Kinship, Evolution of

Kinship, Evolution of Drew Gerkey, University of Maryland, Annapolis, MD, USA Ó 2015 Elsevier Ltd. All rights reserved.

Abstract This article introduces core concepts and theories in the evolution of kinship and reviews empirical research that applies these perspectives to understand individual physiology, behavior, and social structure. After presenting theoretical definitions and methods used to measure genetic relatedness, the article reviews the mechanisms individuals use to recognize one another as kin. Research on inclusive fitness and kin selection demonstrates how relatedness between individuals affects individual actions and social interactions. This work establishes connections between the evolution of kinship and research on multilevel selection and major transitions in the evolution of complexity. A brief review suggests how the unique features of human kinship can illustrate the interactions between evolution, culture, and multiple pathways of inheritance.

Introduction Kinship is a fundamental component of evolutionary theory. In the natural sciences, the term is used to define relationships between individuals who are genetically related (see Kin Selection). Two individuals who are kin possess similar genetic material due to a shared common ancestor. Therefore, kinship emerges from one of the evolution’s fundamental conditions: the process of transmitting and inheriting genetic material from one generation to the next. Because modes of reproduction can vary from one species to the next, precise measures of genetic relatedness between individuals must derive from the particular processes of genetic replication and transmission for each species. Yet, because all species reproduce, species-specific measures of genetic relatedness, their effects on the physiology and behavior of individuals, and the social structures arising from interactions among kin can be compared across species to investigate general evolutionary patterns and principles. In the broadest sense, all living organisms are kin because all share a common ancestor, although the precise connections among contemporary and extinct species are often far in the past and only partially known. Thus, kinship can be understood as a continuum, extending from investigations of an organism’s physiology and behavior in the present and near past to the deepest evolutionary histories of all life forms. The fact that core principles of kinship can be extended across the entire range of this continuum illustrates the importance of kinship in evolutionary theory. This article introduces core concepts and theories in the evolution of kinship and briefly reviews the diverse empirical research that applies these perspectives to understand individual physiology, behavior, and social structure. The first section focuses on the essence of kinship relatedness, explaining how this term is calculated and the variations that arise from different modes of reproduction across species. The second section examines how relatedness between individuals affects social interactions by reviewing research on inclusive fitness and kin selection. The third section describes mechanisms of kin recognition, which are fundamental to linking calculations of relatedness to individual actions and social interactions. The fourth section presents research on common social structures that emerge from kin selection, including

44

reproduction, parental investment, cooperative breeding, and group formation. The fifth section shifts toward the broader end of the kinship continuum to establish connections between the evolution of kinship and deeper evolutionary histories, including research on multilevel selection, genomic imprinting, and major transitions in the evolution of complexity. Finally, the article concludes with human kinship, suggesting how the various ways our species defines relatedness can illustrate the interactions between evolution, culture, and multiple pathways of inheritance.

Relatedness Relatedness between two individuals is the essence of kinship. Evolutionary scientists define relatedness in genetic currencies, because the process of genetic replication and transmission across generations is a fundamental component of evolution. Although Darwin understood that the act of reproduction transmitted traits from one generation to the next, he and his contemporaries famously lacked accurate, detailed knowledge of these processes (see Evolution, History of). Gregor Mendel’s research on genetic inheritance and hybridization was published several years after Darwin’s On the Origin of Species, but its importance was not understood until research on genetics began to coalesce in the early years of the twentieth century. Even then, it was not until several decades later – through the research of Ronald A. Fisher, Sewall Wright, J.B.S Haldane, and others – that the theory of evolution by natural selection was integrated with population genetics to establish the ‘modern synthesis’ between heredity and evolution. A key development leading up to the modern synthesis was Wright’s coefficient of relationship, which defined the relatedness between two individuals as the sum of correlation coefficients calculated for every genealogical path connecting them to a common ancestor. In most cases, this correlation coefficient equals the probability that two individuals share a gene via descent from a common ancestor, above the random expectation that individuals share a gene due to membership in a population or species. This probability is now most often known as the coefficient of relatedness, or simply r.

International Encyclopedia of the Social & Behavioral Sciences, 2nd edition, Volume 13

http://dx.doi.org/10.1016/B978-0-08-097086-8.81041-7

Kinship, Evolution of The coefficient of relatedness can range in value from one – between identical twins, clones, or one’s relatedness to self – to values negligibly greater than zero – between individuals whose closest common ancestor lies many generations in the past. How one calculates r depends on the species’ mode of reproduction. For example, in a species that reproduces asexually by budding offspring from a parent, the coefficient of relatedness between parents and offspring – and among siblings – will equal one. In this case, because all of the offspring’s genes are received from the parent, there is 100% probability that a gene found in one will appear in the other (setting aside variation introduced by mutation). However, in a diploid species that reproduces sexually – like our own – each offspring inherits half of his or her genes from each parent. In this case, a simple way to calculate the coefficient of relatedness is to (1) define the genealogical pathways that connect two individuals, (2) value each link in the path according to the probability of inheriting a gene, (3) multiply the probabilities for each link on a path connecting two individuals, and (4) sum the product of probabilities for each path. For example, two full siblings are connected by a genealogical path via the father (0.5
0.5 ¼ 0.25) plus a path via the mother (0.5
0.5 ¼ 0.25). When we add the product of probabilities along each path (0.25 þ 0.25), we obtain a coefficient of relatedness equal to 0.5. This method for calculating coefficients of relatedness works for all sexually reproducing diploid species, but must be altered to produce correct results for species with different modes of reproduction. In practice, there are multiple ways one can measure coefficients of relatedness. First, one can collect genealogical information for all individuals in a population, and then use this information to apply the simple method described above, known as the ‘pedigree method’ (Queller, 2010). This method is accurate as long as one obtains genealogical information for each individual with sufficient generational depth. Unfortunately, in many cases it is difficult to obtain genealogies that go beyond a few generations, limiting the practical usefulness of the pedigree method in some contexts. Fortunately, advances in genetic sequencing have enabled additional techniques based on variable neutral genetic markers (Weir et al., 2006). For example, short tandem repeats of DNA (microsatellites) or single-nucleotide polymorphisms (SNPs) can be compared between two individuals to ascertain their coefficient of relatedness with high accuracy. Although this method can be useful when genealogical information is absent or difficult to obtain, specialized equipment and skills for genetic sequencing are necessary, posing difficulties for researchers who lack the ability to implement these techniques.

