How Grandparents Matter

Low birth rates in developed societies reflect women’s difficulties in combining work and motherhood. While demographic research has focused on the role of formal childcare in easing this dilemma, evolutionary theory points to the importance of kin. The cooperative breeding hypothesis states that the wider kin group has facilitated women’s reproduction during our evolutionary history. This mechanism has been demonstrated in pre-industrial societies, but there is no direct evidence of beneficial effects of kin’s support on parents’ reproduction in modern societies. Using three-generation longitudinal data anchored in a sample of grandparents aged 55 and over in 1992 in the Netherlands, we show that childcare support from grandparents increases the probability that parents have additional children in the next 8 to 10 years. Grandparental childcare provided to a nephew or niece of childless children did not significantly increase the probability that those children started a family. These results suggest that childcare support by grandparents can enhance their children’s reproductive success in modern societies and is an important factor in people’s fertility decisions, along with the availability of formal childcare.     

Kin recognition in Aleochara bilineata could support the kinship theory of genomic imprinting

Genomic imprinting corresponds to the differential expression of a gene according to its paternal or maternal origin. The kinship theory of genomic imprinting proposes that maternally or paternally inherited genes may be in conflict over their effects on kin differently related along the paternal or maternal line. Most examples supporting the kinship theory of imprinting deal with competition between offspring for maternal resources. However, genomic imprinting may also explain differential behavioral expression toward kin whenever sibs are more related to each other via one parental sex than the other. Unfortunately, nothing is currently known about imprinting associated with a behavioral phenotype in insects. Here we report the first evidence of such a maternally imprinted behavior. We show that the solitary parasitoid larvae of Aleochara bilineata Gyll (Coleoptera; Staphylinidae), which avoid superparasitizing their full sibs, also avoid their cousins when they are related to them through their father, but not when they are related to them through their mother. A genetic kin recognition mechanism is proposed to explain this result and we conclude that genomic imprinting could control the avoidance of kin superparasitism in this species and have a profound influence on decision-making processes.     

Relatedness and Social Behaviors in <Emphasis Type="Italic">Cercopithecus solatus</Emphasis>

Inclusive fitness and kin selection theories predict that organisms will evolve biased behavior toward kin when the inclusive fitness benefits outweigh the costs of such behaviors. Researchers have long observed that primates bias their behavior toward relatives, particularly maternal kin. We examined the effect of kinship on social behaviors in a semifree-ranging colony of Cercopithecus solatus, a poorly studied forest guenon species. We used microsatellite loci and paternity analyses to determine the degree of relatedness between individuals, as well as kinship. Individuals biased some of their behavior according to relatedness. Specifically, related individuals are more spatially associated and less aggressive toward each other. When we replaced the relatedness coefficients with defined kin categories, Cercopithecus solatus seemed to behave preferentially toward maternal kin versus paternal kin. Even though the setting of the colony and the small sample size limit our conclusions, we discuss the potential implications of our finding for the study of the impact of kin selection in primate social relationships.     

Distribution of Affiliative Behavior Across Kin Classes and Their Fitness Consequences in Mandrills

Multimale–multifemale primate groups are ideal models to study the impact of kinship on the evolution of sociality. Indeed, the frequent combination of female philopatry and male reproductive skew produces social systems where both maternal and paternal kin are co‐resident. Several primates are known to bias their behavior toward both maternal and paternal kin. Moreover, allocation of affiliation toward paternal kin has been shown to depend on the availability in maternal kin: Female baboons invest more in paternal kin after the loss of preferred maternal kin. Here, we examined how affiliation co‐varies across kin classes in juvenile mandrills (Mandrillus sphinx), an Old World primate living in a multimale–multifemale society. While affiliation levels observed with the mother and with maternal half‐sibs co‐varied positively, especially in young females, we found that levels of affiliation among paternal half‐sibs correlated negatively with levels of affiliation among individuals from the same matriline (distant kin), possibly as a result of kin availability. In addition, in social species, social bonds between individuals have been linked to differentiated fitness consequences: More socially integrated individuals generally enjoy higher fitness. We therefore also tested whether affiliation during early life impacts fitness. We showed that the global amount of affiliation during juvenescence translated into possible reproductive benefits: Females who were more socially integrated gave birth on average a year before females that were less socially integrated. However, age at first reproduction was not predicted by the amount of affiliation exchanged with any particular kin class. These results add to the growing body of evidence demonstrating differential investment in bonding and possible social adjustments among different kin categories and emphasizing once more the adaptive value of sociality.     

