O brother,where art thou? The varying influence of older siblings in rank acquisition by female baboons

Males in sexually dimorphic species like baboons appear to have surprisingly little influence on the reproduction and dominance ranks of their female kin, even though they could potentially increase their fitness by helping their relatives improve their ranks. Male baboons are able to dominate females several years before they emigrate, but their presence has no effect on relatives’ dominance ranks, at least when female kin are present. As a result, females usually acquire ranks within their matriline, above their older sisters. We describe the process of rank acquisition among orphaned and non-orphaned juvenile and adolescent females in a group of free-ranging baboons. Orphaned females were significantly more likely than non-orphaned females to acquire unexpected ranks. Orphaned females with older sisters often acquired ranks within the matriline, but below their older sisters’. Orphaned females with older brothers were likely to rise in rank above their matriline. Females’ interventions on behalf of younger sisters always supported the existing female dominance hierarchy, while males’ interventions tended to act against it. Similarly, in playback experiments, females appeared to be willing to support their younger sister only in disputes with lower-ranking females. In contrast, males appeared to be willing to support their sister even in disputes with higher-ranking females. Fraternal support enables females to improve their dominance ranks, but only if their mothers have died. It remains a puzzle why males have so little influence on their female relatives’ ranks when female kin are present, and so much when they are absent.     

Friendships between males and lactating females in a free-ranging group of olive baboons (Papio hamadryas anubis): evidence from playback experiments

Close association between an anoestrous female at the time of lactation and adult male(s) is relatively rare in mammals, but common in baboons (Papio hamadryas subsp.). The functional significance of these “friendships” remains unclear, however. In chacma baboons (P. h. griseipes), friendships are a counter-strategy to infanticide by immigrant males. Experimental playback of female distress calls in chacma baboons revealed that male friends are more motivated to protect females and infants than are control males. Olive baboons (P. h. anubis) also exhibit friendships, but infanticide is rare, suggesting that friendships provide females with protection from non-lethal aggression (anti-harassment hypothesis) or serve to promote male–infant bonds that later benefit the maturing juvenile (future male caretaker hypothesis). We replicated these playback experiments on a group of olive baboons to test between these hypotheses and to evaluate if the lower costs of non-lethal harassment lessens male protective responsiveness relative to protection from (more costly) infanticide. Spatial data revealed that most lactating females had one to four friend males. Relative to non-friends, friend dyads were characterized by higher rates of allogrooming and infant handling, but less agonism. Female rank was correlated with the number of male friends. Just as in chacma baboons, playback of female screams elicited stronger responses from male friends than control males in support the anti-harassment hypothesis. Compared to the chacma baboon, male olive baboons appeared to exhibit similarly high levels of protective solicitude for female friends although they protect against non-lethal harassment rather than infanticide.     

Social relationships among adult female baboons (papio cynocephalus) I. Variation in the strength of social bonds

Sociality has positive effects on female fitness in many mammalian species. Among female baboons, those who are most socially integrated reproduce most successfully. Here we test a number of predictions derived from kin selection theory about the strength of social bonds among adult female baboons. Our analyses are based on systematic observations of grooming and association patterns among 118 females living in seven different social groups in the Amboseli Basin of Kenya over a 16-year period. Females in these groups formed the strongest bonds with close kin, including their mothers, daughters, and maternal and paternal sisters. Females were also strongly attracted toward females who were close to their own age, perhaps because peers were often paternal sisters. Females’ bonds with their maternal sisters were strengthened after their mother’s deaths, whereas their relationships with their maternal aunts were weakened after their mother’s death. In addition, females formed stronger bonds with their paternal sisters when no close maternal kin were available, and they compensated for the absence of any close kin by forming strong bonds with nonrelatives. Taken together, these data suggest that social bonds play a vital role in females’ lives, and the ability to establish and maintain strong social bonds may have important fitness consequences for females.Joan B. Silk is on sabbatical at Cambridge University from September 2005 to August 2006. Tel.: +44-7929759697; Fax: +44-1223-335460.     

Females alter their song when challenged in a sex-role reversed bird species

Birdsong serves to attract mates and to deter territorial rivals. Even though song is not restricted to males, this dual function has almost exclusively been demonstrated for male song. To test the generality of hypotheses on birdsong, we investigated female song in the sex-role reversed, classically polyandrous African black coucal (Centropus grillii) in the context of female–female competition. We compared spontaneously vocalizing females with females vocally responding to a playback simulating a conspecific intruder. Females changed vocal parameters in response to playbacks: They lowered the pitch of their vocalizations and enhanced the duration of song elements when being challenged. Also, the composition of the vocalizations was altered. There was no significant correlation between pitch and body size parameters in spontaneous song, but there was for response songs, with larger females having a lower pitch. These changes in vocal properties suggest that the vocalizations are important for mutual assessment of competitive abilities in females. Our findings confirm the general role of intrasexual competition in vocal communication of birds.     