Kin Selection and Inclusive Fitness Measuring genetic relatedness between individuals is important because this information can be used to understand the evolution of social interactions. An individual’s actions not only affect his or her own reproductive success, they may also affect the reproductive success of others who interact with that individual. William D. Hamilton developed the concept of inclusive fitness to capture the significance of genetic relatedness for the evolution of these social interactions (Hamilton,

45

1964) (see Kin Selection; Sociobiology: Overview). Whereas an individual’s direct fitness is determined by his or her success in producing offspring, an individual’s inclusive fitness combines an individual’s reproductive success (direct fitness) with the effects that individual’s actions have on the reproductive success of related individuals (indirect fitness). The core insight of inclusive fitness is that a trait that appears to decrease an individual’s direct fitness may actually increase that individual’s inclusive fitness, resolving apparent contradictions between the evolutionary process of natural selection and the persistence of physical traits, behaviors, and social structures that impose net costs on an individual’s direct fitness. Hamilton applied the concept of inclusive fitness to predict the evolution of such costly characteristics with a simple inequality: c < b
r. This inequality states that a physical trait, behavior, or social structure that imposes net costs on an individual’s direct fitness (c) can evolve via natural selection if those costs are less than the benefits of that characteristic for other individuals (b), multiplied by the coefficient of relatedness between them (r). Because the coefficient of relatedness varies between 0 and 1, it effectively devalues the indirect benefits of the costly characteristic as genetic relatedness declines between two individuals. For example, a costly characteristic that reduces an individual’s direct fitness by 1 unit but increases the reproductive success of a full sibling (r ¼ 0.5) by 3 units can evolve via natural selection because the indirect benefit for the individual (3
0.5 ¼ 1.5) exceeds the direct cost of the physical trait, behavior, or social structure. However, that same costly characteristic would be unlikely to evolve as a result of interactions between half siblings (r ¼ 0.25) because the indirect benefits (3
0.25 ¼ 0.75) do not exceed the direct costs (c ¼ 1) for the individual. Although a complete explanation for the evolution of a specific costly trait in a particular species at a given moment in time would involve more complex models from population genetics and evolutionary game theory, the simple inequality above – often known as Hamilton’s rule – provides a useful starting point for investigating the relationship between evolution and kinship that can be applied across a wide range of species and contexts. Understandably, researchers applying Hamilton’s rule tend to focus on variation in coefficients of relatedness. However, it is important not to lose sight of the fact that other elements of the inequality – costs for direct fitness and benefits for indirect fitness – can play an equally important role. Although coefficients of relatedness are often equal for a variety of social relationships, factors that determine direct and indirect fitness can vary significantly across these relationships, particularly in species with multistage life histories. For example, in a diploid, sexually reproducing species like ours, coefficients of relatedness between parents and offspring (r ¼ 0.5) equal coefficients of relatedness between full siblings (r ¼ 0.5). Yet full siblings are almost always closer in age and the periods each depends on his or her parents for support often overlap, creating the potential for conflicts of interest that are more intense than those between parents and offspring. In this example, the greater age differences between parents and offspring can effectively reduce the direct costs of a particular trait, behavior, or social structure for the parent and increase the indirect benefit via aid to the offspring. Direct costs may be lower for parents because older

46

Kinship, Evolution of

individuals often possess greater resources, benefit only marginally from small increases in resources relative to offspring, and hold fewer remaining opportunities to reproduce. In contrast, offspring often possess limited resources, benefit greatly from small increases in resources due to key life history trade-offs at early stages of development, and hold many opportunities to reproduce once reaching adulthood, all of which can significantly increase the indirect benefits of a costly trait held by parents. These asymmetries in age, resources, sensitivity to trade-offs, and reproductive potential are less pronounced among full siblings, meaning that a similar costly trait held by one sibling may be less likely to evolve due to the indirect benefits of providing aid to another sibling who may be competing for parental resources. Variations in coefficients of relatedness will always be important for investigating kinship and the evolution of social interactions, but the example above illustrates why it is important for researchers to also explore factors that affect the other terms of Hamilton’s inequality – the costs and benefits of direct and indirect fitness for physical traits, behaviors, and social structures.

Kin Recognition With sufficient genealogical or genetic data, it is not too difficult for researchers to calculate coefficients of relatedness and investigate how kinship affects social interactions. For the kin who are the focus of this research, however, the information necessary for calculating coefficients of relatedness is often quite limited, raising an important question: How do individuals recognize one another as kin? Because coefficients of relatedness are unobservable, species have developed various kin recognition mechanisms that exploit contextual cues, physical traits, social structures, and other circumstances that correlate reliably with genetic relatedness. On a general level, a kin recognition mechanism includes four essential components (Penn and Frommen, 2010). First, a kin recognition mechanism requires a phenotypic or contextual cue that is sufficiently variable among individuals, is correlated with genetic differences, and either remains stable across an individual’s life span or is at least present during a critical phase when the recognition mechanism operates. Second, a mechanism requires a process of recognition, where an individual perceives a cue and compares it to some template that defines how that cue corresponds to a degree of relatedness. Third, the results of the recognition process are used to apply decision rules that specify how an individual will act according to relatedness. Fourth, these decision rules are assessed and used as the basis of actions that are biased in some way by the relatedness between the two individuals. These four components can take many different forms, but kin recognition mechanisms can be classified based on the kinds of cues they utilize: (1) contextual cues based on spatial proximity and familiarity from past interactions and (2) phenotypic matching via visual, auditory, and olfactory cues.

Contextual Mechanisms Although coefficients of relatedness are not perceptually salient, individuals can often exploit consistent social structures

and environmental patterns to recognize kin. These contextual mechanisms of kin recognition can include spatial proximity due to nests or other persistent residential groups as well as familiarity developed through repeated interactions. A mother who gives birth to offspring can be confident she is related to those offspring, and to the extent those offspring are raised together and interact repeatedly, they can assume they are related to one another. Fathers, however, are often in a more precarious position to make such assumptions, depending on the mating strategies prevalent in the social group (Widdig, 2007). Even in species with a high prevalence of monogamy, extra-pair mating can occur, reducing the effectiveness of spatial proximity as a mechanism of kin recognition for fathers. This variation in the effectiveness of contextual mechanisms opens possibilities for diverging strategies among individuals within a species. One parent may benefit from circumstances that cause another to overestimate relatedness, while the other would benefit from a more accurate assessment, creating dynamic interactions, as in the case of cuckoldry and other forms of sexual conflict involving paternity certainty and kin recognition (Arnqvist and Rowe, 2005). Interestingly, contextual mechanisms of kin recognition often provide opportunities for conflict and exploitation between members of different species, as in the case of brood parasitism. Cuckoo species (family Cuculidae) provide an iconic example, laying their own eggs in the nests of other birds and leaving them to be raised by the unsuspecting parents of the other species. Brood parasitism is often successful due to the victim’s reliance on contextual mechanisms of kin recognition such as the presence of eggs in one’s own nest. Many species have evolved counter-strategies to discriminate their offspring from parasite offspring, in turn resulting in more elaborate attempts at deception by the species practicing brood parasitism (Feeney et al., 2012). Research on incest avoidance and familiarity provides another iconic example of contextual mechanisms of kin recognition, this time with a confluence rather than a conflict of interests among individuals. Building on the ideas of Edvard Westermarck, scholars have examined contexts where individuals raised together display reduced levels of attraction and mating success compared to those raised apart, even when individuals raised together are genetically unrelated. Coresidence is hypothesized as a mechanism allowing individuals to recognize closely related kin (e.g., siblings) and avoid the deleterious effects of mating with them.

