Fitness consequences of spousal relatedness in 46 small-scale societies

Social norms that regulate reproductive and marital decisions generate impressive cross-cultural variation in the prevalence of kin marriages. In some societies, marriages among kin are the norm and this inbreeding creates intensive kinship networks concentrated within communities. In others, especially forager societies, most marriages are between more genealogically and geographically distant individuals, which generates a larger number of kin and affines of lesser relatedness in more extensive kinship networks spread out over multiple communities. Here, we investigate the fitness consequence of kin marriages across a sample of 46 small-scale societies (12 439 marriages). Results show that some non-forager societies (including horticulturalists, agriculturalists and pastoralists), but not foragers, have intensive kinship societies where fitness outcomes (measured as the number of surviving children in genealogies) peak at commonly high levels of spousal relatedness. By contrast, the extensive kinship systems of foragers have worse fitness outcomes at high levels of spousal relatedness. Overall, societies with greater levels of inbreeding showed a more positive relationship between fitness and spousal relatedness.     

Social dynamics of mammals: Reproductive success, kinship and individual fitness

Apparent altruism, in which an individual seemingly decreases its evolutionary fitness by assisting others, can confer benefits if the individual assists kin. Thus, an animal can increase its total or inclusive fitness by producing offspring (direct fitness) and/or helping kin to reproduce (indirect fitness). Although kin selection has been suggested as the mechanism underlying the formation of mammalian societies, many species act as if they attempt to maximize the direct fitness component of their inclusive fitness.     

Resource allocation in a social wasp: effects of breeding system and life cycle on reproductive decisions

Organisms must make important decisions on how to allocate resources to reproduction. We investigated allocation decisions in the social wasp Vespula maculifrons to understand how social insects make reproductive choices. We first determined how annual colonies apportioned resources to growth and reproduction by analysing developing brood. In contrast to expectations, colonies invested in both growth (workers) and reproduction (males) simultaneously. In addition, colonies showed evidence of producing males in pulses and reversing their reproductive choices by decreasing investment in males late in the season. This reversal is consistent with theory suggesting that colonies decrease production in males if fitness of late emerging males is low. To further investigate reproductive decisions within colonies, we determined if the male mates of multiply-mated queens varied in their reproductive success over time. Sperm use by queens did vary over time suggesting that male success may depend on sperm clumping within the female reproductive tract. Finally, we tested if colony sex ratio conformed to expectations under kin selection theory that nestmate relatedness would positively correlate with investment in new queens if workers controlled sex allocation. Surprisingly, the proportion of queens produced by colonies was negatively correlated with nestmate relatedness, suggesting that allocation may be shaped by advantages arising from increased genetic diversity resulting from multiple mating by queens. Overall, our study suggests that the reproductive decisions of colonies are flexible and may depend both on environmental cues arising from energetic needs of the colony and genetic cues arising from mating behaviours of queens.     

Evolutionary limits to self- preservation

A simple mathematical formula can be derived, on the basis of inclusive fitness theory and notions of reproductive value, to represent the residual capacity of an individual to influence his inclusive fitness. This formula involves the individual's remaining reproductive potential in his expected natural lifetime, plus the summated impacts of his continued existence on the remaining reproductive potentials of each of his kin, each weighted by the coefficient of relationship. In theory, this quantity should predict the extent to which self-preservation is optimally expressed in that individual. For asocial species, the value will vary from zero up to the maximal reproductive value observable, and the logic of the Medawar-Williams theory of senescence should apply directly. However, for highly social species like our own, it can be demonstrated that negative values can also obtain, given the conjunction of low residual reproductive potential and burdensomeness toward kin. Much empirical evidence suggests that outright self-destructiveness is often found in circumstances of such conjunction.     

