This introductory note from Philosophical Transactions brought together papers presented at a Discussion Meeting in January 2009 where 15 scientists were invited to review important issues relevant to our understanding of the evolution of society in animals and humans. Their aim was to explore similarities and contrasts in evolutionary mechanisms in different groups of organisms and the relevance of studies of animal societies to humans. I am reproducing it here in full without permission:
Philos Trans R Soc Lond B Biol Sci. 2009 Nov 12; 364(1533): 3127–3133.
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The Evolution of Society
T. Clutton-Brock,1,* S. West,2 F. Ratnieks,3 and R. Foley4
Although the social mechanisms responsible for the development and maintenance of societies in animals and man have fascinated and intrigued philosophers and scientists since classical times, the first systematic consideration of their evolution appears in the Origin of species (Darwin 1859/1958). Much of Darwin’s thinking about the evolution of societies in animals and humans has a distinctly modern feel about it and he commonly anticipates theoretical developments that only occurred 100 years later. Although he did not confront the problem of altruistic behaviour directly, he was aware of the challenge to his theory posed by the evolution of sterile castes in some social insects (Darwin 1859/1958). In Chapter VIII of the ‘Origin of species’, he describes how he thought, at first, that this was fatal to his whole theory of natural selection. Then, in a paragraph that presages Hamilton’s subsequent extension of evolutionary theory, he describes how he realised that ‘the problem is lessened, or, as I believe, disappears, when it is remembered that selection may be applied to the family, as well as to the individual, and may thus gain the desired end.’ (Darwin 1859, p. 230).
In The descent of man (1871), Darwin turned to the evolution of human societies. In Chapter VI, he stresses the contrast between humans and other animals ‘I fully subscribe to the judgement of those writers who maintain that of all the differences between man and the lesser animals, the moral sense or conscience is by far the most important’ (The descent of man, p. 97). He then goes on to argue that the evolution of mutual assistance and the moral senses in humans and other animals are maintained by benefits shared by members of cooperative groups, a suggestion that clearly parallels modern theories of social evolution (Boyd & Richerson 1996; Clutton-Brock 2002). He goes on to point out that many animals live in groups and cooperate with each other and describes how ‘wolves and some other beasts of prey hunt in packs, and aid one another in attacking their victims’, how ‘pelicans fish in concert’ and ‘social animals mutually defend each other’. He describes how vervet monkeys stretch out and groom each others coats and ends by telling a story illustrating the benefits of cooperation:
‘an eagle seizes a young Cercopithecus, which by clinging to a branch, was not at once carried off; it cried loudly for assistance, upon which the other members of the troop, with much uproar, rushed to the rescue, surrounded the eagle, and pulled out so many feathers, that he no longer thought of his prey, but only how to escape. This eagle as Brehm [the source of the story] remarks, assuredly would never again attack a single monkey of a troop’ (p. 101, 102).
For nearly a 100 years from Darwin’s death, scientific attention was focussed on mechanistic and developmental questions rather than functional ones and Darwin’s interest in social evolution and his holistic view of biological adaptation were eclipsed by the growth of other biological subdisciplines. A continuing interest in social behaviour was maintained though the research and writings of naturalists like Henri Fabre, Eugene Marais, the Keatons, Edmund Selous and Eliot Howard. However, although they were experienced naturalists and observers, they lacked Darwin’s theoretical structure, his compelling interest in principles and his readiness to confront exceptions and difficulties.
Not until the late 1930s did a substantial number of professional biologists start to work on the social behaviour of animals. They fell into three main groups. First, there were the founding fathers of animal behaviour, including Julian Huxley (1934, 1938), Konrad Lorenz (1927, 1931, 1935), Niko Tinbergen (1931, 1935, 1936, 1937), Karl von Frisch (1938), Frank Fraser Darling (1937, 1938), Solly Zuckerman (1929, 1932) and Clarence Ray Carpenter (1934, 1935, 1940). Their primary focus was usually on questions concerning the control and development of behaviour, though their research sometimes encompassed functional or comparative aspects of reproductive behaviour. Second, there were a number of animal ecologists, including David Lack (1932, 1933, 1935, 1939, 1943) and A. F. Skutch (1935, 1945, 1960) whose primary interests were the regulation of population density and the evolution of reproductive parameters, including egg size and clutch size. And third, there were the population geneticists, including Ronald Fisher (1930) and J. B. S. Haldane (1932) and later, G. C. Williams (1957) whose principal focus was on the operation of natural selection and the evolution of genetic systems, but whose interests also encompassed the evolution of life histories and social behaviour. Unlike the first two groups, they were well aware of the problems raised by social and altruistic behaviour, though these were tangential to their main interest and usually attracted only passing comments.