Phenotypic Matching Just as members of one species resemble each other more than members of another species, it is possible that more closely related individuals will resemble one another to a greater extent than distantly related individuals. If differences in genetic relatedness are correlated with salient phenotypic characteristics, individuals may be able to recognize kin by assessing phenotypes of other individuals. Penn and Frommen distinguish between three kinds of phenotypic matching: familiarity dependent, familiarity independent, and self-referential (2010: pp. 12–15). Familiarity dependent matching occurs when an individual assesses the phenotype of another individual at one time, and then compares this assessment with perceptions of

Kinship, Evolution of

that same individual’s phenotype at a later time. Put simply, individuals learn what phenotypic traits are associated with kin, and then use these traits to identify those kin as they encounter them again across the life span. Thus, familiaritydependent mechanisms of kin recognition rely on contextual mechanisms discussed earlier – such as spatial proximity – to identify phenotypic traits of kin. These phenotypic traits are then used to identify kin in absence of the original contextual mechanisms, as when siblings disperse from a natal nest. Phenotypic matching can also be extended to unfamiliar individuals. By comparing the phenotypic traits of unfamiliar individuals with phenotypic traits of familiar kin, an individual can extend contextual mechanisms beyond their spatial and temporal restrictions. For example, a contextual mechanism for recognizing siblings that relies on the spatial proximity of a nest and temporal proximity of a litter could lead siblings to become familiar with one another, and then recognize one another by sight, sound, or smell after dispersing from the nest (familiarity-dependent matching). If these visual, auditory, or olfactory cues are somewhat consistent across litters reared by the same parents, then these cues could also be used by individuals to recognize older or younger siblings from separate litters. Because these litters did not share the same nest, neither contextual nor familiarity-dependent mechanisms would allow them to recognize one another as siblings. Failure to recognize siblings from different litters could have significant negative consequences for inclusive fitness, as in the case of inbreeding depression. Individuals who are able to develop familiaritydependent phenotypic cues of relatedness and apply these cues to unfamiliar individuals (familiarity-independent matching) can avoid mating with close relatives and escape the deleterious effects of inbreeding. While potentially effective in a variety of circumstances, these two kinds of phenotypic matching depend on contextual mechanisms to develop templates that associate particular traits with kin. A third kind of phenotypic matching does not depend on any contextual or familiarity mechanisms; it simply depends on an individual’s ability to compare its own phenotype to the phenotypes of unfamiliar individuals. Such self-referential phenotypic matching mechanisms are limited to those visual, auditory, and olfactory traits that an individual can perceive in itself and identify in others. Self-referential mechanisms may be particularly effective when context and familiarity do not allow individuals to accurately assess relatedness, such as when individuals are reared alone, in litters where genetic relatedness varies due to paternity uncertainty, or in litters that include unrelated individuals from the same or another species (Hauber and Sherman, 2001). Although these recognition mechanisms may not always capture precise coefficients of relatedness, it is clear that individuals in many species are successful at using kin recognition mechanisms to guide social interactions and act in ways that increase their inclusive fitness. Evidence of effective kin recognition can be found in a variety of taxa, including humans (Kaminski et al., 2009; Park et al., 2008), nonhuman primates (Silk, 2002; Rendall, 2004), mammals (Griffin and West, 2003; Mateo, 2003), birds (Nakagawa and Waas, 2004; Zelano and Edwards, 2002), fish (Ward and Hart, 2003; Griffiths, 2003), invertebrates (Gherardi et al., 2012), and microbes (Strassmann et al., 2011). In some species, multiple

47

mechanisms may be used in tandem. In other species, mechanisms may operate at specific development stages instead of across the life span. Understanding these processes of kin recognition and investigating their evolution is an important line of inquiry for further research.

Kinship and Social Structure To the extent individuals are able to recognize kin, natural selection should favor physiological traits, behavioral strategies, and social structures that utilize this information to maximize inclusive fitness within the particular constraints of the individual’s environment. Hamilton’s research is considered a fundamental breakthrough in our understanding of the evolution of sociality because it provides a clear concept (inclusive fitness) and a simple rule (c < b
r) that allows us to investigate adaptations that emerge from interactions among individuals with varying degrees of genetic relatedness (Hamilton, 1997). A comprehensive review of the literature building on Hamilton’s work is beyond the scope of this article (Gardner et al., 2011; Queller, 2011). Instead, it will suffice to highlight some broad domains of social structure that are shaped by the evolution of kinship, starting with the foundations of mating and parental care and extending to more elaborate social structures involving cooperation, group defense, and fission–fusion dynamics. Considering the fundamental role of the transmission and inheritance of genetic information in evolution, it should not be surprising that kinship is important for our understanding of reproduction. Genetic relatedness between individuals shapes reproductive strategies at all stages, from choosing potential mates to producing and caring for offspring (Pizzari and Gardner, 2012). In sexually reproducing species, mating with close kin (incest) can have significant, negative effects on offspring survival and reproductive success (inbreeding depression), limiting the inclusive fitness of close kin who mate with one another. There is evidence that mechanisms of kin recognition help related individuals avoid incest in a variety of species (Pusey and Wolf, 1996), including birds (Nakagawa and Waas, 2004), humans (DeBruine, 2005; Rantala and Marcinkowska, 2011), mammals (Mateo, 2002), and insects (Tabadkani et al., 2012). One of the most extensively investigated examples concerns the role of major histocompatibility complex (MHC) genes in regulating mating preferences (Bernatchez and Landry, 2003; Penn and Potts, 1999; Tregenza and Wedell, 2000). MHC molecules vary among individual members of a species, and this diversity plays an important role in immune function, helping to distinguish an individual’s own cells from pathogens and other foreign cells. Genes that code for MHC molecules are transmitted from parents to offspring, and the molecules can be perceived by smell, providing an opportunity for kin recognition via phenotypic matching mechanisms. In addition to the value of avoiding incest, the benefits of MHC diversity for immune function can lead individuals to seek mating partners with dissimilar MHC molecules. There is evidence that MHC genes play a role in partner choice in humans (Havlicek and Roberts, 2009; Wedekind, 2007), primates (Knapp et al., 2006; Setchell and

