Women Behind the Wheel:
How Female Choice Can Steer the Course of Evolution
Bradley R. Hamilton
April 22, 2003
There are many different selective pressures that can alter the appearance of species over time. The most widely discussed of these forms of selection is natural selection, the theory that environmental pressures select against individuals in a population who do not possess traits most conducive to survival. This theory was first put forth by Charles Darwin, in On the Origin of Species. Another form of selection, also described by Darwin is sexual selection. Although this form of selection is not as widely discussed or known to the general public, it is a powerful driving force behind the evolution of species. A great number of species are acted upon by this pressure, from frogs all the way to humans. One of the more important aspects of sexual selection is the female choice theory of sexual selection, under which the female of a species selects mates based on a certain characteristic. There are two competing sub-theories of female choice, both with evidence to support their claims. Also, female choice leads to the interesting paradox of individual fitness versus ³attractiveness.² These topics will be discussed further in this paper.
Sexual selection is defined as ³differential reproduction owing to variation in the ability to attract mates² (Futuyma, 1998). Another way to describe this phenomenon in nature is to say that the appearance and behaviors of organisms is adapted not to help the organism to survive, but rather to more effectively attract mates. This theory of the mechanics behind variation and evolution was first put forth by the man also credited with formulating the theory of natural selection, Charles Darwin. He first touched on the idea in On the Origin of Species, but wrote the book The Decent of Man and Selection in Relation to Sex on the subject. Darwin used this theory of selection in regards to human beings in an attempt to explain the variation between skin colors of the different human races. Because he was unable to explain what particular advantage was given by having black or white skin, he proposed that it was simply because black women preferred black men, and white women preferred white men (Ridley, 1993). He also applied this theory to the peacockıs tail, essentially making the peacock the ³poster species² for female choice. Although the application of sexual selection theory to the human case is probably incorrect (Diamond, 1991), the overall theory is sound. Darwinıs theory of sexual selection and female choice was ignored for a century; it is now becoming more accepted. Additionally, there are now two opposing theories attempting to explain the underlying driving force behind female choice: the Fisher, or ³sexy son² theory and the Good Genes, or ³good sense² theory.
Before discussing the details of the two competing theories, it is important to understand why females need to be choosy about their mate selection, regardless of which theory they seem to be following. The basis for this choosiness comes from the mating pattern followed by most females. In contrast to the general mating pattern of males which is to seek out a high quantity of mates, females seek out a high quality mate. These opposite mating patterns are directly related to the function of each gender in the reproductive process. Because males do not carry the young and are generally less involved in the rearing of offspring than the female, he can most effectively ensure the survival of his genes by fathering as many offspring as he possibly can. In contrast, the female is responsible for carrying the offspring and a majority of the raising. She most effectively passes on her genes by mating with a male that has qualities considered to be the ³best² by that species. In humans, for example, when monogamy, marriage, and the like are disregarded, a baby only requires a one-time act by the father, but requires at least a 9 month commitment from the mother. The female of a species cannot afford to mate indiscriminately, lest he offspring be of ³lesser quality² than others.
Another aspect to consider when discussing female choice is sexual dimorphism. In species where the male has little or no contribution to the raising of the offspring, the difference in appearance between the males and females is very large. The more monogamous a species is, the more the two genders resemble each other. This is clearly evident when comparing pictures of male and female peafowl to pictures of male and female albatrosses.
Figure 1 Peacock Figure 2 Peahens Figure 3 Albatross Mating Dance
This first side of the argument of why females choose who they do is the Fisher theory. This theory, which draws mainly from Sir Ronald Fisherıs insight on despotic fashion and follows Darwinıs thinking that the femaleıs preference is arbitrary, hypothesizes that the underlying reason for sexual selection is that females choose ³beautiful² males so that their offspring will also display the ³beautiful² traits and be able to seduce more females. Because of this, it is also called the ³good taste² or ³sexy son² theory of selection.
The second side to this debate on the driving force of sexual selection is known as the ³Good genes² theory. This theory hypothesizes that while the choice of the female appears to be arbitrary; there is an underlying method to her madness. The exaggerated ornaments and displays of the males are designed to reveal the quality of their genes (Ridley, 1993). Because of the postulation that the females are selecting for signs of good genes, this theory is also called the ³healthy offspring² or ³good sense² theory.
Examples of Sexual Selection
An animal that appears to support the Fisherian theory of sexual selection is peafowl. The trait being selected for by females of this species is the length and coloration of the malesı tails. In this model, there seems to be no good reason in regards to fitness for the female to choose the male with the largest, brightest tail. But instead of mating randomly, the females all seem to be following each otherıs lead and choosing the males with the largest tails. As it turns out, a peahen is more likely to choose a peacock that has just mated over one that has not. These females, because of their preference for long tails, have started a treadmill-like effect. Each successive generation selects males with longer and longer tails because going against this trend, and mating with a short-tailed male would doom their sons to celibacy, and thus decrease the survival rate of their genes. However, by continuing with their trend of selection, the females of the species are giving the individual males a disadvantage when it comes to fitness. Longer tails decrease the ability to fly, and more coloration of the tail makes the peacock more noticeable to predators. But is the peacock truly an example of Fisherıs theory? This will be discussed in the section on the Paradox of Sexual Selection.
