In this review I present basic arguments for why Miller's theory of human mental evolution is unlikely to be correct. First, his contention that uniquely human intellectual traits are sexually selected fitness indicators is largely unsupported by empirical evidence. Second, I contend that more traditional survival selection accounts of human brain evolution can be rescued from his criticisms and stand as adequate explanations for human intelligence. Despite these disagreements with the author, I strongly recommend the book to any readers interested in evolutionary psychology.
2. Miller employs two general types of arguments to support his theory. Throughout the book he uses a form of negative argumentation in which he contends that natural selection for survival ability is inadequate to explain the evolution of human mental capacities such as language, art, creativity, and humour. Given the failure of natural selection to explain such phenomena, he asks, why not try out sexual selection as an alternative explanation? He then employs a more positive form of argumentation in which he contends that many human mental capacities show signs of being sexually selected fitness indicators. I will address the positive argument first, since it is on this argument that the theory must ultimately stand or fall.
3. Much of the first five chapters of the book explore extant models of sexual selection for the purpose of finding sexual choice mechanisms that might explain the evolution of human intelligence. These chapters are the strength of the book. The explanations of these processes are clear and accessible, albeit stripped of the technical details of the primary literature. For the non biologist, I think these chapters make an excellent introduction to the history and status of sexual selection theory.
4. Miller reviews three primary models of sexual selection: Fisherian runaway selection, sensory bias theory, and the costly signaling theory of fitness indicators. The first two models he dismisses as largely inadequate to account for the directional trend toward greater complexity and intelligence in human mental evolution - runaway processes, for instance, could just as likely produce mate preferences for lower intelligence as for higher. This leaves costly signaling theory. Fitness indicators are traits that are so costly to produce that only highly fit individuals can afford to display them. Only those male peacocks that are relatively free of harmful mutations and able to resist the debilitating effects of parasites, for instance, are thought to be able to grow the largest and brightest tails that are most attractive to peahens. Although Miller argues that all three sexual choice processes have likely shaped human mental traits, it is clear that the fitness indicator model does most of the work in his theory of brain evolution.
5. The fitness indicator theory of brain evolution entails that human brain expansion and uniquely human intellectual capacities have no function other than as courtship lures that signal genetic fitness. As Miller states, "our brains are different from other apes not because extravagantly large brains helped us to survive or to raise offspring, but because such brains are simply better advertisements of how good our genes are" (p. 104). The basic idea here is that skills such as language, art, humour, and creative intelligence are so subtle and complex that they are vulnerable to disruption from mutations in any of the many genes that underlie these capacities. As such, only those individuals who are relatively free of deleterious mutations should be able to produce these courtship displays at high levels, much like only peacocks with the lowest mutation load can grow the most elaborate tails.
6. Fitness indicators can only play a significant role in mate choice if they do in fact indicate some beneficial quality that can be passed on to offspring. It is the main flaw of this book that Miller does not clearly indicate what his putative indicators indicate. In numerous instances he writes that skills such as humour, creativity, and altruism may indicate intelligence or social status. It is obviously circular to say that intelligence is being indicated since intelligence itself is alleged to have evolved as an indicator of fitness. Nor can Miller argue that intelligence aided our ancestors' survival prospects, since in that case intelligence ultimately evolved by survival selection and then subsequently became a predictable component of mate choice. Similar arguments apply to social status. Miller mentions that higher status people are more attractive as mates, but if we substitute attractiveness for status his argument then reduces to the proposition that skills like language are attractive because they indicate attractiveness. The only non-circular way the fitness indicator theory could account for human brain expansion would be if intellectual skills were honest signals of heritable components of physical quality. In other words, if our "extravagantly large brains" are "advertisements of how good are genes are," they must be advertising the quality of genes related to physical fitness.
7. Miller presents virtually no evidence that quality of intellectual skills indicates physical quality. He cites one study demonstrating a 20 percent correlation between IQ and physical symmetry (Furlow et al., 1997). This is scant support. Furthermore, despite the fact that his entire theory depends on the high heritability of components of intelligence, he intentionally dodges the debate over the genetic determination of individual differences in intelligence (see p. 410). Indeed, most of the second half of the book simply presents speculative scenarios whereby phenomena such art or language might have evolved to indicate some unspecified component of fitness. As such, the fitness indicator account of mental evolution is left largely unsupported by any empirical evidence.
8. Worse yet, much empirical evidence argues against the fitness indicator explanation of brain evolution. Miller correctly points out that sexually selected fitness indicators tend to be characterized by specific features: they often develop fully only after sexual maturity, they develop poorly in individuals in poor physical condition, and they do not look well adapted for promoting survival. But consider human brain growth and intellectual development. Skills like language are rapidly acquired during early childhood and are highly useful for the child's acquisition of various physical and social skills; it is difficult to think of sexually selected traits in other species that show such clear usefulness during juvenile stages. In addition, children in poor physical condition do not sacrifice brain growth in the same way that secondary sex traits (like peacock tails) tend to atrophy in many species when individuals are physically distressed. Instead, prenatal or childhood malnutrition appears to trigger a battery of physiological mechanisms that sacrifice physical health and growth in order to spare healthy brain development (e.g., Barker, 2001). Likewise, there are many well-known cases of creative geniuses who are/were physically weak, unhealthy, or malnourished; fitness indicators cannot be optional if they are to be honest signals, and, as such, these persons should not exist if high intelligence is an indicator of physical quality. Finally, Miller emphasizes the point that fitness indicators do not look very useful by "traditional survival-of-the-fittest criteria" (p. 106). But his argument with respect to traits such as language and creativity is that they are too useful for survival tasks. This is somewhat akin to arguing that wings are too good at flying, so we should look to sexual choice as an alternative explanation for their evolution. It would be difficult to take such an argument seriously. In sum, human intellectual traits appear to have little in common with extant examples of sexually selected fitness indicators.