48

Kinship, Evolution of

Huchard, 2010), birds (Zelano and Edwards, 2002), fish (Eizaguirre and Lenz, 2010; Reusch et al., 2001), and reptiles (Miller et al., 2009; Olsson et al., 2005). Parents of all species invest energy, time, and material resources to produce offspring, and the patterns of parental investment that emerge can be explained by measuring coefficients of relatedness, investigating mechanisms of kin recognition, and documenting physiological and behavioral traits that are biased by these mechanisms. Genetic relatedness plays a key role in evolutionary theories of parental investment, helping researchers navigate the potential conflicts and confluences of interest among individuals with varying degrees of kinship. The interactions of strategies among kin in the context of reproduction and parental care are complex even when focusing on parents and offspring. These complexities grow significantly when more distantly related kin become involved. Research on cooperative breeding and alloparental care illustrates the importance of kinship for understanding the evolution of social structures involved in reproduction and parental investment. Cooperative breeding occurs when individuals sacrifice some of their own reproductive effort in order to contribute to the reproductive effort of other individuals as alloparents (Komdeur et al., 2008). Alloparents are often – but not always – genetically related to the parents they assist, and evidence suggests that alloparents can recover the direct fitness costs of these strategies through a combination of indirect fitness benefits and enhanced mating opportunities, diminished predation risk, and other benefits of group membership (Bergmüller et al., 2007; Clutton-Brock, 2002; Lukas and Clutton-Brock, 2012). While the indirect fitness benefits of cooperative breeding strategies are an intriguing example of the influence of kinship on social structure, other benefits of group membership found in a wider range of species are also shaped by genetic relatedness. Some of the earliest investigations of kinship and social behavior focused on the production of alarm calls in social birds and rodents. Individuals are vulnerable to predation while foraging outside their burrows or nests, and alarm calls are used to alert group members to the presence of a predator. Because the alarm also attracts the attention of the predator, an individual who sounds the alarm may be exposed to a higher risk of predation than an individual who spots a predator and silently seeks safety. Evidence from a variety of studies suggests that associations between genetic relatedness and alarm calls – mediated by factors such as age, sex, dominance rank, and migration rates – underlie the evolution of this antipredation strategy (Blumstein and Armitage, 1997; Hollén and Radford, 2009), although other factors that affect risks to alarm callers can also be important (Shelley and Blumstein, 2004). Evidence suggests that kinship can also drive the formation and dissolution of social groups. Fission–fusion dynamics (i.e., the dynamic process of merging and splitting between and among subgroups within a population) reflect demographic growth and the availability of resources, and kinship often – but not always – plays an important role in identifying which neighboring groups will combine or which subgroups will cleave apart (Aureli et al., 2008). African savannah elephants live in social groups that vary frequently in spatial location and composition, and genetic relatedness among older

females predicts patterns of fission and fusion (Archie et al., 2006). Similar results arise from research on fission–fusion dynamics in giraffes (Carter et al., 2013), bats (Popa-Lisseanu et al., 2008), rhesus macaques (Widdig et al., 2006), and dolphins (Frère et al., 2010). Even when the boundaries and composition of groups remain more or less stable over time, individuals often disperse from one group to the next according to factors such as age, sex, and dominance rank (Ronce, 2007). These patterns of dispersal have consequences for the relationship between kinship and social structure, particularly the balance between cooperation and competition among kin and non-kin (Lawson Handley and Perrin, 2007; Hatchwell, 2010; Lehmann and Rousset, 2010). Although kinship shapes processes and patterns of reproduction, parental investment, cooperative breeding, defense, and group formation in many species, there are some species that integrate these domains of social life to a much greater extent, embedding individual actions within elaborate social structures shaped by the evolution of kinship. Eusocial species – defined as those that exhibit a reproductive division of labor, cooperative breeding, and overlapping generations within the social group (Wilson, 1971) – are perhaps the most striking examples of kinship’s influence on the evolution of physiology, behavior, and social structure. Many eusocial species combine sterile worker castes with reproductive ‘queens’ that monopolize mating opportunities and benefit from extensive alloparental care, cooperative resource production, and territorial defense provided by other members of the social group. In these cases, some individuals sacrifice their own opportunities to reproduce and devote their energy to increasing the reproduction of a single related female, deriving inclusive fitness benefits entirely from indirect reproduction. Indeed, Hamilton’s original formulation of inclusive fitness and kin selection theory was intended in part to explain the evolution of eusociality in a number of insect species (ants, bees, wasps), which Darwin singled out as a troublesome, potential contradiction to his theory of evolution by natural selection. Since Hamilton, scholars have continued to refine definitions of eusociality (Crespi, 2005; Lacey and Sherman, 2005), nominate additions to the list of eusocial species – including mole rats (Burda et al., 2000), beetles (Biedermann and Taborsky, 2011), shrimp (Duffy and Macdonald, 2010), and humans (Wilson, 2012) – and debate the role of kin selection, group selection, and other evolutionary mechanisms underlying the evolution of eusociality (Gardner and Ross, 2013; Hughes et al., 2008; Wilson and Hölldobler, 2005).

Kinship, Multilevel Selection, and Major Transitions Hamilton’s research on inclusive fitness and kin selection was among the first to demonstrate the advantages of exploring conflicts and confluences of interest across varying levels of biological and social hierarchy. Whereas evolutionary theories of cooperation and conflict had primarily focused on calculating costs and benefits at the level of individual organisms and groups of organisms, Hamilton’s approach utilized what has come to be called ‘the gene’s-eye’ perspective (Dawkins, 1976). This approach entails calculating costs and benefits of a trait from the perspective of a gene that codes for the

Kinship, Evolution of

trait rather than the interests of the individual who carries the gene, opening up the potential for cooperation and conflict to occur at multiple levels simultaneously, including within individuals. This approach revolutionized the study of social interactions because physiology, behaviors, or social structures that entail an apparent cost for an individual can nonetheless evolve due to benefits accruing to the putative gene underlying the trait. Prior to the work of Hamilton, George C. Williams, Robert Trivers, and others, it was common to explain traits that were costly for an individual in terms of their benefits to the individual’s social group or species (Williams, 1966; Trivers, 2002). Although the surge in research adopting the gene’s-eye perspective tipped scholarly consensus on the evolution of cooperation and competition toward explanations that emphasized the interests of genes and individuals at the expense of groups, these debates have been rekindled by a number of researchers who emphasize the importance of natural selection operating at the group level (Sober and Wilson, 1998; Nowak et al., 2010), provoking in turn a strong response from proponents of Hamilton’s approach (Abbot et al., 2011; Bourke, 2011b). One important, positive outcome of this debate has been a renewed interest in multilevel selection (Okasha, 2006) and theories that articulate how evolutionary dynamics operate simultaneously across multiple levels of biological and social hierarchy. Although scholars continue to disagree about the relative importance of natural selection operating at the levels of genes, individuals, and groups in empirical contexts, there is widespread agreement that evolution can, in principle, operate at multiple levels. This consensus emerges in large part from the work of John Maynard Smith and Eörs Szathmáry on ‘major transitions’ in evolution (Maynard Smith and Szathmáry, 1997). A major transition occurs when previously independent units (genes, cells, individuals) combine to form groups, lose the ability to reproduce independently of those groups, and become interdependent units whose evolutionary fate depends in large part on their ability to function cohesively. Although such transitions have clearly occurred in the past – including transitions from prokaryotes to eukaryotes, protists to multicellular organisms, asexual reproduction to sexual reproduction, and solitary to eusocial species – evolutionary scholars still struggle to understand the specific conditions, dynamics, and thresholds that bring about major transitions (Calcott and Sterelny, 2011). The conceptual and methodological tools developed to understand the evolution of kinship – including coefficients of relatedness, kin recognition mechanisms, and inclusive fitness – have a key role to play in this effort because they help scholars link conflicts and confluences of interest at different levels of hierarchy to modes of reproduction and forces of selection operating across these levels, from genes to individuals to groups (Birch, 2012; Bourke, 2011a). Whereas research on multilevel selection and major transitions extends inquiry outward, beyond the tangible lines dividing individuals to investigate less perceptible boundaries of social groups, others continue to pursue the implications of the gene’s eye perspective for understanding equally imperceptible dynamics within individuals. Research on genomic imprinting and kinship is a particularly intriguing example. Genomic imprinting refers to instances when a gene is