Divided destinies: group choice by female savannah baboons during social group fission

Group living provides benefits to individuals while imposing costs on them. In species that live in permanent social groups, group division provides the only opportunity for nondispersing individuals to change their group membership and improve their benefit to cost ratio. We examined group choice by 81 adult female savannah baboons (Papio cynocephalus) during four fission events. We measured how each female’s group choice was affected by several factors: the presence of her maternal kin, paternal kin, age peers, and close social partners, her average kinship to groupmates, and her potential for improved dominance rank. Maternal kin, paternal kin, and close social partners influenced group choice by some females, but the relative importance of these factors varied across fissions. Age peers other than paternal kin had no effect on group choice, and average kinship to all groupmates had the same effect on group choice as did maternal kin alone. Most females were subordinate to fewer females after fissions than before, but status improvement did not drive female group choice; females often preferred to remain with social superiors who were their close maternal kin, rather than improving their own social ranks. We suggest that during permanent group fissions, female baboons prefer to remain with close maternal kin if those are abundant enough to influence their fitness; if they have too few close maternal kin then females prefer to remain with close paternal kin, and social bonds with nonkin might also become influential. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Paternal kin bias in the agonistic interventions of adult female rhesus macaques (Macaca mulatta)

When agonistic interventions are nepotistic, individuals are expected to side more often with kin but less often against kin in comparison with non-kin. As yet, however, few mammal studies have been in a position to test the validity of this assertion with respect to paternal relatedness. We therefore used molecular genetic kinship testing to assess whether adult female rhesus macaques (Macaca mulatta) from the free-ranging colony of Cayo Santiago (Puerto Rico) bias their interventions in ongoing dyadic aggressive interactions towards maternal and paternal half-sisters compared with unrelated females. It turned out that females supported maternal half-sisters significantly more often than paternal half-sisters or non-kin regardless of the costs associated with such interventions. Similarly, females targeted maternal half-sisters significantly less often than non-kin when this was associated with high costs. Unrelated females provided significantly higher mean rates of both high- and low-cost support to each other than did paternal half-sisters. However, females targeted paternal half-sisters significantly less often than non-kin when targeting was at low cost, suggesting that females refrain from intervening against paternal half-sisters. Our data confirm the general view that coalition formation in female mammals is a function of both the level of maternal relatedness and of the costs of intervention. The patterns of coalition formation among paternal kin were found to be more complex, and may also differ across species, but clear evidence for paternal kin discrimination was observed in female rhesus as predicted by kin selection theory.     

Vocal interactions in common nightingales (<Emphasis Type="Italic">Luscinia megarhynchos</Emphasis>): males take it easy after pairing

Seasonal patterns of bird song have been studied intensively with a focus on individual males. However, little is known about seasonal patterns of singing during vocal interactions between males. Vocal interactions have been shown to be important in sexual selection as males may signal aspects of motivation or quality. Here, we investigated in nightingales (Luscinia megarhynchos) whether a male’s behaviour in vocal interactions at different stages of the breeding season is influenced by its mating status. We examined how males that differ in their subsequent mating success respond to a non-interactive, nocturnal playback presented during the period of mate attraction and subsequently during the egg-laying period. We found that mated males overlapped fewer songs and had a lower song rate during the egg-laying period compared to their responses during the mate-attraction period, whereas unpaired males did not vary in their responses between the two periods. Our results suggest that mating status is a key factor affecting singing behaviour in vocal interactions and that a time-specific singing pattern like song overlapping is used flexibly during vocal interactions. Because song overlapping is thought to be a signal of aggression in male–male vocal interactions, it seems that males vary the level of aggression in vocal interactions according to their mating status and to the stage in the breeding season.     

