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Clash of the Titans

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Clash of the Titans Fall Focus on Books Clash of the Titans The Social Conquest of Earth. Edward E. O. Wilson defends the notion manipulation (Reeve and Keller 1997). O. Wilson. W. W. Norton (Liveright), that humans are eusocial by recalling Therefore, he writes in Social Conquest 2012. 352 pp., illus. $27.95. (ISBN that early hominins adopted collec- on page 144, 978-0-87140-413-8 hardcover). tive child rearing in a fixed location defended by some group members The origin and evolution while others dispersed to forage, scav- of eusocial insects can be dward O. Wilson is an expert on enge, or hunt (Burkart et al. 2009, viewed as processes driven by Esocial insects, but early in his Chapais 2009, Hrdy 2009, Gintis and individual-level natural selec- career, he addressed human sociality. van Schaik 2012, Pagano 2012). All tion. It is best tracked from His book Sociobiology (1975) initi- known eusocial species went through queen to queen from one gen- ated a field that has become a major a similar stage of collective brood eration to the next, with the research area in the behavioral sci- rearing. With alloparenting (the pro- workers of each colony pro- ences and included a controversial vision of parental care by individuals duced as phenotypic exten- chapter on human social evolution. other than the recipient’s biological sions of the mother queen.… In The Social Conquest of Earth, E. O. parent) in a fixed location established, The defending worker is part Wilson updates his earlier ground- E. O. Wilson argues, there is strong of the queen’s phenotype, as breaking treatment of Homo sapiens. selection on traits that improve coop- teeth and fingers are part of He stakes out a strong position on erative behavior, which would culmi- your own phenotype. the levels-of-selection debate, rejects nate in eusociality. inclusive-fitness theory, and redefines To supporters of inclusive-fitness eusociality to include Homo sapiens. Clash of the Titans theory, these statements are outrageous The book is based on several articles E. O. Wilson’s theory thus diverges and strike a blow at population genet- published in professional journals, from the widely held view that ics itself. E. O. Wilson and his coau- including those of E. O. Wilson and human sociality can be explained by thors simply could not be believed. Hölldobler (2005); D. S. Wilson and invoking Hamilton’s (1964a, 1964b) Because of its visibility in the journal Wilson (2007); E. O. Wilson (2008); inclusive-fitness theory. Inclusive- Nature, Nowak, Tarnita, and Wilson’s and, most prominently, Nowak, Tar- fitness theory shows that a person- (2010) critique of inclusive-fitness the- nita, and Wilson (2010). ally costly behavior can spread if the ory has drawn the collective ire of a E. O. Wilson’s work has stirred up behavior offers sufficient benefits to host of prominent population bio- a vigorous—and sometimes highly genetically related individuals. E. O. logists. Nature subsequently published intemperate—debate that has shaken Wilson now rejects this theory, writ- several brief communications in which the very foundations of population ing in The Social Conquest of Earth Nowak, Tarnita, and Wilson’s (2010) biology. In this review, I address the (p. 51) that claims were vigorously rejected, one of fundamental issues involved and sug- which had 134 signatures (Abbot et al. gest a resolution that may be accept- The foundations of the gen- 2011, Boomsma et al. 2011, Strass- able to both sides of this clash of the eral theory of inclusive fitness man et al. 2011). Rousset and Lion Titans. based on the assumptions of (2011) accused Nowak, Tarnita, and E. O. Wilson’s treatment of euso- kin selection have crumbled, Wilson (2010) of saying nothing new ciality in The Social Conquest of Earth while evidence for it has grown and of using “rhetorical devices.” They is a major innovation. A species is equivocal at best.… Inclusive- then attacked the journal Nature itself, customarily defined as eusocial if it fitness theory, often called kin arguing (p. 1390) that is composed of colonies in each of selection theory, is both math- which there is a reproductive divi- ematically and biologically The publication of this article sion of labor, as in the cases of social incorrect. illustrates more general con- bees and termites, in whose societies cerns about the publishing a single or a few individuals (queens E. O. Wilson favors the more tradi- process.