49

expressed (or not) depending on whether it is inherited from a mother or a father (Pomiankowski, 2002). David Haig proposes an explanation for patterns in genomic imprinting that derives inspiration from Hamilton’s work, suggesting potential conflicts of interest between maternal and paternal genes can be used to predict the presence of imprinted genes and their effects on physiology and behavior (Haig, 2004). For example, genes regulating parental investment might be expected to demand greater resources from the mother when inherited from the father than when inherited from the mother, due to the difference in costs and benefits of maternal investment from the perspective of each parent. The best documented example concerns a gene encoding for insulin-like growth factor 2 (IGF2) in mammals, which is only expressed when inherited from the father and compels the offspring to demand greater resources from the mother in-utero (Reik et al., 2003). IGF2 and other examples of genomic imprinting illustrate ongoing cooperation and conflict at the genetic level, alluding to deeper evolutionary histories of conflicting interests that were mitigated, but not entirely resolved, by major transitions (Burt and Trivers, 2008).

Kinship and Culture This review of research on the evolution of kinship has focused on describing key concepts, methods, and theories at a general level in order to illustrate the potential for complementary research across species. However, in order to support consilience across the divide between the natural and social sciences (Wilson, 1998), it is important to consider insights from the long tradition of research on human kinship, which is often unfamiliar to evolutionary scholars in the natural sciences. Although biological dimensions of human kinship have long been acknowledged and investigated by social scientists, cross-cultural variations in the way people define and recognize kin – as well as implications for social structures – have been the primary focus of research (Parkin and Stone, 2004). A complete review of the cultural and biological dimensions of human kinship is beyond the scope of this article (see Cronk and Gerkey, 2007; Kurland and Gaulin, 2005). Here it will suffice to briefly reframe research on human kinship in relation to the conceptual structure for the evolution of kinship offered above, moving from kinship terminologies to some common social structures that emerge from the interaction of biological and cultural definitions of relatedness. In this task, brevity is accomplished by focusing on insights from the growing body of research by social scientists (particularly anthropologists) who integrate evolutionary and cultural perspectives (Shenk and Mattison, 2011). While evolutionary scholars define relatedness in genetic currencies, social scientists define relatedness by following the cultural categories utilized by the people with whom they work. Cultural definitions of relatedness vary dramatically from one place to the next, evident in different kin terminologies that lump and split social relationships into categories that often depart from those defined by biological coefficients of relatedness. Although this variation is impressive, it is important to acknowledge that the observed variation in kin

50

Kinship, Evolution of

terms does not exhaust the full range of logical possibilities for lumping and splitting kin (Kemp and Regier, 2012). In other words, cross-cultural variations in kin terminologies exhibit patterns, and these patterns may provide clues to understanding why people’s cultural definitions of relatedness differ from relatedness defined in genetic currencies. Kin terminologies often split or lump kin according to a limited number of factors, including gender (male or female), laterality (paternal or maternal), generation (older or younger), and genealogical distance (close or distant) (Jones, 2010; Jordan, 2011). Although kin terminologies establish cultural calculations of relatedness that certainly differ from biological calculations of relatedness, this disconnect is often quickly – and perhaps mistakenly – assumed to mean that concepts and hypotheses derived from evolutionary theory are irrelevant for understanding human kinship. However, it is interesting to note that the same factors people use to split or lump categories of kin often direct our attention to consistent variations among individuals and social structures that may have consequences for inclusive fitness. In other words, kin terminologies may convey information about the fitness consequences of interacting with kin – culturally defined – by combining coefficients of genetic relatedness with factors crucial to calculating the costs and benefits of interactions with different individuals. Recall that evolutionary scientists studying inclusive fitness and kin selection in other species have warned against focusing exclusively on variation in coefficients of relatedness and ignoring factors that affect costs to direct fitness and benefits to inclusive fitness, which are both important parts of Hamilton’s inequality. Similarly, it may be unwise for scholars studying human kinship to use disconnects between cultural and biological definitions of relatedness as a reason to ignore evolutionary theory’s relevance. Instead, the wide variety and consistent patterns in human kin terminologies may provide a guide for developing and testing hypotheses about the relationship between cultural and biological definitions of relatedness and exploring the importance of inclusive fitness in human social structures. Evolutionary anthropologists have begun to investigate the intersections of cultural and biological definitions of relatedness in a variety of social domains where human kinship is important. Some have used inclusive fitness and kin selection to investigate the evolution of marriage practices, including monogamy (Fortunato and Archetti, 2010), polygyny (Borgerhoff Mulder et al., 2006), and polyandry (Starkweather and Hames, 2012) (see Marriage Systems, Evolution of). Others have synthesized research on nonhuman primate social dynamics with anthropological research on kinship to understand the role of exogamy – marrying outside one’s kin group – in extending cooperation to and restricting competition among wider social circles (Chapais, 2008). Similar approaches have been used to understand human mating, marriage, and child care as cooperative breeding strategies that have parallels in nonhuman primates and other mammals (Hrdy, 2011). Unilineal descent systems – where membership in a group is traced along paternal or maternal lineages – provide another common pattern in human kinship that can be understood by applying concepts and tools from evolutionary theory. Researchers have found that higher levels of extra-pair mating

