Parent–offspring and sibling conflict in Galápagos fur seals and sea lions

Parent–offspring conflict theory is well supported by theoretical arguments. However, empirical observations are often difficult to interpret and have contradicted one of its most appealing predictions that parent and offspring should disagree over killing of nest or littermates. We present the first examples of deadly conflict between siblings of different cohorts. In Galápagos fur seals (Arctocephalus galapagoensis) and sea lions (Zalophus wollebaeki), mothers often wean their single offspring at 2 years. This leads to a situation where up to 23% of all pups are born while the older sibling is still being nursed. Younger siblings are disadvantaged by being born lighter than neonates without older still dependent siblings. Pups born while an older sib is still dependent grow less in early life (fur seal) and suffer increased early mortality (both species) through direct aggression or scramble competition with the older sibling. This effect is much stronger in years of high sea surface temperature (El Niño) indicating low marine productivity and if the older offspring is a male. In both species, mothers interfere aggressively in this conflict by defending the younger offspring. In years of El Niño, intense resistance to maternal aggression by the older offspring happens frequently in the fur seal. Such resistance against weaning can induce maternal neglect of the newborn. Given substantial year to year variation in offspring growth, maternal aggression forces weaning in the older sibling only if it has reached sufficient size to support itself by foraging. In Galápagos fur seals, pups with older siblings can either represent insurance against loss of older offspring or extra reproductive value.     

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.     

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.     

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.     

Low aggression levels and unbiased sex ratios in a prey-rich environment: no evidence of siblicide in Ngorongoro spotted hyenas (<Emphasis Type="Italic">Crocuta crocuta</Emphasis>)

Avian models of facultative siblicide predict that rates of sibling aggression and the incidence of siblicide should be lower in prey-rich than prey-poor environments, and that siblicide should only occur when fitness benefits outweigh costs. We tested these predictions by comparing data from spotted hyena (Crocuta crocuta) twin litters in the Ngorongoro Crater, Tanzania, a habitat with a high density of resident prey (176 animals/km²) with similar data from the adjacent Serengeti National Park where density of resident prey is low (3.3 animals/km²). As predicted, rates of sibling aggression in Crater twin litters were substantially lower than those among twin siblings in the Serengeti. There was no evidence of siblicide in the Crater, in contrast to the Serengeti, where facultative siblicide occurs frequently. The growth rate of Crater cubs in singleton litters was similar to that of cubs in twin litters, whereas the growth rate of Serengeti singletons was higher than that of cubs in twin litters. Thus despotic behavior by dominant Crater cubs was unlikely to provide fitness benefits, while dominant Serengeti cubs that eliminated their sibling benefited from increased growth and enhanced survival. Previous studies have demonstrated biases in the sex-composition of hyena litters due to facultative siblicide. No such biases were apparent in Crater litters. Our results provide strong evidence that levels of sibling aggression in spotted hyenas are adjusted in an adaptive manner, and that siblicide is facultative and resource dependent. Our results do not support the idea of pre-natal manipulation of offspring sex by female spotted hyenas in response to changes in resource abundance.     

Association patterns among male and female spotted hyenas (Crocuta crocuta) reflect male mate choice

Although female animals tend to be choosier than males in selecting mates, sexual selection theory predicts that males should also be choosy when female fecundity varies. Reproductive success among female spotted hyenas varies greatly with social rank. Our goals were therefore to determine whether male hyenas preferentially associate with high-ranking females, and whether male preferences are affected by female reproductive state. Interactions between adult males and females were observed intensively, and association indices calculated for all male-female pairs, over a 7-year period in one population of free-living hyenas. Males initiated most affiliative interactions with females, and males associated most closely with females that were likeliest to be fertile. High- and middle-ranking males associated most closely with high-ranking females, but low-ranking males associated equally closely with females in all rank categories. We used molecular markers to determine the paternity of cubs born during the study period, and found that sires associated more closely with the mothers of those cubs than did non-sires, particularly during the last months before conception. These association data indicate that male spotted hyenas do indeed exhibit selective mate choice, and that they prefer females likeliest to maximize male reproductive success.     

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.     

