The Essence of
Sexual Selection of the Evolutionary Past
Remains in Existence Today
Sexual selection is the theory that competition for mates between individuals of the same sex drives the evolution of certain traits. Many traits such as smooth skin or fur, antlers, colorful plumage, strong muscles, and fluid motions appear not only to enable hunting or gathering but also to be important sexual attractors, especially in the more intelligent species. In 1871 Charles Darwin emphasized that sexual selection was qualitatively different from natural selection, and he compared sexual selection to the artificial selection of domesticated animals. Observation has shown that in several animal species males have conspicuous traits, which seem to be unnecessary or even handicaps for the males, but females of the same species appear to favor them. Among the theories of sexual selection, there are currently three main theories being examined in the explanation of female choice. Even though new theories have been created since Darwin, sexual selection still brings up controversial issues. It is important to understand the sexual selection theory because much of our modern science developed without recognizing that sexual selection could have played an important role in the evolution of the human body, the human mind, human behavior, or human culture. Overall, sexual selection is just as controversial today as when Darwin first proposed the idea.
Sexual selection theory is concerned with 'the advantages that certain individuals have over others of the same sex and species, in exclusive relation to reproduction¹ (Darwin 1871). Sexual selection arises from sexual competition among individuals for access to mates and has given rise to the evolution of such bizarre traits as the antlers of stags, the horns of antelopes, the tail of the peacock (Pavo cristatus), bird song, frog croaks, and the extravagant colors of many fish and birds. Darwin in his 1871 publication was the first person to realize the explanation for the evolution and maintenance of these bizarre traits that obviously do not enhance the survival prospects of individuals, and therefore cannot be explained by natural selection. On the other hand, extravagant secondary sexual characteristics are costly. They often reduce survival prospects and can only be maintained by sexual selection.
Two mechanisms are involved in the sexual selection process. One mechanism is intrasexual selection, in which mate competition between individuals of the chosen sex, usually males, for access to females, has resulted in the evolution of weaponry such as antlers and horns, but also increases in mere male size that provide some individuals with an advantage over others for access to females. The second mechanism is intersexual selection, which is mate choice by individuals of the choosy sex, usually females, that has resulted in the evolution of many bizarre traits such as the tail of the peacock, beautiful coloration in birds and fish, and many kinds of vocalization. Humans are not much different from other organisms by having evolved sexual size dimorphism due to male-male competition (remember that more than 90% of all same-sex homicide involves men in their early twenties when mate competition is intense (Daly and Wilson 1988)), musculature and other features due to the effects of testosterone at puberty, and breasts and facial beauty due to the effects of estrogens and male choice.
The advantages of sexual selection, as seen from the point of view of the choosy part, may come in either of the following ways (Andersson 1994). Females may choose males with exaggerated features simply because such signals indicate the presence of direct fitness benefits that enhance the reproductive success of choosy individuals. Males with a high quality territory, males providing nuptial gifts, males without contagious parasites, and males with sperm of better fertilizing ability all provide females with benefits. Male displays may also signal benefits that females do not acquire directly, but only indirectly in the next generation through the success of the offspring (Fisher 1930). If the male signal and the female preference both have a genetic basis, choosy females will on average pair up with males with exaggerated secondary sexual characteristics, and the mate preference and the signal will become genetically coupled as a result of this process. The male trait and the female preference will coevolve to more extreme versions that enhance male mating success until the mating benefit is balanced by an oppositely directed natural selection pressure, or until the genetic variance in either female preference or male trait become depleted. There is little empirical evidence for this mechanism (Andersson 1994), but it is likely to work in most contexts and will work better in mating systems with an extreme skew in mating success.
Darwin () emphasized that sexual
selection was qualitatively different from natural selection in that it could
act far faster and could explain leaps of transformation that natural selection
might not be able to approach. He
compared sexual selection to the artificial selection of domesticated animals,
both processes exhibiting a relative lightening speed of change. Darwin followed Lyell's non-cataclysmic
orientation in suggesting that evolution generally followed a slow gradual path,
but in his discussions of sexual selection (Cronin ) the restraints were off.