9. The negative arguments against survival selection explanations of human brain evolution dominate most of the book. Early on these arguments are very general in nature, while in the second half of the book Miller argues why specific skills such as morality or humour could not have evolved by survival selection alone. In general, I think Miller is too critical of potential survival selection explanations of human mental evolution.
10. Miller argues that three problems confound survival benefit explanations of human mental evolution - his Gang of Three. The first problem is why such large brains are found only in humans if they bestow great enough survival benefits to justify their high metabolic costs. The second problem concerns the time lag between the achievement of modern brain size about 100,000 years ago and the appearance of technological innovations like agriculture tens of thousands of years later (this is taken to indicate a poor correlation between brain evolution and survival benefits). Finally, Miller asserts that there are no "plausible" survival benefits of many human abilities such as art, music, and humour.
11. I think many survival selection theories could deal with the above problems, but I am especially partial to Tooby and DeVore's (1987) take on human behavioral evolution. They argue that human brain evolution allowed entry into what they call the "cognitive niche" - the ability to survive via the use of cause and effect mental models whereby one can invent and learn flexible solutions to various survival problems. Whereas most predator and prey strategies are genetically fixed in the short-term, human causal reasoning allowed our ancestors to make "surprise attacks" that evaded slowly evolving plant and animal defences. As Tooby and DeVore (1987) point out, this reasoning ability opened up food sources such as "[b]urrowing animals, underground storage organs, nuts, seeds, bone marrow, birds, fish, mollusks, tool accessible nests, plant foods whose toxins can be neutralized through processing and cooking," and so on (p. 209). These and many other survival benefits may have accounted for human brain expansion and the concomitant increase in creative intelligence.
12. I think the Gang of Three presents few problems for the cognitive niche argument. Start with the question of why other species have not entered this niche. One thing made clear from artificial intelligence research is that it is very difficult to design a physical system with human-like intelligence. As such, the human brain may occupy a very remote peak in an adaptive fitness landscape, one that requires a sequence of low probability events to reach. Although non-human primates appear to possess the preadaptations that have allowed them to approach this peak, their ecological proximity to humans may have led to competitive exclusion from the cognitive niche. In addition, a number of uniquely human characteristics such as bipedalism may have promoted the final steps in the evolution of human intelligence (see Tooby & DeVore, 1987). Finally, it is certainly not the case that the limiting factor in speciation is the possibility of useful innovations. One of the strongest barriers to speciation, instead, is the canalizing force of co-adapted gene complexes (cf. Mayr, 1970). Non-human primates may not have evolved human-like intelligence in part because there was no reoccurrence of the chance events that allowed the reorganization of ape genotypes into the hominid pattern.
13. The other two problems present even fewer difficulties. The time lag between achievement of modern brain size and the advent of technology is irrelevant since technology is not alleged to be one of the survival benefits that explain brain evolution. A similar argument may apply to the alleged absence of explanations for traits such as music, art, and humour. Many such traits are thought to be by-products of the creative intelligence that allows exploitation of the cognitive niche, and as such they require no specific selective explanation. Miller is antagonistic toward the concept of by-products, but offers no principled argument against it. In sum, I find the idea that humans evolved greater intelligence in order to exploit the benefits of the cognitive niche far more persuasive than the idea that the human brain evolved as a sexually selected fitness indicator.
14. The rest of Miller's negative arguments are addressed in separate chapters on art, morality, language, and humour. Space limitations preclude close examination of these arguments. In general, I found some of Miller's discussions of these topics to be incomplete. For instance, he dismisses kin selection and reciprocal altruism as inadequate explanations for human morality, but ignores the increasingly influential literature on indirect reciprocity (e.g., Alexander, 1987; Nowak & Sigmund, 1998). In addition, I think these chapters would have been much more effective had Miller proposed empirical means of distinguishing between survival, by-product, and fitness indicator explanations of these particular topics. As it is, he simply states the case for the sexual choice model without doing much to point out how his position might be tested.
15. Clearly, I disagree with most of the arguments made in The Mating Mind. Nonetheless, I enjoyed reading the book and recommend it to anyone interested in evolutionary aspects of human psychology. Miller's arguments are generally clear, often original, and always thought provoking. I admire Miller's resolve in constructing such an ambitious, novel, and controversial theory; often a thankless task given the innumerable ways that large theories can fall apart. I think ambitious theories should be judged not only by their degree of empirical confirmation, but also on the quality of research and debate that they engender. I hope this review in some way contributes to the vitality of the debate over The Mating Mind.
Alexander, R. D. (1987). The biology of moral systems. Hawthorne, NY: Aldine.
Barker, D. J. P. (2001, June). The fetal origins of adult disease. Plenary session presented at the annual meeting of the Human Behavior and Evolution Society, London, England.
Furlow, F. B., Armijo-Prewitt, T., Gangestad, S. W., & Thornhill, R. (1997). Fluctuating asymmetry and psychometric intelligence. Proceedings of the Royal Society (London) B, 264, 823-830.
Mayr, E. (1970). Populations, species, and evolution. Cambridge, MA: Belknap.
Miller, G. F. (2000) The mating mind: How sexual choice shaped the evolution of human nature. New York: Anchor Books.
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
Nowak, M. A., & Sigmund, K. (1998). Evolution of indirect reciprocity by image scoring. Nature, 393, 573-577.
Tooby, J., & DeVore, I. (1987). The reconstruction of hominid behavioral evolution through strategic modeling. In W. G. Kinsey (Ed.), The evolution of human behavior: Primate models. Albany: SUNY Press.