Experimental evidence for kin-biased helping in a cooperatively breeding vertebrate

The widespread belief that kin selection is necessary for the evolution of cooperative breeding in vertebrates has recently been questioned. These doubts have primarily arisen because of the paucity of unequivocal evidence for kin preferences in cooperative behaviour. Using the cooperative breeding system of long-tailed tits (Aegithalos caudatus) in which kin and non-kin breed within each social unit and helpers are failed breeders, we investigated whether helpers preferentially direct their care towards kin following breeding failure. First, using observational data, we show that not all failed breeders actually become helpers, but that those that do help usually do so at the nest of a close relative. Second, we confirm the importance of kinship for helping in this species by conducting a choice experiment. We show that potential helpers do not become helpers in the absence of close kin and, when given a choice between helping equidistant broods belonging to kin and non-kin within the same social unit, virtually all helped at the nest of kin. This study provides strong evidence that kinship plays an essential role in the maintenance of cooperative breeding in this species

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.Our research has received funding from the DST-NRF Centre of Excellence at the Percy FitzPatrick Institute of African Ornithology (South Africa), FEDER (Operational Programme for Competitiveness Factors – COMPETE) and Portuguese Foundation for Science and Technology (FCT; PTDC/BIA-BEC/103818/2008), Project “Biodiversity, Ecology and Global Change” co-financed by North Portugal Regional Operational Programme 2007/2013 (ON.2), under the NSRF, ERDF. to RC, the region Languedoc Roussillon to CD, the Natural Environment Research Council (UK) to BJH, St John's College, Cambridge and the University of Cape Town to CNS , and the European programme Marie Curie-IRSES (FP7-PEOPLE-2012-IRSES; ‘Cooperation’ 318994). This research was conducted within the International Associate Laboratory LIA “Biodiversity and Evolution”.This is the final version of the article. It first appeared from Wiley via http://dx.doi.org/10.1111/1365-2656.12377 Data are available from Dryad digital repository http://dx.doi.org/10.5061/dryad.mk44

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'

Temporal variation in fitness pay-offs promotes cooperative breeding in long-tailed tits Aegithalos caudatus

abstract: Cooperative breeding is paradoxical because some individuals forego independent reproduction and instead help others to reproduce. The ecological constraints model states that such behavior arises because of constraints on independent reproduction. Spatial variation in constraints has been shown to co-vary with the incidence of cooperative breeding in correlational and experimental studies. Here, we examine whether temporally variable ecological constraints can act in a similar way to promote cooperative breeding in the atypical system of long-tailed tits Aegithalos caudatus. In this species, individuals may switch reproductive tactics from breeding to helping within the same breeding season. Using 7 yr of field data, we show that reproductive success declined seasonally because of declines in brood size, nestling weight, and juvenile survival. The survival to breeding age of chicks from nests with helpers was higher than for chicks from nests without helpers, and since helpers usually helped at the nest of a close relative, they accrued inclusive fitness benefits. We used these data to model the expected fitness payoffs of breeding and helping at different times during the season. The model shows that late in the breeding season, the fitness payoff from a kin-directed helping tactic becomes greater than that from independent breeding. The behavioral switch predicted by the model is consistent with the observed switch from breeding to helping, which shows that cooperative breeding may evolve as a way of making the best of a bad job at the end of a temporally constrained breeding season

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.The authors' research received funding from the Natural Environment Research Council (NERC, UK; NE/G018588/1 and NE/K015257/1) to BJH, the DST-NRF Centre of Excellence at the Percy FitzPatrick Institute of African Ornithology and the Portuguese Science and Technology Foundation (FCT PTDC/BIA-BEC/103818/2008) to RC, the CNRS and region Languedoc Roussillon to CD, St John’s College, Cambridge, and the University of Cape Town to CNS, and the European MC-IRSES (FP7-PEOPLE-2012-IRSES; ‘Cooperation’ 318994) to RC, CD, REvD and BJH.This is the final version of the article. It first appeared from Wiley via http://dx.doi.org/10.1111/mec.1330

Adult helpers increase the recruitment of closely related offspring in the cooperatively breeding rifleman

Indirect fitness benefits gained through kin-selected helping are widely invoked to explain the evolution of cooperative breeding behavior in birds. However, the impact of helpers on productivity of helped broods can be difficult to determine if the effects are confounded by territory quality or if the benefit of helpers is apparent only in the long term. In riflemen Acanthisitta chloris, helping and group membership are effectively decoupled as adult helpers are individuals that have dispersed from their natal territory and live independently from breeders in “kin neighborhoods.” Nevertheless, helpers direct their care toward close relatives, suggesting that helping provides indirect fitness benefits. The aim of this study was to examine the benefits of helpers to recipient offspring in the rifleman, investigating both short- and long-term effects. The total amount of food delivered to nestlings in helped broods was greater than that received by broods without helpers. This did not result in any short-term increase in nestling mass or nestling body condition nor was there any reduction in length of the nestling period at helped nests. However, helpers were associated with a significant increase in juvenile recruitment, with twice the proportion of fledglings surviving to the next breeding season from helped broods relative to unhelped broods. Thus, helpers gain indirect fitness by improving the survival of kin, and in contrast to a previous study of riflemen, we conclude that kin selection has played a key role in the evolution of cooperative breeding in this species

Social dynamics in nonbreeding flocks of a cooperatively breeding bird: causes and consequences of kin associations

Kin selection is regarded as a key process in the evolution of avian cooperative breeding, and kinship influences helper decisions in many species. However, the effect of kinship on nonbreeding social organization is still poorly understood despite its potential fitness implications. Here, we investigated the origins and consequences of kin associations in nonbreeding flocks of long-tailed tits, Aegithalos caudatus, an atypical cooperative breeder where helpers are failed breeders that redirect care towards relatives living in kin neighbourhoods. We found that kinship is an important factor in initial grouping decisions; all members of a nuclear family initially joined the same flock and failed breeders chose to flock with their relatives. Flocks that merged during the nonbreeding season also contained relatives. In contrast to these findings of positive kin association, when long-tailed tits switched flocks they tended to disperse into flocks with fewer relatives, although such switches often occurred with kin. In a playback experiment, we found no evidence that aggression shown towards members of other flocks was affected by kinship, indicating that kin associations result from a preference to flock with relatives rather than a constraint on flocking with nonrelatives. Finally, using social network analysis, we show that fine-scale nonbreeding associations among individuals were positively related to kinship, and that these nonbreeding associations were reflected in helping decisions in the subsequent breeding season, in addition to the previously reported effects of kinship and proximity. We conclude that long-tailed tits prefer to associate with kin when not breeding, and suggest that by doing so they gain either nepotistic benefits within flocks or future indirect benefits during breeding

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

1. 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 restricted to scent-marking territorial animals, so its potential breadth of application has not been tested. 2. Here, we apply MHRA to a population of long-tailed tits (Aegithalos caudatus), a non15 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. 3. 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, to uncover the effect of these on the mechanisms of home range formation. 4. 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. 5. 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

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