Susan C. Alberts

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.

True paternal care in a multi-male primate society

Although male parental care is rare among mammals, adult males of many cercopithecine primate species provide care for infants and juveniles. This care is often in the form of grooming, carrying, support in agonistic interactions, and protection against infanticide. For these behaviours to be interpreted as true parental care, males must selectively direct care towards their own offspring and this care must result in fitness benefits. With the exception of males defending probable offspring from infanticide, male primates living in multi-male, multi-female social groups have not been shown to selectively direct care towards their own offspring. We determined paternity for 75 juveniles in a population of wild savannah baboons (Papio cynocephalus) and collected data on interventions in agonistic disputes by adult males on behalf of juveniles as a form of male care. Here we show that adult males differentiate their offspring from unrelated juveniles and selectively support their offspring in agonistic disputes. As support in agonistic disputes is likely to contribute to rank acquisition and protect juveniles from injury and stress, this can be considered true parental care.

Balancing Costs and Opportunities: Dispersal in Male Baboons

Young male baboons typically disperse from their group of birth as they near adult size and may continue to migrate between social groups throughout their lives. Long-term data on dispersal and residence patterns of male baboons in Amboseli National Park, Kenya, were available for 110 males in the population, including 43 that were monitored during their natal dispersal. These data enabled us to provide not only a detailed evaluation of the effects of reproductive competition on dispersal but also the first direct estimates of the costs of dispersal in male primates and one of the few direct estimates of fitness costs associated with breeding in the natal group. Males underwent natal dispersal at a median age of 8.5 yr (range, 6.8-13.4 yr) and subsequently remained in nonnatal groups for a median tenure of 24 mo (range, 1-138 mo). Half of the males in the study engaged in moderate to extensive reproductive activity before natal dispersal. Reproductive costs associated with breeding in the natal group were suggested by the high mortality of offspring for whom natal males were their likely fathers, even though maternal relatives avoided mating with each other. Dispersal involved considerable time spent alone, and therefore the costs of dispersal were substantial, because of mortality risks and missed reproductive opportunities during dispersal. Female availability and male mating success apparently affected both natal and secondary dispersal patterns. We present a model of dispersal tendency in order to explicate the ways in which differences in population density, predation risk, and the distribution of mating opportunities among groups might result in complex dispersal patterns that are consistent with both the results of the present study and the disparate empirical reports in the literature.

Queuing and queue-jumping: long-term patterns of reproductive skew in male savannah baboons, Papio cynocephalus

In many animals, variance in male mating success is strongly correlated with male dominance rank or some other measure of fighting ability. Studies in primates, however, have varied greatly in whether they detect a relationship between male dominance rank and mating success. This variability has led to debate about the nature of the relation between rank and mating success in male primates. We contribute to the resolution of this debate by presenting an analysis of the relationship between dominance rank and male mating success over 32 group-years in a population of wild savannah baboons. When data were pooled over the entire period, higher-ranking males had greater access to fertile females. However, when we examined successive 6-month blocks, we found variance in the extent to which rank predicted mating success. In some periods, the dominance hierarchy functioned as a queue in which males waited for mating opportunities, so that rank predicted mating success. In other periods, the queuing system broke down, and rank failed to predict mating success when many adult males were in the group, when males in the group differed greatly in age, and when the highest-ranking male maintained his rank for only short periods. The variance within this single population is similar to the variance observed between populations of baboons and between species of primates. Our long-term results provide strong support for the proposition that this variance is not an artefact of methodological differences between short-term studies, but is due to true variance in the extent to which high-ranking males are able to monopolize access to females.  2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.

The ties that bind: genetic relatedness predicts the fission and fusion of social groups in wild African elephants

Many social animals live in stable groups. In contrast, African savannah elephants (Loxodonta africana) live in unusually fluid, fission–fusion societies. That is, ‘core’ social groups are composed of predictable sets of individuals; however, over the course of hours or days, these groups may temporarily divide and reunite, or they may fuse with other social groups to form much larger social units. Here, we test the hypothesis that genetic relatedness predicts patterns of group fission and fusion among wild, female African elephants. Our study of a single Kenyan population spans 236 individuals in 45 core social groups, genotyped at 11 microsatellite and one mitochondrial DNA (mtDNA) locus. We found that genetic relatedness predicted group fission; adult females remained with their first order maternal relatives when core groups fissioned temporarily. Relatedness also predicted temporary fusion between social groups; core groups were more likely to fuse with each other when the oldest females in each group were genetic relatives. Groups that shared mtDNA haplotypes were also significantly more likely to fuse than groups that did not share mtDNA. Our results suggest that associations between core social groups persist for decades after the original maternal kin have died. We discuss these results in the context of kin selection and its possible role in the evolution of elephant sociality.

