Anja Widdig

Paternal relatedness and age proximity regulate social relationships among adult female rhesus macaques

Kin selection promotes the evolution of social behavior that increases the survival and reproductive success of close relatives. Among primates, maternal kinship frequently coincides with a higher frequency of grooming and agonistic aiding, but the extent to which paternal kinship influences adult female social relationships has not yet been investigated. Here, we examine the effect of both maternal and paternal kinship, as well as age proximity, on affiliative interactions among semifree-ranging adult female rhesus macaques, Macaca mulatta. Kinship was assessed by using both microsatellites and DNA-fingerprinting. Our study confirms that the closest affiliative relationships characterize maternal half-sisters. We provide evidence that adult females are significantly more affiliative with paternal half-sisters than with nonkin. Furthermore, paternal kin discrimination was more pronounced among peers than among nonpeers, indicating that age proximity has an additional regulatory effect on affiliative interactions. We propose that kin discrimination among cercopithecine primates emerges from ontogenetic processes that involve phenotype matching based on shared behavioral traits, such as inherited personality profiles, rather than physiological or physical characteristics.

A longitudinal analysis of reproductive skew in male rhesus macaques

One of the basic tenets of sexual selection is that male reproductive success should be large in polygynous species. Here, we analysed 6 years of molecular genetic data from a semi–free–ranging population of rhesus macaques (Macaca mulatta), using Nonacs B index, to assess the level of male reproductive skew in the study troop. On average, the top sire in each year produced 24% of the infants, while 71% of troop males sired no offspring at all. Consequently, 74% of infants had at least one paternal half–sibling in their own birth cohort. Reproductive success was greatest for high–ranking males, males who spent the whole mating season in the troop and males of 9–11 years of age. Heterozygosity for major histocompatibility complex (MHC) class II gene DQB1 was the strongest single predictor of male reproductive success. A negative relationship suggestive of female mate choice was noted between the B index and the proportion of extra–group paternities. Reproductive skew was not associated with relatedness among potential sires or with female cycle synchrony. We conclude that reproductive skew in male rhesus macaques is best accounted for by the ‘limited–control’ model, with multiple factors interacting to regulate individual reproductive output.

Paternal kin discrimination: the evidence and likely mechanisms

One of the most important assumptions of kin selection theory is that individuals behave differently towards kin than non‐kin. In mammals, there is strong evidence that maternal kin are distinguished from non‐kin via familiarity. However, little is known about whether or not mammals can also recognize paternal kin as many female mammals, including primates, mate with multiple males near the time of conception, potentially concealing paternal kinship. Genetic data in several mammalian species with a promiscuous mating system and male‐biased dispersal reveal a high skew in male reproduction which leads to co‐residing paternal half‐siblings. In most primates, individuals also form stable bisexual groups creating opportunities for males to interact with their offspring. Here I consider close paternal kin co‐resident in the same social group, such as father‐offspring and paternal half‐siblings (i.e. animals sharing the same father but who were born to different mothers) and review mammalian studies of paternal kin discrimination. Furthermore, I summarize the most likely mechanisms of paternal kin discrimination (familiarity and phenotype matching). When familiarity is the underlying mechanism, mothers and/or the sire could mediate familiarity among paternal half‐siblings as well as between fathers and offspring assuming mothers and/or fathers can assess paternity. When animals use phenotype matching, they might use their fathers’ template (when the father is present) or self (when the father is absent) to assess paternal kinship in others. Available evidence suggests that familiarity and phenotype matching might be used for paternal kin discrimination and that both mechanisms might apply to a wide range of social mammals characterized by a high skew in male reproduction and co‐residence of paternal kin. Among primates, suggested evidence for phenotype matching can often have an alternative explanation, which emphasizes the crucial importance of controlling for familiarity as a potential confounding variable. However, the mechanism/s used to identify paternal kin might differ within a species (as a function of each individual’s specific circumstances) as well as among species (depending upon the key sensory modalities of the species considered). Finally, I discuss the possible cues used in paternal kin discrimination and offer suggestions for future studies.

