RESEARCH ARTICLES Is the peacock merely beautiful or also honest?* Raghavendra Gadagkar Centre for Ecological Sciences, Indian Institute of Science, Bangalore 560 012, India and Evolutionary and Organismal Biology Unit, Jawaharlal Nehru Centre for Advanced Scientific Research, Jakkur, Bangalore 560 064, India natural world. What Darwin had in mind were the con- Darwin proposed the theory of sexual selection to spicuous, extravagant, often cumbersome and almost waste- account for the evolution of extravagant secondary ful, secondary sexual characters seen in males of many sexual characters often seen in males because he argued that utilitarian natural selection cannot permit their animal species—the antlers of many deer, the colours, evolution. Although the idea of sexual selection was calls and displays of many male insects and birds and disbelieved or neglected for a long time, today it con- above all, the train of the peacock. In The Descent of 2 stitutes an active area of research. Starting with Dar- Man and Selection in Relation to Sex , Darwin argued win, the enormous, cumbersome train of the peacock that such characters could not have been shaped by natu- has been the prime example of sexually selected traits. ral selection as they were likely to be detrimental to the And yet, almost nothing relevant to sexual selection survival of their bearers, being wasteful in terms of was known about the peacock until very recently. In resources and energy and making them more vulnerable the last ten years or so, observations and experiments to predators. To account for such characters, Darwin pro- on a free-ranging, feral population of the Indian pea- posed the theory of Sexual Selection that he said operates cock in the Whipsnade Park in Bedfordshire in the because of ‘the advantage which certain individuals have UK and some experiments in a commercial peacock farm that breeds birds for food and as show birds, by over other individuals of the same sex and species, in Marion Petrie and her colleagues have finally justified exclusive relation to reproduction’. In other words, what the peacock as an icon of sexual selection by female an individual loses in terms of lower probability of sur- choice. The peacock appears to fulfil nearly every vival may be more than compensated by increased pro- expectation of the theory of sexual selection: peahens bability of getting more and better mates. prefer peacocks with elaborate trains probably recog- nizing them by the symmetry of their trains and bene- fit from doing so because of improved survival of their Male–male competition and female choice chicks. Peacocks with elaborate trains themselves appear to be better survivors with larger fat reserves and higher levels of immunocompetence. These find- Darwin proposed two mechanisms of sexual selection— ings support theories which suggest that peacocks with male–male competition and female choice. The antlers of elaborate trains are selected because of the handicap deer and the horns of antelopes and indeed of many bee- they carry rather than in spite of it. Thus the pea- tles, help males to compete with other males of the same cock’s train is not merely beautiful but is also an hon- species for access to the best or largest number of est indicator of male quality. Although the peacock is females. Such male–male competition was easily accep- deeply entrenched in Indian mythology, culture and ted by Darwin’s contemporaries. But clearly the pea- folklore and it is widely distributed in the country, cock’s train could hardly be helpful in male–male battles. research from India has regrettably made no signi- If peahens prefer to mate with peacocks with most elabo- ficant contribution to recent research justifying the rate trains for some reason however, then the situation peacock as a prime example of sexual selection and making it a frontrunner in modern studies of sexual would be quite different. Darwin therefore argued that selection. characters such as the peacock’s train must be selected due to female choice. Any reduction in the probability of survival of a peacock, on account of his enormous train Natural selection and sexual selection which makes his getaway from a predator clumsy, can be more than compensated by better access to females. But We all know how easy it is to fall in love with our pet why should peahens prefer peacocks that can barely ideas and theories even if they are fairly trivial. It is escape from predators? Darwin argued that females have remarkable therefore that Charles Darwin maintained, a sense of beauty and are excited and charmed by the 1 even as he wrote his Origin of Species , that natural extravagant ornaments and displays of the best males. selection is inadequate to explain some features of the Darwin’s contemporaries refused to accept this idea and found it impossible to believe that deer and birds, let *Dedicated to