From genes to religion, and back: A review by Bernard Crespi: Levels of Selection in Evolution. Edited by Laurent Keller. Princeton University Press, Princeton. 1999. 272 pp. ISBN: 0 691 00703 9 (Cloth) $59.50; ISBN: 0 691 00704 7 (Paper) $16.95.

During my last meeting with W. D. Hamilton, he told me of his new theory for the origins of religions. By his hypothesis, many religions were started by persons who were able by force of personality to persuade or cajole members of a social group into becoming more co-operative among themselves, through enhancement of within-group unity. Some of the resulting increase in available group resources would be funnelled to the religious leaders, and the lion’s share remained with the newly devout, so all benefit. Natural selection among religions then promotes assimilation at best, or annihilation at worst, of competitors while, within religious groups, outspoken heretics are burned in this world and quiet ones presumably roast in the next. This book has as its goal the analysis of how such conflict and co-operation between and within levels of selection has given rise to genes, cells, multicellular organisms and social groups, and how the properties of these units, be they transposons, cancer, egg-laying hymenopteran workers or religious beliefs, have been shaped by multilevel selection. The book begins with overviews of multilevel selection theory (Reeve and Keller, and Leigh), and ends with a review of selection among cell and species lineages (Nunney). In between, we learn about current theory for the origin of life and cells (Szathmáry), sex and multicellularity (Michod), co-operation among insects (Keller and Reeve) and culture in humans (Maynard Smith), and how in each case conflicts have almost miraculously given rise to new, integrated levels and forms of biological organization. We marvel at the running battles and uneasy alliances and truces between the genes in genomes (Pomiankowski), the two sexes (Lessells), parents and offspring (Godfray), vertebrates in social groups (Kitchen and Packer) and species in communities (Herre), each a consequence of genetic conflict and confluence of interest. In the end, we are left with strong traces of the unity of life’s processes: how competition can generate co-operation which in turn creates new opportunities for cheating, and how conflicts of interest are resolved or not by force, policing, coercion, bribery or self-restraint in the genome or savanna. The lofty goals of this book are nicely addressed by a brilliant collection of authors, each of whom provides a well-written and scholarly review. As a result, the book should be of considerable interest to all evolutionary biologists, from miners of the gene banks to gene-culture coevolutionists. But forgive me if I am left wanting more, and left wondering if one of the motivations of this book, the crucifixion of group selection’s passionate adherents (see Pollock, 1989; Sober & Wilson, 1998), has not taken on undue fervour. Where in this book are the unrelated cofounding ants that provide such a beautiful example of classical group selection ( Rissing et al., 1989 )? Where is the myxoma virus evolving lower virulence by group selection (see Lewontin, 1970; also Herre, 1993)? And where are Hamilton’s (1975) and Alexander’s (1989) arguments that group selection has driven much of human evolution? There are new insights from these phenomena and views, even if a between-group perspective is mathematically equivalent to the spectacularly successful gene-centred dogma. Make no mistake, this is a stunning, remarkable and timely book. But it could have taken its subject much further by including such a top-down group-selectionist perspective, and by exploring the convergences and parallels between formerly disparate situations. What are the similarities and differences in why and how division of labour evolves, among genes, cells, organisms and mutualistic species? Is it coincidence that division into germ and soma in primitive multicellular forms, and division of social insect colonies into morphologically distinct queen and worker castes, occur at similar colony sizes? Are the mitochondria that cause cytoplasmic male sterility usefully considered eusocial? When do we expect and find interminable arms races between conflicting elements, instead of stable polymorphism maintained by opposing selection at different levels, or one party taking all? A synthesis chapter at the end of this book could have addressed these questions and more by drawing on material scattered throughout its pages, and set the course for future studies. But then, perhaps it is enough that the book will stimulate another towards this goal. In the mountains of Switzerland live colonies of ants that are apparently infected by a virus causing them to lose their kin recognition abilities. These colonies send forth wandering missionaries who spread the virus which, like a religion, leads to a unity born from sharing of horizontally transmitted elements rather than sharing of genes by kinship. The memes in this book deserve to be similarly spread, but also probed and questioned. Only by this process will we come to understand how life, genomes, humans and all other levels and units of selection have evolved.

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