Rhesus macaques (Macaca mulatta) as living fossils of hominoid personality and subjective well-being.

Personality dimensions capturing individual differences in behavior, cognition, and affect have been described in several species, including humans, chimpanzees, and orangutans. However, comparisons between species are limited by the use of different questionnaires. We asked raters to assess free-ranging rhesus macaques at two time points on personality and subjective well-being questionnaires used earlier to rate chimpanzees and orangutans. Principal-components analysis yielded domains we labeled Confidence, Friendliness, Dominance, Anxiety, Openness, and Activity. The presence of Openness in rhesus macaques suggests it is an ancestral characteristic. The absence of Conscientiousness suggests it is a derived characteristic in African apes. Higher Confidence and Friendliness, and lower Anxiety were prospectively related to subjective well-being, indicating that the connection between personality and subjective well-being in humans, chimpanzees, and orangutans is ancestral in catarrhine primates. As demonstrated here, each additional species studied adds another fold to the rich, historical story of primate personality evolution.

AFFILIATION AND AGGRESSION AMONG ADULT FEMALE RHESUS MACAQUES: A GENETIC ANALYSIS OF PATERNAL COHORTS

Kin selection promotes the evolution of social behaviour that increases the survival and reproductive success of close relatives. One prerequisite for kin selection is that individuals have the ability to discriminate between kin and nonkin. Studies incorporating data on paternal kinship are still rare, but in species with a high male reproductive skew, many adult females will be paternal half siblings. Using both microsatellites and DNA-fingerprinting, we here analyse data on paternal relatedness in order to compare the influence of maternal and paternal kinship on rates of affiliative and aggressive interactions among semi free-ranging adult female rhesus macaques (Macaca mulatta). Because paternal half siblings tend to be peers whereas maternal half siblings are almost always nonpeers, we also examine the interactions between age proximity and genetic relatedness on social behaviour. Genetic analyses show that male reproductive success is strongly skewed with 75% of infants within the troop having a paternal half sibling in the same age cohort. The highest rates of both affiliation and aggression occur among maternal half sisters. Adult females are significantly more affiliative, but not more aggressive, with paternal half sisters than with nonkin. Affiliative relationships declined in conjunction with increasing age difference among paternal half sisters, but the reverse effect was found for affiliative relationships among maternal half siblings. No association emerged among nonkin. Among both maternal and paternal kin, rates of affiliative and aggressive interactions increase as the degree of relatedness increased, thereby questioning the concept of a relatedness threshold as a mediator of social interactions in rhesus macaques. The asymmetry in affiliation and aggression between maternal and paternal half siblings, and the effect of age proximity on partitioning social interactions suggests that context-dependent kin discrimination characterises rhesus macaques. Paternal kin discrimination probably results from an interaction between phenotype matching and familiarity, rather than from one process or the other.

Maternal investment in rhesus macaques (Macaca mulatta): reproductive costs and consequences of raising sons

Abstract Maternal investment in offspring is expected to vary according to offspring sex when the reproductive success of the progeny is a function of differential levels of parental expenditure. We conducted a longitudinal investigation of rhesus macaques to determine whether variation in male progeny production, measured with both DNA fingerprinting and short tandem repeat marker typing, could be traced back to patterns of maternal investment. Males weigh significantly more than females at birth, despite an absence of sex differences in gestation length. Size dimorphism increases during infancy, with maternal rank associated with son’s, but not daughter’s, weight at the end of the period of maternal investment. Son’s, but not daughter’s, weight at 1 year of age is significantly correlated with adult weight, and male, but not female, weight accounts for a portion of the variance in reproductive success. Variance in annual offspring output was three- to fourfold higher in males than in females. We suggest that energetic costs of rearing sons could be buffered by fetal delivery of testosterone to the mother, which is aromatized to estrogen and fosters fat accumulation during gestation. We conclude that maternal investment is only slightly greater in sons than in daughters, with mothers endowing sons with extra resources because son, but not daughter, mass has ramifications for offspring sirehood. However, male reproductive tactics supersede maternal investment patterns as fundamental regulators of male fitness.

