Experimentally increased food resources in the natal territory promote offspring philopatry and helping in cooperatively breeding carrion crows

Kin-based societies, where families represent the basic social unit, occur in a relatively small number of vertebrate species. In the majority of avian kin societies, families form when offspring prolong their association with the parents on the natal territory. Therefore, the key to understanding the evolution of families in birds is to understand natal philopatry (i.e. the tendency to remain on the natal territory). It has been shown that, within populations, the strength of the association between parents and offspring (i.e. family stability) increases when offspring dispersal is constrained by external environmental factors, but it is unclear whether and how family wealth influences juvenile dispersal decisions. Here, we show that young carrion crows (Corvus corone corone) from territories that were food-supplemented year-round were more philopatric and more likely to help at their family's nest than the unfed ones. The results suggest that offspring philopatry and helping behaviour are influenced by the quality of 'home' and that the availability of food resources positively affects the cohesion of the family.     

Out of Gondwanaland; the evolutionary history of cooperative breeding and social behaviour among crows, magpies, jays and allies

Cooperative breeding is comparatively rare among birds in the mainly temperate and boreal Northern Hemisphere. Here we test if the distribution of breeding systems reflects a response to latitude by means of a phylogenetic analysis using correlates with geographical range among the corvids (crows, jays, magpies and allied groups). The corvids trace their ancestry to the predominantly cooperative 'Corvida' branch of oscine passerines from the Australo-Papuan region on the ancient Gondwanaland supercontinent, but we could not confirm the ancestral state of the breeding system within the family, while family cohesion may be ancestral. Initial diversification among pair-breeding taxa that are basal in the corvid phylogeny, represented by genera such as Pyrrhocorax and Dendrocitta, indicates that the corvid family in its current form could have evolved from pair-breeding ancestors only after they had escaped the Australo-Papuan shield. Within the family, cooperative breeding (alloparental care/family cohesion) is strongly correlated to latitude and its predominance in species maintaining a southerly distribution indicates a secondary evolution of cooperative breeding in the lineage leading away from the basal corvids. Multiple transitions show plasticity in the breeding system, indicating a response to latitude rather than evolutionary inertia. The evolutionary background to the loss of cooperative breeding among species with a northerly distribution is complex and differs between species, indicating a response to a variety of selection forces. Family cohesion where the offspring provide alloparental care is a main route to cooperatively breeding groups among corvids. Some corvid species lost only alloparental care, while maintaining coherent family groups. Other species lost family cohesion and, as a corollary, they also lost the behaviour where retained offspring provide alloparental care.     

Prolactin and helping in birds: has natural selection strengthened helping behavior?

The evolution of helping behavior in birds has been hotly debated.Hamilton's inclusive fitness theory has received much supportfrom ecological cost-benefit studies; however, the hypothesisthat helping has not been selected per se but is simply a phenotypicallyplastic response to altered social conditions has been proposed.In this view helping by nonbreeding birds occurs when at independencethey fail to leave their parents and are exposed to the criticalstimulus, the begging of young birds to be fed. We report thatlevels of prolactin, a hormone associated with parental behavior,are conspicuously higher in an avian species with helpers, theMexican jay (Aphelocoma ultramarina), than in a congeneric andsympatric species without helpers, the western scrub jay (A.californica). Specifically, prolactin in the nonbreeding membersof the helping species is higher than the level found in thebreeders of the congeneric nonhelping species. In addition,prolactin levels in nonbreeders rise well before the appearanceof begging young. These findings reject the phenotypic plasticityhypothesis based purely on a response to begging young and suggestthat prolactin is involved in the physiology of helping behaviorin birds as part of a complex adaptation.     