Female reproductive competition within families in rural Gambia

Many studies show that the extended human family can be helpful in raising offspring, with maternal grandmothers, in particular, improving offspring survival. However, less attention has been given to competition between female kin and co-residents. It has been argued that reproductive conflict between generations explains the evolution of menopause in cooperatively breeding species where females disperse, and that older females are related to the offspring of younger females through their sons, whereas younger, incoming females are unrelated to older females. This means the pattern of help will be asymmetric, so older females lose in reproductive conflict and become 'sterile helpers'. Here, we seek evidence for female reproductive competition using longitudinal demographic data from a rural Gambian population, and examine when women are helping or harming each other's reproductive success. We find that older women benefit and younger women suffer costs of reproductive competition with women in their compound. But the opposite is found for mothers and daughters; if mother and daughter's reproductive spans overlap, the older woman reduces her reproduction if the younger woman (daughter) reproduces, whereas daughters' fertility is unaffected by their mothers' reproduction. Married daughters are not generally co-resident with their mothers, so we find not only competition effects with co-resident females, but also with daughters who have dispersed. Dispersal varies across human societies, but our results suggest reproductive conflict could be influencing reproductive scheduling whatever the dispersal pattern. A cultural norm of late male marriage reduces paternal grandmother/daughter-in-law reproductive overlap almost to zero in this population. We argue that cultural norms surrounding residence and marriage are themselves cultural adaptations to reduce reproductive conflict between generations in human families.     

The validity and value of inclusive fitness theory

Social evolution is a central topic in evolutionary biology, with the evolution of eusociality (societies with altruistic, non-reproductive helpers) representing a long-standing evolutionary conundrum. Recent critiques have questioned the validity of the leading theory for explaining social evolution and eusociality, namely inclusive fitness (kin selection) theory. I review recent and past literature to argue that these critiques do not succeed. Inclusive fitness theory has added fundamental insights to natural selection theory. These are the realization that selection on a gene for social behaviour depends on its effects on co-bearers, the explanation of social behaviours as unalike as altruism and selfishness using the same underlying parameters, and the explanation of within-group conflict in terms of non-coinciding inclusive fitness optima. A proposed alternative theory for eusocial evolution assumes mistakenly that workers' interests are subordinate to the queen's, contains no new elements and fails to make novel predictions. The haplodiploidy hypothesis has yet to be rigorously tested and positive relatedness within diploid eusocial societies supports inclusive fitness theory. The theory has made unique, falsifiable predictions that have been confirmed, and its evidence base is extensive and robust. Hence, inclusive fitness theory deserves to keep its position as the leading theory for social evolution.     

The fitness consequences of kin-biased dispersal in a cooperatively breeding bird

Cooperative alliances among kin may not only lead to indirect fitness benefits for group-living species, but can also provide direct benefits through access to mates or higher social rank. However, the immigrant sex in most species loses any potential benefits of living with kin unless immigrants disperse together or recruit relatives into the group in subsequent years. To look for evidence of small subgroups of related immigrants within social groups (kin substructure), we used microsatellites to assess relatedness between immigrant females of the cooperatively breeding superb starling, Lamprotornis superbus. We determined how timing of immigration led to kin subgroup formation and if being part of one influenced female fitness. Although mean relatedness in groups was higher for males than females, 26% of immigrant females were part of a kin subgroup with a sister. These immigrant sibships formed through kin recruitment across years more often than through coalitions immigrating together in the same year. Furthermore, females were more likely to breed when part of a kin subgroup than when alone, suggesting that female siblings form alliances that may positively influence their fitness. Ultimately, kin substructure should be considered when determining the role of relatedness in the evolution of animal societies.     

Hypothetical rankings of prospective husbands for female kin in lowland Nicaragua: consensus analysis indicates high agreement and associations with wealth and hunting skill

In preindustrial societies, kin may exert influence on the mating choices of women, but there have been few systematic studies of the preferred characteristics of husbands for female kin. In an indigenous Mayangna and Miskito community, photographs of 29 male household heads were presented to informants, who ranked the men on three characteristics: desirability as a spouse, hunting ability and wealth. For the desirability rankings, informants were asked to consider the advice that they would give to young female relatives and rank the men based on the qualities that such women should seek in a husband. Consensus analysis indicates that there is high agreement among informants on all three sets of rankings. There is no evidence that the age and sex of informants are associated with variation in evaluations of the desirability of men, which suggests that the evaluations by reproductively active women do not significantly differ from rankings by other informants. Multivariate analysis indicates that perceptions of both a man's wealth and his hunting ability are positively associated with his desirability as a prospective husband for female kin. By contrast, a strong kin-based social network, as measured by the presence of consanguineal kin in the community, seems unimportant to a man's desirability as a husband. Although it remains unclear to what extent hunting ability is a signal of phenotypic quality, these results support predictions that individuals will encourage female kin to marry men who are good resource providers. Finally, compared to a conventional reliability analysis, consensus analysis is demonstrated as a superior method for assessing both unidimensionality and subgroup variation in informant rankings.     

