This book is very interesting, and well worth reading. It is also deeply flawed. It concerns Darwin’s “other” great idea: That sexual selection (SS) is an evolutionary force driven by arbitrary aesthetic choices, rather than by the environmental imperatives...
This book is very interesting, and well worth reading. It is also deeply flawed.
It concerns Darwin’s “other” great idea: That sexual selection (SS) is an evolutionary force driven by arbitrary aesthetic choices, rather than by the environmental imperatives that drive natural selection (NS). (Descent of Man, and Selection in Relation to Sex, 1871)
Darwin’s theory of sexual selection had two components: Male-male competition for access to females, and female selection of males based on preference for male behavioral and physical traits. The idea of male-male competition has never been controversial, but female choice has often been dismissed, ignored, or presumed to be a variant of natural selection.
Prum takes Darwin’s idea about female mate choice* and runs with it, arguing that:
• Female mate choice is often based on arbitrary and aesthetically pleasing (i.e., sexually attractive) male traits rather than characteristics that show adaptive fitness; thus, sexual selection is essentially different than natural selection. SS is arbitrary in that just about any trait may become the target for female preference.
• This dynamic causes coevolution of male characteristics and female preferences, because the male trait and the female preference for it are both inherited by their offspring.
• This coevolution can readily lead to a “Runaway Process” in which females come to prefer and males come to display very exaggerated traits. (R.A. Fisher developed the Runaway hypothesis many decades ago.)
• Aesthetic Remodelling of males takes place in species in which females have succeeded in establishing autonomy in the mating process. Males become more attractive by evolving appearance and displays preferred by females, but also by not being sexually coercive towards females – because coercive males are unlikely to be selected as mates in these species.
• SS is a strong driver of evolution, speciation in particular, because the arbitrary nature of sexual tastes can drive different populations in different sexual-display directions, to the point that members of these populations no longer recognize each other as suitable mate material.
• SS is such a strong force that the results can run counter to the adaptive results of natural selection; i.e., sexual selection can result in reduced fitness.
*Prum talks primarily about female choice and male display rather than the other way around because that is by far the more common pattern. There are exceptions; most notably humans, in which each sex displays to the other, and both sexes are choosy.
Prum argues strenuously that sexual selection is driven by perceptions of beauty and sexual pleasure rather than any utilitarian purpose such as finding the fittest mate; he sums up these ideas as “Beauty Happens,” or “BH.” Later in the book he adds “Pleasure Happens.”
Much of his material is well-argued and supported with very interesting empirical evidence, mostly about birds. (Prum is a renowned ornithologist.). He is very convincing concerning the arbitrary origin of many of the traits females prefer in males; this book will likely change the way you think about animal evolution, at least to some degree.
The latter part of the book concerns humans. It is much more speculative than the sections on birds, but Prum’s ideas about how mate choice has evolved in humans are interesting and generally seem plausible. I will not detail these ideas except to say that the most interesting involve the behavioral remodeling of ancestral human males. The results are that human males are kinder and less sexually coercive, by a long shot, than most of our nearest relatives, and on top of that human males provide parental care, which no other great ape male does, not even the famously peaceable Bonobo.*** additional note months later: the revelations of, and the necessity for, the MeToo movement suggest that male humans’ tendency toward sexual coercion is a lot greater than Prum ( or I) thought. It’s still less than that of chimpanzees, but as women have been telling the rest of us in no uncertain terms, there’s still an awful lot of coerciveness amongst us.***
All of these ideas are important and well worth considering, which is why I recommend the book. But there are also serious weaknesses. They all concern Prum’s animus towards the adaptationist viewpoint; i.e., the theory that evolved features (including mating displays) are essentially about fitness.
First problem (less important than the others): Prum’s unpleasant tone towards those he disagrees with. I will give one example; there are many more. Prum attacks Alfred Russell Wallace (justifiably), and immediately extends the attack to every adaptationist thinker since—Wallace, he says, uses “. . . the characteristic style of adaptationist argument – mere stubborn insistence.” (p. 34)
Such sweeping and sneering generalizations appear throughout the book. This is an unattractive and unenlightening trait in a book about science.
Second and more essential problem: Arbitrary criteria vs. fitness–indicating criteria. Prum has convinced me that many mating criteria are arbitrary in origin--but he further argues, at great length, that most sexual displays provide no information at all about male fitness, and this seems highly questionable. He gives multiple examples of strenuous and exacting male displays, which require that the males be vigorous, healthy, and often very precise. And he emphasizes that many female animals are extremely picky about which males they choose. The choosiness of females implies they can discern very subtle differences in display quality – which suggests that fitness (all that vigor, health, and precision) is one very possible factor in those choices.
Oddly enough, in his argument about the irrelevance of fitness Prum echoes various Victorian critics of sexual selection whom he had previously eviscerated. When Darwin published his theory of sexual selection, Wallace and others (all men) claimed that female animals were too insensate to recognize or appreciate fancy male traits. Prum quite rightly says that these men were totally wrong about female animals’ perceptual abilities. But then he says that female animals probably can’t tell a more-fit from a less-fit male (p. 80). I am curious whether Prum realizes how much he sounds like those misogynistic Victorians.
Prum says that if mate choice concerns fitness, every teensy element of sometimes very complex displays must have been naturally selected for the information it provides about fitness. And every such display element must have been better at showing fitness than all possible alternative display components. I don’t buy it. I accept that mate-choice criteria may be arbitrary in origin – but arbitrary criteria, singly and in combination, nonetheless place demands on the displaying male. Such demands cost energy. Less fit males (e.g., those that are weak, diseased, or parasite-ridden) will be less able to perform such displays adequately. If Prum were to show us mating displays that favor inept, unhealthy, or weak males as much as their fitter counterparts he would have a stronger argument. He has described no such cases.