Delayed dispersal and prolonged brood care in a family‐living beetle

Delayed juvenile dispersal is an important prerequisite for the evolution of family‐based social systems, such as cooperative breeding and eusociality. In general, young adults forego dispersal if there are substantial benefits to remaining in the natal nest and/or the likelihood of dispersing and breeding successfully is low. We investigate some general factors thought to drive delayed juvenile dispersal in the horned passalus beetle, a family‐living beetle in which young adults remain with their families in their natal nest for several months before dispersing. Fine‐scale population genetic structure indicated high gene flow between nest sites, suggesting that constraints on mobility are unlikely to explain philopatry. Young adults do not breed in their natal log and likely disperse before reaching breeding age, suggesting that they do not gain direct reproductive benefits from delayed dispersal. We also examined several ways in which parents might incentivize delayed dispersal by providing prolonged care to adult offspring. Although adult beetles inhibit fungal growth in the colony by manipulating both the nest site and deceased conspecifics, this is unlikely to be a major explanation for family living as both parents and adult offspring seem capable of controlling fungal growth. Adult offspring that stayed with their family groups also neither gained more mass nor experienced faster exoskeleton development than those experimentally removed from their families. The results of these experiments suggest that our current understanding of the factors underlying prolonged family living may be insufficient to explain delayed dispersal in at least some taxa, particularly insects.     

Offspring retention in the Siberian jay {Perisoreus infaustus): the prolonged brood care hypothesis

We examined aggressive behavior in Siberian jay groups containingboth retained offspring and immigrant juveniles during winterfeeding and during breeding. Selective tolerance of retainedoffspring by parental birds in winter suggests that cooperationevolved through kin selection. Parents exhibited a self-restraintin aggression towards retained offspring at food in winter.Comparatively, nonkin immigrants were aggressively preventedfrom sharing food by the local pair. Parental tolerance in wintercould bring inclusive fitness gains through the direct kin componentif retained offspring experience relaxed competition and enhancedsurvival. Parental tolerance would then favor the evolutionof delayed dispersal. There is no evidence that delayed dispersalamong Siberian jays should have evolved because of indirectfitness benefits to retained offspring from helping to raiseyounger siblings. Offspring retained by parents did not participatein incubation, feeding or nest defense.     

Dispersal of sibling coalitions promotes helping among immigrants in a cooperatively breeding bird

Kin selection is a major force in social evolution, but dispersal is often assumed to reduce its impact by diluting kinship. In most cooperatively breeding vertebrates, in which more than two individuals care for young, juveniles delay dispersal and become helpers in family groups. In long-tailed tits (Aegithalos caudatus), however, offspring disperse to breed and helpers are failed breeders that preferentially aid kin. Helping also occurs among immigrants, but their origins are unknown and cooperation in these cases is poorly understood. Here, we combine long-term demographic and genetic data from our study population to investigate immigration and helping in this species. We first used a novel application of parentage analysis to discriminate between immigrants and unknown philopatric recruits. We then cross-checked sibship reconstruction with pairwise relatedness estimates to show that immigrants disperse in sibling coalitions and helping among them is kin biased. These results indicate that dispersal need not preclude sociality, and dispersal of kin coalitions may help maintain kin-selected cooperation in the absence of delayed dispersal.     

Cognitive adaptations of social bonding in birds

The 'social intelligence hypothesis' was originally conceived to explain how primates may have evolved their superior intellect and large brains when compared with other animals. Although some birds such as corvids may be intellectually comparable to apes, the same relationship between sociality and brain size seen in primates has not been found for birds, possibly suggesting a role for other non-social factors. But bird sociality is different from primate sociality. Most monkeys and apes form stable groups, whereas most birds are monogamous, and only form large flocks outside of the breeding season. Some birds form lifelong pair bonds and these species tend to have the largest brains relative to body size. Some of these species are known for their intellectual abilities (e.g. corvids and parrots), while others are not (e.g. geese and albatrosses). Although socio-ecological factors may explain some of the differences in brain size and intelligence between corvids/parrots and geese/albatrosses, we predict that the type and quality of the bonded relationship is also critical. Indeed, we present empirical evidence that rook and jackdaw partnerships resemble primate and dolphin alliances. Although social interactions within a pair may seem simple on the surface, we argue that cognition may play an important role in the maintenance of long-term relationships, something we name as 'relationship intelligence'.     

Ravens judge competitors through experience with play caching

Complex social behavior builds on the mutual judgment of individuals as cooperation partners and competitors [1]. Play can be used for assessing the others' dispositions in humans and nonhuman mammals [2], whereas little is known about birds. Recently, food-caching corvids have been found to rival primates in their ability to judge the behaviors and intentions of others in competition for hidden food [3]. Here, we show that ravens Corvus corax quickly learn to assess the competitive strategies of unfamiliar individuals through interactions with them over caches with inedible items and subsequently apply this knowledge when caching food. We confronted birds with two human experimenters who acted differently when birds cached plastic items: the pilferer stole the cached objects, whereas the onlooker did not. Birds responded to the actions of both experimenters with changing the location of their next object caches, either away from or toward the humans, as if they were testing their pilfering dispositions. In contrast, ravens instantly modified their caching behavior with food, preventing only the competitive human from finding the caches. Playful object caching in a social setting could thus aid ravens in evaluating others' pilfering skills.     