These three distinct lines of thinking persisted into the 1950s and they were still largely separate by the end of that decade. For example, neither of Niko Tinbergen’s two synthetic books, Social behaviour in animals (1953) and The study of instinct (1955) cite either Darwin or Fisher. However, by 1960, both theoretical and empirical research was beginning to turn to topics that overlapped all three areas of interest. Comparative studies of social behaviour (especially studies of birds by Gordon Orians (1961, 1962) and John Crook (1962, 1964, 1965) revealed that the size and structure of social groups and the form of mating systems were closely related to variation in habitat and diet, stimulating interest in functional interpretations of social behaviour and providing detailed examples both of selfish and altruistic behaviour. In addition, research on population dynamics in birds showed that territoriality played an important part in regulating population density, focusing the interests of ecologists and ethologists on its evolution and function (Lack 1954, 1966). Finally, the development of a theoretical framework accounting for the evolution of life histories (Medawar 1952; Cole 1954; Williams 1957) led to a growing interest in the adaptive significance of apparently altruistic behaviour.
Two specific developments acted as catalysts for the rapid changes that followed. The first was the publication of Wynne Edwards’ monumental book Animal dispersion in relation to social behaviour (1962). Wynne Edwards claimed that many animals adaptively limited their numbers in advance of resource shortage to improve the probability that the group or population would survive. Group displays had evolved, he suggested, to allow their members to assess population density and to adjust their reproductive output accordingly. Other aspects of social behaviour, including territoriality and dominance hierarchies, were closely involved in the regulation of animal numbers and had evolved for this purpose. Wynne Edwards’ theory was directly contrary both to Darwin’s persistent emphasis on individual variation in reproduction as the keystone of evolution as well as to the perception of many ecologists that animal populations were limited directly by the availability of resources (Lack 1954, 1966) so neither population geneticists nor ecologists could ignore the challenge. The general application of Wynne Edwards’ theory was attacked and refuted (Hamilton 1963; Maynard Smith 1964; Lack 1966; Williams 1966a,b) and the ensuing controversy drew attention to the fact that many functional explanations of social and reproductive behaviour relied on putative benefits to groups or populations. This eventually led to a critical revaluation of many of these ideas, culminating in G. C. Williams’ influential review of adaptation (1966).
The second development was the explanation of altruism and sterility in Hymenoptera by W. D. Hamilton. In 1963, Hamilton published a brief paper arguing that altruism could evolve if it increased the fitness of relatives and, the following year, introduced the concept of inclusive fitness to account for the evolution of worker sterility in Hymenoptera and of alarm calls in vertebrates (Hamilton 1964). Subsequently, Maynard Smith (1964) named Hamilton’s process ‘kin selection’ to distinguish it from group selection and used it to produce a formal model of the evolution of alarm calls (Maynard Smith 1965). In contrast to many of his contemporaries working on the evolution of vertebrate-breeding systems (see above), Hamilton’s thinking owed much to Fisher. He describes how his interest in the evolution of animal societies and altruism.
‘began for me while I was an undergraduate reading natural sciences at the University of Cambridge in 1958. I discovered R. A. Fisher’s The genetical theory of natural selection in the St John’s College Library and immediately realised that this was the key to the understanding of evolution that I had long wanted. I became a Fisher freak and neglected whole courses in my efforts to grasp the book’s extremely compressed style and reasoning. I quickly noticed, however, that Fisher’s arguments implied a basically different interpretation of adaptation from what I was hearing from most of my lecturers and reading in other books. Was adaptation mainly for the benefit of species (the lecturers’ view) or for the benefit of individuals (Fisher’s view)? Clearly it was Fisher who had thought out his Darwinism properly; where interpretations differed, therefore, he must be right—but were the others always wrong? I started on what seemed the key theme in this puzzle—altruism. Did it exist? Could one evolve it in a model? (Hamilton 1988, p. 15)
Hamilton’s theory of kin selection (Hamilton 1964) provided the basis for adaptive interpretations of many forms of altruistic and cooperative behaviour. However, there were some types of cooperation that could not be explained in this way. In particular, why should members of different species (who could not possibly be closely related) cooperate with each other? And why should unrelated conspecifics sometimes assist each other? One possible explanation was that, as Darwin had suggested, cooperating individuals gained shared mutualistic benefits but explanations of this kind smacked of group selection and had difficulty in explaining why cooperation was not replaced by cheating strategies. An alternative explanation of apparently altruistic actions involving unrelated individuals was produced by R. L. Trivers in 1971. Trivers argued that if individuals assisted each other in turn and the costs of assistance were relatively low to donors while the benefits were high to recipients, reciprocal assistance (reciprocity) could evolve among individuals that were unrelated to each other. Cheats (individuals who accepted favours but did not return them) might initially be at an advantage but selection would subsequently favour individuals that discriminated against them and cooperated selectively with individuals that had assisted them in the past. This form of cooperation was originally referred to as ‘reciprocal’ altruism but this can lead to confusion since cooperation of this kind is mutually beneficial in the long term rather than altruistic (Dugatkin 1997; West et al. 2007; Clutton-Brock in press).