Female aggressive response and hormonal correlates—an intrusion experiment in a free-living passerine

The optimal mating system is rarely the same for males and females—whereas males usually benefit from attracting additional females to the territory, this could incur costs for the resident female. Females should therefore prevent prospecting females from settling on the territory. We studied the male and female behavioral and hormonal responses to simulated female territorial intrusions in free-living bluethroats during the pre-laying period. In the study population, polygyny occurs with potential fitness costs for the resident female. We recorded different aspects of aggressive behavior before and after presentation of a live female decoy and playback of female song. These behaviors were compared with a set of intrusions using a male decoy. At the end of a trial, the birds were captured, and blood samples were analyzed for androstenedione, testosterone, estradiol and corticosterone. During the pre-intrusion period, none of the females were observed. Females generally responded strongly to the female decoy by increased flight rate, vocalizations, and by conspicuous perching. Nearly half of the males displayed to the female decoy but never while the resident female was present. We suggest that resident female aggression in bluethroats prevents courtship by her mate and signals her mating status to the female intruder. Female aggression could therefore prevent additional females to settle on the territory and shape the mating system. Females that responded with song had higher levels of estradiol. These findings suggest that estradiol may support aggression in breeding female birds.     

More than friends? Behavioural and genetic aspects of heterosexual associations in wild chacma baboons

In mammals, fathers are facultative caretakers, and male care is expected to evolve only if it is directed towards related young. Yet, in several promiscuous primate societies, males seem to care for infants despite a presumably low paternity confidence. In cercopithecines, cohesive associations (‘friendships’) between a lactating female and an adult male are frequent and provide the female and her infant with protection against various sources of aggression, including infanticide. However, the benefits gained by males through such relationships remain unclear, in part, because the relatedness between males and their protected infants has rarely been examined. Moreover, little is known about the nature of the cues underlying kin discrimination by males in societies where females mate polyandrously. In this study, we combine behavioural and genetic data from wild chacma baboons (Papio ursinus) in Namibia to investigate (1) whether males are related to their friend’s infant and (2) whether similarity between the major histocompatibility complex (MHC) genotype of males and infants (potentially perceived through odour phenotype) favours the establishment of friendships. We first show that males share close genetic ties with their friend’s infants, most often by having sired the infant. Secondly, we find that male–infant MHC (Class II–DRB) similarity, in contrast to paternity, does not predict male–infant associations. Overall, our results clarify the nature of the evolutionary benefits gained by males in these heterosexual associations, which can be considered as true paternal care. However, the proximate mechanisms underlying paternity recognition remain to be identified.     

Female chacma baboons form strong, equitable, and enduring social bonds

Analyses of the pattern of associations, social interactions, coalitions, and aggression among chacma baboons (Papio hamadryas ursinus) in the Okavango Delta of Botswana over a 16-year period indicate that adult females form close, equitable, supportive, and enduring social relationships. They show strong and stable preferences for close kin, particularly their own mothers and daughters. Females also form strong attachments to unrelated females who are close to their own age and who are likely to be paternal half-sisters. Although absolute rates of aggression among kin are as high as rates of aggression among nonkin, females are more tolerant of close relatives than they are of others with whom they have comparable amounts of contact. These findings complement previous work which indicates that the strength of social bonds enhances the fitness of females in this population and support findings about the structure and function of social bonds in other primate groups.     

Temporal overlap of female kin in Columbian ground squirrels (Spermophilus columbianus)

Summary Columbian ground squirrels (Spermophilus columbianus) were live-trapped from 5 to 7 years at three sites in southwestern Alberta, Canada. The two most common adult matrilineal relatives for 2-year-old females were the mother and a 1 year older non-littermate sister. Co-occurrence of female kin depended firstly on size and sexual composition of litters and secondly on age-specific survival and recruitment rates. Adult matrilineal kin frequently coexisted among breeding females of this species, leading us to predict a social system strorgly influenced by nepotism. However, the life history traits of S. columbianus suggest an adult female kin cluster unlike that found for other species of Spermophilus in which littermate sisters are common. If availability of adult female kin influences kin-differential behaviour, then female S. columbianus should favour mothers, daughters and non-ittermate sisters.     

Exogenous testosterone increases female aggression in the European starling (<Emphasis Type="Italic">Sturnus vulgaris</Emphasis>)

In the European starling, Sturnus vulgaris, optimal mating systems differ between males and females. Males gain from polygyny, whereas monogamy increases female fitness. The cost of polygyny to females lead to intense female–female competition, and it has previously been shown that the intensity of female aggression during the pre-breeding period can predict the realised mating system. The physiological regulation of such female aggression in starlings is not yet known. This study examines the role of testosterone in mediating aggressive behaviours involved in intra-specific reproductive competition in female starlings. Testosterone levels were experimentally elevated with testosterone implants in females during the pre-laying period. To simulate a situation in which an additional female tried to mate with the focal female’s mate, a caged female was presented close to a nest-site to which the male could attract a secondary female. Testosterone was significantly related to several behaviours involved in female–female interactions. Females with testosterone implants spent significantly more time close to the caged female and produced more song bouts than control females. In contrast, male behaviour was unrelated to the experimental status of the mate. Females mated to males that attracted a secondary female were less aggressive towards the caged female than those that remained monogamously mated. The effect of exogenous testosterone in this study indicates that androgens may mediate social behaviours in female starlings during the breeding season.     