Food sharing and affiliation: An experimental and longitudinal study in cockatiels (Nymphicus hollandicus)

Food sharing has attracted much attention because of its apparently altruistic nature and its link to prosociality. However, food sharing has been mostly studied in a reproductive context, during courtship and parental care, where the fitness benefits are obvious. We still lack a clear understanding of the functions of food sharing outside any reproductive context and within social groups of same‐aged peers. Previous studies suggest that cofeeding, the action to let another animal feed from the same monopolizable food source, may be used to build and strengthen bonds between individuals. This may be particularly crucial in social birds forming long‐term associations between mates or siblings such as psittacids and corvids. Here, we investigated food sharing and affiliative behaviors such as allopreening in a psittacine species, namely in a group of captive juvenile cockatiels (Nymphicus hollandicus) consisting of five siblings and five unrelated birds. Our main objective was to study the developmental pattern of food sharing over time and its implication in social bonding depending on kinship, affiliation, and sex. Studying cockatiels in this context is providing many new information since most of the studies on food sharing in birds focused on corvids. We found that, contrary to jackdaws, cockatiels continued to share food with multiple individuals, although the frequency of cofeeding as well as the number of cofeeding partners decreased over time. Cockatiels shared more food with their siblings than with other conspecifics but they were not more likely to do cofeeding with birds of the opposite sex. We also found evidence that young cockatiels exchanged more food with those from whom they received food (reciprocity) and, to a lesser extent, allopreening (interchange), than from other cockatiels. Our findings suggest that in cockatiels, food sharing within social groups serves the formation (and maintenance) of affiliative bonds, especially between siblings, rather than pair bonds, but might additionally be explained by reciprocity, interchange, and harassment avoidance.     

Genetic monogamy in single-male groups of acorn woodpeckers, Melanerpes formicivorus

Acorn woodpeckers have one of the most complex social systems of any bird species. Breeding units range in size from monogamous pairs to groups of 15 birds that include multiple breeding males and females as well as nonreproductive helpers-at-the-nest. Groups form when young remain at their natal nest to help their parents breed or when single-sex coalitions of siblings disperse to fill a reproductive vacancy on another territory. Plural breeding and helping behaviour are thought to be favoured through indirect fitness benefits for individuals that would otherwise be unable to breed due to a shortage of reproductive vacancies on territories with acorn stores. We report the results of multi-locus DNA fingerprinting of 51 offspring from 18 nests of 16 socially monogamous pairs of acorn woodpeckers. If socially monogamous females mate outside the pair-bond, indirect fitness benefits for cobreeders and helpers will be significantly reduced. Monogamous pairs accounted for all but one of the 51 offspring we tested; the single exception was apparently sired by the putative father, but the putative mother was excluded from maternity. Our results indicate that individuals remaining on their natal territories as helpers are generally the genetic offspring of the pair they help. They also suggest that single-sex coalitions offspring dispersing together from nests of socially monogamous pairs will be full-siblings.     

The origin of helping: the role of variability in reproductive potential

We investigate the relationship between variation in reproductive potential among members of a family and genetic relatedness to determine which combinations favor natural selection for helping behavior. Conditions favoring helping are derived for the helper, the recipient, and the parents of these individuals. Our analysis reveals that a factor of general significance in the evolution of social organisms is variability in reproductive potential among offspring of a parent. To a limited extent this factor has already been appreciated because of its implicit role in "facultative altruism" and "parental manipulation", or suppression of offspring or sibs; however, the unifying role of variance per se and the ways by which it may act have not been widely appreciated. We show that suppression as a source of intra-brood variance is less powerful in the evolution of sociality than other, natural, sources of variance. The facts of natural history appear to be more consistent with a model utilizing natural variance than with a variance-enhancement model for most vertebrates. We present models for discrete and for overlapping generations. Fecundity of young potential helpers relative to adults is an important source of variance for the origin of helping.     