Prof. S. Ramaseshan on his 80th birthday. alone insects, could have a sense of beauty. Thomas e-mail: [email protected] Henry Huxley, Darwin’s self-appointed advocate of the 1012 CURRENT SCIENCE, VOL. 85, NO. 7, 10 OCTOBER 2003 RESEARCH ARTICLES theory of evolution, who was sometimes referred to as is preferred by the peahen merely because it is beautiful Darwin’s bulldog, tried to persuade Darwin to drop the and not because it is also an honest signal of the peacock’s idea of sexual selection altogether. Among Darwin’s con- ability to survive. temporaries, Alfred Russell Wallace, the co-discoverer of the principle of natural selection, being ‘more Darwinian than Darwin himself’, came out most strongly against the Zahavi’s handicap principle theory of sexual selection, arguing that natural selection was adequate to explain everything in nature, including Of the many theories proposed for sexual selection in the peacock’s train3. See Hiraiwa-Hasegawa4 for an inte- general and female choice in particular, the one most resting commentary on why the world was so slow in different from Fishers’ run-away selection theory is the accepting Darwin’s theory of sexual selection. handicap principle proposed by Amotz Zahavi. Zahavi made the radical suggestion that the peacock’s long tail is Fisher’s run-away selection selected precisely because it is a handicap, not in spite of being a handicap. By carrying around such a handicap of If Darwin’s contemporaries were sceptical of his theory a tail and by not yet having succumbed to a predator, the of sexual selection, his successors ignored it almost com- peacock reliably demonstrates to females that he is indeed pletely, for nearly a hundred years. Today, however, sexual very fit6. Zahavi derived from this idea a far-reaching gene- selection is one of the most vigorously pursued branches ral principle that animal signals in general must impose a of modern evolutionary biology. Both male–male compe- differential cost, a handicap, on the signaler in order to be tition as well as female choice are widely accepted mecha- reliable and thus resistant to faking7. It is the dispropor- nisms of sexual selection. Much progress has been made tionate cost to low quality males that is imposed by the in thinking about, and to some extent in understanding, handicap which prevents them from cheating. The scien- why females might choose particular males—what’s in it tific community rejected Zahavi’s ideas outright. Several for them if the males are not necessarily the best survi- distinguished theoretical evolutionary biologists wrote vors? Ronald Fisher, one of the architects of the genetical mathematically sophisticated papers arguing that the handi- theory of evolution was the first to propose a model of cap principle cannot work. One paper was actually entitled female choice. Fisher argued that at first, the slightly ‘The handicap mechanism of sexual selection does not exaggerated male character, such as an intermediate sized work’8. train of the peacock might well be correlated with male Then everything changed in 1990 when Alan Grafen quality (ability to survive). At this stage females will be published two papers showing, with the aid of more eco- selected to prefer peacocks with long trains. Later the nomically inspired mathematical models, that Zahavi’s very fact that peahens prefer males with elaborate and handicap principle can indeed work, both in the evolution long trains can drive selection on peacocks to grow trains of honest signals in general and in the context of sexual even longer and more elaborate than is good for their selection9,10. Today, Zahavi’s handicap idea and the more survival. Fisher called this process run-away selection5. It general, costly, honest signal idea are widely accepted is ironical that Fisher, who produced precise mathemati- and have considerably altered the way in which we model cal models for all his theories, left this one alone unfor- and study animal communication and behavioural evo- mulated in mathematical language and therefore untested lution. The well-known evolutionary biologist John May- even for its plausibility. But today there exist mathematical nard Smith has graciously admitted publicly that he was models that justify Fisher’s arguments—run-away sexual wrong in hastily concluding that Zahavi’s idea was in selection can indeed work in the manner that Fisher error. But of course Maynard Smith said it in his inimita- thought it might. A crucial aspect of Fisher’s theory, and ble style11: ‘I was cynical about the idea when I first one that contrasts with other theories (see below), is that heard it, essentially because it was expressed in words peahens continue to be selected to prefer peacocks with rather than in a mathematical model. This may seem an long trains even after such peacocks are no longer the odd reason, but I remain convinced that formal models are best survivors.