… Nature’s extravagant and their mates) reproduce and other tional individual-fitness-maximization editorial characterization of the castes do not. In humans, by contrast, model in understanding advanced paper as “the first mathemati- adults are generically reproductives. eusociality, which is defined as occur- cal analysis of inclusive-fitness ring if the workers are sterile or if theory” recklessly tramples on worker reproduction is suppressed nearly 50 years of accumulated doi:10.1525/bio.2012.62.11.8 by policing (Frank 1995) or queen knowledge. www.biosciencemag.org November 2012 / Vol. 62 No. 11 • BioScience 987 Fall Focus on Books In passing sentence on The Social cooperate with other genes in promot- only replicators—the sole entities that Conquest of Earth, Dawkins (2012) ing the success of the genome as a are preserved in the evolutionary pro- concluded, “To borrow from Dorothy whole. Of course, the same argument cess. Individuals, in Dawkins’s view, Parker, this is not a book to be tossed applies to inclusive fitness at the level are simply vehicles that genes build to lightly aside. It should be thrown with of the individual in an advanced euso- shuttle themselves successfully from great force.” cial colony. one body to another. Unlike genes, By contrast, some supporters of genotypes and groups of genotypes Hamilton’s rule and its limitations Hamilton’s rule take the notion that are transitory in sexually reproducing Kin selection theory holds that an genes maximize inclusive fitness as the species, he argues; they are broken up allele for helping another will spread very core of evolutionary biological and reorganized continually by sexual if a mathematical inequality known theory. For instance, West and col- recombination. as Hamilton’s rule holds. The rule says leagues (2011, p. 233) explained that But, in fact, genomes are replicators that the allele will spread if the benefit “since Darwin, the only fundamen- as much as genes are, and the pheno- from the help, in terms of fitness to tal change in our understanding of types that genomes control include the recipient, multiplied by the recipi- adaptation has been Hamilton’s devel- metazoan individuals and social ent’s degree of relatedness to the bene- opment of inclusive-fitness theory.… groups, such as E. O. Wilson’s eusocial factor, is greater than the cost to the The idea [is] that organisms can be colonies and human societies. This is benefactor. Degree of relatedness is usu- viewed as maximizing agents.” so because a gene promotes the fitness ally understood as the probability that of its host only if it is complemented an allele is identical in the benefactor by a well-orchestrated configura- and the recipient by common descent. tion of genes with which it interacts In box 1, I derive a generalization of (Sober and Lewontin 1982, Hammer- Hamilton’s rule that relaxes key, usu- stein and Leimar 2006, Noble 2011). ally unstated (and often implausible) Species-defining loci in the genome assumptions about the costs and ben- are therefore necessarily homozygous efits of helping behavior to relatives and identical in both members of a versus nonrelatives that are essential mating pair so that crossing over and in the derivation of the standard form meiosis do not destroy the integrity of of Hamilton’s rule. My generalization these complementary loci. Of course, makes clear that an allele that causes this assertion must be qualified to deal helping can spread even if it reduces with introns and exons, dominance, the mean fitness of the population. maternal–paternal conflicts, auto- It follows that Hamilton’s rule does The technical literature says other- somal and sex-linked chromosomes, not explain eusociality and, indeed, is wise. The conditions under which evolu- fitness-neutral base replacements, and focused on what may be a minor subset tionary dynamics lead to inclusive-fitness the like. But these adjustments do not of the biological conditions that favor maximization have been carefully stud- weaken the integrity of the genome. the fitness of a gene and promote coop- ied by Alan Grafen and his fellow We may call the genes that support eration in metazoan cells and social researchers, who have shown that this phenotypic commonality the spe- species (Hammerstein and Leimar Darwinian population dynamics entail cies’ core genome. The core genome is a 2006); the absence of inclusive-fitness- inclusive-fitness maximization at the replicator and, therefore, subject to the maximizing behavior even when Ham- individual and gene levels, but only laws of natural selection. ilton’s rule is satisfied is widely observed assuming that fitness effects are addi- in social species (Queller and Strass- tive (Grafen 1999, 2006, Gardner and Levels of selection mann 1998, Nonacs 2011). The cooper- Welsh 2011, Gardner et al. 2011). But, In urging a harmonious resolution ation of genes in metazoan cells (Leigh of course, the additivity assumption to the clash of the Titans, Okasha 1971) and in social groups (Bowles and implies that a = = 0 in the general- (2012) suggested that the level of selec- Gintis 2011) is therefore effected by ized Hamilton rule, which is expressed tion is a matter of personal choice or selection at a higher level than the gene in equations 3 and 5 in box 1, in ease of analysis, because mathemati- itself.
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