The theoretical basis of much of our current understanding of the evolution of breeding systems was laid during the decade following the publication of Hamilton’s theory of kin selection (Hamilton 1964). Hamilton’s (1971) ‘selfish herd’ theory showed that sociality itself could confer benefits to individuals without benefiting the entire group if the chance that an individual would be selected by a predator was diluted as the number of individuals close to it increased. He subsequently examined the conditions favouring selfish and spiteful behaviour within social groups (Hamilton 1964, 1971, 1972). Maynard Smith (1974) and Parker (1974) introduced game theory models to explain why competitors did not always seek to maximize damage to their opponents and to account for ‘ritualization’ of aggressive behaviour. Trivers (1974) explored conflicts of interest between parents and their offspring arguing that, in sexually reproducing organisms, the genetic interests of parents will commonly differ from those of their progeny, who should often favour higher levels of parental expenditure higher than their parents’ optima. Darwin’s writing on sexual selection was re-examined and extended. Trivers (1972) argued that the reasons why males typically compete more intensely for mates than do females was linked to their lower expenditure on progeny, coining the term ‘parental investment’ to cover all forms of parental expenditure associated with rearing offspring. Fisher’s (1930) explanation of the equality of most vertebrate sex ratios was re-assessed and Hamilton (1967) showed that the strongly female-biased sex ratios could be favoured where competing males were close relatives. Trivers & Willard (1973) argued that, in sexually dimorphic vertebrates where sons were more costly to rear than daughters, females who conceived sons but could not afford to rear them should prematurely terminate investment in their progeny—and suggested that this might account for the common trend for mortality to be higher in juvenile males than females. Adaptive explanations of life histories developed in a less dramatic fashion. A number of important reviews laid the basis of what is now known as life-history theory (Gadgil & Bossert 1970; Wilson & Bossert 1971; Pianka 1974; Stearns 1976; Charlesworth 1980). Over the same period, empirical studies of animal breeding systems began to proliferate, focusing more and more on issues of theoretical interest (Lack 1968; Wilson 1971; Clutton-Brock 1974; Jarman 1974).
This period of rapid development of theory culminated in a second monumental book. E. O. Wilson’s Sociobiology, the new synthesis (Wilson 1974) contained relatively few new developments but provided comprehensive reviews of relevant areas of population genetics, demography, life-history theory and animal behaviour. Wilson stressed their inter-relatedness and defined a new sub-discipline, sociobiology, whose principal goal should be ‘an ability to predict features of social organization from a knowledge of population parameters combined with information on the behavioural constraints imposed by the genetic constitution of the species’. He argued that an understanding of the evolution of population parameters (including life history variables) should be one of the principal aims of evolutionary ecology and population biology and predicted that, by the year 2000, sociobiology and behavioural ecology would have become closely allied with population biology and genetics, while traditional ethology and comparative psychology would have been progressively integrated with neurophysiology. The first component of his prediction came about more rapidly than he had anticipated for the theoretical issues raised by the papers of Hamilton, Trivers and Maynard Smith rapidly became the focus of attention in behavioural biology and soon led to the development of an integrated conceptual framework for explaining the ecology and evolution of social behaviour (Krebs & Davies 1978).
After the publication of Wilson’s (1975) review, research on social evolution expanded rapidly. The ideas of Hamilton, Trivers, Maynard Smith and Parker were explored, extended and tested (Krebs & Davies 1984; Krebs & Davies 1991, 1997). A combination of theoretical and empirical studies investigated the contrasts and parallels between cooperative and competitive interactions at different levels—between genes on the same chromosome, between cells and groups of cells, between individuals, families, groups and populations (Wilson 1980; Maynard Smith & Szathmary 1995; Michod & Roze 2001; Hoekstra 2003; Okasha 2006). Building on research on the development of social relationships (Hinde 1974, 1983), research on social vertebrates (and primates in particular) explored the development and maintenance of relationships and the ways by which individuals attempt to manipulate the behaviour of others to their own advantage (Clutton-Brock & Parker 1995a,b; Whiten & Byrne 1997), and the tactics they use to resolve conflicts (de Waal 1993; Aureli & de Waal 2000). New fields of research developed round the evolution of signalling systems (Zahavi 1975; Grafen 1990), cooperation between non-relatives (Axelrod 1984; Sachs et al. 2004; Bergmuller et al. 2007a), the evolution of cooperative breeding (Brown 1987), the extent and causes of reproductive suppression (Vehrencamp 1983a,b) and the resolution of conflicts within social groups (Trivers & Hare 1976; Ratnieks 1988; Boomsma & Grafen 1990; Ratnieks et al. 2006). The adaptive significance of life-history parameters was explored and examined and new theories were developed to account for variation in fecundity (Stearns 1976; Alexander 1991; Bourke 1999), mate choice (Lande 1980; Lande & Arnold 1983), sex allocation (Charnov 1982; Bull 1983; Frank 1990; West 2009), parental care (Clutton-Brock 1991; Godfray 1995a,b) and longevity (Bourke 2007). Following the development of genetic techniques capable of identifying paternity (Jeffreys et al. 1985) it soon came to be appreciated that competition between males extended beyond mating (Birkhead & Møller 1992). These empirical advances were associated with theoretical developments that clarified the links between inclusive fitness and other branches of evolutionary theory, including population and quantitative genetics (Grafen 1985; Frank 1986; Taylor 1990; Queller 1992; Taylor 1996; Wolf et al. 1999; Rousset & Ronce 2004; Gardner et al. 2007), making it easier to develop more general models (Taylor & Frank 1996; Frank 1998) and allowing the biology to lead the maths, rather than vice versa.