In addition to speed of change, sexual selection offers an explanation for some mysteries of evolution that natural selection, for many, had not satisfactorily explained. How birds could have incrementally acquired feathers and flown, when any half way point in the process may have offered few benefits, has been an issue from Mivart to Gould. Wesson () has written that feather evolution may have progressed because the female of the ancestor bird species was picking males with beautiful plumage and selected for big fat colorful feathers that later were found useful for flight (it has been suggested that their origin came for their ability to retain heat).
Sexual selection and its propensity to operate with speed and extreme uniqueness has also been noted when it comes to human beings. Darwin () wrote that humans may have been prepared for language by sexual selection reinforcing the most eloquent (non-verbal) vocalists thereby creating a song-making ability in humans that could later be bridged into language (Darwin ). Darwin believed that the many radical shifts in evolution may have been sexually selected. Other writers have noted that sexual selection in combination with culture, may be the engine behind the extreme speed in human evolution, especially in the last 40,000 years (Wesson 1991).
Female sexual selection is driven by an attraction to novelty (Darwin ), and novelty is characterized by variations in the way things look, sound, smell or feel which can be manifested physiologically and behaviorally. In recounting his observations of sexual displays, Darwin concentrates on changes in looks and sounds paying less attention to behavior (Miller ), yet he noticed that in their displays, animals emphasized either sight or sound, rarely excelling in both (Darwin ).
Darwin () assigned the insights he derived from his observations of nature to human beings. He listed several anomalous human features derived from sexual selection. The human lack of hair he ascribed to male selection of less hairy females (Darwin ), a trait that became generalized to the species. Zahavi (5) concurs in this assessment. Buss (9) gives as an example the relative lightness of skin color at different social stratas in Japanese culture as evidence of males picking females with the specific qualities that Darwin alluded to.
Examples in Animals:
In most sexual species (the seahorse is a notable exception), the males and females have different equilibrium strategies, due to a difference in time investment: the male can potentially spend five or ten minutes impregnating the female, and have a chance at producing offspring. The female, by comparison, may spend as long as a year pregnant (and unable to produce other children during that time). A male is also much less able than a female to be certain about whether or not he is the true parent of a child, and so will be less interested in spending his energy helping a child who may or may not be related to him. As a result of these factors, males are much more willing to mate than females, and so females are the main ones doing the choosing (except in cases of rape, which occurs in certain primate species). This causes sexual selection often to be more pronounced in males than in females: for example, the peacock has elaborate and colorful tail feathers which the peahen lacks.
The peacock's tail is also an example of a trait that, despite decreasing the apparent biological fitness of the organism, still persists. Sexually selected traits tend to become exaggerated: if most females are looking for long-tailed males, then each female individually does better to select a long-tailed male, since then her male children are more likely to succeed. (Of course, the females do not actually have this thought process; this kind of decision is simply an evolutionarily stable strategy.)
Example in Humans:
An example of sexual selection in human evolutionary history is humans' hairlessness relative to the other great apes. This is part of a general physiological resemblence between adult humans and adolescent chimpanzees (adult humans resemble young chimpanzees to a greater extent than they resemble young humans or adult chimpanzees). This youthful appearance may have evolved because males prefer young-looking mates (a young female is more likely to survive pregnancy). Blonde hair lasting into adulthood is another example of a trait that makes a human look younger.
Although our modern societies are much more complex in comparison to the behavioral groups in which our animal cousins dwell, similar evolutionary forces can be seen in our modern cultures even by the non-scientifically informed populace: it is the male with the most resources ("outward stuff" that he can display -- profession, salary, automobiles, oil wells, clothes, physical appearance, ability to tell jokes, compose sonatas, build monuments, and even belonging to a racial and ethnic background that resembles the dominate culture, etc.) who would be considered a "winner" in that environment where the female resides at that fecundated moment in her life; statistics prove that these features are what attracts human female's attention today in modernity. She chooses the male that she considers the best to carry her genes into the next generation and will give her children the best advantages available.
Three main theories with no direct benefits for the female have been evoked to explain the evolution of male traits and female preferences for them: ³Fisherian runaway process² (Fisher 1915), ³indicator model² (Zahavi 1975), and ³sensory exploitation model² (Ryan 1990).