Kin Selection in Primate Groups

Altruism poses a problem for evolutionary biologists because natural selection is not expected to favor behaviors that are beneficial to recipients, but costly to actors. The theory of kin selection, first articulated by Hamilton (1964), provides a solution to the problem. Hamilton's well-known rule (br > c) provides a simple algorithm for the evolution of altruism via kin selection. Because kin recognition is a crucial requirement of kin selection, it is important to know whether and how primates can recognize their relatives. While conventional wisdom has been that primates can recognize maternal kin, but not paternal kin, this view is being challenged by new findings. The ability to recognize kin implies that kin selection may shape altruistic behavior in primate groups. I focus on two cases in which kin selection is tightly woven into the fabric of social life. For female baboons, macaques, and vervets maternal kinship is an important axis of social networks, coalitionary activity, and dominance relationships. Detailed studies of the patterning of altruistic interactions within these species illustrate the extent and limits of nepotism in their social lives. Carefully integrated analyses of behavior, demography, and genetics among red howlers provide an independent example of how kin selection shapes social organization and behavior. In red howlers, kin bonds shape the life histories and reproductive performance of both males and female. The two cases demonstrate that kin selection can be a powerful source of altruistic activity within primate groups. However, to fully assess the role of kin selection in primate groups, we need more information about the effects of kinship on the patterning of behavior across the Primates and accurate information about paternal kin relationships.     

The effects of residential locality on parental and alloparental investment among the Aka foragers of the central African Republic

In this paper I examine the intracultural variability of parental and alloparental caregiving among the Aka foragers of the Central African Republic. It has been suggested that maternal kin offer higher frequencies of allocare than paternal kin and that maternal investment in infants will decrease when alloparental assistance is provided. Behavioral observations were conducted on 15 eight- to twelve-monthold infants. The practice of brideservice and the flexibility of Aka residence patterns offered a means to test the effect of maternal residence on parental and alloparental investment. There was significant variation in the frequency of investment and who supplied care to infants depending on whether mothers resided with their kin or their husbands’ kin. However, in spite of the variation in allocare, when all categories of caregivers were examined collectively, infants received similar overall levels of care. Courtney L. Meehan is a Ph.D. student in cultural anthropology at Washington State University. Her research interests include parenting, alloparenting, female social networks, and female-female cooperation and competition.     

Female rhesus macaques discriminate unfamiliar paternal sisters in playback experiments: support for acoustic phenotype matching

Widespread evidence exists that when relatives live together, kinship plays a central role in shaping the evolution of social behaviour. Previous studies showed that female rhesus macaques (Macaca mulatta) recognize familiar maternal kin using vocal cues. Recognizing paternal kin might, however, be more difficult as rhesus females mate promiscuously during the possible conception period, most probably concealing paternity. Behavioural observations indicate that semi free-ranging female rhesus macaques prefer to associate with their paternal half-sisters in comparison to unrelated females within the same group, particularly when born within the same age cohort. However, the cues and mechanism/s used in paternal kin discrimination remain under debate. Here, we investigated whether female rhesus macaques use the acoustic modality to discriminate between paternal half-sisters and non-kin, and tested familiarity and phenotype matching as the underlying mechanisms. We found that test females responded more often to calls of paternal half-sisters compared with calls of unrelated females, and that this discrimination ability was independent of the level of familiarity between callers and test females, which provides, to our knowledge, the first evidence for acoustic phenotype matching. Our study strengthens the evidence that female rhesus macaques can recognize their paternal kin, and that vocalizations are used as a cue.     

