Phil. Trans. R. Soc. B (2012) 367, 2253–2265 doi:10.1098/rstb.2011.0285 Review Aesthetic evolution by mate choice: Darwin’s really dangerous idea Richard O. Prum* Department of Ecology and Evolutionary Biology, and Peabody Museum of Natural History, Yale University, New Haven, CT 06520, USA Darwin proposed an explicitly aesthetic theory of sexual selection in which he described mate pre- ferences as a ‘taste for the beautiful’, an ‘aesthetic capacity’, etc. These statements were not merely colourful Victorian mannerisms, but explicit expressions of Darwin’s hypothesis that mate prefer- ences can evolve for arbitrarily attractive traits that do not provide any additional benefits to mate choice. In his critique of Darwin, A. R. Wallace proposed an entirely modern mechanism of mate preference evolution through the correlation of display traits with male vigour or viability, but he called this mechanism natural selection. Wallace’s honest advertisement proposal was stri- dently anti-Darwinian and anti-aesthetic. Most modern sexual selection research relies on essentially the same Neo-Wallacean theory renamed as sexual selection. I define the process of aes- thetic evolution as the evolution of a communication signal through sensory/cognitive evaluation, which is most elaborated through coevolution of the signal and its evaluation. Sensory evaluation includes the possibility that display traits do not encode information that is being assessed, but are merely preferred. A genuinely Darwinian, aesthetic theory of sexual selection requires the incor- poration of the Lande–Kirkpatrick null model into sexual selection research, but also encompasses the possibility of sensory bias, good genes and direct benefits mechanisms. Keywords: sexual selection; natural selection; aesthetics; beauty; adaptation 1. INTRODUCTION anything is rarely even entertained. Sexual selection For more than two decades, I have been interested in has become a field in which the role of natural selec- the role of arbitrary, Fisherian sexual selection mech- tion on mating preferences is usually assumed, rarely anisms in the evolution of sexually dimorphic, discussed, largely beyond testing and even redefined ornamental traits in polygynous birds [1–3]. During into the definition of sexual selection itself. this same period, this intellectual perspective has The prospect of null model debate in intersexual become increasingly marginalized within evolutionary selection will sound familiar to those with broad inter- biology. Recently, I reframed my view [4] by proposing ests in evolutionary biology and ecology. The previous, that the Lande–Kirkpatrick (LK) mechanism of similar debates on neutral theory in evolutionary gen- sexual selection by mate choice [5–7], which is etics and on null models in community ecology took based on Fisher’s verbal model [8–10], is the appro- years to resolve. Following those historical examples, priate null model for evolution of traits and to be effective, I should repeat the same arguments preferences by intersexual selection [4]. I stated that over and over for a decade or more. Gradually, intel- the wholesale rejection of LK mechanism in the early lectual change will occur as the majority of the 1990s has led to the rejection of testability itself [4]. workers in the field realize that attempting to do The result is that the study of sexual selection has science without a null hypothesis is underproductive become a weak science that largely seeks to confirm at best, and unscientific or faith-based at worst. Demo- the adaptive hypotheses it assumes—i.e. that natural graphic turnover will also occur as new researchers that selection on mating preferences is the determining join the field adopt the null model viewpoint, and force in intersexual selection. In this intellectual others retire or turn to other questions. Although the environment, failure to confirm an honest indication LK null model publication is recent, I will not follow or adaptive signalling hypotheses merely means that these historical examples. Rather, I will expand the the researchers have failed to work hard enough to argument substantially to address a related core issue do so. With the exception of sensory bias research pro- in sexual selection that has been marginalized for grammes, the possibility that traits are not indicating over 100 years since Darwin’s [11] original sexual selection proposal—the question of aesthetics. I will document that our modern sexual selection *[email protected] theory is intellectually Wallacean in structure, and One contribution of 11 to a Theme Issue ‘Sexual selection, social that it is based on some of the very same arguments conflict and the female perspective’. that A. R. Wallace deployed in order to kill Darwin’s 2253 This journal is q 2012 The Royal Society 2254 R. O. Prum Review. Aesthetic evolution aesthetic view of sexual selection—namely honest indi- their charms before the females would have been cation. I recommend reviving the Darwin–Wallace thrown away; and this is impossible to admit. debate on sexual selection and the limits of natural [11, p. 