Cost, risk, and avoidance of inbreeding in a cooperatively breeding bird.

Inbreeding is often avoided in natural populations by passive processes such as sex-biased dispersal. But, in many social animals, opposite-sexed adult relatives are spatially clustered, generating a risk of incest and hence selection for active inbreeding avoidance. Here we show that, in long-tailed tits (Aegithalos caudatus), a cooperative breeder that risks inbreeding by living alongside opposite-sex relatives, inbreeding carries fitness costs and is avoided by active kin discrimination during mate choice. First, we identified a positive association between heterozygosity and fitness, indicating that inbreeding is costly. We then compared relatedness within breeding pairs to that expected under multiple mate-choice models, finding that pair relatedness is consistent with avoidance of first-order kin as partners. Finally, we show that the similarity of vocal cues offers a plausible mechanism for discrimination against first-order kin during mate choice. Long-tailed tits are known to discriminate between the calls of close kin and nonkin, and they favor first-order kin in cooperative contexts, so we conclude that long-tailed tits use the same kin discrimination rule to avoid inbreeding as they do to direct help toward kin.

Individual variation explains ageing patterns in a cooperatively breeding bird, the long-tailed tit Aegithalos caudatus.

Alloparental care in cooperatively breeding species may alter breeder age-specific survival and reproduction and subsequently senescence. The helping behaviour itself might also undergo age-related change, and decisions to help in facultative cooperative breeders are likely to be affected by individual condition. Helpers in long-tailed tits Aegithalos caudatus assist relatives after failing to raise their own brood, with offspring from helped nests being more likely to recruit into the breeding population. Using data collected over 25 years, we examined the age trajectories of survival and reproduction in adult long-tailed tits to determine how these were affected by the presence or absence of helpers and how helper behaviour changed with age. There was evidence for increased reproductive performance with breeder age, but no effect of age on the probability of survival. We found no evidence of significant senescent decline in survival or reproductive performance, although individuals accrued less inclusive fitness in their last year of life. Lifetime reproductive success was positively related to both reproductive life span and body mass. Within a season, breeders that were assisted by helpers enjoyed greater reproductive success through enhanced offspring recruitment in the following year. We found no evidence that age affected an individual's propensity to help, or the amount of indirect fitness accrued through helping. We found a positive correlation between life span and multiple components of reproductive success, suggesting that individual variation in quality underpins age-related variation in fitness in this species. Helping decisions are driven by condition, and lifetime inclusive fitness of immigrants was predicted by body mass. These findings further support individual heterogeneity in quality being a major driver for fitness gains across the life course of long-tailed tits.

Fine-scale genetic structure reflects limited and coordinated dispersal in the colonial monk parakeet, Myiopsitta monachus.

The genetic structure of animal populations has considerable behavioural, ecological and evolutionary implications and may arise from various demographic traits. Here, we use observational field data and molecular genetics to determine the genetic structure of an invasive population of monk parakeets, Myiopsitta monachus, at a range of spatial scales, and investigate the demographic processes that generate the observed structure. Monk parakeets construct large nests that can house several pairs occupying separate chambers; these nests are often aggregated within nesting trees. We determined patterns of relatedness within compound nests, within nesting trees and between trees. Spatial autocorrelation analyses of pairwise genetic relatedness revealed fine-scale genetic structure with relatives of both sexes spatially clustered within, but not beyond, nesting trees. In addition, males were more related to males sharing their compound nests than to other males occupying the same nesting tree. By contrast, males and females within compound nests were not significantly more closely related than elsewhere in the same tree, and we found no evidence for inbreeding. Adults showed high breeding site fidelity between years despite considerable disturbance of nest sites. Natal dispersal was female-biased, but dispersal distances were relatively short with some natal philopatry observed in both sexes. Sibling coalitions, typically of males, were observed amongst both philopatric and dispersing birds. Our results show significant clustering of kin within compound nests and nesting trees resulting from limited and coordinated natal dispersal, with subsequent breeding site fidelity. The resulting genetic structure has implications for social behaviour in this unusual parrot species.