Kin recognition in social bees

Kin recognition in social insects has become a central issue in sociobiology because studies of the recognition abilities of social insects provide a test of kin selection theory. W.D. Hamilton(1) formalized kin selection theory by showing how individuals can gain fitness by increasing the reproductive output of relatives (kin). The social interactions of individuals, or groups, should be influenced by the genetic structure of the population. The ability to recognize kin can increase the adaptive value of social behavior by modulating it according to genetic relationship. From this, the specific prediction emerges: if individuals can distinguish among others with which they interact on the basis of the degree to which they are related, then behavior should be biased preferentially toward more closely related reproductive individuals.     

Inheritance of wealth as human kin investment

Like many other animals, humans appear to have evolved to invest time and energy in their relatives in order to maximize inclusive fitness. Inheritance of material wealth may be a uniquely human form of kin investment. If fitness-maximizing dispositions do influence will-makers, beneficiaries may be favored according to their relatedness and reproductive value. An analysis of 1000 probated wills showed that this was the case. Close relatives were favored over distant kin, as were kin of higher reproductive value. Wealthier decedents favored male kin, while poorer decedents favored females. This pattern might reflect a facultative shifting of resources toward males when the family's resources are sufficient to ensure reproductive competitiveness, and toward the safer option of females when resources are less abundant. The results support the possibility that fitness-maximizing dispositions do influence will-makers. It is likely that such dispositions are flexible and responsive to the physical and social environment.     

Policing and punishment across the domains of social evolution

Several decades of research in humans, other vertebrates, and social insects have offered fascinating insights into the dynamics of punishment (and its subset, policing), but authors have only rarely addressed whether there are fundamental joint principles underlying the maintenance of these behaviors. Here we present a punisher/bystander approach rooted in inclusive fitness logic to predict which individuals should take on punishing roles in animal societies. We apply our scheme to societies of eusocial Hymenoptera and nonhuman vertebrate social breeders, and we outline potential extensions for understanding conflict regulation among cells in metazoan bodies and unrelated individuals in human societies. We highlight that: 1) no social unit is expected to express punishment behavior unless it collects positive inclusive fitness benefits that surpass alternative benefits of bystanding; 2) punishment with public good benefits can be maintained through either direct fitness benefits (coercion) or indirect fitness benefits (correction) or both; 3) differences across social systems in the distributions of power, relatedness, and reproductive options drive variation in the extent to which individuals actively punish; and 4) inclusive fitness logic captures many punishment‐relevant evolutionary and ecological variables in a single framework that appears to apply across very different types of social arrangements. Synthesis Researchers have long observed that individuals in animal societies punish (and by extension, police) each other, but they have rarely investigated whether general principles underlie this behavior across social arrangements. In this paper, we present a punisher/bystander approach rooted in inclusive fitness logic to predict which individuals should take on punisher roles in animal societies. We apply the approach to eusocial insects and cooperatively breeding vertebrates and outline extensions towards the control of cancer cell lineages and punishment in human groups. We highlight how variation in specific social variables may drive differences in punishing/policing across the social domains.     

Kin selection in Columbian ground squirrels: direct and indirect fitness benefits

Empirical and theoretical studies have supported kin selection by demonstrating nepotism or modelling its conditions and consequences. As an alternative, we previously found that female Columbian ground squirrels had greater direct fitness when more close kin were present. Extending those results, we used population matrix methods to calculate minimum estimates of individual fitness, estimated direct and indirect components of fitness, estimated inclusive fitness by adding the direct fitness (stripped of estimated influences of the social environment) and indirect fitness components together, and finally looked for inclusive fitness benefits of associations with close kin who seem to be 'genial neighbours'. We examined the estimated fitness of a sample of 35 females for which complete lifetimes were known for themselves, their mothers and their littermate sisters. Six of these females had no cosurviving adult close kin, and their direct fitness was significantly lower than 29 females with such kin (λ = 0.66 vs. λ = 1.23). The net fitness benefit of the presence of close kin was thus 0.57. The estimated indirect component of fitness through benefits to the direct fitness of close kin was 0.43. Thus, estimated inclusive fitness for females with cosurviving close kin (λ = 1.09) was significantly greater than that for females without surviving close kin (viz., λ = 0.66). The presence of closely related and philopatric female kin appeared to result in considerable fitness benefits for female ground squirrels, perhaps through the behavioural mechanisms of lowered aggression and other forms of behavioural cooperation.     