Paternal Relatedness Predicts the Strength of Social Bonds among Female Rhesus Macaques

Forming strong, equitable, and enduring social bonds with a few individuals in a group carries adaptive benefits in terms of increased longevity, offspring survival and paternity success in birds and mammals, including humans. These recent insights generated a new interest in the factors creating variation in the strength of social relationships. Whether and how animals discriminate paternal kin from non-kin and bias their social behavior accordingly is being debated. This study explores the relative importance of dominance rank, age, maternal and paternal relatedness in shaping dyadic affiliative relationships in a group of 30 captive rhesus macaque females. The strength of social relationships, measured by the composite sociality index from observational data, was independently predicted in GLMMs by both maternal and paternal relatedness as well as rank similarity. In addition, social bonds between paternal half-sisters were stronger than between distantly related kin suggesting that females biased their affiliative effort towards paternal relatives. Despite identical relatedness coefficients bonds between mothers and their daughters were three times as strong as those between full sisters. Together these results add to the growing body of evidence for paternal kin biases in affiliative behavior and highlight that females prefer descendent over lateral kin.     

The Influence of Kinship on Familiar Natal Migrant Rhesus Macaques (Macaca mulatta)

In most primate species, females remain in the natal group with kin while males disperse away from kin around the time of puberty. Philopatric females bias their social behavior toward familiar maternal and paternal kin in several species, but little is known about kin bias in the dispersing sex. Male dispersal is likely to be costly because males encounter an increased risk of predation and death, which might be reduced by dispersing together with kin and/or familiar males (individuals that were born and grew up in same natal group) or into a group containing kin and/or familiar males. Here we studied the influence of kinship on familiar natal migrant rhesus macaques (Macaca mulatta) on Cayo Santiago, Puerto Rico, by combining demographic, behavioral, and genetic data. Our data suggest that kinship influences spatial proximity between recent natal immigrants and males familiar to them. Immigrants were significantly nearer to more closely related familiar males than to more distantly related individuals. Within a familiar subgroup, natal migrants were significantly closer to maternal kin, followed by paternal kin, then non-kin, and finally to males related via both the maternal and paternal line. Spatial proximity between natal immigrants and familiar males did not decrease over time in the new group, suggesting that there is no decline in associations between these individuals within the first months of immigration. Overall, our results might indicate that kinship is important for the dispersing sex, at least during natal dispersal when kin are still available.     

Perspective: maternal kin groups and the origins of asymmetric genetic systems-genomic imprinting, haplodiploidy, and parthenogenesis

The genetic systems of animals and plants are typically eumendelian. That is, an equal complement of autosomes is inherited from each of two parents, and at each locus, each parent's allele is equally likely to be expressed and equally likely to be transmitted. Genetic systems that violate any of these eumendelian symmetries are termed asymmetric and include parent-specific gene expression (PSGE), haplodiploidy, thelytoky, and related systems. Asymmetric genetic systems typically arise in lineages with close associations between kin (gregarious siblings, brooding, or viviparity). To date, different explanatory frameworks have been proposed to account for each of the different asymmetric genetic systems. Haig's kinship theory of genomic imprinting argues that PSGE arises when kinship asymmetries between interacting kin create conflicts between maternally and paternally derived alleles. Greater maternal than paternal relatedness within groups selects for more "abstemious" expression of maternally derived alleles and more "greedy" expression of paternally derived alleles. Here, I argue that this process may also underlie origins of haplodiploidy and many origins of thelytoky. The tendency for paternal alleles to be more "greedy" in maternal kin groups means that maternal-paternal conflict is not a zero-sum game: the maternal optimum will more closely correspond to the optimum for family groups and demes and for associated entities such as symbionts. Often in these circumstances, partial or complete suppression of paternal gene expression will evolve (haplodiploidy, thelytoky), or other features of the life cycle will evolve to minimize the conflict (monogamy, inbreeding). Maternally transmitted cytoplasmic elements and maternally imprinted nuclear alleles have a shared interest in minimizing agonistic interactions between female siblings and may cooperate to exclude the paternal genome. Eusociality is the most dramatic expression of the conflict-reducing effects of haplodiploidy, but its original and more widespread function may be suppression of intrafamilial cannibalism. In rare circumstances in which paternal gene products gain access to maternal physiology via a placenta, PSGE with greedy paternal gene expression can persist (e.g., in mammals).     