Over the same period, long-term studies of recognizable individuals provided novel insights into animal societies as well as the information necessary to explore new questions (Clutton-Brock et al. 1982; Woolfenden & Fitzpatrick 1984; Koenig & Mumme 1987; Betzig et al. 1988; Hoogland 1995). In addition, the increasing range of societies that had been examined in detail generated reviews of social behaviour and breeding systems in insects (Wilson 1971; Bourke & Franks 1995; Choe & Crespi 1997), fishes (Thresher 1984), birds (Brown 1987; Koenig & Dickinson 2004) and non-human mammals (Jarman 1974; Smuts 1986a,b; Gittleman 1989; Mann et al. 2000; Wolff & Sherman 2007). Quantitative comparisons of interspecific data were used to test evolutionary hypotheses and to explore relationships between social behaviour, life histories and ecological parameters (Clutton-Brock 1974; Clutton-Brock & Harvey 1978, 1979; Harvey & Pagel 1991). The framework of evolutionary thinking was also extended to the analysis of human behaviour, relationships and societies (Daly & Wilson 1983; Betzig et al. 1988; Barrett et al. 2002; Hrdy 2009). Theoretical studies investigated the evolution of the unusual characteristics of humans, including the development of culturally acquired adaptations (Boyd & Richerson 1996). In parallel, empirical studies of tribal societies generated quantative data on behaviour, energetics, life-history parameters and demography that could be used to test ecological and evolutionary theories and predictions (Betzig et al. 1988; Borgerhoff Mulder 1988; Hill & Hurtado 1996).
Today, we understand more about the evolution of society than Darwin did. Nevertheless, the field of social evolution continues to develop rapidly and there are still many unresolved problems and many contentious areas. There is an ongoing debate as to whether social systems should be regarded as superorganisms with adaptive characteristics of their own or whether they are best interpreted as byproducts of the adaptive strategies of individuals (Okasha 2006; Wilson & Wilson 2007). There is still disagreement about the distinction between kin selection and group selection as well as about the relative importance of selection operating at different levels (West et al. 2007, 2008; Wilson & Wilson 2007) and the relative importance of mutualism, reciprocity and coercion in maintaining cooperative behaviour is contentious (Clutton-Brock 2002, in press; West et al. in press). Evolutionary explanations of sex differences have recently been the target of criticism (Gowaty 2004; Tang-Martinez & Ryder 2005) and some would even like to see the theory of sexual selection abandoned altogether (Roughgarden et al. 2006; Roughgarden 2009). Contrasting models of variation in reproductive skew and the proximate mechanisms responsible for reproductive suppression in cooperative societies are still widely debated (Vehrencamp 1983a,b; Reeve & Keller 1995; Clutton-Brock 1998; Clutton-Brock et al. 2001b; Creel & Creel 2001; Magrath et al. 2004). Finally, there is little agreement over the origins of human society; the sequence in which human characteristics developed or the relevance of studies of animal societies to understanding those of humans (Rodseth et al. 1991; Wrangham et al. 1999; Zhou et al. 2004; Hrdy 2009).