One animal whose selection pattern tends to support the ³Good genes² theory of sexual selection is the red jungle fowl. This the cocks of this species, like itsı descendant the farmyard rooster, display a large number of decorations which the hens do not possess. These include long, curved tail feathers, a bright ruff around the neck, a red comb on the head, and morning ³wake up² call. In experiments, a female was given the choice of two males, one raised in good health, the other with a roundworm infection. This infection did not significantly affect the cockıs feathers, beak, or bone length, but did cause the eyes and comb to be clearly less colorful than the healthy male. By observing which male the females chose, it was seen that the females paid much more attention to the condition of the eyes and comb than to the feathers because they routinely chose the healthy male over the roundworm infected one. However, fake combs attached to the malesı heads failed to attract females because the females found them to bizarre (Zuk, 1992). The biochemical reason for the red comb is carotenoid pigments. What makes this a telling sign of health is the fact that carotenoids cannot be synthesized by the body and must be obtained from the diet. The ability of their bodies to extract these chemicals and deliver them to tissues depends a great deal upon the health of the animal. Those with bacterial or parasitical infections simply cannot incorporate the chemicals into their tissues as well as healthy individuals, even if they are fed the exact same amount. Therefore, the brightness level of carotenoid-filled tissues is a clearly visible sign of infection, and this trait is very often selected for by species demonstrating the ³Good gene² version of sexual selection (Zuk, press).
One notable instance of sexual selection that appears to run counter to the whole ³female choice² theory of sexual selection is the case of the tungara frog, studied by Michael Ryan. The mating call of this frog consists of a long ³whine² followed by a ³chuck² noise. What makes this interesting is that of all its close relatives, only one of which also makes the ³chuck² noise, at least one of the ³chuck-less² females prefer the ³chucking² call over the call of their own species. To construct a human analogy, this was ³like discovering that a New Guinea tribesman found women in white wedding dresses more attractive than women dressed in tribal gear² (Ridley, 1993). This would seem to suggest that the preference for the ³chuck² was preexisting in females and that males discovered and exploited this. These finding go against female choice, be it in the form of Fisherıs sexy son theory or the Good genes theory, because the overall theory of female choice predicts that the evolution of the ornament and the evolution of the femalesı preference for this ornament would have gone hand-in-hand. Instead, these results point to the females having a predetermined preference long before the trait arose in males. A peahen would have long tails with bright ³eyes² on them while peacocks still looked like large chickens (Ryan, 1991).
Aspects Related to Sexual Selection
Sexual selection also has an impact on many other aspects of an organism. Because of the nature of female choice and sexual selection, both physical characteristics of an organism and the behavior of an organism can be influenced by the selection. Two of the aspects are and have been influenced by sexual selection are competition and symmetry of features.
One of the most noticeable impacts of sexual selection is male-male competition. Because the females of species that engage in such behavior are only interested in selecting the best male available, the males compete with one another in order to gain the attention of the female, with the winner of such competitions being allowed to father the offspring. This behavior makes the males of such species a sort of ³genetic sieve² (Ridley, 1993). Due to the fact that females of a species are only interested in a limited number of traits, males possessing those traits, usually to extremes, father the majority of the offspring. Only the ³superior² males are allowed to pass on their genes to the next generation, while the genes of the ³inferior² are removed from the population. There are two major effects on the population that this ³genetic sieve² has. First of all, the genes that make the ³inferior² males ³inferior,² such as those for short tails in peacocks, go to extinction in the population. Secondly, this same process leads to an overall decrease in the genetic diversity of the population.