61]; * sentence added in second edition) selection in evolution. On the whole, birds appear to be the most aesthetic In general, I think history of science is best left to of all animals, excepting of course man, and they have professionals in that field. Further, I am suspicious nearly the same taste for the beautiful as we have. of any argument, including my own, that one view [11, p. 466] should be preferred because it has a purer, more [Male birds] charm the female by vocal and instru- direct Darwinian heritage. However, the most recent mental music of the most varied kinds. [11, p. 466] and relevant scientific antecedents to the perspective I am proposing come from Darwin’s Descent of man; It is important to establish what Darwin’s language so the historical analysis I present here is specifically meant in modern terms. Darwin lacked our modern relevant to contemporary scientific progress. Further, sensitivity to avoiding anthropomorphizing his sub- the historic details of Darwin’s and Wallace’s debate jects. Rather, he was actively engaged in reducing the over sexual selection reveal, in a surprising stark way, distinctions between humans and animals. But that we are still engaged in the same fundamental Darwin was not trying to shock his readers. He used issues [12], except that Darwin’s actual opinions these aesthetic terms as ordinary language without have rarely been considered in over a century. To any special semantic or cultural implications. Darwin incorporate Darwin’s ideas into the contemporary was specifically proposing that animals (mostly scientific literature, I will define a process of aesthetic females) were making sensory and cognitive evalu- evolution. I propose that the integration of the LK null ations of display traits, and making mate choices model into sexual selection research is required to based on those evaluations. Darwin used ‘taste for achieve the explicitly aesthetic sexual selection theory the beautiful’ to refer to differential behavioural that Darwin proposed. I will briefly discuss advantages response to a secondary sexual sensory stimulus. of the LK null [4], and reject some misconceptions While this aspect of Darwin’s opinion was highly con- about its implementation in sexual selection research. troversial at the time [12], it is mainstream now. If that were the only issue, there would be no need for us to revive Darwin’s use of aesthetic language. 2. DARWIN’S AESTHETIC THEORY OF Our contemporary terms cover this meaning. MATE CHOICE Darwin’s use of aesthetic language, however, The most revolutionary and challenging feature of implied something more than merely sensory percep- Charles Darwin’s proposed mechanism of evolution tion, evaluation and cognitive mating preference. by mate choice is that it was explicitly aesthetic. Darwin hypothesized that the aesthetic capacities of Darwin repeatedly wrote of mating preferences as an different species evolved differences in mating prefer- ‘aesthetic faculty’ and described them as ‘a taste for ence that could be merely pleasing for their own sake the beautiful’. Darwin’s references to aesthetics and and without any other value, meaning or utility. Just beauty were not analogies, or colourful Victorian like the breeders of different ornamental chickens or mannerisms. Rather, they were central to every pigeons, Darwin hypothesized that each species has attempt he made to explain this proposed mechanism evolved to it own ‘standards of beauty’. In modern of evolution, and to his conception of its evolutionary parlance, Darwin’s proposal is that many secondary consequences. Darwin’s aesthetic view was central to sexual ornaments are entirely arbitrary—merely suc- his motivation for proposing sexual selection as a dis- cessful because they are preferred, not because they tinct evolutionary mechanism. In all the bicentennial provide or communicate to the female any particular praise for Darwin’s many brilliant scientific insights, information about additional benefits [4]. Darwin I know of no piece of writing that has specifically used aesthetic language because it carried a non- and enthusiastically embraced Darwin’s explicitly aes- utilitarian meaning that he specifically intended. For thetic viewpoint. Today, Darwin’s notion of an example, Darwin wrote, aesthetic science of mate choice is treated like a crazy aunt in the evolutionary attic. She is not to be The case of the male Argus Pheasant is eminently spoken of. Here, I enthusiastically embrace Darwin’s interesting, because it affords good evidence that the aesthetic view and encourage its adoption by the most refined beauty may serve as a sexual charm, field as a whole. and for no other purpose. [11, p. 516] Darwin was explicit, repeated and adamant in maintaining that the evolution of secondary sexual This non-utilitarian result of sexual selection was in characters by mate choice was an aesthetic mechanism direct contrast to utilitarian natural selection, which of evolution. For example, he wrote: is exactly why Darwin proposed that they are separate With the great majority of animals, however, the taste evolutionary mechanisms.