The Pattern of Helping in the Bell Miner Revisited: A Reply to Jamieson and Craig

Jamieson & Craig (1987) have argued that the feeding of nestlings by nonparental birds may simply be an unselected consequence of delayed dispersal in cooperatively breeding birds in which philopatric individuals are responding to the stimulus of begging young in their vicinity (see also Jamieson 1986, 1989). Jamieson & Craig (1990) recently criticized my attempt to examine what they describe as this “unselected” hypothesis of Williams (1966) and several selectionist (or adaptive) hypotheses for the current utility of helping behaviour in the bell miner (Manorina melanophrys) (Clarke 1989). In this paper I address specific issues raised by Jamieson & Craig (1990), especially whether the unselected hypothesis is an adequate explanation of the pattern of helping in the bell miner. I will also attempt to highlight the difficulty of formulating specific predictions from the unselected hypothesis and the apparent ease with which it can be modified to accommodate departures from its general predictions.     

Cognitive ornithology: the evolution of avian intelligence

Comparative psychologists interested in the evolution of intelligence have focused their attention on social primates, whereas birds tend to be used as models of associative learning. However, corvids and parrots, which have forebrains relatively the same size as apes, live in complex social groups and have a long developmental period before becoming independent, have demonstrated ape-like intelligence. Although, ornithologists have documented thousands of hours observing birds in their natural habitat, they have focused their attention on avian behaviour and ecology, rather than intelligence. This review discusses recent studies of avian cognition contrasting two different approaches; the anthropocentric approach and the adaptive specialization approach. It is argued that the most productive method is to combine the two approaches. This is discussed with respects to recent investigations of two supposedly unique aspects of human cognition; episodic memory and theory of mind. In reviewing the evidence for avian intelligence, corvids and parrots appear to be cognitively superior to other birds and in many cases even apes. This suggests that complex cognition has evolved in species with very different brains through a process of convergent evolution rather than shared ancestry, although the notion that birds and mammals may share common neural connectivity patterns is discussed.     

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)     

Why offspring delay dispersal: experimental evidence for a role of parental tolerance

Approximately 3% of all bird species live in families based on a prolonged parent-offspring association. Formation of family groups often appears to be associated with various constraints on the possibilities of independent reproduction for the offspring. However, delayed dispersal is not the only alternative for offspring that defer reproduction. To account for the formation of a family group it is also necessary to explain why non-dispersing offspring forego the alternative options to join other groups as 'extra birds' or to become 'floaters' and roam between territories. We removed fathers from Siberian jay Perisoreus infaustus family groups to test the proposal that nepotistic parental tolerance gives the natal territory a special value for the offspring, which they cannot find elsewhere and that makes them stay. In this species, parents are more tolerant of their retained offspring than towards immigrant extra birds. In response to the removal of fathers, retained offspring dispersed, whereas there was no similar response among the unrelated extra birds. Retained offspring, however, left only after despotic immigrant alpha-males replaced removed fathers, indicating that the presence of fathers is an essential motive for offspring to delay their dispersal. By blocking immigrant and unrelated males from becoming alpha-males and by being tolerant themselves, fathers provide a 'safe haven' in the natal territory where retained offspring can avail themselves of available resources without any, or only mild, competitive interference.     

Age‐related reproductive success in dichromatic male Black Redstarts Phoenicurus ochruros: Why are yearlings handicapped?

Reproductive constraints on sexually mature, young birds may be the underlying cause for the evolution and maintenance of delayed plumage maturation in passerine birds. I examined whether yearling male Black Redstarts in non-definitive plumage are reproductively handicapped and explored possible reasons for it. Yearlings raised only half as many young per season as adults. Differential reproductive effort was excluded as a possible source for age-related reproductive success because yearlings and adults did not differ in the frequency of non-breeding or in paternal effort. The lower annual reproductive success of yearlings was attributed to their lower probability of obtaining (multiple) females and adult females. Males mated to adult females raised almost twice as many offspring as males mated to yearling females. I conclude that the proposed preconditions for the evolution and maintenance of delayed plumage maturation do still prevail in the Black Redstart.     