Inclusive fitness consequences of dispersal decisions in a cooperatively breeding bird, the long-tailed tit (Aegithalos caudatus).

Natal dispersal is a demographic trait with profound evolutionary, ecological, and behavioral consequences. However, our understanding of the adaptive value of dispersal patterns is severely hampered by the difficulty of measuring the relative fitness consequences of alternative dispersal strategies in natural populations. This is especially true in social species, in which natal philopatry allows kin selection to operate, so direct and indirect components of inclusive fitness have to be considered when evaluating selection on dispersal. Here, we use lifetime reproductive success data from a long-term study of a cooperative breeder, the long-tailed tit Aegithalos caudatus, to quantify the direct and indirect components of inclusive fitness. We show that dispersal has a negative effect on the accrual of indirect fitness, and hence inclusive fitness, by males. In contrast, the inclusive, predominantly direct, fitness of females increases with dispersal distance. We conclude that the conflicting fitness consequences of dispersal in this species result in sexually antagonistic selection on this key demographic parameter.

Mechanistic home range analysis reveals drivers of space use patterns for a non-territorial passerine.

Home ranging is a near-ubiquitous phenomenon in the animal kingdom. Understanding the behavioural mechanisms that give rise to observed home range patterns is thus an important general question, and mechanistic home range analysis (MHRA) provides the tools to address it. However, such analysis has hitherto been principally restricted to scent-marking territorial animals, so its potential breadth of application has not been tested. Here, we apply MHRA to a population of long-tailed tits Aegithalos caudatus, a non-territorial passerine, in the non-breeding season where there is no clear 'central place' near which birds need to remain. The aim is to uncover the principal movement mechanisms underlying observed home range formation. Our foundational models consist of memory-mediated conspecific avoidance between flocks, combined with attraction to woodland. These are then modified to incorporate the effects of flock size and relatedness (i.e. kinship), to uncover the effect of these on the mechanisms of home range formation. We found that a simple model of spatial avoidance, together with attraction to the central parts of woodland areas, accurately captures long-tailed tit home range patterns. Refining these models further, we show that the magnitude of spatial avoidance by a flock is negatively correlated to both the relative size of the flock (compared to its neighbour) and the relatedness of the flock with its neighbour. Our study applies MHRA beyond the confines of scent-marking, territorial animals, so paves the way for much broader taxonomic application. These could potentially help uncover general properties underlying the emergence of animal space use patterns. This is also the first study to apply MHRA to questions of relatedness and flock size, thus broadening the potential possible applications of this suite of analytic techniques.

Microsatellite characterisation and sex-typing in two invasive parakeet species, the monk parakeet Myiopsitta monachus and ring-necked parakeet Psittacula krameri.

Invasive species can have wide-ranging negative impacts, and an understanding of the process and success of invasions can be vital to determine management strategies, mitigate impacts and predict range expansions of such species. Monk parakeets (Myiopsitta monachus) and ring-necked parakeets (Psittacula krameri) are both widespread invasive species, but there has been little research into the genetic and social structure of these two species despite the potential links with invasion success. The aim of this study was to isolate novel microsatellite loci from the monk parakeet and characterise them in both monk and ring-necked parakeets in order to facilitate future investigations into their behaviour and population ecology. Sex-typing markers were also tested in both species. Of the 20 microsatellite loci assessed in 24 unrelated monk parakeets, 16 successfully amplified and were polymorphic displaying between 2 and 14 alleles (mean = 8.06). Expected heterozygosity ranged from 0.43 to 0.93 and observed heterozygosity ranged from 0.23 to 0.96. Nine of the 20 loci also successfully amplified and were polymorphic in the ring-necked parakeet, displaying between 2 and 10 alleles. Suitable markers to sex both species and a Z-linked microsatellite locus were identified. A multiplex marker set was validated for monk parakeets. These novel microsatellite loci will facilitate fine and broad-scale population genetic analyses of these two widespread invasive species.

Fine-scale genetic structure and helping decisions in a cooperatively breeding bird.