Field playback of male display attracts females in lek breeding sage grouse

Summary Recent correlational studies of lekking sage grouse suggest that male vocal display attracts females. To test this hypothesis further, the natural displays of a territorial male were supplemented with the tape-recorded display of another, reproductively-successful, individual. Significantly, more females approached the speaker's location on days when the recording was played, and also on non-playback days immediately following a playback, than on other non-playback days (Fig. 1). Analysis of male displays indicated that females were responding to the playback itself rather than to changes in male behavior. The after-response following a playback suggests that some females present during a playback remembered its location and approached on a subsequent lek visit. The results provide necessary support for the epigamic function of vocal display, and suggest ways in which female responses to male display may influence lek structure.     

Shoaling decisions in three-spined sticklebacks (<Emphasis Type="Italic">Gasterosteus aculeatus</Emphasis>)—familiarity,kinship and inbreeding

Shoaling with familiar kin is a well-known phenomenon. It has been described both for adult and for fry of three-spined sticklebacks (Gasterosteus aculeatus). However, evidence of preference for kin independent of familiarity is scarce. Furthermore, inbreeding effects have not been studied for shoaling preferences and there is a lack of studies about changes in individuals’ ability to recognise kin during different phases of life history. We gave inbred and outbred, nonreproductive sticklebacks of different age the choice to shoal with a group of familiar siblings vs unfamiliar non-siblings and with unfamiliar siblings vs unfamiliar non-siblings. Subadult sticklebacks preferred to shoal with familiar kin over unfamiliar non-kin, but inbred and outbred individuals had similar preferences. When given the choice between unfamiliar siblings and unfamiliar non-sibs, adult outbred fish preferred the shoal of kin, while inbred fish behaved indifferently. Body characteristics of the group such as body mass, standard length and condition of its members did not significantly explain the shoaling preferences for kin. Thus, sticklebacks were capable of recognising familiar and unfamiliar kin. The latter capability was lost by inbreeding.     

Kin and non-kin interventions in the aggressive disputes of vervet monkeys

Summary Interventions in aggressive disputes were investigated in a free-living troop of vervets (Cercopithecus aethiops sabaeus) in Barbados. Interventions on behalf of kin were more frequent than on behalf of non-kin. Both types of interventions were more likely when the intervening animal outranked the opponent; presumably because retaliation probability, and hence cost of intervening, is low against low ranking opponents. The number of interventions given on behalf of both kin and non-kin increased with the number of disputes in which they were involved. In contrast to kin interventions, the number of interventions given on behalf of non-kin was correlated with that received by non-kin, suggesting that reciprocation is a necessary component of non-kin interventions. Non-kin interventions were more likely when the recipient outranked the opponent, presumably because reciprocation probability is high. Pairs of non-kin form structured reciprocal relationships based on the proportion of interventions allocated to each other, and most non-kin interventions flowed through these relationships. Males intervened on behalf of non-kin more frequently than did females. The implications of the results for the evolution of kin and reciprocal altruism were discussed.     

Seasonal variation in the duetting behaviour of rufous-and-white wrens (<Emphasis Type="Italic">Thryothorus rufalbus</Emphasis>)

Seasonal variation in animal signalling behaviour has been well documented and has contributed much to our understanding of male signals. In contrast, we know little about seasonal variation in female signals or signals produced jointly by males and females, such as the vocal duets of birds. Here, we examine how singing behaviour changes in relation to time of year and breeding stage in rufous-and-white wrens (Thryothorus rufalbus), neotropical songbirds where both males and females sing and where breeding partners coordinate songs to produce vocal duets. We recorded a colour-marked population of birds over an extended time period encompassing multiple breeding stages. Across all time frames and breeding stages, males sang at higher rates than females and male solos were more common than duets or female solos. Males and females showed divergent seasonal patterns of singing. Females sang more often early in the year, during the pre-breeding season, and female song tapered off as the breeding season progressed. Duetting followed a parallel pattern, which resulted from females showing less duet responsiveness to their partner’s songs later in the year. Male independent song rate peaked at the onset of the rainy season – a time when females become fertile – and males showed the highest level of duet responsiveness during this period. Our results suggest that early in the year, duets appear to be cooperative displays, functioning in joint territory defence and/or the coordination of breeding activities. When females are fertile, however, increased duet responsiveness by males is consistent with mate or paternity guarding.     