Corvids avoid odd evaluation by following simple rules in a risky exchange task

In their natural environment, animals often make decisions crucial for survival, such as choosing the best patch or food, or the best partner to cooperate. The choice can be compared to a gamble with an outcome that is predictable but not certain, such as rolling a dice. In economics, such a situation is called a risky context. Several models show that although individuals can generally evaluate the odds of each potential outcome, they can be subject to errors of judgment or choose according to decision-making heuristics (simple decision rules). In non-human primates, similar errors of judgment have been reported and we have recently shown that they also use a decisional heuristics when confronted with a risky choice in an exchange task. This suggests a common evolutionary origin to the mechanisms underlying decision-making under risk in primates. However, whether the same mechanisms are also present in more distantly related taxa needs to be further investigated. Other social species, like corvids, are renowned for their advanced cognitive skills and may show similar responses. Here, we analyse data on corvids (carrion crows, hooded crows, common ravens and rooks) tested in a risky exchange task comparable to the one used in non-human primates. We investigated whether corvids could exchange according to the odds of success or, alternatively, whether they used a heuristic similar to the one used by non-human primates. Instead, most corvids chose a course of action (either a low or high exchange rate) that remained constant throughout the study. In general, corvids’ mean exchange rates were lower compared to non-human primates, indicating that they were either risk-adverse or that they do not possess the cognitive capabilities to evaluate odds. Further studies are required to evaluate the flexibility in exchange abilities of these birds in exchange abilities of these birds.     

Intelligence in Corvids and Apes: A Case of Convergent Evolution?

Intelligence is suggested to have evolved in primates in response to complexities in the environment faced by their ancestors. Corvids, a large-brained group of birds, have been suggested to have undergone a convergent evolution of intelligence [ Emery & Clayton (2004) Science , Vol. 306, pp. 1903–1907 ]. Here we review evidence for the proposal from both ultimate and proximate perspectives. While we show that many of the proposed hypotheses for the evolutionary origin of great ape intelligence also apply to corvids, further study is needed to reveal the selective pressures that resulted in the evolution of intelligent behaviour in both corvids and apes. For comparative proximate analyses we emphasize the need to be explicit about the level of analysis to reveal the type of convergence that has taken place. Although there is evidence that corvids and apes solve social and physical problems with similar speed and flexibility, there is a great deal more to be learned about the representations and algorithms underpinning these computations in both groups. We discuss recent comparative work that has addressed proximate questions at this level, and suggest directions for future research.     

Infant care in a family of siamangs (Hylobates syndactylus) with twin offspring at Berlin Zoo

Infant-carrying in a family group of siamangs with twin offspring was observed during a 2-week period. The twins were about 11 months old at the time of the study. One or both twins were usually carried by their father, but hardly ever by their mother. A considerable amount of infant-carrying was also contributed by the twins' juvenile brother. Helping behavior (defined as the care of offspring by individuals who are not their parents) is not normally known to occur in siamangs or other hylobatids. We suggest that the presence of multiple offspring may have facilitated the occurrence of infant-carrying exhibited by a nonparental family member. This finding may point to one of the mechanisms influencing the occurrence of helping behavior in general.     

Adoption in African wild dogs, Lycaon pictus

Parental care of unrelated young is occasionally misdirected and maladaptive from an individual fitness perspective (e.g. interspecific brood parasitism). Alternatively, adults may'adopt'dependent young and gain direct benefits irrespective of the degree of relatedness. For social species whose fitness is partially a function of group size, direct benefits of increasing group size may provide a mechanism favouring adoption independently of the inclusive fitness consequences. African wild dogs. Lycaon pictus , are social carnivores for which group size has been positively crrelated with reproductive success and competitive ability. Co-operative breeding by wild dogs has been described previously as strongly kin-selected and helpers were assumed to be invariably closely related to offspring. However, observations from this study show that the assumption that helpers are related to those they help is not always valid. A minimum of 25% of study area packs ( n =12) contained nonbreeding adults that provided parental care for unrelated pups. Costs of adopting unrelated weaned wild dog pups are slight or nonexistent except for delayed costs due to later potential conflict with mature same-sex adoptees over access to mates. Immediate and delayed direct benefits identified here are associated with increasing group size and may indicate important mechanisms underlyig adoption and the evolution of helping behaviour in wild dogs.