In animal societies, characteristic demographic and dispersal patterns may lead to genetic structuring of populations, generating the potential for kin selection to operate. However, even in genetically structured populations, social interactions may still require kin discrimination for cooperative behaviour to be directed towards relatives. Here, we use molecular genetics and long-term field data to investigate genetic structure in an adult population of long-tailed tits Aegithalos caudatus, a cooperative breeder in which helping occurs within extended kin networks, and relate this to patterns of helping with respect to kinship. Spatial autocorrelation analyses reveal fine-scale genetic structure within our population, such that related adults of either sex are spatially clustered following natal dispersal, with relatedness among nearby males higher than that among nearby females, as predicted by observations of male-biased philopatry. This kin structure creates opportunities for failed breeders to gain indirect fitness benefits via redirected helping, but crucially, most close neighbours of failed breeders are unrelated and help is directed towards relatives more often than expected by indiscriminate helping. These findings are consistent with the effective kin discrimination mechanism known to exist in long-tailed tits and support models identifying kin selection as the driver of cooperation.

Sex Allocation Patterns across Cooperatively Breeding Birds Do Not Support Predictions of the Repayment Hypothesis.

The repayment hypothesis predicts that reproductive females in cooperative breeding systems overproduce the helping sex. Thanks to well-documented examples of this predicted sex ratio bias, repayment has been considered an important driver of variation in sex allocation patterns. Here we test this hypothesis using data on population brood sex ratios and facultative sex allocation from 28 cooperatively breeding bird species. We find that biased sex ratios of helpers do not correlate with production biases in brood sex ratios, contrary to predictions. We also test whether females facultatively produce the helping sex in response to a deficiency of help (i.e., when they have fewer or no helpers). Although this is observed in a few species, it is not a significant trend overall, with a mean effect size close to zero. We conclude that, surprisingly, repayment does not appear to be a widespread influence on sex ratios in cooperatively breeding birds. We discuss possible explanations for our results and encourage further examination of the repayment model.

Social genetic and social environment effects on parental and helper care in a cooperatively breeding bird.

Phenotypes expressed in a social context are not only a function of the individual, but can also be shaped by the phenotypes of social partners. These social effects may play a major role in the evolution of cooperative breeding if social partners differ in the quality of care they provide and if individual carers adjust their effort in relation to that of other carers. When applying social effects models to wild study systems, it is also important to explore sources of individual plasticity that could masquerade as social effects. We studied offspring provisioning rates of parents and helpers in a wild population of long-tailed tits Aegithalos caudatus using a quantitative genetic framework to identify these social effects and partition them into genetic, permanent environment and current environment components. Controlling for other effects, individuals were consistent in their provisioning effort at a given nest, but adjusted their effort based on who was in their social group, indicating the presence of social effects. However, these social effects differed between years and social contexts, indicating a current environment effect, rather than indicating a genetic or permanent environment effect. While this study reveals the importance of examining environmental and genetic sources of social effects, the framework we present is entirely general, enabling a greater understanding of potentially important social effects within any ecological population.

Fine-scale genetic structure reflects sex-specific dispersal strategies in a population of sociable weavers (Philetairus socius).

Dispersal is a critical driver of gene flow, with important consequences for population genetic structure, social interactions and other biological processes. Limited dispersal may result in kin-structured populations in which kin selection may operate, but it may also increase the risk of kin competition and inbreeding. Here, we use a combination of long-term field data and molecular genetics to examine dispersal patterns and their consequences for the population genetics of a highly social bird, the sociable weaver (Philetairus socius), which exhibits cooperation at various levels of sociality from nuclear family groups to its unique communal nests. Using 20 years of data, involving capture of 6508 birds and 3151 recaptures at 48 colonies, we found that both sexes exhibit philopatry and that any dispersal occurs over relatively short distances. Dispersal is female-biased, with females dispersing earlier, further, and to less closely related destination colonies than males. Genotyping data from 30 colonies showed that this pattern of dispersal is reflected by fine-scale genetic structure for both sexes, revealed by isolation by distance in terms of genetic relatedness and significant genetic variance among colonies. Both relationships were stronger among males than females. Crucially, significant relatedness extended beyond the level of the colony for both sexes. Such fine-scale population genetic structure may have played an important role in the evolution of cooperative behaviour in this species, but it may also result in a significant inbreeding risk, against which female-biased dispersal alone is unlikely to be an effective strategy.