and paternity uncertainty are associated with matrilineal descent systems, perhaps reflecting the fact that calculations of genetic relatedness are more accurate across generations when traced via maternal lines due to diminished paternity certainty among men (Hartung, 1985). Similarly, others have found that the emergence of matrilineal or patrilineal descent in a particular place may be tied to the differential influence of inherited property – whether land, livestock, or status – on reproductive success of daughters and sons. When inheritance favors the reproductive success of sons, patrilineal descent is common, and when inheritance favors daughters, matrilineal descent is common (Fortunato, 2012; Mattison, 2011). A shift in the kind of property inherited can even lead to a shift in descent, as when African Bantu-speaking matrilineal horticulturalists became patrilineal pastoralists (Holden and Mace, 2003). Such instances of change in social structures tied to kinship often reveal underlying dynamics that can be understood using evolutionary theory (Leonetti and Nath, 2009). While pursuing evolutionary research on human kinship, it is important to distinguish culture from behavior. Whereas behaviors are actions that can be directly observed and documented, culture is best defined as socially learned and transmitted information and ideas (Durham, 1992). For example, kin terminologies are socially learned and transmitted ideas about how to recognize kin that are distinct from behavioral interactions among kin, which may of course be informed by kin terminologies but may also be influenced by evolved predispositions. This distinction between culture and behavior is not intended to hold culture and evolution as opposed analytically. Rather, it is intended to define behavior as the domain for explanation, and culture and evolution as two potential pathways through which the information that informs behavior can be transmitted from one generation to the next (Cronk, 1999). For example, one of the primary functions of kin terminologies throughout the world is to define who is and is not allowed to marry and produce children. These prohibitions against incest may operate in tandem with evolved kin recognition mechanisms that help individuals avoid the biological costs of inbreeding. However, these prohibitions often depart from those defined by biological costs, applying asymmetrically – to kin on either the paternal or maternal side of the family, when both are equally related genetically – or extending to distantly related kin who pose little danger for costs of inbreeding. Rather than functioning simply to avoid inbreeding, kin terminologies often structure marital relationships that maintain or transform the boundaries between social groups. The practices of marrying within one’s kin group – endogamy – or outside one’s kin group – exogamy – often function to negotiate social structures, ascribe rights and obligations within groups, and form alliances between groups. Indeed, cultural marriage practices shaped by these aspects of social structure may even come into conflict with evolved kin recognition mechanisms aimed at avoiding inbreeding. A classic example concerns a Taiwanese ‘sim-pua’ marriage practice that betrothed children at an early age and transferred future brides to reside in the households of their future husbands. Despite the cultural prescriptions of these practices, researchers have found that partners in these marriages experienced less marital

Kinship, Evolution of

harmony and produced fewer children than partners who were raised in separate households (Lieberman, 2009; Kushnick and Fessler, 2011; Wolf and Durham, 2004). In this case, evolved kin recognition mechanisms constrain the variation of cultural kinship practices, evident when we document associations between particular behaviors (incidences of marital strife, offspring produced), cultural practices (sim-pua marriages), and conditions that trigger evolved propensities (coresidence during early childhood). This approach to studying human kinship can be used to explore interactions between culture and evolution as part of the growing research on gene-culture coevolution (Richerson and Boyd, 2004) (see Human Cooperation, Evolution of). Although many aspects of human kinship are unlikely to have close parallels in other species – such as kin terminology and unilineal descent – these exceptions can be valuable for understanding fundamental social dynamics that apply more broadly. For example, eusociality and cooperative breeding are found in relatively few species, but their unique features allow us to test predictions about inclusive fitness and multilevel selection that should, in principle, explain the conditions that lead to the presence or absence of both novel and common social structures. Although many important questions along these lines remain unanswered, this review of the evolution of kinship has highlighted some key concepts, theories, and empirical studies that provide a solid foundation for future work.

Acknowledgment DG was supported by the University of Maryland and NSF Award #DBI-1052875 to the National Socio-Environmental Synthesis Center.

See also: Human Cooperation, Evolution of; Incest Prohibition, Origin and Evolution of; Kin Selection; Marriage Systems, Evolution of; Sociobiology: Overview.

Bibliography Abbot, P., et al., 2011. Inclusive fitness theory and eusociality. Nature 471 (7339), E1–E4 author reply E9–E10. Archie, E.A., Moss, C.J., Alberts, S.C., 2006. The ties that bind: genetic relatedness predicts the fission and fusion of social groups in wild African elephants. Proceedings of the Royal Society B: Biological Sciences 273 (1586), 513–522. Arnqvist, G., Rowe, L., 2005. Sexual Conflict. Princeton University Press, Princeton. Aureli, F., et al., 2008. Fission? Fusion dynamics: new research frameworks. Current Anthropology 49 (4), 627–654. Bergmüller, R., et al., 2007. Integrating cooperative breeding into theoretical concepts of cooperation. Behavioural Processes 76 (2), 61–72. Bernatchez, L., Landry, C., 2003. MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? Journal of Evolutionary Biology 16 (3), 363–377. Biedermann, P.H.W., Taborsky, M., 2011. Larval helpers and age polyethism in ambrosia beetles. Proceedings of the National Academy of Sciences of the United States of America 108 (41), 17064–17069. Birch, J., 2012. Collective action in the fraternal transitions. Biology & Philosophy 27 (3), 363–380. Blumstein, D.T., Armitage, K.B., 1997. Does sociality drive the evolution of communicative complexity? A comparative test with ground-dwelling sciurid alarm calls. The American Naturalist 150 (2), 179–200.