Human kin recognition is self- rather than family-referential

Inclusive fitness theory predicts that organisms will tend to help close kin more than less related individuals. In a variety of birds and mammals, relatives are recognized by comparing their phenotype to an internal representation or template, which might be learned through either repeated exposure to family members or self-inspection. Mirrors are ubiquitous now, but were absent during our evolutionary history; hence it is hard to predict, and empirically unknown, whether human kin recognition is family- or self-referential. Here we put this issue to the strongest possible test by comparing nepotistic behaviour towards self- versus co-twin-resemblant individuals. Seventy monozygotic and dizygotic twins were shown same-sex faces, covertly manipulated to resemble either themselves or their co-twin, and indicated which individual they would prefer in two prosocial contexts. Self-resemblant faces were significantly preferred to twin-resemblant faces, showing that visual information about the self supersedes that about close family members in the kin-recognition template. Because, under conditions of paternal uncertainty, a reliable family-referent template could be based only on one''s mother and maternal relatives, a unique advantage of self-referent phenotype matching is the possibility of (consciously or unconsciously) identifying one''s father and paternal relatives as kin.     

The Impact of male reproductive skew on kin structure and sociality in multi‐male groups

Patterns of within‐group relatedness are expected to affect the prospects for cooperation among group members through kin selection. It has long been established that dispersal patterns determine the availability of kin and there is ample evidence of matrilineal kin biases in social behavior across primate species. However, in 1979, Jeanne Altmann¹ suggested that mating patterns also influence the structure of within‐group relatedness; high male reproductive skew and the frequent replacement of breeding males leads to relatively high levels of paternal relatedness and age‐structured paternal sibships within groups. As a consequence of frequent replacement of breeding males, relatedness among offspring of a given female will be reduced to the half‐ rather than full‐sibling level. Depending on the number of sires and degree of relatedness among mothers, members of the same birth cohort may be as closely related as maternal siblings. If animals are able to recognize their paternal kin and exhibit biases in favor of them, this may influence the distribution of cooperation and the intensity of competition within groups of primates. Here, I summarize the evidence that serves as the basis for Altmann's predictions and review evidence regarding whether or not the availability of paternal kin also leads to paternal kin bias among primates.     

Consequences of group fission for the patterns of relatedness among rhesus macaques

When mammalian social groups exceed their optimal size, they often tend to split. In view of the potential evolutionary benefits, it should be more advantageous for animals to stay with kin, rather than nonkin, during such fission events. In the present study, the spontaneous fission of two social groups, R and S, of rhesus macaques living on Cayo Santiago, Puerto Rico, provided the opportunity to compare the kinship structure of the corresponding parent and daughter groups, using information on both maternal and paternal relatedness. In both instances, maternal half-siblings and pairs of animals from the same family were significantly more prevalent in the fission products than in the parent group. During the split of group R, significantly more paternal half-siblings stayed in the remnants of the parent group than joined the seceding group. Our findings are compatible with previous behavioural studies demonstrating that female primates bias their social behaviour more to maternal than to paternal kin, but that both types of half-siblings prefer each other more than unrelated animals. It remains to be clarified by future research, however, whether the observed co-segregation of paternal half-sibs in our study reflects active choice or is a by-product of the group-specific kin structures, prior to fission.     

