cooperative behaviour within a natural population also has a heritable component. Using a seven-generation pedigree in a wild population of western bluebirds (Sialia mexicana), we show significant heritable variation for the propensity to help rather than breed, as well as for the probability of having a helper at the nest. We also document a strong positive relationship between a bird's lifespan and its prospect of receiving help when breeding, in accordance with earlier comparative studies across species. These findings provide useful insights into the possible mechanisms which have led to the evolution of cooperative breeding and other social systems.     

Do avian cooperative breeders live longer?

Cooperative breeding is not common in birds but intriguingly over-represented in several families, suggesting that predisposing factors, similar ecological constraints or a combination of the two facilitate the evolution of this breeding strategy. The life-history hypothesis proposes that cooperative breeding is facilitated by high annual survival, which increases the local population and leads to a shortage of breeding opportunities. Clutch size in cooperative breeders is also expected to be smaller. An earlier comparative analysis in a small sample of birds supported the hypothesis but this conclusion has been controversial. Here, I extend the analysis to a larger, worldwide sample and take into account potential confounding factors that may affect estimates of a slow pace of life and clutch size. In a sample of 81 species pairs consisting of closely related cooperative and non-cooperative breeders, I did not find an association between maximum longevity and cooperative breeding, controlling for diet, body mass and sampling effort. However, in a smaller sample of 37 pairs, adult annual survival was indeed higher in the cooperative breeders, controlling for body mass. There was no association between clutch size and cooperative breeding in a sample of 93 pairs. The results support the facilitating effect of high annual survival on the evolution of cooperative breeding in birds but the effect on clutch size remains elusive.     

Within-species differences in primate social structure: evolution of plasticity and phylogenetic constraints

Primate socioecological studies have attempted to derive general frameworks using the average behavioural traits of species or genera to place them into categories. However, with the accumulation of primate studies, it is timely to place more emphasis on understanding within-species variation in social structure. In this review we have four objectives. First, we examine within-species variation in the potential determinants of social structure, including diet, demography, predation and infanticide, and document considerable variation. Second, we present case studies of within-species variation in social structure to illustrate the potential magnitude of this variation. For example, there are cases within a single interbreeding population where multi-male, uni-male, fission–fusion and monogamous groups are found. Third, by examining widespread primate lineages that occur in a variety of habitats, we note that there are differences in the magnitude of variation in social structures across different lineages and as a result we consider phylogenetic constraints on phenotypic variation in social structure. Finally, we reflect on the implications of extensive variation in social structure. We suggest that primate social structure will represent a combination of adaptation to present-day environment and phylogenetic inertia. To advance our understanding of the relative contribution of phylogeny versus ecology we propose two approaches. One approach is to compare groups in the same interbreeding population that inhabit different ecological conditions. Any differences that are found can be attributed to ecological differences, since phylogeny should not play a role within a single population. The second approach is to study distantly related species that have similar social structures to illustrate how similar ecological pressures might be operating to select for parallel social structures.     

Towards a unified theory of cooperative breeding: the role of ecology and life history re-examined

We present quantitative models that unify several adaptive hypotheses for the evolution of cooperative breeding in a single framework: the ecological constraints hypothesis, the life-history hypothesis and the benefits-of-philopatry hypothesis. Our goal is to explain interspecific variation in the occurrence of cooperative breeding in terms of interspecific variation in life-history traits and ecological conditions. We analyse two models, according to whether or not helpers can inherit their parents' territory. Major results are (i) territory inheritance always promotes cooperative breeding; (ii) if territories are not inherited, neither ecological constraints nor variation in life-history traits predict interspecific variation in cooperative breeding; and (iii) if territories are inherited, the mechanism of density regulation is crucial in determining which factors promote cooperative breeding. If density dependence acts on the probability to obtain a free territory or on the survival of dispersers, variation in ecological constraints cannot explain variation in cooperative breeding. Lower adult mortality favours helping, not because it reduces the availability of free territories, but because it enhances the direct benefits of helpers. If density dependence acts on fecundity, lower probability of obtaining a free territory and lower survival of dispersers promote cooperative breeding. In this case, lower adult mortality works against the evolution of helping. We suggest that the difference between birds and social insects in the covariance between cooperative breeding and life-history traits is due to different mechanisms of density regulation that operate in these taxa, and we explain how natural selection on habitat choice might have caused these different mechanisms to operate.     