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.

Life at the top: rank and stress in wild male baboons

Alpha males have higher stress levels than beta males in a wild baboon society. In social hierarchies, dominant individuals experience reproductive and health benefits, but the costs of social dominance remain a topic of debate. Prevailing hypotheses predict that higher-ranking males experience higher testosterone and glucocorticoid (stress hormone) levels than lower-ranking males when hierarchies are unstable but not otherwise. In this long-term study of rank-related stress in a natural population of savannah baboons (Papio cynocephalus), high-ranking males had higher testosterone and lower glucocorticoid levels than other males, regardless of hierarchy stability. The singular exception was for the highest-ranking (alpha) males, who exhibited both high testosterone and high glucocorticoid levels. In particular, alpha males exhibited much higher stress hormone levels than second-ranking (beta) males, suggesting that being at the very top may be more costly than previously thought.

Growth rates in a wild primate population: ecological influences and maternal effects

Growth rate is a life-history trait often linked to various fitness components, including survival, age of first reproduction, and fecundity. Here we present an analysis of growth-rate variability in a wild population of savannah baboons (Papio cynocephalus). We found that relative juvenile size was a stable individual trait during the juvenile period: individuals generally remained consistently large-for-age or small-for-age throughout development. Resource availability, which varied greatly in the study population (between completely wild-foraging and partially food-enhanced social groups), had major effects on growth. Sexual maturity was accelerated for animals in the food-enhanced foraging condition, and the extent and ontogeny of sexual dimorphism differed with resource availability. Maternal characteristics also had significant effects on growth. Under both foraging conditions, females of high dominance rank and multiparous females had relatively large-for-age juveniles. Large relative juvenile size predicted earlier age of sexual maturation for both males and females in the wild-feeding condition. This confirmed that maternal effects were pervasive and contributed to differences among individuals in fitness components.

Sexual selection in wild baboons: from mating opportunities to paternity success

In mammals, high dominance rank among males is often associated with mating success. However, mating opportunities do not automatically translate into offspring production; observed mating success may be discordant with offspring production, for three reasons. (1) Observed mating may be nonrepresentative of actual mating if some mating is surreptitious (decreasing the chance that it will be observed), (2) mating may be nonrandom if some males allocate more mating effort to females with high fertility (i.e. if some males differentially invest in higher fertility mating) and (3) conception success may be nonrandom if sperm competition or sperm selection play a role in conception. We performed a genetic analysis of paternity in the well-studied savannah baboon, Papio cynocephalus, population in the Amboseli basin, eastern Africa, in order to measure the concordance between observed mating success and actual offspring production. We found that observed mating success was generally a good predictor of paternity success, that high-ranking males had higher paternity success than lower-ranking males, and that male density and male rank stability contributed to variance in male paternity success. We found little evidence for successful surreptitious mating (although subadult males did occasionally produce offspring, apparently using this strategy), and no clear evidence for differential sperm success or sperm depletion (although we could not rule them out). However, we found clear evidence that high-ranking males showed mate choice, concentrating their mating efforts on females experiencing conceptive rather than nonconceptive cycles.

Mate guarding constrains foraging activity of male baboons

For many species, mate guarding results in dramatic departures from normal behaviour that reflect compromised attention to feeding and other activities. Such departures have previously been diYcult to document in primates, however. Data were gathered on two aspects of male behaviour that were predicted to be constrained during consortships, individual travel distance and duration of feeding bouts, for wild male baboons, Papio cynocephalus, in and out of mate-guarding episodes. In each case, consorting males were compared with themselves outside of consortships, and, in the case of distance travelled, they were compared also with non-consorting males matched for sample time and location. Males travelled significantly shorter distances while consorting than while not consorting, with the result that consorting males travelled distances similar to those travelled by females. Males also had significantly shorter feeding bouts while consorting. The shorter travel distances and feeding bouts experienced by consorting males may represent important constraints on male foraging activity, and probably result in decreased energy intake during mate guarding. Seasonal and non-seasonal breeding patterns will have diVerent consequences for the magnitude of fluctuations in energy stores and depletions experienced during mate guarding, and costs of mate guarding in species that breed non-seasonally will be more diYcult to document because they are necessarily smaller and temporally dispersed. When considered across the lifespan, however, mate guarding costs to non-seasonal breeders may equal or exceed costs to seasonal breeders. ? 1996 The Association for the Study of Animal Behaviour