Paternal-age and birth-order effect on the human secondary sex ratio.

Because of conflicting results in previous analyses of possible maternal and paternal effects on the variation in sex ratio at birth, records of United States live births in 1975 were sorted by offspring sex, live birth order (based on maternal parity), parental races, and, unlike prior studies, ungrouped parental ages. Linear regression and logistic analysis showed significant effects of birth order and paternal age on sex ratio in the white race data (1.67 million births; 10,219 different combinations of independent variables). Contrary to previous reported results, the paternal-age effect cannot be ascribed wholly to the high correlation between paternal age and birth order as maternal age, even more highly correlated with birth order, does not account for a significant additional reduction in sex-ratio variation over that accounted for by birth order alone.     

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.     

Behavior of Japanese monkey (Macaca fuscata) mothers and neonates at parturition

Parturitional behavior in 12 caged Macaca fuscatawas analyzed. Wild-caught mothers showed adequate maternal behaviors immediately following the neonate’s expulsion. Parity differences existed in the behaviors; primiparae were more idiosyncratic than were multiparae. Among multiparae, those with two or more offspring were uniformly adequate, but those with a single birth experience varied in the adequacy of the maternal care they provided at parturition. Mothers embraced and licked their neonates and had ventroventral contact with them frequently immediately after parturition but decreased these behaviors after expulsion of the placenta. In contrast, mothers showed allogrooming after consuming the placenta. Placentophagy was correlated with the level of orality represented by maternal licking behaviors. An isolation-reared primipara reacted to her newborn in a basically negative manner, although she showed little actual aggression. She showed a rapid shift in her negative behavior during the immediate postpartum period. This mother’s newborn sought contact with her, indicating the neonate’s active role in establishing a stable mother-neonate bond.     

Mechanisms of kin discrimination inferred from pedigrees and the spatial distribution of mates

Where animals avoid inbreeding, different mechanisms of kin discrimination can leave different 'signatures' in the patterns of observed mate relationship. For example, consider a species with no paternal care. If a female avoids mating with familiar individuals, one would expect a deficit of offspring whose parents are maternal half-siblings, but paternal half-siblings would be unfamiliar with each other and thus have offspring at the frequency expected by chance. If spatial cues are used to avoid inbreeding, a female would be expected to produce few offspring with males (even unrelated males) living near her birth site. We searched for these and other signatures with data from a long-term study of banner-tailed kangaroo rats, Dipodomys spectabilis, in Arizona, USA, using a combination of intensive censusing, mapping of available dens, microsatellite-based parentage determination, and a randomization routine that determines the numbers of offspring expected if females in the population mate indiscriminately among the males available to them. The data are consistent with the hypothesis that kangaroo rats discriminate kin by familiarity developed via association early in life, rather than by using spatial cues or self-referential phenotype matching. Our approach should be widely applicable as a means of assessing the degree to which kin discrimination exists (in contexts like nepotism as well as inbreeding avoidance) and in inferring what cues animals use to assess categories of relationship.     