Differential aggressiveness between fire salamander (<Emphasis Type="Italic">Salamandra infraimmaculata</Emphasis>) larvae covaries with their genetic similarity

Responding differentially to kin and non-kin is known to be adaptive in many species. One example is the inclusive fitness benefits of reducing aggression toward closer relatives. Little is known, however, about the ability of animals to assess differential degrees of genetic relatedness and to respond accordingly with differential levels of aggression. In the present study, we tested whether aggressiveness between body mass-matched pairs of fire salamander (Salamandra infraimmaculata) larvae covaried with the genetic similarity between them. We quantified aggressiveness at three levels of genetic similarity by selecting pairs within and across pools from recently genotyped populations. We also assessed aggression between pairs of siblings. Aggression and associated injuries decreased as genetic similarity increased across the groups. These findings suggest that cannibalistic salamanders can assess their degree of genetic relatedness to conspecifics and vary their behavioral responses depending on the degree of similarity between them along a genetic relatedness continuum.     

Maternal response to neonatal sibling conflict in the spotted hyena, <Emphasis Type="Italic">Crocuta crocuta</Emphasis>

Among spotted hyenas, Crocuta crocuta, neonatal aggression in twins is a well-known phenomenon and serves to establish intra-litter dominance soon after birth. As the stronger more aggressive cub presumably attains dominance over its twin, intra-litter dominance presents mothers with an ideal opportunity to assess individual cub fitness and, thereafter, to selectively favor one cub over the other. This study quantified maternal response to sibling conflict in 26 sets of twins born to 16 wild-living females to determine whether mothers of different social ranks exhibited favoritism towards sons or daughters, or in the case of same-sex twins, the dominant or subordinate cub. Maternal response to sibling conflict did not vary with litter sex composition, suggesting that mothers do not favor offspring of one sex over the other. All mothers intervened when their cubs fought and sometimes punished their cubs. Higher-ranking mothers more often punished both cubs, while lower-ranking mothers were more selective and punished the dominant cub. Where sibling aggression was most extreme, rather than favor the dominant sibling, mothers of all ranks made concessions to the subordinate cub that included procuring private nursing bouts for the subordinate and temporarily housing twins in separate dens, presumably to decrease sibling conflict. These findings represent a complex example of parent–offspring conflict and support both the insurance cub hypothesis and resource tracking hypothesis that mothers endeavor to keep all offspring alive for as long as possible in the event that the dominant sibling dies or that resources provide for the rearing of twins. This contribution is part of the special issue “Sibling competition and cooperation in mammals” (guest editors: Robyn Hudson and Fritz Trillmich).     

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.     

Benefits of kin association: related and familiar zebrafish larvae (<Emphasis Type="Italic">Danio rerio</Emphasis>) show improved growth

Zebrafish (Danio rerio) larvae prefer the olfactory cues of kin to non-kin. We examined the potential benefits of kin preference by comparing growth rate, shoaling, and aggressive behavior in juvenile zebrafish housed in groups of either familiar kin or unfamiliar non-kin. Over an observation period of 5 days, the animals grew 33% more in kin groups; however, neither shoaling nor the frequency of aggressive interactions was different in groups of related versus unrelated individuals. Shoaling behavior increased with increasing observation time and increasing age, while aggressive behavior remained the same. We conclude that associating with kin probably creates a less stressful environment that allows for higher growth rates, which can lead to higher direct fitness based on increased survival and earlier reproduction. Kin recognition leading to kin-structured groups may therefore be under positive selection.     

Social relationships among adult female baboons (Papio cynocephalus) II. Variation in the quality and stability of social bonds

A growing body of evidence suggests that social bonds have adaptive value for animals that live in social groups. Although these findings suggest that natural selection may favor the ability to cultivate and sustain social bonds, we know very little about the factors that influence the quality or stability of social bonds. Here, we draw on data derived from a 16-year study of baboons living in seven different social groups in the Amboseli basin of Kenya to evaluate the quality and stability of social bonds among females. Our results extend previous analyses, which demonstrate that females form the strongest bonds with close maternal and paternal kin, age mates (who may be paternal kin), and females who occupy similar ranks but are not maternal relatives. Here we show that the same factors influence the quality and strength of social bonds. Moreover, the results demonstrate that the quality of social bonds directly affects their stability.     

Kin recognition by juvenile predatory mites: prior association or phenotype matching?