Antagonistic effect of helpers on breeding male and female survival in a cooperatively breeding bird.

1. Cooperatively breeding species are typically long lived and hence, according to theory, are expected to maximize their lifetime reproductive success through maximizing survival. Under these circumstances, the presence of helpers could be used to lighten the effort of current reproduction for parents to achieve higher survival. 2. In addition, individuals of different sexes and ages may follow different strategies, but whether male and female breeders and individuals of different ages benefit differently from the presence of helpers has often been overlooked. Moreover, only one study that investigated the relationship between parental survival and the presence of helpers used capture-mark-recapture analyses (CMR). These methods are important since they allow us to account for the non-detection of individuals that are alive in the population but not detected, and thus, the effects on survival and recapture probability to be disentangled. 3. Here, we used multi-event CMR methods to investigate whether the number of helpers was associated with an increase in survival probability for male and female breeders of different ages in the sociable weaver Philetairus socius. In this species, both sexes reduce their feeding rate in the presence of helpers. We therefore predicted that the presence of helpers should increase the breeders' survival in both sexes, especially early in life when individuals potentially have more future breeding opportunities. In addition, sociable weaver females reduce their investment in eggs in the presence of helpers, so we predicted a stronger effect of helpers on female than male survival. 4. As expected we found that females had a higher survival probability when breeding with more helpers. Unexpectedly, however, male survival probability decreased with increasing number of helpers. This antagonistic effect diminished as the breeders grew older. 5. These results illustrate the complexity of fitness costs and benefits underlying cooperative behaviours and how these may vary with the individuals' sex and age. They also highlight the need for further studies on the sex-specific effects of helpers on survival.

Cooperative investment in public goods is kin directed in communal nests of social birds.

The tragedy of the commons predicts social collapse when public goods are jointly exploited by individuals attempting to maximize their fitness at the expense of other social group members. However, animal societies have evolved many times despite this vulnerability to exploitation by selfish individuals. Kin selection offers a solution to this social dilemma, but in large social groups mean relatedness is often low. Sociable weavers (Philetairus socius) live in large colonies that share the benefits of a massive communal nest, which requires individual investment for construction and maintenance. Here, we show that despite low mean kinship within colonies, relatives are spatially and socially clustered and that nest-building males have higher local relatedness to other colony members than do non-building males. Alternative hypotheses received little support, so we conclude that the benefits of the public good are shared with kin and that cooperative investment is, despite the large size and low relatedness of these communities, kin directed.

Genetic analysis reveals diverse kin-directed routes to helping in the rifleman Acanthisitta chloris.

The social organization of cooperatively breeding species is extremely variable, with diverse social group composition and patterns of relatedness. Species that exhibit alternative routes to helping within the same population are potentially useful systems to investigate the causes and fitness consequences of diverse evolutionary pathways to cooperative behaviour. In this study, we use microsatellite markers and field observations to describe helping behaviour and patterns of relatedness in the unusual cooperative breeding system of the rifleman Acanthisitta chloris. First, we show that rifleman helpers consist of a remarkably diverse demographic, including males and females, who may be adult or juvenile, failed breeders or nonbreeders, or even successful breeders that simultaneously feed their own brood. Adult helpers mostly helped at first-brood nests, while first-brood juveniles assisted their parents at second broods. Second, we show that rifleman pairs are strictly sexually monogamous, and helpers did not gain any current reproductive success through helping. Third, genotyping showed that contrary to previous assumptions, helpers were closely related to the recipients of their care and preferentially directed care towards relatives over contemporaneous nests of nonrelatives. Finally, we show that variation in helper provisioning effort was attributed to age: juvenile helpers provisioned less than adults and were less responsive to the demands of a growing brood. Overall, our results show that the diverse routes to helping in this unusual species are driven by the common theme of kinship between helper and recipients, resulting in a previously underestimated potential for helpers to gain indirect fitness benefits.

