Guest blog: The Peacock's Tale
This week's post is by Dave Wisker, a graduate student in Molecular Ecology at the University of Central Missouri.
It's the creationist's dream. If actual evidence of creation is too much to hope for, how about a peer-reviewed paper in a respected journal overturning one of the icons supporting a major element of Darwin's theory?. Sexual selection in peafowl is definitely one of those icons. There appeared to be ample empirical evidence that peahen's preference for more elaborate trains on their mates has led to the spectacular male tail displays we see today. A series of papers in the 1990's by behavioral ecologist Marion Petrie and others seemed to solidly support this, and there is also evidence that elaborate tails may indicate good genes (Petrie et al, 1991; Petrie and Williams, 1993;.Loyau et al, 2005a). This, in itself, is a challenge to an older idea that the peacock's tail shows how arbitrary female preferences can be amplified to extremes by a "runaway"? process (Fisher, 1958). But, whatever their evolutionary origin, the preference itself has rarely been questioned.
However, a recent paper published in Animal Behaviour (http://tinyurl.com/4t69v5), "Peahens do not prefer males with more elaborate trains"?, challenges the conventional wisdom.
Mariko Takahashi and her colleagues studied a feral population of peafowl in Japan for seven years, and report finding "no evidence that peahens expressed any preference for peacocks with more elaborate trains (i.e., trains having more ocelli, a more symmetrical arrangement or a greater length), similar to other studies of galliforms showing that females disregard male plumage."? Intelligent Design and creationist groups have already praised this paper, saying it has demonstrated that the conventional evolutionary explanation for the peacock's tail is little more than a "just so"? story. A look at this paper and those from some representative studies that came to a different conclusion seems in order. Note: all of the studies looked at additional aspects of tail morphology besides eyespot number/symmetry, but this essay will focus only on this particular feature, for space reasons and because it is the heart of the 'controversy'. In addition, all of the biologists involved agree that tail ornamentation is only one of several display cues that a female uses in selecting a mate.
Takahashi's group noted that the number of eyespots, or ocelli, and their symmetry varies during an individual male's lifetime. So they photographed every male's train each season over the seven years, and devised a "Fluctuating Assymetry "index (FA) for each bird. The FA is defined as "a percentage of the number of eyespot pairs having lost one of the pair from a symmetrical linear position divided by the total number of eyespot pairs on the train."? The lower the FA value, the higher the symmetry, with a value of zero indicating perfect symmetry. They also used the number of eyespots as a different metric. Studies by Petrie & Halliday (1994) and Loyau et al (2005b), which did find that females prefer males with more elaborate trains, used eyespot number only. Petrie and Halliday removed 20 of the outermost eyespots from their treatment males using scissors (they did this without disturbing the length of the train), and used eyespot number as their metric. Loyau et al did not experimentally alter the eyespot number, but used the number of ocelli as their metric as well. So it appears all three studies used the same elaboration metric in at least part of their analysis.
Mating success was another metric. Petrie and Halliday used number of copulations for each male (after displaying and being accepted by a female), and the change in number of copulations for each male, if any, after eyespot removal. Loyau et al also recorded number of copulations after being accepted by a female. Takahashi et al took a different approach. They estimated male mating status "using female courtship behaviours. This was done to decrease the likelihood of excluding possible mates from the analyses because of limited observations."? Females show three categories of behavior when in a male territory: passing by the male, passively receiving his display, or actively soliciting a display by "run-around"? behavior. Takahashi's group noted that females who perform multiple "run-around"? behavior for a male often accept that male for copulation later, so they considered any female who performed more than two successive run-arounds for a male as having made a "preferred visit"?, and counted that as a successful copulation. This could be a crucial source of error, if a significant number of females performed multiple run-arounds but did not accept the male for copulation later, or if they copulated after less than three run-arounds. It's certainly worth investigating separately.
Takahashi et al point out that some of the studies which found a positive correlation between male mating success and train elaboration may be flawed because they only observed the birds in the morning, missing the crucial evening period of sexual activity. The creationists have especially harped on this. While it is true that Petrie and Halliday only observed in the morning, Loyau et al's paper specifically states they made observations from 0500 to 1700 hours. So that factor may not be significant in explaining the discordant results.
The Japanese authors also discuss other factors that may explain the different conclusions, namely sample size, length of study, and the age of the males involved. The advantage their study has over the others is the number of individuals (around twice that of the others), length of the study and the range of ages of the males. It is not clear, however, if those factors contributed significantly to the results.
Finally, this paper makes a very interesting observation: all of the studies of peafowl have shown very little natural variation in male train elaboration, regardless of the metric used. This suggests--to me at least--that one has to very careful in evaluating reproductive success, because the positive correlations were not particularly strong. If the males lack enough variation for females to make a choice, then it will be exceedingly difficult to discern female preference for elaborate trains in the wild. The fact that Petrie and others have added experimental variation and detected apparent selection gives one reason to think that, at this point, the evidence still suggests that females do prefer males with more elaborate trains. Suppose your hypothesis was that women prefer men with cars. If every man in your study group had a car, it would be hard to tell, from simple observation, whether female preferences were the cause of car ownership or not. You would need to take away some cars and see whether that has any effect. So the creationist's dream remains just that. However, these studies do inspire more research questions. How strong is the selection, if it exists? Is the low natural variation a direct result of female preference, that is, has the population reached its physiological limit for train elaboration? Does predation control the further runaway growth in train size/elaboration? What effect will this low natural variation have on the future of female preferential behavior? For example, Takahashi et al. found that a behavior known as "shivering"? be important. It looks like a fertile field for further investigation.
Fisher RA (1958). The Genetical Theory of Natural Selection, 2nd Revised ed. Dover. 291 pp.
Loyau A, M Saint Jalme, C Cagniant and G Sorci (2005a). Multiple sexual advertisements honestly reflect health status in peacocks (Pavo cristatus). Behav. Ecol. Sociobiol. 58: 552-557
Loyau A, M Saint Jalme, C Cagniant and G Sorci (2005b). Intra-and intersexual selectiojn for multiple traits in the peacock (Pavo cristatus). Ethology 111: 810-820
Petrie M, TR Halliday and C Saunders (1991). Peahens prefer peacocks with more elaborate trains. Anim. Behav. 44: 585-586
Petrie M and A Williams (1993). Peahens lay more eggs for peacocks with larger trains. Proc. R. Soc. Lond. B 251: 127-131.
Petrie M and TR Halliday (1994). Experimental and natural changes in the peacock's (Pavo cristatus) train can affect mating success. Behav. Ecol. Sociobiol. 35: 213-217
Takahashi M, H Aritat, M Hiraira-Hasegawa, and T Hasegawa (2008). Peahens do not prefer peacocks with more elaborate trains. Anim. Behav. 75: 1209-1219