REFERENCES
- Alexander R. D. 1991The evolution of eusociality. In The biology of the naked mole-rat (eds Sherman P. W., Jarvis J. U. M., Alexander R. D., editors. ), pp. 3–44 Princeton, NJ: Princeton University Press [Google Scholar]
- Aureli F., de Waal F. B. M. 2000Natural conflict resolution San Francisco, CA: University of California Press [Google Scholar]
- Axelrod R. 1984The evolution of cooperation New York, NY: Basic Books [Google Scholar]
- Barrett L., Dunbar R., Lycett J. E. 2002Human evolutionary psychology Princeton, NJ: Princeton University Press [Google Scholar]
- Bergmuller R., Bshary R., Johnstone R. A., Russell A. F. 2007aIntegrating cooperative breeding and cooperation theory. Behav. Process. 76, 61–72 (doi:10.1016/j.beproc.2007.07.001) [PubMed] [Google Scholar]
- Betzig L., Borgerhoff Mulder M., Turkes P., editors. (eds) 1988Human reproductive behaviour Cambridge, UK: University Press [Google Scholar]
- Birkhead T. R., Møller A. P. 1992Sperm competitions in birds London, UK: Academic Press [Google Scholar]
- Boomsma J. J., Grafen A. 1990Intraspecific variation in ant sex ratios and the Trivers–Hare hypothesis. Evolution 44, 1026–1034 (doi:10.2307/2409564) [PubMed] [Google Scholar]
- Borgerhoff Mulder M. 1988Reproductive success in three Kipsigi cohorts. In Reproductive success (ed. Clutton-Brock T. H., editor. ), pp. 419–435 Chicago, IL: University Press [Google Scholar]
- Bourke A. F. G. 1999Colony size, social complexity and reproductive conflict in social insects. J. Evol. Biol. 12, 245–257 (doi:10.1046/j.1420-9101.1999.00028.x) [Google Scholar]
- Bourke A. F. G. 2007Kin selection and the evolutionary theory of aging. Ann. Rev. Ecol. Syst. 38, 103–128 [Google Scholar]
- Bourke A. F. G., Franks N. R. 1995Social evolution in ants Princeton, NJ: Princeton University Press [Google Scholar]
- Boyd R., Richerson P. J. 1996Why culture is common, but cultural evolution is rare. Proc. Br. Acad. 88, 77–93 [Google Scholar]
- Brown J. L. 1987Helping and communal breeding in birds Princeton, NJ: Princeton University Press [Google Scholar]
- Bull J. J. 1983Evolution of sex determining mechanisms Menlo Park, CA: Benjamin/Cummings [Google Scholar]
- Charlesworth B. 1980Evolution in age-structured populations Cambridge, UK: Cambridge University Press [Google Scholar]
- Charnov E. L. 1982The theory of sex allocation Princeton, NJ: Princeton University Press [Google Scholar]
- Choe J. L., Crespi B. J., editors. (eds) 1997Mating systems in insects and arachnids Cambridge, UK: University Press [Google Scholar]
- Clutton-Brock T. H. 1974Primate social organisation and ecology. Nature 250, 539–542 (doi:10.1038/250539a0) [Google Scholar]
- Clutton-Brock T. H. 1991The evolution of parental care Princeton, NJ: Princeton University Press [Google Scholar]
- Clutton-Brock T. H. 1998Reproductive skew: disentangling concessions from control. A reply to Emlen and Reeve. Trends Ecol. Evol. 13, 459 (doi:10.1016/S0169-5347(98)01470-0) [PubMed] [Google Scholar]
- Clutton-Brock T. H. 2002Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296, 69–72 (doi:10.1126/science.296.5565.69) [PubMed] [Google Scholar]
- Clutton-Brock T. Cooperation between non-kin: reciprocity, mutualism or manipulation? Nature In press. [PubMed] [Google Scholar]
- Clutton-Brock T. H., Harvey P. H. 1978Mammals, resources and reproductive strategies. Nature 273, 191–195 (doi:10.1038/273191a0) [PubMed] [Google Scholar]
- Clutton-Brock T. H., Harvey P. H. 1979Comparison and adaptation. Proc. R. Soc. Lond. B 205, 547–565 (doi:10.1098/rspb.1979.0084) [PubMed] [Google Scholar]
- Clutton-Brock T. H., Parker G. A. 1995aPunishment in animal societies. Nature 373, 209–216 (doi:10.1038/373209a0) [PubMed] [Google Scholar]
- Clutton-Brock T. H., Parker G. A. 1995bSexual coercion in animal societies. Anim. Behav. 49, 1345–1365 (doi:10.1006/anbe.1995.0166) [Google Scholar]
- Clutton-Brock T. H., Guinness F. E., Albon S. D. 1982Red deer: the behaviour and ecology of two sexes Edinburgh, UK: University Press [Google Scholar]
- Clutton-Brock T. H., et al. 2001bCooperation, conflict and concession in meerkat groups. Science 291, 478–481 (doi:10.1126/science.291.5503.478) [PubMed] [Google Scholar]
- Cole L. C. 1954The population consequences of life history phenomena. Quart. Rev. Biol. 29, 103–137 [PubMed] [Google Scholar]