Fisher introduced a theory where the female preference for a specific male trait is genetically connected to this trait. Females choosing attractive males will have attractive sons, which are again favored by the females. The phenomenon reinforces itself when the females choose more and more exaggerated male traits and the males develop bigger handicaps. At the same time female choice also leads indirectly to a higher demand for the male trait, because of the positive genetic correlation between male trait and female preference for it. This goes on until the male handicap (and the female preference for it) reduces the fitness of the male (and female) too much, and the handicap is restricted by natural selection. An ultimate version of Fisher¹s theory, ³sexy son hypothesis², was presented by Weatherhead and Robertson (1979). They suggested that females mating with attractive males will actually suffer from reduced reproduction success, but this will be compensated for by the high mating success of their sons. Fisher did not present any mathematical model for his theory, but such models have been introduced later, by Lande (1981) and Hamilton and Zuk (1982). Also, Kodric-Brown and Brown (1984) presented a model for the evolution of ³arbitrary² mating preferences, preferences directed at characters that may not themselves be the cause of variation in fitness, but which may reflect that variation due to genetic correlations with directly selected characters.
The indicator model is based on an idea that the male¹s trait gives the female information on the male¹s fitness. This model was first presented by Zahavi (1975). He suggested that the male¹s handicap is a test of his condition. A male with a better level of fitness can produce a more extreme trait than a male with a lower level of fitness, supposing that the male trait is restricted by natural selection (the trait is costly for the male). The indicator model is also called the ³handicap principle² and, according to some of its modified forms, the ³good genes theory². The good genes theory suggests that the male trait reflects the male¹s overall genetic quality (Kodric-Brown and Brown 1984). One variation of the indicator theory is the parasite model of Hamilton and Zuk (1982). In this model sexually selected traits are expected to reveal information about the male¹s resistance to parasites. The condition of the male trait shows the female whether the male has (or has had) parasites, enabling the females to choose males which are most resistant to parasites.
Sensory exploitation hypothesis (Ryan 1990) suggests that female preferences do not coevolve with male sexual signals. According to this model, the male trait is favored simply by virtue of its manipulative effect on a pre-existing bias in the sensory system of females. Biases in female preferences evolve for reasons unrelated to sexual selection. Contrary to the two models presented above, the male trait and female preference for the trait are not expected to have a tightly correlated evolution.
Empirical evidence for the validity of sexual selection theories is limited. Both Fisherian and indicator models require the existence of genetic variation in male trait and female preference, as well as genetic correlation between the two traits. The prime way to distinguish between these models is to look at the effect of mate choice on mating success (Fisherian model) and genetic quality (indicator model) of offspring. Most of the evidence supporting the indicator theory comes from studies tracing the consequences of mate choice on the fitness of the female¹s offspring. Wesson (1991) has reported that the black breast stripe in great tits (Parus major) is a sexually selected trait, and the males with the largest stripes have the best surviving offspring. In collared flycatchers (Ficedula albicollis) the size of the forehead patch of the male is found to contribute genetically to the fledging condition of the nestlings (Miller 1994). House finch (Carpodacus mexicanus) females prefer bright colored males, because they get resources and possibly also genetic benefits for the offspring (Wesson 1991). In great reed warblers (Acrocephalus arundinaceus), females choose mates according to the territory quality and song repertoire of males. The post-fledging survival of the offspring is correlated with their father¹s song repertoire (Andersson 1994). Also, in Nauphoeta cinerea cockroaches (Miller 1994), Drosophila melanogaster, Pavo cristatus peacocks and Hyla versicolor gray tree frogs, offspring fitness has been found to increase if the female can choose her mate (Weatherhead and Robertson 1979).
There are also a few examples supporting the sensory exploitation theory. Male calls in Physalaemus pustulosus frogs seem to have evolved towards a low carrier frequency, preferred by the females. This seems to be because the structure of the female¹s ear is more sensitive to low than high frequency. Also, the females of a related species, P. coloradorum, have this preference, but the males of this species cannot produce lower frequency ³chucks². This suggests that the preference for low frequency calls already existed in females before the chucks evolved in males (Ryan 1990). Buss (1989) has studied genus Xiphophorus, which consists of swordless platyfish and swordtails. In this genus, swordlessness is the primitive state. In platyfishes (Xiphophorus maculatus), the females have been found to prefer conspecific males with artificial swords over those without swords, despite evidence that the common ancestor of platyfish and swordtails was swordless (Buss 1989). In water mites (Neumania papillator), the courting males vibrate their legs fanning pheromones towards the females. Females respond to this vibration as they do to moving prey and recognize the males as potential mates only after the males have deposited spermatophores. It seems that male vibration has evolved as a response for female movements.
