Genes, Games and the Sexes Natural Selection Selects the Fittest, but the the Sexes, Rather Than Competition

NATURE|Vol 458|30 April 2009 SPRING BOOKS OPINION

Genes, games and the sexes Natural selection selects the fittest, but the the sexes, rather than competition. fittest need not be selfish, according to two new The two tiers break the genetic deter- books. Starting from different backgrounds, minism implicit in single-tier evo- evolutionary biologist Joan Roughgarden lutionary models by granting and anthropologist and primatologist more plasticity to individu- Sarah Blaffer Hrdy converge on als of both sexes when that message regarding sex and bargaining. The main reproduction. innovation, however, The authors also converge concerns the bar- on another point. Theorists gaining process go wrong less because of the itself, and involves assumptions they know they game theory. are making, and more because of Game theory tra- the ones they don’t. Roughgarden ditionally analyses an interac- shows how modellers can agree tion between two players; in about the maths and the results of this case, a male and a female. particular models, yet, thanks to Mathematician John Nash rival metaphysical assumptions, developed its principal theo- still disagree fiercely about the rems in the 1950s, including verbal narratives they attach to the concept of Nash equi- the models. For Blaffer Hrdy, libria, whereby neither player the problem is simpler: it stems in a game can do better by largely from the sex of the research- changing strategies. John ers. She is interested in primate, ape and human Maynard-Smith introduced mothers. Early researchers were mostly men, game theory to biology — by but recently, large numbers of women scientists between the sexes. Since Angus Bateman’s fly focusing on fitness pay-offs to interacting indi- have been asking new questions and noticing experiments, females have been portrayed as viduals in evolving populations, he attempted different things. investing more in their gametes, and therefore to capture what happens at both the individual The Genial Gene is the being choosy about their and population levels. latest round in the debate The Genial Gene: Deconstructing mates. Males invest little Roughgarden complains that Maynard- between Roughgarden’s Darwinian Selfishness in their gametes, mate Smith introduced only the competitive half of social-selection theory by Joan Roughgarden with as many females as game theory. She introduces the cooperative and sexual-selection University of California Press: 2009. possible and compete with half, based on organisms communicating, bar- theory. Many have con- 272 pp. $24.95, £14.95 other males to do so. But gaining and allocating side-payments to each tributed to it, but I shall Roughgarden proposes other. Cooperation between the sexes leads concentrate on Rough- Mothers and Others: The Evolutionary that anisogamy originally to Nash bargaining solutions, not to Nash garden’s responses to Origin of Mutual Understanding evolved to ensure contact competitive equilibria. Different behavioural her most thoughtful by Sarah Blaffer Hrdy between male and female solutions at the developmental tier then trans- critic, zoologist Tim Belknap/Harvard University Press: gametes. Pursuing this to late into alternative evolutionary outcomes. Clutton-Brock. 2009. 432 pp. $29.95, £19.95, €21.00 the genetic and cellular As someone who works on the developmen- Roughgarden starts levels, she generates an tal process of niche construction, whereby by differentiating sex from the terms male and alternative theory of reproduction. the actions of organisms generate feedback female. Sex is the combining of gametes from Roughgarden’s approach includes both in evolution by modifying natural selection two parents. The production of large gametes by developmental and evolutionary processes. She pressures in environments, I like Roughgar- females and small ones by males — anisogamy also explains reproductive behaviour as a proc- den’s two tiers. — is thought to be responsible for competition ess of bargaining and communication between That does not mean Roughgarden is correct,

Your Inner Fish: A Journey Into the Splendors and Miseries of the Brain: 3.5-Billion-Year History of the Human Body Love, Creativity and the Quest for Human by Neil Shubin (Penguin, £9.99) Happiness Neil Shubin “delves into human gristle, by Semir Zeki (Wiley-Blackwell, £16.99) interpreting the scars of billions of years of Semir Zeki examines the brain’s ability to seek evolution that we carry inside our bodies”, wrote knowledge and form concepts in creative areas Carl Zimmer in his review (Nature 451, 245; such as music, art and literature. He gives us an 2008). “The simple, passionate writing may insight into how the brain functions, what this turn more than a few high-school students into means for happiness, and how even negative aspiring biologists.” emotions can be a source of creativity.