- Creel S., Creel N. M. 2001The African wild dog: behavior, ecology and conservation Princeton, NJ: University Press [Google Scholar]
- Daly M., Wilson M. 1983Sex, evolution and behavior Boston, MA: Willard Grant Press [Google Scholar]
- Darwin C. 1859/1958The origin of species New York, NY: The Modern Library [Google Scholar]
- de Waal F. B. M. 1993Primate social conflict (eds Mason W. A., Mendoza S. P., editors. ). Albany, NY: State University of New York Press [Google Scholar]
- Dugatkin L. A. 1997Cooperation among animals: an evolutionary perspective Oxford, UK: University Press [Google Scholar]
- Frank S. A. 1986Hierarchical selection theory and sex ratios. I. General solutions for structured populations. Theoret. Popul. Biol. 29, 312–342 (doi:10.1016/0040-5809(86)90013-4) [PubMed] [Google Scholar]
- Frank S. A. 1990Sex allocation theory for birds and mammals. Ann. Rev. Ecol. Syst. 21, 13–56 (doi:10.1146/annurev.es.21.110190.000305) [Google Scholar]
- Frank S. A. 1998Foundations of social evolution Princeton, NJ: University Press [Google Scholar]
- Gadgil M., Bossert W. H. 1970Life historical consequences of natural selection. Am. Nat. 104, 1–24 (doi:10.1086/282637) [Google Scholar]
- Gardner A., West S. A., Barton N. H. 2007The relation between multilocus population genetics and social evolution theory. Am. Nat. 169, 207–226 (doi:10.1086/510602) [PubMed] [Google Scholar]
- Gittleman J. L. 1989Carnivore group living: comparative trends. In Carnivore behaviour, ecology and evolution (ed. Gittleman J. L., editor. ), pp. 183–207 Ithaca, NY: Cornell University Press [Google Scholar]
- Godfray H. C. J. 1995aEvolutionary theory of parent–offspring conflict. Nature 376, 133–138 (doi:10.1038/376133a0) [PubMed] [Google Scholar]
- Godfray H. C. J. 1995bSignaling of need between parents and young: parent–offspring conflict and sibling rivalry. Am. Nat. 146, 1–24 (doi:10.1086/285784) [Google Scholar]
- Gowaty P. A. 2004Sex roles, contests for the control of reproduction and sexual selection. In Sexual selection in primates (ed. Kappeler P., editor. ), pp. 163–221 Cambridge, UK: University Press [Google Scholar]
- Grafen A. 1985A geometric view of relatedness. Oxford Surv. Evol. Biol. 2, 28–29 [Google Scholar]
- Grafen A. 1990Biological signals as handicaps. J. Theoret. Biol. 144, 517–546 (doi:10.1016/S0022-5193(05)80088-8) [PubMed] [Google Scholar]
- Hamilton W. D. 1963The evolution of altruistic behavior. Am. Nat. 97, 354–356 (doi:10.1086/497114) [Google Scholar]
- Hamilton W. D. 1964The genetical evolution of social behaviour. I. II. J. Theoret. Biol. 7, 1–52 (doi:10.1016/0022-5193(64)90038-4) [PubMed] [Google Scholar]
- Hamilton W. D. 1971Geometry for the selfish herd. J. Theoret. Biol. 31, 295–311 (doi:10.1016/0022-5193(71)90189-5) [PubMed] [Google Scholar]
- Hamilton W. D. 1972Altruism and related phenomena, mainly in social insects. Ann. Rev. Ecol. Syst. 3, 193–232 (doi:10.1146/annurev.es.03.110172.001205) [Google Scholar]
- Hamilton W. D. 1988The genetical theory of social behaviour 1. Citation classic in Current Contents No. 40, p. 16. [J. Theor. Biol.7, 1–16]. [Google Scholar]
- Harvey P. H., Pagel M. D. 1991The comparative method in evolutionary biology Oxford, UK: University Press [Google Scholar]
- Hill K., Hurtado M. A. 1996Ache life history New York, NY: Aldine de Gruyter [Google Scholar]
- Hinde R. A. 1974Biological bases of human social behaviour New York, NY: McGraw Hill [Google Scholar]
- Hinde R. A. 1983Primate social relationships Oxford, UK: Blackwells [Google Scholar]
- Hoekstra R. 2003Power to the genome: who suppresses the outlaw? In Genetic and cultural evolution of cooperation (ed. Hammersteiin P., editor. ), pp. 257–270 Dahlem Workshop Reports series Cambridge, MA: MIT Press [Google Scholar]
- Hoogland J. L. 1995The black-tailed prairie dog: social life of a burrowing mammal Chicago, IL: University of Chicago Press [Google Scholar]
- Hrdy S. B. 2009Mothers and others Harvard, USA: Belknap Press [Google Scholar]
- Jarman P. J. 1974The social organisation of antelope in relation to their ecology. Behaviour 48, 215–267 (doi:10.1163/156853974X00345) [Google Scholar]
- Jeffreys A. J., Wilson V., Thein S. L. 1985Hypervariable ‘minisatellite’ regions in human DNA. Nature 314, 67–73 (doi:10.1038/314067a0) [PubMed] [Google Scholar]
- Koenig W., Dickinson J., editors. (eds) 2004Ecology and evolution of cooperative breeding in birds Cambridge, UK: University Press [Google Scholar]