Third problem: Prum’s unconvincing dismissal of Amotz Zahavi’s Handicap Principle. This important and influential adaptationist idea argues that organisms often evolve characteristics that look counter-productive at first glance; e.g., the peacock’s tail. That appendage looks like a terrible burden; why does he have it? The handicap principle says, in effect, that it’s a boast about fitness – the peacock is saying to the peahen “I am so amazingly fit that I can survive lugging this tail around. No predator has caught me despite the difficulty of running or flying with this thing, and its perfection shows I am resistant to the ravages of parasites. And your babies, honey, will inherit my fitness.” This is a “fitness” argument, obviously, and therefore Prum rejects it. I can’t evaluate all the details of Prum’s dismissal (although see below), but I perceive a considerable irony – Prum’s SS displays look just like Zahavian handicaps to me. Per Prum, males have developed costly aesthetic displays in response to female preferences, just as, per Zahavi, they have developed costly handicaps to advertise their fitness to those same females. It looks more like a difference in perspective and terminology than a true difference in substance.
Fourth problem: Prum is dishonest, I think, about the evolution of Zahavian handicaps. First he describes how an arbitrarily selected sexual display trait may run counter to optimal adaptiveness. Then he very plausibly explains that the evolution of such a trait must therefore strike some kind of equilibrium between its sexual attractiveness and its adaptive drawbacks (p. 41). But when he speaks of the handicap principle, he derisively (and amusingly – pp. 44-48) claims that the handicap principle would inevitably lead to handicaps of such extremity that the organism would die. He utterly fails to consider whether Zahavian handicaps would develop in the same way as maladaptive Prumian sexual traits; i.e., whether an equilibrium would develop. I can’t see any way this is other than dishonest. It makes me wonder if there are other dishonest arguments that I didn’t recognize.
(I highly recommend Zahavi’s 1997 book The Handicap Principle. You may not buy all his arguments, but if you’re interested in evolution, I guarantee you will find it fascinating.)
Fifth problem: Prum’s tendency to caricature the views of adaptationists. They are all absolutists, per Prum, who believe “Natural selection must be true, and all sufficient, because it is such a powerful and rationally attractive idea” (p. 44). Note that this sentence implies that natural selection has not been proved (NS “must be true . . . because it is . . . an attractive idea”). But the larger problem is the phrase that adaptationists think NS must be “ all sufficient.” Certainly most evolutionists think NS is the primary force sculpting organisms, but the many books about evolution that I have read over the past 40 or so years always acknowledge that other forces are also at work. The comment quoted above is one of many in which Prum creates a straw-man absolutist adaptationist who is actually quite rare.
Sixth problem: The Null Hypothesis. Prum points out that good scientific hypotheses must be falsifiable, and says that this requires a null hypothesis for any given set of observations or experiments (p. 68 ff.). The null hypothesis, in essence, is that an apparent correlation between two phenomena is due to chance, rather than to anything special. To support an alternative hypothesis (e.g., say, the hypothesis that superior fitness is causally correlated with high mating success), experimenters must refute the null hypothesis; i.e., they must show that their results are unlikely to be due to chance.
Prum says that the appropriate null hypothesis for the theory that mating displays are about fitness is his own Beauty Happens theory. I.e., to prove that displays are about fitness, experimenters must prove that displays are NOT about aesthetic sexual attractiveness. I am unable to grasp the argument. Apparently BH is equivalent to chance? Because display traits are arbitrary, maybe?
But the fact that I can’t grasp this argument is not my greatest concern. Rather, I find it indefensible that Prum spends pages prescribing a null hypothesis for adaptationist hypotheses – but he never once describes the appropriate null hypothesis for his own Beauty Happens theory. I have the (perhaps-mistaken) impression that he thinks no null hypothesis is required for BH. But if so, he seems to have forgotten his own starting point – a scientific theory must be falsifiable.
Seventh problem: The guy who wrote about all the same stuff years earlier. Much of Prum’s book sounded familiar to me, so I rooted around my bookshelves and found The Mating Mind by Geoffrey Miller, published in 2000, and reread the whole thing. It is almost the same book as Prum’s regarding the components of sexual selection, including similar but much deeper material about humans, with one major difference--Miller is an adaptationist, and believes that those Runaway-process-arbitrarily-chosen-aesthetically-pleasing-behaviorally-remodelled display traits tend to impart information about fitness.
So Prum mentions Miller exactly once, and dismisses him with a misleading comment about one paragraph in Miller’s book (p. 279). It strikes me as thoroughly dishonest that Prum fails to mention that Miller wrote about ALL the same ideas 15 years earlier. Obviously he disagrees with Miller about fitness in particular; that doesn’t seem a sufficient reason to ignore this closely related book. Given Prum’s own tendency towards unpleasant innuendo, I feel justified in speculating that he didn’t want to call attention to the fact that Miller beat him to the punch on a great many particulars.
(I highly recommend The Mating Mind. It’s clearly written, comprehensive, thought-provoking, and lacking the animosity that infects Prum’s book.)
I have spent much more time detailing my problems with Prum’s book than spelling out what I like, but I will repeat what I said at the beginning: The Evolution of Beauty is a worthwhile and eye-opening book. But don''t read it uncritically.