Paternity alone does not predict long-term investment in juveniles by male baboons

Adult male chacma baboons (Papio hamadryas ursinus) form preferential associations, or friendships, with particular lactating females. Males exhibit high levels of affiliative contact with their friends’ infants and defend them from potentially infanticidal attacks (Palombit et al. 1997). Little is known about males’ associations with juveniles once they have passed the period of infanticidal risk. We conducted an observational, experimental, and genetic study of adult male and juvenile chacma baboons in the Moremi Reserve, Botswana. We identified preferential associations between males and juveniles and used behavioral data and a playback experiment to explore whether those associations have potential fitness benefits for juveniles. We determined whether males preferentially invest in care of their own offspring. We also determined how often males invest in care of their former friends’ offspring. The majority of juveniles exhibited preferential associations with one or two males, who had almost always been their mother’s friend during infancy. However, in only a subset of these relationships was the male the actual father, in part because many fathers died or disappeared before their offspring were weaned. Male caretakers intervened on behalf of their juvenile associates in social conflicts more often than they intervened on behalf of unconnected juveniles, and they did not appear to differentiate between genetic offspring and unrelated associates. Playbacks of juveniles’ distress calls elicited a stronger response from their caretakers than from control males. Chacma males may provide care to unrelated offspring of former friends because the costs associated with such care are low compared with the potentially high fitness costs of refusing aid to a juvenile who is a possible offspring.     

Infant handling and mortality in yellow baboons (<Emphasis Type="Italic">Papio cynocephalus</Emphasis>): evidence for female reproductive competition?

This study examines negative and positive infant handling behavior in 24 free-ranging yellow baboon infants (Papio cynocephalus) studied over a 5-year period in Mikumi National Park, Tanzania. We test predictions of the female reproductive competition hypothesis to explain patterns of infant handling behavior by adult females (excluding the infants mother) in relation to observed cases of infant mortality by age 3 months (25% of infants in this study). Results show that: (1) low-ranking infants received more negative infant handling than high-ranking infants; conversely high-ranking infants received more positive infant handling; (2) female kin engaged in higher levels of positive infant handling than did non-kin, whereas non-kin showed higher levels of negative infant handling; (3) rates of negative infant handling varied by season, with high levels at the onset of the rainy season; and (4) high level of negative infant handling was a significant predictor of infant mortality by age 3 months (infant rank and sex did not predict survival). We discuss how the occurrence and interpretation of infant handling behavior in the literature has likely been confused by different definitions of this behavior, as well as differences in the socio-ecological context in which this behavior occurs.Communicated by C. Nunn     

Local genetic structure and relatedness in a solitary mammal, Neotoma fuscipes

We used DNA microsatellites to investigate temporal and spatial patterns of local genetic differentiation and relatedness in a solitary mammal, the dusky-footed woodrat (Neotoma fuscipes). Patterns of genetic variation were measured relative to spatial clusters, or neighborhoods, of woodrats. We detected significant genetic differentiation among woodrat neighborhoods in two populations spanning multiple habitat types and densities. Estimates of θ _ST among neighborhoods ranged 0.034–0.075 and were comparable to levels reported in social mammals. Genetic differentiation at such a local scale is noteworthy because it occurred in the absence of any physical barriers to gene flow, suggesting that the patterns observed are linked to the nonrandom patterns of mating and dispersal that characterize woodrat social structure. Genetic differentiation and relatedness among neighborhoods were even higher when only resident females were analyzed. These results are consistent with a pattern of female philopatry and male-biased dispersal in woodrats. Geographic distance and relatedness were inversely correlated in adult females at intermediate densities, but not at low densities. Nonetheless, matrilineal genetic structure was apparent even at low woodrat densities based on estimates of θ _ST among neighborhoods of resident females that were significantly greater than zero and consistently greater than estimates including all individuals. In summary, this study demonstrates a matrilineal genetic structure in dusky-footed woodrats. In addition, our results support the idea that intermediate densities may be better at facilitating the formation of spatial kin clusters than either extreme. An erratum to this article can be found at