- Koenig W. D., Mumme R. L. 1987Population ecology of the cooperatively breeding acorn woodpecker Princeton, NJ: Princeton University Press [Google Scholar]
- Krebs J. R., Davies N. B. 1978Behavioural ecology: an evolutionary approach Oxford, UK: Blackwell Scientific Publications [Google Scholar]
- Krebs J. R., Davies N. B. 1984Behavioural ecology: an evolutionary approach Oxford, UK: Blackwell Scientific Publications [Google Scholar]
- Krebs J. R., Davies N. B. 1991Behavioural ecology: an evolutionary approach Oxford, UK: Blackwell [Google Scholar]
- Krebs J. R., Davies N. B. 1997An introduction to behavioural ecology, 4th edn Oxford, UK: Blackwell Scientific [Google Scholar]
- Lack D. 1954The natural regulation of animal numbers Oxford, UK: University Press [Google Scholar]
- Lack D. 1966Population studies of birds Oxford, UK: University Press [Google Scholar]
- Lack D. 1968Ecological adaptation for breeding in birds London, UK: Methuen [Google Scholar]
- Lande R. 1980Sexual dimorphism, sexual selection and adaptation in polygenic characters. Evolution 34, 292–305 (doi:10.2307/2407393) [PubMed] [Google Scholar]
- Lande R., Arnold S. J. 1983The measurement of selection on correlated characters. Evolution 37, 1210–1226 (doi:10.2307/2408842) [PubMed] [Google Scholar]
- Magrath R. A., Johnstone R. A., Heinsohn R. G. 2004Reproductive skew. In Ecology and evolution of cooperative breeding in birds (eds Koenig W., Dickinson J., editors. ), pp. 157–176 Cambridge, UK: University Press [Google Scholar]
- Mann J., Connor R. C., Tyack P. L., Whitehead H., editors. (eds) 2000Celacean societies Chicago, IL: University Press [Google Scholar]
- Maynard Smith J. 1964Group selection and kin selection. Nature 201, 1145–1147 (doi:10.1038/2011145a0) [Google Scholar]
- Maynard Smith J. 1965The evolution of alarm calls. Am. Nat. 99, 59–63 [Google Scholar]
- Maynard Smith J. 1974The theory of games and the evolution of animal conflicts. J. Theor. Biol. 47, 209–221 [PubMed] [Google Scholar]
- Maynard Smith J., Szathmary E. 1995The major transitions in evolution New York, NY: Freeman [Google Scholar]
- Medawar P. B. 1952An unsolved problem of biology London, UK: H.K. Lewis & Co [Google Scholar]
- Michod R. E., Roze D. 2001Cooperation and conflict in the evolution of multicellularity. Heredity 86, 1–7 (doi:10.1046/j.1365-2540.2001.00808.x) [PubMed] [Google Scholar]
- Okasha S. 2006Evolution and the levels of selection Oxford, UK: University Press [Google Scholar]
- Parker G. A. 1974Assessment strategy and the evolution of fighting behaviour. J. Theor. Biol. 47, 223–243 [PubMed] [Google Scholar]
- Pianka E. R. 1974Evolutionary ecology New York, NY: Harper and Row [Google Scholar]
- Queller D. C. 1992Quantitative genetics; inclusive fitness and group selection. Am. Nat. 139, 540–558 (doi:10.1086/285343) [Google Scholar]
- Ratnieks F. L. W. 1988Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am. Nat. 132, 217–236 (doi:10.1086/284846) [Google Scholar]
- Ratnieks F. L. W., Foster K. R., Wenseleers T. 2006Conflict resolution in insect societies. Ann. Rev. Entomol. 51, 581–608 (doi:10.1146/annurev.ento.51.110104.151003) [PubMed] [Google Scholar]
- Reeve H. K., Keller L. 1995Partitioning of reproduction in mother–daughter versus sibling associations: a test of optimal skew theory. Am. Nat. 145, 119–132 (doi:10.1086/285731) [Google Scholar]
- Rodseth L., Wrangham R. W., Harrigan A., Smuts B. B. 1991The human community as a primate society. Curr. Anthropol. 32, 221–254 (doi:10.1086/203952) [Google Scholar]
- Roughgarden J. 2009. In The genial gene: deconstructing Darwinian selfishness San Francisco, CA: University of California Press [Google Scholar]
- Roughgarden J., Oishi M., Akcay E. 2006Reproductive social behavior: cooperative games to replace sexual selection. Science 311, 965–969 (doi:10.1126/science.1110105) [PubMed] [Google Scholar]
- Rousset F., Ronce O. 2004Indirect fitness for traits affecting metapopulation demography. Theoret. Popul. Biol. 65, 127–141 (doi:10.1016/j.tpb.2003.09.003) [PubMed] [Google Scholar]
- Sachs J. L., Mueller U. G., Wilcox T. P., Bull J. J. 2004The evolution of cooperation. Quart. Rev. Biol. 79, 135–160 [PubMed] [Google Scholar]
- Smuts B. B. 1986aSexual competition and mate choice. In Primate societies (eds Smuts B. B., Cheney D. L., Seyfarth R. M., Wrangham W. R., Struhsaker T. T., editors. ). Chicago, IL: University of Chicago Press [Google Scholar]