Kin recognition, the biased treatment of conspecific individuals based on genetic relatedness, is a widespread phenomenon in animals. The most common mechanisms mediating kin recognition are prior association (familiarity) and phenotype matching. Recognition based on prior association allows identifying familiar individuals. Recognition based on phenotype matching is an extension of prior-association-based recognition and allows identifying familiar and unfamiliar individuals due to a shared phenotypic trait. I investigated which of the two mechanisms is used by cannibalistic juvenile predatory mites, Phytoseiulus persimilis. Protonymphs that were associated with either siblings or non-kin discriminated familiar and unfamiliar larvae and preferentially cannibalized the latter irrespective of genetic relatedness. In contrast, despite previous association with either siblings or non-kin, protonymphs did not discriminate unfamiliar sibling and unfamiliar non-kin larvae. Association in the larval stage therefore mediated kin recognition based on familiarity, but not phenotype matching in cannibalistic P. persimilis protonymphs. Furthermore, in the presence of a familiar prey individual, sibling cannibalism occurred significantly sooner than non-kin cannibalism. This quick sibling cannibalism may have been the consequence of preferential association of siblings and/or may indicate the occurrence of an alternative cannibal phenotype. I discuss the adaptive significance of prior-association-based recognition for P. persimilis juveniles and emphasize the ability of P. persimilis to use multiple recognition mechanisms in dependence of the ontogeny and the ecological context.     

Maternal response to neonatal sibling conflict in the spotted hyena, <Emphasis Type="Italic">Crocuta crocuta</Emphasis>

Among spotted hyenas, Crocuta crocuta, neonatal aggression in twins is a well-known phenomenon and serves to establish intra-litter dominance soon after birth. As the stronger more aggressive cub presumably attains dominance over its twin, intra-litter dominance presents mothers with an ideal opportunity to assess individual cub fitness and, thereafter, to selectively favor one cub over the other. This study quantified maternal response to sibling conflict in 26 sets of twins born to 16 wild-living females to determine whether mothers of different social ranks exhibited favoritism towards sons or daughters, or in the case of same-sex twins, the dominant or subordinate cub. Maternal response to sibling conflict did not vary with litter sex composition, suggesting that mothers do not favor offspring of one sex over the other. All mothers intervened when their cubs fought and sometimes punished their cubs. Higher-ranking mothers more often punished both cubs, while lower-ranking mothers were more selective and punished the dominant cub. Where sibling aggression was most extreme, rather than favor the dominant sibling, mothers of all ranks made concessions to the subordinate cub that included procuring private nursing bouts for the subordinate and temporarily housing twins in separate dens, presumably to decrease sibling conflict. These findings represent a complex example of parent–offspring conflict and support both the insurance cub hypothesis and resource tracking hypothesis that mothers endeavor to keep all offspring alive for as long as possible in the event that the dominant sibling dies or that resources provide for the rearing of twins.     

Nursing of own and foster offspring by Utah prairie dogs (<Emphasis Type="Italic">Cynomys parvidens</Emphasis>)

From 1995 through 2005, I studied nursing among Utah prairie dogs (Cynomys parvidens) living under natural conditions at Bryce Canyon National Park, UT, USA. I observed 850 aboveground nursings, which involved 122 mothers and 248 juveniles from 134 litters. Most of the mothers that nursed aboveground were middle-aged, and most nursing juveniles had been coming aboveground for 1–3 weeks. Most nursings involved a single juvenile, lasted 1–10 min, and occurred between 1800 hours and 2000 hours. Seventy-five percent of nursings (598/796) involved a mother suckling her own juvenile offspring; the other 24.9% (198/796) involved a mother suckling another mother’s offspring (i.e., communal nursing). Communal nursings involved juveniles of the home territory, and many communal nursings (74/198 = 37.4%) involved close kin such as half-siblings, grandoffspring, full-nieces, and full-nephews; other communal nursings (37/198 = 18.7%) involved more distant kin such as full-second cousins and full-third cousins. Of seven hypotheses that might explain the evolution of communal nursing, evidence supports the importance of two: elevated inclusive fitness via indirect selection and communal nursing as a cost of coloniality.     