The socio‐genetics of a complex society: female gelada relatedness patterns mirror association patterns in a multilevel society

Multilevel societies with fission–fusion dynamics—arguably the most complex animal societies—are defined by two or more nested levels of organization. The core of these societies are modular social units that regularly fission and fuse with one another. Despite convergent evolution in disparate taxa, we know strikingly little about how such societies form and how fitness benefits operate. Understanding the kinship structure of complex societies could inform us about the origins of the social structure as well as about the potential for individuals in these societies to accrue indirect fitness benefits. Here, we combined genetic and behavioural data on geladas (Theropithecus gelada), an Old World Monkey, to complete the most comprehensive socio‐genetic analysis of a multilevel society to date. In geladas, individuals in the core social ‘units’, associate at different frequencies to form ‘teams’, ‘bands’ and, the largest aggregations, ‘communities’. Units were composed of closely related females, and females remained with their close kin during permanent fissions of units. Interestingly, female–female relatedness also significantly predicted between‐unit, between‐team and between‐band association patterns, while male–male relatedness did not. Thus, it is likely that the socio‐genetic structure of gelada society results from females maintaining associations with their female relatives during successive unit fissions—possibly in an attempt to balance the direct and indirect fitness benefits of group living. Overall, the persistence of associations among related females across generations appears to drive the formation of higher levels of gelada society, suggesting that females seek kin for inclusive fitness benefits at multiple levels of gelada society.     

Evolution of monogamous marriage by maximization of inclusive fitness

The majority of human societies allow polygynous marriage, and the prevalence of this practice is readily understood in evolutionary terms. Why some societies prescribe monogamous marriage is however not clear: current evolutionary explanations—that social monogamy increases within‐group co‐operation, giving societies an advantage in competition with other groups—conflict with the historical and ethnographic evidence. We show that, within the framework of inclusive fitness theory, monogamous marriage can be viewed as the outcome of the strategic behaviour of males and females in the allocation of resources to the next generation. Where resources are transferred across generations, social monogamy can be advantageous if partitioning of resources among the offspring of multiple wives causes a depletion of their fitness value, and/or if females grant husbands higher fidelity in exchange for exclusive investment of resources in their offspring. This may explain why monogamous marriage prevailed among the historical societies of Eurasia: here, intensive agriculture led to scarcity of land, with depletion in the value of estates through partitioning among multiple heirs. Norms promoting high paternity were common among ancient societies in the region, and may have further facilitated the establishment of social monogamy. In line with the historical and ethnographic evidence, this suggests that monogamous marriage emerged in Eurasia following the adoption of intensive agriculture, as ownership of land became critical to productive and reproductive success.     

Structure and function in mammalian societies

Traditional interpretations of the evolution of animal societies have suggested that their structure is a consequence of attempts by individuals to maximize their inclusive fitness within constraints imposed by their social and physical environments. In contrast, some recent re-interpretations have argued that many aspects of social organization should be interpreted as group-level adaptations maintained by selection operating between groups or populations. Here, I review our current understanding of the evolution of mammalian societies, focusing, in particular, on the evolution of reproductive strategies in societies where one dominant female monopolizes reproduction in each group and her offspring are reared by other group members. Recent studies of the life histories of females in these species show that dispersing females often have little chance of establishing new breeding groups and so are likely to maximize their inclusive fitness by helping related dominants to rear their offspring. As in eusocial insects, increasing group size can lead to a progressive divergence in the selection pressures operating on breeders and helpers and to increasing specialization in their behaviour and life histories. As yet, there is little need to invoke group-level adaptations in order to account for the behaviour of individuals or the structure of mammalian groups.     