Sexual selection was controversial, yet was never focused on by theorists early in the century as a selective process as powerful as natural selection. Many theorists today agree with Darwin that sexual selection may be the primary selective process in human evolution. There are theorists that believe that sexual selection is the most powerful force in species evolution, but not all theorists feel this way (Miller 1994). Human hairlessness and language, Darwin believed, could be explained by sexual selection. Also, males and females could pick different qualities in each other resulting in various irregular human features. In The Descent of Man, Darwin pointed to Africa as the likely origin of our species and to apes as our closest relatives. Wallace, Darwin¹s co-creator of natural selection, was a strong opponent of sexual selection. Many theoreticians ignored the theory altogether. Fisher, in 1930, rescued the theory from oblivion with his theory of runaway sexual selection, which now has mathematical models that support Darwin¹s conjectures. Only beginning in the 1970¹s were male-male competition and female choice supported again as important processes in evolutionary theory.
A current argument within the evolutionary movement today is that there are not two separate parts to natural selection but only one. Thus, all of science is now faced with the formidable task of accepting the argumentative case that it is the female, through her choices, that is really driving the evolutionary force in nature because it willingly forces the male into aggressive positions of competitiveness with each other to attract the female. The instigator of this recent paradigm shift in the merging of natural and sexual selection may be credited to the theories brought forth by Geoffrey Miller in his 2000 book, Mating Mind: How Sexual Choice Shaped the Evolution of the Human
Mind, which argues that all advances and embellishments in the arts, sciences, governments, businesses, and the various industrial and military complexes are really adornments, peacock tails, created by males in which to woo and be selected by females in the evolutionary need to transfer one's genes.
Another current issue concerning a problem with mate choice and sexual selection theory, and something that was pointed out already by Sir Julian Huxley (1923), is that in monogamous species display behaviors do not end with the choice of a partner. Instead displaying continues throughout the breeding season and often throughout the whole existence of the pair bond. It is unclear what information is being transmitted since pair formation is already completed. Some examples of display types performed by members of a pair that seem hard to explain by theories of sexual selection are nest relief, greeting and triumph ceremonies in birds, duetting, allopreening and allogrooming, sexuality and ritualized copulations, and courtship after pair formation. Not only do monogamous pairs engage in display, but it also occurs in other co-operative bonds, such as between allies in group-living primates and during the time consuming mating acts of simultaneous hermaphrodites.
It is important to understand the peculiar history of sexual selection theory because virtually all of 20th century psychology, anthropology, paleontology, primatology, and cognitive science, as well as the social sciences and humanities, developed without recognizing that sexual selection could have played any important role in the evolution of the human body, the human mind, human behavior, or human culture. Since biologists have embraced sexual selection, we must face the possibility that most current theories of human behavior and culture are inadequate, because they may have vastly under-estimated the role of sexual competition, courtship, and mate choice in human affairs.
Currently, sexual selection is one of the fastest-growing and most exciting areas of evolutionary biology and animal behavior. Recent biological work can be found in the journals American Naturalist, Animal Behavior, Behavioral Ecology and Sociobiology, Evolution, Heredity, Journal of Theoretical Biology, Nature, and Science. Research on sexual selection in humans appears often in the journals Behavioral and Brain Sciences, Ethology and Sociobiology, Human Nature, and Psychological Review. The best recent theoretical and empirical review of sexual selection is Andersson (1994) and the best historical review is Cronin (1992), but Darwin's (1871) foundational work The Descent of Man, and Selection in Relation to Sex still rewards careful and repeated reading.
In conclusion, sexual selection is the study of what might be called beauty perception and its role in mating competition in plants and animals. Human obsession with beauty is no different than similar obsessions in other organisms. It is no coincidence that many people have been able to exploit this fact that is not a consequence of a male chauvinistic society. Humans are sexually size dimorphic with males being larger than females, females limiting male reproductive success, and male resources being the ultimate goal for female mate preferences. Given this evolutionary past and the way in which even current human behavior closely matches this history, it is unlikely that we can change human nature to just a small degree. What can be done is attempts to build societies that emphasize the strengths and weaknesses of the two sexes rather than trying to impose sexual equality (that is doomed to fail) onto our appearances and psychologies, traits that have evolved during millions of years in our primate evolutionary past.
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