Sex differences in the ontogeny of social behavior in pikas: possible relationships to dispersal and territoriality

Summary A laboratory study on the ontogeny of social behavior in pikas (Ochotona princeps), an alpine lagomorph, was conducted to determine the role of early relationships between adult females and young and among siblings in the development of territorial and dispersal behaviors. Sex differences during development were examined because field studies have reported greater dispersal distances in young females than young males. At birth, females were significantly heavier than males. There were no sex differences in nursing frequency until after the 2nd week of age, when males initiated more nursing attempts than females. By the end of the weaning period (weeks 5 and 6), adult females became non-interactive with young, but aggression of young toward littermates and the mother increased until the eighth week. At this time, young males outweighed their sibling females. Young were dominant over their mothers by the age of 5 weeks, and young males were dominant over their sibling females.Sex differences were observed in aggression, scent-marking, exploratory activity, and submissive vocalizations, with higher rates in young males, except for submissive vocalizations, which were higher in females (Table 2). Vocalizations and scent-marking behavior increased over time, and were positively correlated with interaction rates.These data support the hypothesis that female young disperse farther than male young largely as the result of unsuccessful competition with male siblings for available territories close to the birthplance. A dispersal strategy for pkkas is proposed.     

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.     

Female tree swallows (<Emphasis Type="Italic">Tachycineta bicolor</Emphasis>) increase offspring heterozygosity through extrapair mating

Recent attention has focused on genetic compatibility as an adaptive function for why females engage in extrapair mating. We tested the genetic compatibility hypothesis in tree swallows (Tachycineta bicolor) over five breeding seasons using data from ten microsatellite loci. Tree swallows are socially monogamous passerines exhibiting high levels of extrapair paternity. Overall, we found that 47% of offspring were the result of extrapair fertilizations, and 83% of females produced at least one extrapair offspring. Consistently for all years, extrapair offspring were more heterozygous than their maternal half-siblings, which is in accordance with the genetic compatibility hypothesis. The difference was largely caused by the high heterozygosity of extrapair offspring sired by unknown males, suggesting that females are engaging in extrapair copulations with geographically distant males to increase the likelihood of being inseminated by a more compatible mate. Our findings support the idea that postcopulatory mechanisms are important for females when assessing potential sires for their offspring.     

Age cohorts as paternal sibships

Summary Characteristics of a populations's reproductive system affect the degree of relatedness within the age cohorts and maternal sibships of that population. Two consequences of a small litter size, particularly of size one, a relatively polygynous mating system at any one time period, and frequent replacement of reproductively active males over successive periods, are that (1) the set of offspring that each female produces (a maternal sibship) will usually consist of halfsiblings, and (2) within a social group the members of each age cohort will be closely related, either all forming one paternal sibship (half-siblings) if there is only one reproductively active male at a time, or in the case of several reproductively active males, a set of individuals whose mean relatedness is some-what ower than in the one-father case. In the present paper, degree of relatedness within each of these two subgroups is calculated on the basis of a simple model. I then examine effects of the various reproductive parameters on this relatedness and compare maternal sibships and age cohorts in the relative degree of relatedness within them. Age cohorts will often be identifiable, closely related units, paternal sibships in the extreme case. Age cohorts may be important in the evolution of family altruism. They differ from maternal sibships in interesting ways that may affect the kinds of behaviors that are likely to evolve.     

Kinship and social tolerance among female and juvenile wild house mice: kin bias but not kin discrimination

Kin-biased social tolerance among house mice has been interpreted in terms of kin discrimination. However, several lines of evidence suggest it may instead be an incidental artifact of group member discrimination. This leads to very different predictions about the social consequences of relatedness within and between social groups. Social interactions between wild-stock adult female and juvenile house mice (Mus domesticus) established in neighbouring territorial groups within enclosures reveal relatedness to dominant males within groups as the major factor determining social tolerance of juveniles by females. Relatedness to the female herself had no significant independent effect on responses indicating tolerance. Females were generally more aggressive toward neighbouring-group juveniles (all unrelated to females) compared with those from their own group (all related to females), but were most aggressive toward neighbouring juveniles sired by the neighbouring dominant male. They were also more aggressive toward their own-group juveniles that had been sired by the neighbouring dominant but only when encountered in the neighbouring territory and with a greater bias against female juveniles. Females were least aggressive toward own-group juveniles sired by their own-group dominant male. The sire-bias in tolerance among females is similar to that reported among the dominant males themselves in an earlier study. As a result of the combined sire-bias in tolerance by adult males and females, juveniles sired by their own-group dominant males become less likely to intrude into a neighbouring territory with time. Overall, the results suggest that differences in social tolerance reflect discrimination on the basis of social group membership rather than relatedness between interactants and thus provide strong experimental evidence in support of incidental kin bias rather than kin discrimination.