A striking thesis in the 'Mating Mind' (Miller, 2000) is that humans became brainy through sexual selection. An examination of the various processes that Miller identifies leads to the conclusion that his arguments do not support this thesis.
2. Before considering the arguments it is fair to point out that the book was not written for a professional scientific audience but, rather, the audience of 'Walking with Dinosaurs'. Maybe the art of popular science writing has moved on but I longed for the clarity of argument and metaphor in 'The Selfish Gene' -- it's a point that Miller is sensitive to too, "Scientists learn to derogate ... popular science books that try to present serious ideas in attractive form." [P424] so I will just pick out the ideas.
3. 'The Mating Mind' is structured into three parts: a good popular introduction to natural and sexual selection, three chapters on the mechanics of how sexual selection might grow a brain, and six chapters on the implications of a sexually selected brain. The thesis turns on the arguments in the middle part. Miller identifies three textbook processes of sexual selection: Fisherian runaway sexual selection, selection for fitness indicators, and exploitation of sensory biases.
4. Runaway sexual selection certainly provides a conceivable route to bigger brains (and initially attracted Miller to the field) however there are also serious problems with it as an explanation. Through accident, females choose males who are witty (the connection between wit and brain size is assumed and unsubstantiated), her sons are then more likely to be witty and mate also, thus establishing a positive feedback cycle for a runaway wit. With feathers, it is easy to imagine that the psychological machinery necessary to detect a well-maintained plumage could produce a super-normal response to a peacock's trail; it is less easy to imagine that the apparatus necessary to detect wit would know a super-normal one if it saw one. It is a prerequisite for runaway selection that females respond preferentially to a super-normal stimulus, otherwise the chain of positive-feedback will be broken. If a female's wit detectors could respond to a super-normal stimulus, and wit is correlated with brain size, then the theory predicts that males and only males would have big brains (Lande's law of equal inheritance notwithstanding).
5. Miller's attempt to reconstruct the theory requires that female humour detectors develop with male wit, upon the assumption that it takes the same machinery to detect wit as it does to produce it. Even if such female development was cost free (which it is not, the human brain has a fixed cost of its extended development time as well as consuming some 30% of the resting basal metabolic rate) runaway sexual selection can not work within such a scheme -- with no super-normal response, females without witty genes are unable to discriminate between normal and super wits. Having journeyed though a series of false starts, such considerations force Miller to finally discard runaway sexual selection, his most promising argument, as a sexual selection process that could furnish humans with big brains.
6. Fitness indicator theory is often invoked to argue, amongst many other traits, that mate choice is influenced by facial symmetry, being an indicator of a well tuned developmental system; since the brain is a complex system it too is susceptible to developmental mishaps, and its outward exposure through behaviour offers an indicator upon which mate choice can act. Such a scheme can establish a signal but not drive it in any particular direction. Miller argues that a process like Zahavi's handicap theory (for an indicator to be honest it should be costly to produce, otherwise it will be faked and then ignored) could encourage larger brains for fitter males; such brains would be more costly to maintain while enabling more complex displays, like wit. As such, indicator theory is certainly useful for explaining female adaptations to detect certain male behavioural traits (e.g. vocalisations), however it is not clear that (for handicap theory just as runaway theory) it is evolutionarily stable for females to pay the cost of a bigger brain to drive the evolution of costly mental male traits (wit?).
7. Sensory bias theory also provides arguments in favour of the shaping of brains by mate choice. If there exists an unexploited sensory preference in either males or females then it would be predicted that ornaments, physical or mental, evolve to stimulate that preference. Again this theory is useful for explaining the establishment of particular traits rather than providing the directing force of evolution that a larger brain would require.
8. Considering all three mechanisms that Miller proposes, and their interaction, a reasonable conclusion might be that mate choice can certainly shape the evolution of a brain (uncontroversial) but offers little insight into why humans have big brains (the implicit thesis). This is the conclusion that Miller arrives at too, "Of course, about 90 percent of our psychological adaptations evolved through standard natural and social selection," [P133] although I am not sure where the 90 percent figure comes from.
9. The remaining 300 pages of the 'Mating Mind' explore a large number of evolutionary just so stories full of amusing anthropological anecdotes covering topics such as art, morality, sport, dance, language, poetry, music and creativity. Some of the stories are old and some new, however Miller has a habit of making jarring statements, "An Olympic medal in swimming can be more sexually attractive than erotic dancing because swimming is a better fitness indicator," [P256] or, "Perhaps stripes became popular sexual ornaments across many species because stripes are optimal stimuli for activating the visual cortex," [P144] (it is neither clear that stripes are popular sexual ornaments, they are more often explained as disruptive camouflage or warning patterns, nor that they excite the visual system more than any other high contrast signal).
10. Miller has certainly offered a great deal of creative speculation in the construction of stories about how all sorts of human capacities have been shaped by the forces of selection, especially sexual selection. However, despite all its words, the 'Mating Mind' lacked the wit to woo over its central thesis that because of sexual attraction humans are brainy. Indeed, it was nice of the publishers to include a recent photograph of the author no longer sporting his shoulder-length wavy locks.
Miller,G.F. (2000) The Mating Mind: How Sexual Choice Shaped the Evolution of Human Nature. Heinemann
Miller,G.F. (2001) Precis of: The Mating Mind: How Sexual Choice Shaped the Evolution of Human Nature. PSYCOLOQUY 12(008) http://www.cogsci.soton.ac.uk/cgi/psyc/newpsy?12.008