Ecological and demographic correlates of helping behaviour in a cooperatively breeding bird.

The evolution of cooperation is a persistent problem for evolutionary biologists. In particular, understanding of the factors that promote the expression of helping behaviour in cooperatively breeding species remains weak, presumably because of the diverse nature of ecological and demographic drivers that promote sociality. In this study, we use data from a long-term study of a facultative cooperative breeder, the long-tailed tit Aegithalos caudatus, to investigate the factors influencing annual variation in helping behaviour. Long-tailed tits exhibit redirected helping in which failed breeders may become helpers, usually at a relative's nest; thus, helping is hypothesised to be associated with causes of nest failure and opportunities to renest or help. We tested predictions regarding the relationship between annual measures of cooperative behaviour and four explanatory variables: nest predation rate, length of the breeding season, population-level relatedness and population density. We found that the degree of helping was determined principally by two factors that constrain successful independent reproduction. First, as predicted, cooperative behaviour peaked at intermediate levels of nest predation, when there are both failed breeders (i.e. potential helpers) and active nests (i.e. potential recipients) available. Second, there were more helpers in shorter breeding seasons when opportunities for renesting by failed breeders are more limited. These are novel drivers of helping behaviour in avian cooperative breeding systems, and this study illustrates the difficulty of identifying common ecological or demographic factors underlying the evolution of such systems.

Partner intrinsic characteristics influence foraging trip duration, but not coordination of care in wandering albatrosses Diomedea exulans.

Long-lived monogamous species gain long-term fitness benefits by equalizing effort during biparental care. For example, many seabird species coordinate care by matching foraging trip durations within pairs. Age affects coordination in some seabird species; however, the impact of other intrinsic traits, including personality, on potential intraspecific variation in coordination strength is less well understood. The impacts of pair members' intrinsic traits on trip duration and coordination strength were investigated using data from saltwater immersion loggers deployed on 71 pairs of wandering albatrosses Diomedea exulans. These were modeled against pair members' age, boldness, and their partner's previous trip duration. At the population level, the birds exhibited some coordination of parental care that was of equal strength during incubation and chick-brooding. However, there was low variation in coordination between pairs and coordination strength was unaffected by the birds' boldness or age in either breeding stage. Surprisingly, during incubation, foraging trip duration was mainly driven by partner traits, as birds which were paired to older and bolder partners took shorter trips. During chick-brooding, shorter foraging trips were associated with greater boldness in focal birds and their partners, but age had no effect. These results suggest that an individual's assessment of their partner's capacity or willingness to provide care may be a major driver of trip duration, thereby highlighting the importance of accounting for pair behavior when studying parental care strategies.

Learned kin recognition cues in a social bird.

In many cooperatively breeding birds, kin selection has an important role in the evolution and maintenance of social behaviour, and 'helpers' can maximize indirect fitness gains by preferentially allocating care to close relatives. Although there is evidence for kin-biased helping behaviour in several species, the mechanism of kin recognition underlying this behaviour is poorly understood. Vocalizations are the most commonly used cues in avian recognition systems, but the effectiveness of vocal signals as reliable recognition cues must depend on how they are acquired. However, there have been no experimental studies of the development of vocal recognition cues in cooperative birds; indeed, the ontogeny of all bird vocalizations other than song is poorly known in any species. Here, we show that cooperatively breeding long-tailed tits (Aegithalos caudatus) can discriminate between kin and non-kin according to the individual-specific characteristics of contact calls, and show experimentally that individuals learn these calls from provisioning adults during the nestling period. Finally, we show that the pattern of cooperative behaviour in this species is consistent with the use of recognition cues learned through association.

Avian reproduction: role of ecology in the evolution of cooperative breeding.

A new comparative analysis of the speciose and socially diverse family of African starlings provides evidence that cooperative breeding has evolved in unpredictable, seasonal environments.

Kinship affects investment by helpers in a cooperatively breeding bird.