51

Borgerhoff Mulder, M., Nunn, C.L., Towner, M.C., 2006. Cultural macroevolution and the transmission of traits. Evolutionary Anthropology: Issues, News, and Reviews 15 (2), 52–64. Bourke, A.F.G., 2011a. Principles of Social Evolution. Oxford University Press, Oxford. Bourke, A.F.G., 2011b. The validity and value of inclusive fitness theory. Proceedings of the Royal Society B: Biological Sciences 278 (1723), 3313–3320. Burda, H., et al., 2000. Are naked and common mole-rats eusocial and if so, why? Behavioral Ecology and Sociobiology 47 (5), 293–303. Burt, A., Trivers, R.L., 2008. Genes in Conflict: the Biology of Selfish Genetic Elements. Harvard University Press, Cambridge. Calcott, B., Sterelny, K. (Eds.), 2011. The Major Transitions in Evolution Revisited. MIT Press, Cambridge. Carter, K.D., et al., 2013. Fission–fusion dynamics in wild giraffes may be driven by kinship, spatial overlap and individual social preferences. Animal Behaviour 85 (2), 385–394. Chapais, B., 2008. Primeval Kinship: How Pair-Bonding Gave Birth to Human Society. Harvard University Press, Cambridge. Clutton-Brock, T., 2002. Breeding together: kin selection and mutualism in cooperative vertebrates. Science (New York) 296 (5565), 69–72. Crespi, B.J., 2005. Social sophistry: logos and mythos in the forms of cooperation. Annales Zoologici Fennici 42 (6), 569–571. Cronk, L., 1999. That Complex Whole: Culture and the Evolution of Human Behavior. Westview Press, Boulder. Cronk, L., Gerkey, D., 2007. Kinship and descent. In: Dunbar, R.I.M., Barrett, L. (Eds.), Oxford Handbook of Evolutionary Psychology. Oxford University Press, Oxford, pp. 463–478. Dawkins, R., 1976. The Selfish Gene. Oxford University Press, Oxford. DeBruine, L.M., 2005. Trustworthy but not lust-worthy: context-specific effects of facial resemblance. Proceedings of the Royal Society B: Biological Sciences 272 (1566), 919–922. Duffy, J.E., Macdonald, K.S., 2010. Kin structure, ecology and the evolution of social organization in shrimp: a comparative analysis. Proceedings of the Royal Society B: Biological Sciences 277 (1681), 575–584. Durham, W.H., 1992. Co-evolution: Genes, Culture, and Human Diversity. Stanford University Press, Stanford. Eizaguirre, C., Lenz, T.L., 2010. Major histocompatibility complex polymorphism: dynamics and consequences of parasite-mediated local adaptation in fishes. Journal of Fish Biology 77 (9), 2023–2047. Feeney, W.E., Welbergen, J.A., Langmore, N.E., 2012. The frontline of avian brood parasite-host coevolution. Animal Behaviour 84 (1), 3–12. Fortunato, Laura, 2012. The evolution of matrilineal kinship organization. Proceedings of the Royal Society B: Biological Sciences 279 (1749), 4939–4945. Fortunato, L., Archetti, M., 2010. Evolution of monogamous marriage by maximization of inclusive fitness. Journal of Evolutionary Biology 23 (1), 149–156. Frère, C.H., et al., 2010. Home range overlap, matrilineal and biparental kinship drive female associations in bottlenose dolphins. Animal Behaviour 80 (3), 481–486. Gardner, A., West, S.A., Wild, G., 2011. The genetical theory of kin selection. Journal of Evolutionary Biology 24 (5), 1020–1043. Gardner, Andy, Ross, L., 2013. Haplodiploidy, Sex-Ratio Adjustment, and Eusociality. The American Naturalist, pp. E60–E67. Gherardi, F., Aquiloni, L., Tricarico, E., 2012. Revisiting social recognition systems in invertebrates. Animal Cognition 15 (5), 745–762. Griffin, A.S., West, Stuart A., 2003. Kin discrimination and the benefit of helping in cooperatively breeding vertebrates. Science (New York) 302 (5645), 634–636. Griffiths, S.W., 2003. Learned recognition of conspecifics by fishes. Fish and Fisheries 4 (3), 256–268. Haig, D., 2004. Genomic imprinting and kinship: how good is the evidence? Annual Review of Genetics 38, 553–585. Hamilton, W.D., 1964. The genetical evolution of social behaviour. I. Journal of Theoretical Biology 7 (1), 1–16. Hamilton, W.D., 1997. Narrow Roads of Gene Land: the Collected Papers of W. D. Hamilton. In: Evolution of Social Behavior, vol. 1. Oxford University Press, Oxford. Hartung, J., 1985. Matrilineal inheritance – new theory and analysis. Behavioral and Brain Sciences 8 (5), 661–670. Hatchwell, B.J., 2010. Cryptic kin selection: kin structure in vertebrate populations and opportunities for kin-directed cooperation. Ethology 116 (3), 203–216. Hauber, M.E., Sherman, P.W., 2001. Self-referent phenotype matching: theoretical considerations and empirical evidence. Trends in Neurosciences 24 (10), 609–616. Havlicek, J., Roberts, S.C., 2009. MHC-correlated mate choice in humans: a review. Psychoneuroendocrinology 34 (4), 497–512. Holden, C.J., Mace, R., 2003. Spread of cattle led to the loss of matrilineal descent in Africa: a coevolutionary analysis. Proceedings of the Royal Society B: Biological Sciences 270 (1532), 2425–2433.

52

Kinship, Evolution of

Hollén, L.I., Radford, A.N., 2009. The development of alarm call behaviour in mammals and birds. Animal Behaviour 78 (4), 791–800. Hrdy, S.B., 2011. Mothers and Others: the Evolutionary Origins of Mutual Understanding. Harvard University Press, Cambridge. Hughes, W.O.H., et al., 2008. Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science (New York) 320 (5880), 1213–1216. Jones, D., 2010. Human kinship, from conceptual structure to grammar. Behavioral and Brain Sciences 33 (05), 367–381. Jordan, F.M., 2011. A phylogenetic analysis of the evolution of Austronesian sibling terminologies. Human Biology 83 (2), 297–321. Kaminski, G., et al., 2009. Human ability to detect kinship in strangers’ faces: effects of the degree of relatedness. Proceedings of the Royal Society B: Biological Sciences 276 (1670), 3193–3200. Kemp, C., Regier, T., 2012. Kinship categories across languages reflect general communicative principles. Science (New York) 336 (6084), 1049–1054. Knapp, L.A., Robson, J., Waterhouse, J.S., 2006. Olfactory signals and the MHC: a review and a case study in Lemur catta. American Journal of Primatology 68 (6), 568–584. Komdeur, J., et al., 2008. The evolution and ecology of cooperative breeding in vertebrates. In: Encyclopedia of Life Sciences. John Wiley & Sons, Ltd, Chichester, pp. 1–8. Kurland, J.A., Gaulin, S.J.C., 2005. Cooperation and conflict among kin. In: The Handbook of Evolutionary Psychology. John Wiley & Sons, Hoboken, pp. 447–482. Kushnick, G., Fessler, D.M.T., 2011. Karo Batak cousin marriage, Cosocialization, and the Westermarck hypothesis. Current Anthropology 52 (3), 443–448. Lacey, E.A., Sherman, P.W., 2005. Redefining eusociality: concepts, goals and levels of analysis. Annales Zoologici Fennici 42 (6), 573–577. Lawson Handley, L.J., Perrin, N., 2007. Advances in our understanding of mammalian sex-biased dispersal. Molecular Ecology 16 (8), 1559–1578. Lehmann, L., Rousset, F., 2010. How life history and demography promote or inhibit the evolution of helping behaviours. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 365 (1553), 2599–2617. Leonetti, D.L., Nath, D.C., 2009. Age at first reproduction and economic change in the context of differing kinship ecologies. American Journal of Human Biology: The Official Journal of the Human Biology Council 21 (4), 438–447. Lieberman, D., 2009. Rethinking the Taiwanese minor marriage data: evidence the mind uses multiple kinship cues to regulate inbreeding avoidance. Evolution and Human Behavior 30 (3), 153–160. Lukas, D., Clutton-Brock, T., 2012. Life histories and the evolution of cooperative breeding in mammals. Proceedings of the Royal Society B: Biological Sciences 279 (1744), 4065–4070. Mateo, J.M., 2002. Kin-recognition abilities and nepotism as a function of sociality. Proceedings of the Royal Society B: Biological Sciences 269 (1492), 721–727. Mateo, J.M., 2003. Kin recognition in ground squirrels and other rodents. Journal of Mammalogy 84 (4), 1163–1181. Mattison, S.M., 2011. Evolutionary contributions to solving the “matrilineal puzzle”: a test of Holden, Sear, and Mace’s model. Human Nature (Hawthorne, N.Y.) 22 (1–2), 64–88. Maynard Smith, J., Szathmáry, E., 1997. The Major Transitions in Evolution. Oxford University Press, Oxford. Miller, H.C., et al., 2009. Influence of major histocompatibility complex genotype on mating success in a free-ranging reptile population. Proceedings of the Royal Society B: Biological Sciences 276 (1662), 1695–1704. Nakagawa, S., Waas, J.R., 2004. O sibling, where art thou? A review of avian sibling recognition with respect to the mammalian literature. Biological Reviews 79 (1), 101–119. Nowak, M.A., Tarnita, C.E., Wilson, E.O., 2010. The evolution of eusociality. Nature 466 (7310), 1057–1062. Okasha, S., 2006. Evolution and the Levels of Selection. Oxford University Press, Oxford. Olsson, M., et al., 2005. MHC, health, color, and reproductive success in sand lizards. Behavioral Ecology and Sociobiology 58 (3), 289–294. Park, J.H., Schaller, M., Van Vugt, M., 2008. Psychology of human kin recognition: heuristic cues, erroneous inferences, and their implications. Review of General Psychology 12 (3), 215–235. Parkin, D., Stone, L., 2004. Kinship and Family: an Anthropological Reader. WileyBlackwell, London. Penn, D.J., Frommen, J.G., 2010. Kin recognition: an overview of conceptual issues, mechanisms and evolutionary theory. In: Kappeler, P.M. (Ed.), Animal Behavior: Evolution and Mechanisms. Springer, Heidelberg, pp. 55–85. Penn, D.J., Potts, W.K., 1999. The evolution of mating preferences and major histocompatibility complex genes. The American Naturalist 153 (2), 145–164. Pizzari, T., Gardner, Andy, 2012. The sociobiology of sex: inclusive fitness consequences of inter-sexual interactions. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 367 (1600), 2314–2323.