The second aspect of an organism that sexual selection tends to greatly effect is the symmetry of the organismıs body. This has to do with the tendency of animals, including humans, to consider more symmetrical features to be more beautiful. This result of sexual selection was first discussed by Anders Moller and Andrew Pomiankowski in 1991 to settle the dispute between the Fisher and Good genes schools of thought of female choice. It is well known that body features develop more symmetrically if the individual faced low amounts of stress during development. If there is something wrong during development, it is very likely that the features will turn out asymmetrical (Thornhill and Sauer, 1992). Therefore, the possession (or lack of) symmetry in an individual can be a clue to fitness. Those with the greatest degree of symmetry would be those that were most able to thrive as a juvenile. If the Fisher hypothesis of female choice is correct, there would be no expected relationship between the size of the character being selected for and itsı symmetry. In contrast, if the Good gene theory is correct, the selected for characteristic would be the most symmetrical when it is largest. That would indicate that the individual had both the best genes and the least amount of stress. While studying swallows, Moller noticed that the males with the longest tails also had the most symmetrical tails. This runs counter to the length-symmetry relationship for other types of feathers where feathers closer to the average length show a greater degree of symmetry. By altering the length and/or symmetry of the malesı tails, Moller found that longer tails led to sooner mating and more offspring, and that within each length class, those with more symmetry fared better than those with less symmetry (Moller, 1992). This research seemed to support the Good genes theory until further studies on other birds were conducted. With further research, Moller and Pomiankowski determined that species interested in only one trait, for example swallows with tail length, tend to follow the Good genes theory as those with the most symmetrical tail of the same length will most often be chosen as a mate. In contrast, those species interested in more than one trait, for example pheasants with long tails, facial roses, and colorful feather patterns, tend to follow Fisherıs theory of female choice. These species select the male with the largest or brightest trait, regardless of its symmetry (Moller and Pomiankowski, press).
Paradox of Sexual Selection
With the obvious importance of sexual selection, there arises a paradox in regards to itısı mechanics. This paradox occurs because many times, the over exaggeration of the trait being selected for, such as the peacockıs tail, can prove to be a great disadvantage to the survival of the male possessing the trait. These larger tails become a hindrance to flight, thus making the peacock easier for a predator to catch. The peacock also suffers from a second disadvantage to itsı own survival, itsı bright plumage. This makes the peacock, as well as males of other species in which females choose bright color, stand out more readily than more drably colored species. These consequences of female choice lead to the question of what is more important to an animal: itsı own individual survival or the passing on of itsı genes? As previously mentioned research has shown, the answer is most like the latter. In the case of the peacock, the largest, brightest tail, a disadvantage to individual survival, is nearly always selected for by the females. A possible solution to this paradox came from Amotz Zahavi in 1975. He suggested that the greater the handicap to the male, the more honest of a signal sent to the female. Because he was able to survive long enough to reproduce with the disadvantage, he was giving a signal that he had a higher genetic quality, suggesting that the tail would evolve faster if it was a handicap than if it was not. This goes opposite to Fisherıs prediction, which said that the tail would stop evolving once it became too severe of a handicap (Zahavi, 1975). His theories have been vindicated in recent years, with the addition of two subtleties. One is that the handicap must not only affect survival and reflect quality but must do it in a graduated way. That is to say, the weaker the male with the disadvantage, the harder it would be for him to maintain it. Secondly, the handicap must be designed to best reveal deficiency, such as male swans having difficulty maintaining his plumage.
In closing, we have seen that the female choice of aspect of sexual selection can have many impacts and influences on a species. Female preference for a characteristic, be it simply an aesthetic preference or a choice based on a signal that the male possesses good genes, can, for example, drive a simple, chicken-like bird to the colorful peacock of today. In driving evolution in this way, female choice also has an impact on behaviors, such as male-male competition, and other physical characteristics such as the symmetry of certain traits. The preferences of females also can lead to an interesting paradox of survival versus reproduction. What happens when the trait that females so covet causes the males to be easier targets for predators? As Zahavi has suggested, and been vindicated on, this ensures that female is able to choose a male that has both the desired trait and the good genes to survive despite itsı negative impact on his survivability. Female choice, and in turn sexual selection, is truly one of the strongest driving forces behind the evolution of species.
Figure 1 taken from www.denverzoo.org
Figure 2 taken from www.noahslostark.com
Figure 3 taken from www.midwayislandphotos.com
Diamond, J. M. 1991. The Rise and Fall of the Third Chimpanzee. Radius, London.
Futuyma, J. D. 1998. Evolutionary Biology, Third Edition. Sinauer Associates, Inc,. Sunderland, Massachusetts.
Moller, A. P. 1992. Female preference for symmetrical male sexual ornaments. Nature 357: 238-240.
Moller, A. P. and Pomiankowski, A. 1993. Fluctuating asymmetry and sexual selection. Genetica 89: 267-279.
Ridley, M. 1993. The Red Queen: Sex and the Evolution of Human Nature. Penguin Books. New York, New York.
Ryan, M. J. 1991. Sexual selection and communication in frogs. Trends in Ecology and Evolution 6: 351-355.
Thornhill, R., and Sauer, P. 1992. Genetic sire effects on the fighting ability of sons and daughters and mating success of sons in a scorpion fly. Animal Behaviour 43: 255-264
Zahavi, A. 1975. Mate selection a selection for a handicap. Journal of Theoretical Biology 53: 205-214
Zuk, M. 1992. The role of parasites in sexual selection: current evidence and future directions. Advances in the Study of Behavior 21: 39-68
Zuk, M. 1994. Immunology and the evolution of behavior. In: Behavioral Mechanisms in Evolutionary Biology (ed. L. Real), 354-368. University of Chicago Press, Chicago.