Helping behaviour in cooperative breeding systems has been attributed to kin selection, but the relative roles of direct and indirect fitness benefits in the evolution of such systems remain a matter of debate. In theory, helpers could maximize the indirect fitness benefits of cooperation by investing more in broods with whom they are more closely related, but there is little evidence for such fine-scale adjustment in helper effort among cooperative vertebrates. In this study, we used the unusual cooperative breeding system of the long-tailed tit Aegithalos caudatus to test the hypothesis that the provisioning effort of helpers was positively correlated with their kinship to broods. We first use pedigrees and microsatellite genotypes to characterize the relatedness between helpers and breeders from a 14 year field study. We used both pedigree and genetic approaches because long-tailed tits have access to pedigree information acquired through social relationships, but any fitness consequences will be determined by genetic relatedness. We then show using both pedigrees and genetic relatedness estimates that alloparental investment by helpers increases as their relatedness to the recipients of their care increases. We conclude that kin selection has played a critical role in moulding the investment decisions of helpers in this cooperatively breeding species.

Consequences of 'load-lightening' for future indirect fitness gains by helpers in a cooperatively breeding bird.

1. Helpers that invest energy in provisioning the offspring of related individuals stand to gain indirect fitness benefits from doing so. First, if the helper's effort is additional to that of the parents (additive) the productivity of the current breeding attempt can be increased. Secondly, if the parents reduce their workload (compensation) this can result in future indirect fitness gains to the helper via increased breeder survival; termed 'load-lightening'. 2. Long-tailed tits (Aegithalos caudatus) have a cooperative breeding system in which helpers assist kin and parents exhibit both additive and compensatory reactions in the presence of helpers. Offspring from helped nests are heavier and more likely to recruit into the breeding population, thus helpers gain indirect fitness benefits from increasing the productivity of the current breeding attempt. Despite breeders' reduction of feeding effort in the presence of helpers, previous investigations found no subsequent increase in breeder survival. 3. The aim of this study was to test the hypothesis that load-lightening resulted in indirect fitness benefits for helpers. We used data from a 14-year study to investigate the provisioning rate, survival and future fecundity of male and female long-tailed tits that did and did not receive help at the nest. 4. We found an asymmetrical response to the presence of helpers at large brood sizes. Males reduced their feeding rate more than females, and this differential response was reflected in a significant increase in male survival when provisioning large broods assisted by helpers. We found no evidence of any increase in future fecundity for helped breeders. 5. The finding that males reduce their provisioning rate in the presence of helpers (at large brood sizes) to a greater degree than females, and that this is reflected in an increase in survival rate for males only, implies that the survival increase is caused by the reduction in work-rate rather than a non-specific benefit of a larger group size. 6. The marginal benefits of help for breeder survival are likely to be more difficult to identify than the increased productivity at helped nests, but should not be overlooked when investigating the potential indirect fitness gains that supernumeraries can accrue by helping.

Helping decisions and kin recognition in long-tailed tits: is call similarity used to direct help towards kin?

Most cooperative breeders live in discrete family groups, but in a minority, breeding populations comprise extended social networks of conspecifics that vary in relatedness. Selection for effective kin recognition may be expected for more related individuals in such kin neighbourhoods to maximize indirect fitness. Using a long-term social pedigree, molecular genetics, field observations and acoustic analyses, we examine how vocal similarity affects helping decisions in the long-tailed tit Aegithalos caudatus. Long-tailed tits are cooperative breeders in which help is typically redirected by males that have failed in their own breeding attempts towards the offspring of male relatives living within kin neighbourhoods. We identify a positive correlation between call similarity and kinship, suggesting that vocal cues offer a plausible mechanism for kin discrimination. Furthermore, we show that failed breeders choose to help males with calls more similar to their own. However, although helpers fine-tune their provisioning rates according to how closely related they are to recipients, their effort was not correlated with their vocal similarity to helped breeders. We conclude that although vocalizations are an important part of the recognition system of long-tailed tits, discrimination is likely to be based on prior association and may involve a combination of vocal and non-vocal cues. This article is part of the theme issue 'Signal detection theory in recognition systems: from evolving models to experimental tests'.