Pomiankowski, A., 2002. Genomic imprinting. In: The Oxford Encyclopedia of Evolution. Oxford University Press, Oxford, pp. 423–428. Popa-Lisseanu, A.G., et al., 2008. Highly structured fission–fusion societies in an aerial-hawking, carnivorous bat. Animal Behaviour 75 (2), 471–482. Pusey, A., Wolf, M., 1996. Inbreeding avoidance in animals. Trends in Ecology & Evolution 11 (5), 201–206. Queller, D.C., 2010. Kin selection and relatedness. In: Breed, M., Moore, J. (Eds.), Encyclopedia of Animal Behavior. Elsevier, pp. 247–252. Queller, D.C., 2011. Expanded social fitness and Hamilton’s rule for kin, kith, and kind. Proceedings of the National Academy of Sciences of the United States of America 108 (Suppl.), 10792–10799. Rantala, M.J., Marcinkowska, U.M., 2011. The role of sexual imprinting and the Westermarck effect in mate choice in humans. Behavioral Ecology and Sociobiology 65 (5), 859–873. Reik, W., et al., 2003. Regulation of supply and demand for maternal nutrients in mammals by imprinted genes. The Journal of Physiology 547 (Pt 1), 35–44. Rendall, D., 2004. Kin bias: proximate and functional processes. In: Chapais, B., Berman, C.M. (Eds.), Kinship and Behaviour in Primates. Oxford University Press, Oxford, pp. 295–316. Reusch, T.B., et al., 2001. Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism. Nature 414 (6861), 300–302. Richerson, P.J., Boyd, R., 2004. Not by Genes Alone: How Culture Transformed Human Evolution. University of Chicago Press, Chicago. Ronce, O., 2007. How does it feel to be like a rolling stone? Ten questions about dispersal evolution. Annual Review of Ecology, Evolution, and Systematics 38 (1), 231–253. Setchell, J.M., Huchard, E., 2010. The hidden benefits of sex: evidence for MHC-associated mate choice in primate societies. BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology 32 (11), 940–948. Shelley, E.L., Blumstein, D.T., 2004. The evolution of vocal alarm communication in rodents. Behavioral Ecology 16 (1), 169–177. Shenk, M.K., Mattison, S.M., 2011. The rebirth of kinship. Human Nature 22 (1–2), 1–15. Silk, J., 2002. Kin selection in primate groups. International Journal of Primatology 23 (4), 849–875. Sober, E., Wilson, D.S., 1998. Unto Others: the Evolution and Psychology of Unselfish Behavior. Harvard University Press, Cambridge. Starkweather, K.E., Hames, R., 2012. A survey of non-classical polyandry. Human Nature (Hawthorne, N.Y.) 23 (2), 149–172. Strassmann, J.E., Gilbert, O.M., Queller, D.C., 2011. Kin discrimination and cooperation in microbes. Annual Review of Microbiology 65, 349–367. Tabadkani, S.M., Nozari, J., Lihoreau, M., 2012. Inbreeding and the evolution of sociality in arthropods. Die Naturwissenschaften 99 (10), 779–788. Tregenza, T., Wedell, N., 2000. Genetic compatibility, mate choice and patterns of parentage: invited review. Molecular Ecology 9 (8), 1013–1027. Trivers, R.L., 2002. Natural Selection and Social Theory: Selected Papers of Robert Trivers. Oxford University Press, Oxford. Ward, A.J.W., Hart, P.J.B., 2003. The effects of kin and familiarity on interactions between fish. Fish and Fisheries 4 (4), 348–358. Wedekind, C., 2007. Body odours and body odour preferences in humans. In: Dunbar, R.I.M., Barrett, L. (Eds.), Oxford Handbook of Evolutionary Psychology. Oxford University Press, Oxford, pp. 315–320. Weir, B.S., Anderson, A.D., Hepler, A.B., 2006. Genetic relatedness analysis: modern data and new challenges. Nature Reviews. Genetics 7 (10), 771–780. Widdig, A., et al., 2006. Consequences of group fission for the patterns of relatedness among rhesus macaques. Molecular Ecology 15 (12), 3825–3832. Widdig, Anja, 2007. Paternal kin discrimination: the evidence and likely mechanisms. Biological Reviews of the Cambridge Philosophical Society 82 (2), 319–334. Williams, G.C., 1966. Adaptation and Natural Selection. Princeton University Press, Princeton. Wilson, E.O., 1998. Consilience: the Unity of Knowledge. Alfred A. Knopf, New York. Wilson, E.O., 1971. The Insect Societies. Harvard University Press, Cambridge. Wilson, E.O., 2012. The Social Conquest of Earth. W. W. Norton, New York. Wilson, E.O., Hölldobler, B., 2005. Eusociality: origin and consequences. Proceedings of the National Academy of Sciences of the United States of America 102 (38), 13367–13371. Wolf, A.P., Durham, W.H. (Eds.), 2004. Inbreeding, Incest, and the Incest Taboo. Stanford University Press, Stanford. Zelano, B., Edwards, S.V., 2002. An MHC component to kin recognition and mate choice in birds: predictions, progress, and prospects. The American Naturalist 160 (Suppl.), S225–S237.