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Sexual Selection and the Evolution of Beauty: Two Views Egbert Giles Leigh Jr*

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Sexual Selection and the Evolution of Beauty: Two Views Egbert Giles Leigh Jr* Leigh Jr Evo Edu Outreach (2018) 11:13 https://doi.org/10.1186/s12052-018-0087-5 Evolution: Education and Outreach BOOK REVIEW Open Access Sexual selection and the evolution of beauty: two views Egbert Giles Leigh Jr* Abstract This is a review of Ryan’s A Taste for the Beautiful and Prum’s The Evolution of Beauty, two books that show how sexual selection by female choice can favor the evolution of beauty. Book details as mates, what criteria females use to choose, and how A Taste for the Beautiful: Te Evolution of Attraction, by their choices afect evolution. Tese books will interest Michael J. Ryan. this Journal’s readers because they suggest that evolution Princeton NJ: Princeton University Press. 2018. pp. is not a purely utilitarian process: females often favor the x + 200. ISBN 978-0-691-16726-8. H/b $27.95. evolution of beauty for its own sake, choosing males for Te Evolution of Beauty: How Darwin’s Forgotten Te- their beauty in form, color and behavioral displays, char- ory Shapes the Animal World—and Us, by Richard O. acteristics which may, like Hardy’s (1967, pp. 101, 119– Prum. 120, 150) number theory, be of no practical use whatever. New York: Doubleday. 2017. pp. xii + 429. ISBN 978-0- Darwin (1871, p. 257) distinguished non-adaptive 385-53721-6. H/b $30.00. sexual from adaptive natural selection very carefully, New York: Anchor Books. 2018. pp. xiv + 428. ISBN remarking that sexual selection applies to character- 978-0-345-80457-0. S/b $17.00. istics which “serve only to give one male an advantage over another” although “the less well-endowed males, if Book Review time were allowed them… (would) pair with the females; Sexual selection occurs when animals of one sex com- and they would, in all other respects… be equally well pete to mate with members of the other. Members of one adapted for their ordinary habits of life. In such cases sex (usually males) may fght each other for the privilege sexual selection must have come into play, for the males of mating with members of the other, as in deer or sea have acquired their present structures, not from being lions. In many other species, such as peacocks, males better ftted to survive in the struggle for existence, but compete to attract mates by beauty of appearance or from having gained an advantage over other males.” In behavior, leaving females free to choose whom to mate other words, Darwin defned sexual selection as a pro- with, a process called female choice (Darwin 1871; Fisher cess which did not enhance adaptation. Tis fact seems 1930). Darwin developed the concept of sexual selec- almost unknown to evolutionary biologists, too few of tion because he realized that natural selection could not whom have read Darwin (1871) with sufcient attention. explain the evolution of a male peacock’s array of long Sexual selection was largely ignored for the frst tail-feathers which, despite its beauty, almost annihilates hundred years after Darwin (1871), because it seemed its possessor’s ability to escape from predators (Darwin irrelevant to the battle to vindicate natural selection on 1871, vo1. 2, p. 97). Both books reviewed here focus on variation arising without regard to its bearers’ needs as sexual selection by female choice: how males of difer- a viable cause of adaptation. Competition among males ent species compete to persuade females to choose them for females seemed an obvious aspect of the struggle for existence. If considered at all, female choice was invoked as an engine of adaptation, as (it was assumed) *Correspondence: [email protected] they would choose to mate with the best adapted males. Smithsonian Tropical Research Institute, Panama City, Panama © The Author(s) 2018. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat​iveco​mmons​.org/licen​ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Leigh Jr Evo Edu Outreach (2018) 11:13 Page 2 of 6 Tis attitude was too utilitarian for any to consider how simple choice experiments, and studies of ear physiol- beauty evolved. Biologists, moreover, were not subtle ogy and auditory nerve activity. enough to see that genetic systems must be specifcally Ryan next discusses constraints on, and general fea- adapted to make natural selection favor adaptive evolu- tures of, sexual selection. Te range of an animal’s sen- tion. Williams (1966, p. 27) considered segregation dis- sory abilities is limited by the data-processing capacity tortion—biasing meiosis in heterozygotes in one’s own of its brain, and its array of sensory abilities, which is favor—as just another way an allele could