Coalition formation among male Barbary macaques (Macaca sylvanus)

A coalition is formed when one animal intervenes in an ongoing conflict between two parties to support one side. Since support of one party is also an act against the other party, coalitions are triadic interactions involving a supporter, a recipient, and a target. The purpose of this study was to test which of three possible theories explains coalition formation among male Barbary macaques: 1) Males support kin to enhance their indirect fitness (kin selection). 2) Males support nonkin to receive future reciprocal support (reciprocal altruism). 3) Males pursue self‐interests and immediately benefit via nonkin support (cooperation). Coalition formation was investigated among 31 semi‐free male Barbary macaques in the Salem Monkey Park, Germany during the mating season. The results show: 1) Males intervened more often in dyadic conflicts in which a related opponent was involved and supported related opponents more than unrelated opponents. Close kin supported each other more often than distant kin. 2) Some evidence for reciprocal support was found. However, reciprocity was probably a by‐product of targeting the same individuals for dominance. 3) Coalition formation among nonkin is best interpreted as cooperation, based on self‐interests. Male Barbary macaques seem to intervene more often to stabilize and less often to improve their rank. Although our data were limited, the results revealed that kin support, reciprocal support, and cooperative support were all involved in coalition formation among male Barbary macaques. Am. J. Primatol. 50:37–51, 2000.

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.

A longitudinal study of age-specific reproductive output and body condition among male rhesus macaques, Macaca mulatta

In many mammalian species, male reproductive success appears to climb sharply at young adulthood, form a brief plateau during prime ages, and decline among older animals, a pattern often attributed to reduced physical condition with ageing. However, solid evidence to either substantiate or refute this profile among nonhuman primates is lacking. Here, we combine a decade of genetic analysis of paternity among free-ranging rhesus macaques, Macaca mulatta, with information about body condition in order to evaluate how changes in morphology might govern age-specific reproduction among males. We show that age-specific reproductive success traverses the same life history profile as found in other mammals, but reductions in reproductive output with advanced age were associated with reduced chances of survivorship rather than accompanied by diminished body condition. We demonstrate that variance in male age at onset of reproduction is three times greater than variance in female age at onset of reproduction. We provide the first evidence from primates that age-specific reproductive output among males is not a consequence of age-related changes in body condition, but reflects social and demographic factors.

Patterns of interventions and the effect of coalitions and sociality on male fitness

In group living animals, especially among primates, there is consistent evidence that high‐ranking males gain a higher reproductive output than low‐ranking males. Primate studies have shown that male coalitions and sociality can impact male fitness; however, it remains unclear whether males could potentially increase their fitness by preferentially supporting and socializing with females. Here we investigate patterns of male interventions and the effect of coalitions and sociality on male fitness in rhesus macaques (Macaca mulatta) with particular focus on male–female interactions. We combined behavioural observations collected on Cayo Santiago with genetic data analysed for male reproductive output and relatedness. Our results revealed that the ten top‐ranking males provided the majority of all male support observed. In contrast to other primates, male rhesus macaques mainly formed all‐down coalitions suggesting that coalitions are less likely used to enhance male dominance. Males supporting females during and before their likely conception were not more likely to fertilize those females. We also found no evidence that males preferably support their offspring or other close kin. Interestingly, the most important predictor of male support was sociality, since opponents sharing a higher sociality index with a given male were more likely to be supported. Furthermore, a high sociality index of a given male–female dyad resulted in a higher probability of paternity. Overall, our results strengthen the evidence that sociality affects fitness in male primates, but also suggest that in species in which males queue for dominance, it is less likely that males derive fitness benefits from coalitions.