Kinship,sex, and fitness in a Caribbean community

Patterns of human kinship commonly involve preferential treatment of relatives based on lineal descent (lineages) rather than degree of genetic relatedness (kindreds), presenting a challenge for inclusive fitness theory. Here, we examine effects of lineage and kindred characteristics on reproductive success (RS) and number of grandchildren for 130 men and 124 women in a horticultural community on Dominica. Kindreds had little effect on fitness independently of lineage characteristics. Fitness increased with the number of lineal relatives residing in the community but decreased beyond an apparently optimal lineage size, suggesting resource enhancement and competition among kin. Female-biased patrilineage sex ratio was positively associated with men’s fitness, while male-biased matrilineage sex ratio was positively associated with women’s fitness. Number of brothers in the community was negatively associated with men’s, but not women’s, fitness. Parents and number of sisters had no effect on either male or female reproduction; however, women with younger sisters had higher RS, suggesting benefits of kin support for childcare. In sum, imposed norms for lineage social organization may enhance lineal ancestors’ inclusive fitness at a cost to individual inclusive fitness. Research was supported by grants from the National Science Foundation (BNS 8920569 and SBR 9205373); the University of Missouri Research Board to MVF; the Earthwatch Center for Field Research to MVF, Marsha B. Quinlan, and RJQ; and the B.S.U. Center for International Programs and Office of Academic Research and Sponsored Programs to RJQ. Marsha Quinlan and Napoleon Chagnon provided valuable advice on earlier drafts. Ed Hagen gave generous help with Descent software for kinship analysis. Many friends, teachers, and consultants in Bwa Mawego contributed generously to this study: the Durand clan—Juranie, Jonah, Elford, Induria, Margelia, Eugenia, Lillia, Elquimedo, Zexia, Delfine, Wilford, Nathalie, and Sarah; the Warringtons—Martina, Amatus, Onia, Belltina, Zabius, Sarah-Gene, and Heckery; the Laudats—Eddie, Benedict, and Dellie; the Laurents—Aron and Tito; the Lewises—Eddie, Melanie, Eulina, Spliffy, Ganjala, Julina, Jalina, and Marietta; Franklin Vigilante; Lawrence Prosper; Edmund Sanderson; Alex and Tita Alie; and especially Mistress Didi and Mr. McField Coipel. Rob Quinlan is Assistant Professor of Anthropology at Ball State University. His main interests include human evolutionary ecology, reproductive development, parental care, kinship, and medical anthropology. He has conducted fieldwork in Dominica since 1993. Mark Flinn is Associate Professor of Anthropology and Psychological Sciences at the University of Missouri-Columbia. His main interests include evolutionary theory, childhood stress, family relationships, and health. He has conducted fieldwork in Dominica every year since 1987.     

Hamilton's rule and kin competition: the Kipsigis case

Evolutionary studies of human behavior have emphasized the importance of kin selection in explaining social institutions and fitness outcomes. Our relatives can nevertheless be competitors as well as sources of altruism. This is particularly likely when there is local competition over resources, where conflict can lead to strife among nondispersing relatives, reducing or even negating the effects of relatedness on promoting altruism. Here, I present demographic data on a land-limited human population, utilizing large within-population variation in land ownership to determine the interactions between local resource competition and the benefits of kin in enhancing child survival, a key component of fitness in this population. As predicted, wealth affects the extent of kin altruism, in that paternal relatives (specifically father's brothers) appear to buffer young children from mortality much more effectively in rich than in poor households. This interaction effect is interpreted as evidence that the extent of nepotism among humans depends critically on resource availability. Further unanticipated evidence that maternal kin play a role in buffering children from mortality in situations where paternal kin control few resources speaks to the important role that specific local circumstance plays in shaping kin contributions to child welfare.     

Blood is not always thicker than water:The limited effect of kin selection on human kinship in the traditional Chinese family

To examine the importance of kin selection in shaping human societies, this study analyzed the kinship system practiced in traditional China for two millennia and teased apart its underlying genetic and other, presumably cultural, components.The results demonstrate that, in the traditional patrilineal Chinese family, both genetic relatedness and the cultural factor of generation were important in determining kinship status for male agnates (genetically related relatives). For female agnates, however, only genetic relatedness was important. Another surprising finding was that the influence of gender was not as important as genetic relatedness. The most interesting finding in this study, however, was that kin selection and culture (I.e., seniority in generation and age) played vastly different roles in different lineages in the Chinese family: for collateral (indirect) agnates, genetic relatedness was the most important factor in determining their kinship status, but for lineal (direct) agnates, its importance was overridden by seniority in generation and age, a cultural factor. Several other bio-cultural factors also explained a considerable amount of variance in kinship status. Since kinship profoundly affected, and was often the foundation of, the legal and social systems in dynastic China, kin selection, while its strength may differ remarkably between lineal and collateral relatives, could act as a selective force in Chinese families.