acquire selec- shaped by what it needs to know to fnd food and escape tive advantage. In fact, fair, unbiased meiosis is needed predators. Tus nocturnal bats depend more on echolo- to ensure adaptive evolution (Leigh 1991) because this cation and smell than vision for navigating and fnding suppresses conficts between the advantage of particu- food. Moreover, animals respond to proportional difer- lar alleles and the common interest of the autosomal ences in signal strength (Weber’s law): a tungara female genes. As we shall see, sexual selection by female choice that easily distinguishes between a one-chuck and a two- bears on both themes, the evolution of beauty, and chuck call hears little diference between six- and seven- resolving conficts between individual advantage and chuck calls. Tese factors all afect a female’s response to the good of the group. a male’s courtship signals. A female often integrates vari- I frst discuss Ryan’s book, a balanced, comprehen- ous stimuli in choosing a mate. Te stimulus that causes sive account of the bases of male attractiveness and a Drosophila female to respond to a courting male is the female choice. Working with tungara frogs in Panama, odor of a specifc male pheromone, but the sound of the he was frst to document decisive infuence of female male’s stylized wing-buzzing, the sight of his athletic choice on male mating success in the wild (Ryan 1980). dancing, and his taste (courting males do a lot of grop- He and his students have studied in detail the bases of ing, tasting with their legs) infuence her decision to mate and infuences on sexual selection in these frogs (Ryan, (Ryan, pp. 38–39). Ryan discusses the molecular mecha- chapter 2), revealing a marvelously complex story. A nisms behind a female Drosophila’s preference for a par- tungara frog’s call is either a simple whine (as in all calls ticular odor and a particular taste. of other species of its genus), or a whine followed by A female’s frst priority is choosing a mate of her spe- one or more chucks. Te whine is species-specifc, and cies. Tus, in the tungara genus, female brains and ears the “amphibian papilla” in a tungara’s ear is tuned to be are tuned to respond only to whines of males of their spe- most responsive to whines of its own species. A tungara cies. Some males, however, may more closely match the female placed between two speakers, one broadcasting female’s criteria of being in her species, so they appear only whines, the other, whines followed by chucks, is six more attractive (beautiful?) to her, even if they enhance times more likely to approach the speaker broadcasting her reproduction no more than their fellows would. Here, whines with chucks. Whines with chucks also cause sexual selection is purely aesthetic. Moreover, some auditory nerves to send stronger signals to the brain. female aesthetic preferences seem utterly unrelated to a Although supplementing whines with attractive chucks male’s quality as a mate (whether he enables her to pro- costs little extra energy, males are reluctant to add duce more or better ofspring). Just as a female frog in chucks, which attract predatory bats that eat male frogs species which never make chucks prefers synthetic calls when they aggregate to call for mates. Females also pre- where chucks are added to whines of her species, so a fer deeper chucks, which larger males, more likely to female platyfsh in a species whose males lack sword-like fertilize all their eggs, make—because they hear them tails prefers males of her species to whom the experi- better! Ears of all species of this genus of frog have a menter has added a sword-like tail (Ryan, pp. 41–42). “basal papilla,” tuned to 2200 Hz, even though only A female does beneft by choosing a “quality” mate that tungara frogs add chucks (averaging 2500 Hz) to their enables her to have more or better ofspring. Quality may whines. Since the basal papilla is tuned to 2200 Hz, refect better health, better condition, or better genes. females can hear deeper, lower-frequency chucks more Tus calls of male tungara frogs infected by the poten- easily. Ryan’s discovery illustrates his care: many would tially lethal chytrid fungus, which could infect his mates, have concluded that females choose larger males with are far less attractive than those of normal males (Ryan, deeper chucks because they fertilize more eggs, and p. 79). But she rarely practices eugenics. Ryan’s third stopped the study. Finally, females in other species chapter is based primarily on birds, fsh and frogs. Tese whose males never make chucks are more attracted to are easier to study experimentally, but their responses synthetic calls with chucks added to the whines of their to sexual stimuli may be governed more often by fxed species.
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