- Smuts B. B. 1986bGender, aggression and influence. In Primate societies (eds Smuts B. B., Cheney D. L., Seyfarth R. M., Wrangham W. R., Struhsaker T. T., editors. ). Chicago, IL: University of Chicago Press [Google Scholar]
- Stearns S. C. 1976Life-history tactics: a review of the ideas. Quart. Rev. Biol. 51, 3–48 [PubMed] [Google Scholar]
- Tang-Martinez Z., Ryder T. B. 2005The problem with paradigms: Bateman’s world view as a case study. Integr. Comp. Biol. 45, 821–830 (doi:10.1093/icb/45.5.821) [PubMed] [Google Scholar]
- Taylor P. D. 1990Allele-frequency change in a class structured population. Am. Nat. 135, 95–106 (doi:10.1086/285034) [Google Scholar]
- Taylor P. D. 1996Inclusive fitness arguments in genetic models of behaviour. J. Math. Biol. 34, 654–674 (doi:10.1007/BF02409753) [PubMed] [Google Scholar]
- Taylor P. D., Frank S. A. 1996How to make a kin selection model. J. Theoret. Biol. 180, 27–37 (doi:10.1006/jtbi.1996.0075) [PubMed] [Google Scholar]
- Thresher R. E. 1984Reproduction in reef fishes Neptune City, NJ: T. F. H. Publications [Google Scholar]
- Trivers R. L., Hare H. 1976Haplo-diploidy and the evolution of the social insects. Science 191, 249–263 (doi:10.1126/science.1108197) [PubMed] [Google Scholar]
- Vehrencamp S. L. 1983aA model for the evolution of despotic versus egalitarian societies. Anim. Behav. 31, 667–682 (doi:10.1016/S0003-3472(83)80222-X) [Google Scholar]
- Vehrencamp S. L. 1983bOptimal degree of skew in cooperative societies. Am. Zool. 23, 327–335 [Google Scholar]
- West S. A. 2009Sex allocation Princeton, NJ: University Press [Google Scholar]
- West S. A., Griffin A. S., Gardner A. 2007Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. J. Evol. Biol. 20, 415–432 (doi:10.1111/j.1420-9101.2006.01258.x) [PubMed] [Google Scholar]
- West S. A., Griffin A. S., Gardner A. 2008Social semantics: how useful has group selection been? J. Evol. Biol. 21, 374–385 [Google Scholar]
- West S. A., Mouden C. E., Gardner A. In press Social evolution theory and its application to the evolution of cooperation in humans. [Google Scholar]
- Whiten A., Byrne R. W. 1997Machiavellian Intelligence II Cambridge, UK: University Press [Google Scholar]
- Williams G. C. 1957Pleiotropy, natural selection, and the evolution of senescence. Evolution 11, 398–411 (doi:10.2307/2406060) [Google Scholar]
- Williams G. C. 1966aAdaptation and natural selection: a critique of some current evolutionary thought Princeton, NJ: University Press [Google Scholar]
- Williams G. C. 1966bNatural selection, the costs of reproduction, and a refinement of Lack’s principle. Am. Nat. 100, 687–690 (doi:10.1086/282461) [Google Scholar]
- Wilson E. O. 1971The insect societies Cambridge, MA: Belknap Press [Google Scholar]
- Wilson E. O. 1974Sociobiology, the new synthesis Boston, MA: Harvard University Press [Google Scholar]
- Wilson D. S. 1980The natural selection of populations and communities Menlo Park, CA: Benjamin Cummings [Google Scholar]
- Wilson E. O., Bossert W. H. 1971A primer of population biology Sunderland, MA: Sinauer Associates [Google Scholar]
- Wilson D. S., Wilson E. O. 2007Rethinking the theoretical foundation of sociobiology. Quart. Rev. Biol. 82, 327–348 [PubMed] [Google Scholar]
- Wolf J. B., Brodie E. D., Moore A. J. 1999Interacting phenotypes and the evolutionary process. II. Selection resulting from social interactions. Am. Nat. 153, 254–266 (doi:10.1086/303168) [PubMed] [Google Scholar]
- Wolff J. O., Sherman P. W. 2007Rodent societies as model systems. In Rodent societies (eds Wolff J. O., Sherman P. W., editors. ). Chicago, IL: University Press [Google Scholar]
- Woolfenden G. E., Fitzpatrick J. W. 1984The Florida scrub jay: demography of a cooperative-breeding bird Princeton, NJ: University Press [Google Scholar]
- Wrangham R. W., Jones J. H., Laden G., Pilbeam D., Conklin-Brittain N. 1999The raw and the stolen—cooking and the ecology of human origins. Curr. Anthropol. 40, 567–594 (doi:10.1086/300083) [PubMed] [Google Scholar]
- Zahavi A. 1975Mate selection: a selection for a handicap. J. Theoret. Biol. 53, 205–214 (doi:10.1016/0022-5193(75)90111-3) [PubMed] [Google Scholar]
- Zhou W.-X., Sornette D., Hill R. A., Dunbar R. 2004Discrete hierarchical organisation of social group sizes. Proc. R. Soc. Lond. B 272, 439–444 (doi:10.1098/rspb.2004.2970) [PMC free article] [PubMed] [Google Scholar]