nor is sexual selection wrong. The awkward data for sexual-selection theory are not yet Managing nature as Earth warms decisive. Also, as the mutual concessions and careful arguments between Clutton-Brock and Climate change is transforming the world permanent species loss: “At best, we seem to be Roughgarden show, there is often little empirical as we know it. It disrupts biological clocks, witnessing wholesale changes in nearly every ground between them. Sexual selection starts pushes species to different latitudes and alti- ecosystem on Earth. At worst, we may be wit- with competition, but admits cooperation as a tudes and shrinks biological diversity. It also nessing the extinction of life as we’ve known by-product. Social selection starts with mutual challenges humanity to question its relation- it.” The former statement is true, but the lat- regard and cooperation, but admits competi- ship with Earth; global warming is the antith- ter is extreme. In Yosemite and Yellowstone tion when bargains break down. To compete, esis of responsible stewardship. We look to national parks in the United States, Barnosky selfish genes must cooperate. To cooperate, science for guidance on how to turn back the reports changes in the composition and loca- genial genes must compete. It is difficult to sort hand of humankind, but it can provide only tions of species. But these places are not yet between them. But Roughgarden succeeds in partial answers. Science is imperfect, unfeeling experiencing profound species loss. The pub- re-opening issues long thought closed. and slow compared with the steady rise of the lic needs to understand how climate change is Blaffer Hrdy’s book is narrower in scope but global thermometer. altering life on Earth and that such threats are also provocative. She argues that unlike other Into this mix of responsibilities, human very serious, but I worry that scientists risk a apes, Homo sapiens could never have evolved identity and scientific uncertainty comes backlash if their primary message is the worst- if human mothers had been required to raise Anthony Barnosky’s new case scenario. their offspring on their own. Human infants book. Unlike other accounts Heatstroke: Nature in an Age Climate is a major deter- are too helpless and too expensive in their of climate change, Heatstroke of Global Warming minant of where a species demands for care and resources. So human looks at the issue from the by Anthony D. Barnosky lives and how species inter- females have to line up helpers — sometimes perspective of plants and Island Press: 2009. act. Biologists also know extending beyond their own kin — to raise animals. He introduces us to 288 pp. $26.95, £16.99 that climate change will their young. That requires both males and the Irish elk, the pack rat and outpace evolution for a great females to invest heavily in social skills for bar- biologists such as Jim Patton, a professor at the number of organisms, although perhaps not gaining with other members of their groups. University of California, Berkeley — species for bacteria, viruses and some insects. Bar- Blaffer Hrdy suggests that females in ances- and people that are helping to reveal the biotic nosky describes the result as “like taking a tral hunting and gathering groups may have signature of climate change. color portrait and rendering it in black and thrived because they were free to be flexible in Using many case studies, Barnosky explains white, or stripping all the harmonic notes this way. Female flexibility was reduced when how worldwide changes in climate are altering out of a symphony”. But not all organisms humans established settlements requiring male the reproductive rates, timing of breeding and will be affected negatively; some will flour- coalitions to defend them, probably leading to living conditions of creatures. He is spot on in ish. We need to figure out if climate change greater control of females by males. his description of new and exciting scientific is eroding the species that humans value and More rides on these books than the rela- findings, portraying them in an accessible and replacing them with those that cause harm. tionship between the sexes. In her last chapter, compelling way. Such findings include pre- And we must identify which species will Roughgarden distinguishes between Charles dictions of the existence of climates with no be most affected, which ones will muddle Darwin’s repeatedly verified theory of “descent modern counterparts within 100 years, and a through and which will rise to prominence. with modification”, versus Herbert Spencer’s careful reconstruction of past climatic effects This information will help us to determine unverified notion of the “survival of the fittest”. on small mammal communities. The reader what sort of biotic world climate change is It was Spencer who encouraged social Darwin- becomes engulfed in a world of scientific creating and what steps we might take to ism. Clearly we can go wrong if we attach faulty discovery, searching through bones, walking affect that change. metaphors and narratives to evolutionary the- transects to record the numbers of animal and If we heed Barnosky’s call to care about the ory. The most refreshing aspect of both these plant species, and looking back across history impacts of climate change, we must reduce books is the challenges they offer to what we to reveal the influence of climate on life. the greenhouse gases that we emit into the thought we already knew. ■ This is not a happy book. Barnosky sounds atmosphere and capture those already there. John Odling-Smee is an emeritus fellow at the alarm about the biological effects of We could also help some species out. Mansfield College, University of Oxford, Oxford climate change, but his gloom and doom Heatstroke describes the strategy of assisted OX1 3TF, UK. message could alienate readers. He repeat- migration — helping a species to relocate to e-mail: [email protected] edly asserts that climate change will lead to a place where it might be expected to thrive.

The Ten Most Beautiful Experiments The Silent Deep: The Discovery, Ecology, by George Johnson and Conservation of the Deep Sea (Vintage, £8.99) by Tony Koslow George Johnson’s book covers ten of the most (Univ. Chicago Press, $22.50) historically significant experiments in science — Describing the huge variety of ocean life “with including Isaac Newton’s prisms and Ivan Pavlov’s textbook depth on all aspects of deep-sea dogs. He does justice to each experiment, showing science and conservation,” (Mark Schrope, how ingenious and elegant it was — and how the Nature 447, 909–910; 2007), Tony Koslow process of experimenting may be as important as examines how oceanography has developed and the conclusion. discusses human exploitation of the seas.