No evidence for divergence in male harmfulness or female resistance in response to changes in the opportunity for dispersal

The outcome of sexual conflict can depend on the social environment, as males respond to changes in the inclusive fitness payoffs of harmfulness and harm females less when they compete with familiar relatives. Theoretical models also predict that if limited male dispersal predictably enhances local relatedness while maintaining global competition, kin selection can produce evolutionary divergences in male harmfulness among populations. Experimental tests of these predictions, however, are rare. We assessed rates of dispersal in female and male seed beetles Callosobruchus maculatus, a model species for studies of sexual conflict, in an experimental setting. Females dispersed significantly more often than males, but dispersing males travelled just as far as dispersing females. Next, we used experimental evolution to test whether limiting dispersal allowed the action of kin selection to affect divergence in male harmfulness and female resistance. Populations of C. maculatus were evolved for 20 and 25 generations under one of three dispersal regimens: completely free dispersal, limited dispersal and no dispersal. There was no divergence among treatments in female reproductive tract scarring, ejaculate size, mating behaviour, fitness of experimental females mated to stock males or fitness of stock females mated to experimental males. We suggest that this is likely due to insufficient strength of kin selection rather than a lack of genetic variation or time for selection. Limited dispersal alone is therefore not sufficient for kin selection to reduce male harmfulness in this species, consistent with general predictions that limited dispersal will only allow kin selection if local relatedness is independent of the intensity of competition among kin.     

Cooperation and conflict between women in the family

Here I review recent research on reproductive conflict between females in families and how it influences their reproductive behaviour. Kin selection can favor cooperation between parent and offspring, siblings, or unrelated co‐residents who share interests in other family members such as grand‐offspring. However, these are also the individuals most likely to be sharing resources, and so conflict can also emerge. While substantial interest has arisen in evolutionary anthropology, especially over the last two decades, in the possibility of cooperative breeding in humans, less attention has been paid to reproductive conflict among female kin. Communal breeding in animals is generally understood as emerging from competition over the resources needed to breed. Competition for household resources is a problem that also faces human families. Models suggest that in some circumstances, inclusive fitness can be maximized by sharing reproduction rather than harming relatives by fighting with them, even if the shares that emerge are not equal. Thus, competition and cooperation turn out to be strongly related to each other. Reproductive competition within and between families may have underpinned the biological evolution of fertility patterns (such as menopause) and the cultural evolution of marriage, residence, and inheritance norms (such as late male marriage or primogeniture), which can enhance cooperation and minimize the observed incidence of such conflicts.     

Design, Development and Decisions

Evolutionary ideas and modern biological knowledge have important roles to play in the understanding of human behaviour. Nevertheless, it is deeply misleading to regard humans as robots in the grip of their genes. A well designed brain should respond to the consequences of behaviour; if an understanding of the likely consequences can be achieved without actually performing the act, then a person who knows that they will be rewarded or punished for certain acts is bound to be influenced by that knowledge. A brain designed in that way facilitates the evolution of societies with explicit social approval of certain activities and explicit disapproval of others. The evolutionary approach to psychology does not imply that individuals do not make free choices. Individuals clearly do make a big difference to what happens in their lives through their decisions. They may be surprised by the consequences of their own actions. A well designed brain should be able to anticipate the consequences of various courses of action and choose between them on the basis of their likely costs and benefits. Planning before doing is clearly of great advantage. People do make well considered decisions and they benefit from doing so.     

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.     

Social Context and Reproductive Potential Affect Worker Reproductive Decisions in a Eusocial Insect

Context-dependent decision-making conditions individual plasticity and is an integrant part of alternative reproductive strategies. In eusocial Hymenoptera (ants, bees and wasps), the discovery of worker reproductive parasitism recently challenged the view of workers as a homogeneous collective entity and stressed the need to consider them as autonomous units capable of elaborate choices which influence their fitness returns. The reproductive decisions of individual workers thus need to be investigated and taken into account to understand the regulation of reproduction in insect societies. However, we know virtually nothing about the proximate mechanisms at the basis of worker reproductive decisions. Here, we test the hypothesis that the capacity of workers to reproduce in foreign colonies lies in their ability to react differently according to the colonial context and whether this reaction is influenced by a particular internal state. Using the bumble bee Bombus terrestris, we show that workers exhibit an extremely high reproductive plasticity which is conditioned by the social context they experience. Fertile workers reintroduced into their mother colony reverted to sterility, as expected. On the contrary, a high level of ovary activity persisted in fertile workers introduced into a foreign nest, and this despite more frequent direct contacts with the queen and the brood than control workers. Foreign workers'' reproductive decisions were not affected by the resident queen, their level of fertility being similar whether or not the queen was removed from the host colony. Workers'' physiological state at the time of introduction is also of crucial importance, since infertile workers failed to develop a reproductive phenotype in a foreign nest. Therefore, both internal and environmental factors appear to condition individual reproductive strategies in this species, suggesting that more complex decision-making mechanisms are involved in the regulation of worker reproduction than previously thought.