Beyond trophic morphology: stable isotopes reveal ubiquitous versatility in marine turtle trophic ecology

The idea that interspecific variation in trophic morphology among closely related species effectively permits resource partitioning has driven research on ecological radiation since Darwin first described variation in beak morphology among Geospiza. Marine turtles comprise an ecological radiation in which interspecific differences in trophic morphology have similarly been implicated as a pathway to ecopartition the marine realm, in both extant and extinct species. Because marine turtles are charismatic flagship species of conservation concern, their trophic ecology has been studied intensively using stable isotope analyses to gain insights into habitat use and diet, principally to inform conservation management. This legion of studies provides an unparalleled opportunity to examine ecological partitioning across numerous hierarchical levels that heretofore has not been applied to any other ecological radiation. Our contribution aims to provide a quantitative analysis of interspecific variation and a comprehensive review of intraspecific variation in trophic ecology across different hierarchical levels marshalling insights about realised trophic ecology derived from stable isotopes. We reviewed 113 stable isotope studies, mostly involving single species, and conducted a meta‐analysis of data from adults to elucidate differences in trophic ecology among species. Our study reveals a more intricate hierarchy of ecopartitioning by marine turtles than previously recognised based on trophic morphology and dietary analyses. We found strong statistical support for interspecific partitioning, as well as a continuum of intraspecific trophic sub‐specialisation in most species across several hierarchical levels. This ubiquity of trophic specialisation across many hierarchical levels exposes a far more complex view of trophic ecology and resource‐axis exploitation than suggested by species diversity alone. Not only do species segregate along many widely understood axes such as body size, macrohabitat, and trophic morphology but the general pattern revealed by isotopic studies is one of microhabitat segregation and variation in foraging behaviour within species, within populations, and among individuals. These findings are highly relevant to conservation management because they imply ecological non‐exchangeability, which introduces a new dimension beyond that of genetic stocks which drives current conservation planning. Perhaps the most remarkable finding from our data synthesis is that four of six marine turtle species forage across several trophic levels. This pattern is unlike that seen in other large marine predators, which forage at a single trophic level according to stable isotopes. This finding affirms suggestions that marine turtles are robust sentinels of ocean health and likely stabilise marine food webs. This insight has broader significance for studies of marine food webs and trophic ecology of large marine predators. Beyond insights concerning marine turtle ecology and conservation, our findings also have broader implications for the study of ecological radiations. Particularly, the unrecognised complexity of ecopartitioning beyond that predicted by trophic morphology suggests that this dominant approach in adaptive radiation research likely underestimates the degree of resource overlap and that interspecific disparities in trophic morphology may often over‐predict the degree of realised ecopartitioning. Hence, our findings suggest that stable isotopes can profitably be applied to study other ecological radiations and may reveal trophic variation beyond that reflected by trophic morphology.     

Is Cooperative Breeding Associated With Bigger Brains? A Comparative Test in the Corvida (Passeriformes)

The cognitive demands of a social existence favour the evolution of relatively large brains and neocortices in primates. Comparable tests of sociality and brain size/structure in birds have not been performed, despite marked similarities in the social systems of birds and mammals. Here, we test whether one aspect of avian sociality, cooperative breeding, is associated with an increase in brain size across 155 species of the passeriform parvorder Corvida. Using conventional and phylogeny‐corrected statistics, we examined the correlated evolution of relative brain size and: the presence/absence of cooperative breeding, percentage of nests that are cooperative and cooperatively breeding group size. Most of the comparisons yielded non‐significant results, which suggests that cooperative breeding is not related to relative brain size in this parvorder. There are a number of potential explanations for our findings. First, changes in brain region size may be correlated with cooperative breeding without affecting overall brain size. Secondly, cooperatively breeding birds might not possess more complex social behaviour than non‐cooperatively breeding birds. Thirdly, relatively large brains might be ancestral in this parvorder. This may predispose them to evolve the range of complex behaviours found in this group, including extreme sociality. Finally, ecological and/or developmental factors might play a more significant role than social behaviour in the diversification of avian brain size. Assessing these alternatives requires more information on the neural and cognitive differences between bird species.     

Reproductive skew, costs, and benefits of cooperative breeding in female wood mice (Apodemus sylvaticus)

Two current models seek to explain reproduction of subordinatesin social groups: incentives given by dominants for peacefullyremaining in the group (reproductive skew model) or incompletecontrol by dominants. These models make different predictionsconcerning genetic relatedness between individuals for thedistribution of reproduction and the stability of cooperativebreeding associations. To test these models and to furtherexplore the relationships between reproductive skew, geneticrelatedness, and investment of each participant, we performedbehavioral observations of female wood mice (Apodemus sylvaticus)raising pups communally. Our results do not support previousmodels. Differences in lifetime reproductive success were significantlygreater within mother—daughter pairs than within pairsof sisters or unrelated females. Subordinate females of eitherbreeding unit did not differ in their direct reproduction.Calculations of inclusive fitness based on our results leadto the following predictions: (1) Communal nests should occuronly when ecological circumstances prevent solitary breeding.(2) Subordinate females gain the highest inclusive fitnessjoining their mothers; they also show the highest nursing investment.(3) Mothers should accept daughters, who have no opportunityfor solitary breeding. (4) Dominant sisters and unrelated femalesshould reject subordinate females because cooperative breedingreduces their reproductive success. However, breeding unitsof dominant sisters and unrelated females nevertheless occurand can be explained by our finding that such females significantlyreduce nursing time, which may help them save energy for futurebreeding cycles. Our data demonstrate that both genetic relatednessand investment skew are important in the complex evolutionof reproductive skew in cooperative breeding.