Spring Books

Nature 458, 1111-1112 (30 April 2009) | doi:10.1038/4581111a; Published online 29 April 2009

Genes, games and the sexes

John Odling-Smee1

BOOK REVIEWEDThe Genial Gene: Deconstructing Darwinian Selfishness

by Joan Roughgarden

University of California Press: 2009. 272 pp. $24.95, £14.95

BOOK REVIEWEDMothers and Others: The Evolutionary Origin of Mutual Understanding

by Sarah Blaffer Hrdy

Belknap/Harvard University Press: 2009. 432 pp. $29.95, £19.95, euro21.00

Genes, games and the sexes

Natural selection selects the fittest, but the fittest need not be selfish, according to two new books. Starting from different backgrounds, evolutionary biologist Joan Roughgarden and anthropologist and primatologist Sarah Blaffer Hrdy converge on that message regarding sex and reproduction.

The authors also converge on another point. Theorists go wrong less because of the assumptions they know they are making, and more because of the ones they don't. Roughgarden shows how modellers can agree about the maths and the results of particular models, yet, thanks to rival metaphysical assumptions, still disagree fiercely about the verbal narratives they attach to the models. For Blaffer Hrdy, the problem is simpler: it stems largely from the sex of the researchers. She is interested in primate, ape and human mothers. Early researchers were mostly men, but recently, large numbers of women scientists have been asking new questions and noticing different things.

The Genial Gene is the latest round in the debate between Roughgarden's social-selection theory and sexual-selection theory. Many have contributed to it, but I shall concentrate on Roughgarden's responses to her most thoughtful critic, zoologist Tim Clutton-Brock.

Roughgarden starts by differentiating sex from the terms male and female. Sex is the combining of gametes from two parents. The production of large gametes by females and small ones by males — anisogamy — is thought to be responsible for competition between the sexes. Since Angus Bateman's fly experiments, females have been portrayed as investing more in their gametes, and therefore being choosy about their mates. Males invest little in their gametes, mate with as many females as possible and compete with other males to do so. But Roughgarden proposes that anisogamy originally evolved to ensure contact between male and female gametes. Pursuing this to the genetic and cellular levels, she generates an alternative theory of reproduction.

Roughgarden's approach includes both developmental and evolutionary processes. She also explains reproductive behaviour as a process of bargaining and communication between the sexes, rather than competition. The two tiers break the genetic determinism implicit in single-tier evolutionary models by granting more plasticity to individuals of both sexes when bargaining. The main innovation, however, concerns the bargaining process itself, and involves game theory.

Game theory traditionally analyses an interaction between two players; in this case, a male and a female. Mathematician John Nash developed its principal theorems in the 1950s, including the concept of Nash equilibria, whereby neither player in a game can do better by changing strategies. John Maynard-Smith introduced game theory to biology — by focusing on fitness pay-offs to interacting individuals in evolving populations, he attempted to capture what happens at both the individual and population levels.

Roughgarden complains that Maynard-Smith introduced only the competitive half of game theory. She introduces the cooperative half, based on organisms communicating, bargaining and allocating side-payments to each other. Cooperation between the sexes leads to Nash bargaining solutions, not to Nash competitive equilibria. Different behavioural solutions at the developmental tier then translate into alternative evolutionary outcomes. As someone who works on the developmental process of niche construction, whereby the actions of organisms generate feedback in evolution by modifying natural selection pressures in environments, I like Roughgarden's two tiers.

That does not mean Roughgarden is correct, nor is sexual selection wrong. The awkward data for sexual-selection theory are not yet decisive. Also, as the mutual concessions and careful arguments between Clutton-Brock and Roughgarden show, there is often little empirical ground between them. Sexual selection starts with competition, but admits cooperation as a by-product. Social selection starts with mutual regard and cooperation, but admits competition when bargains break down. To compete, selfish genes must cooperate. To cooperate, genial genes must compete. It is difficult to sort between them. But Roughgarden succeeds in re-opening issues long thought closed.

Blaffer Hrdy's book is narrower in scope but also provocative. She argues that unlike other apes, Homo sapiens could never have evolved if human mothers had been required to raise their offspring on their own. Human infants are too helpless and too expensive in their demands for care and resources. So human females have to line up helpers — sometimes extending beyond their own kin — to raise their young. That requires both males and females to invest heavily in social skills for bargaining with other members of their groups. Blaffer Hrdy suggests that females in ancestral hunting and gathering groups may have thrived because they were free to be flexible in this way. Female flexibility was reduced when humans established settlements requiring male coalitions to defend them, probably leading to greater control of females by males.

More rides on these books than the relationship between the sexes. In her last chapter, Roughgarden distinguishes between Charles Darwin's repeatedly verified theory of “descent with modification”, versus Herbert Spencer's unverified notion of the “survival of the fittest”. It was Spencer who encouraged social Darwinism. Clearly we can go wrong if we attach faulty metaphors and narratives to evolutionary theory. The most refreshing aspect of both these books is the challenges they offer to what we thought we already knew.

  1. John Odling-Smee is an emeritus fellow at Mansfield College, University of Oxford, Oxford OX13TF, UK.
    Email: john.odling-smee@anthro.ox.ac.uk

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