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Abstract. Sexual selection arises from the advantages that individuals have over others of the same sex and species in mating competition for reproduction. This process may give rise to extravagant sexual characters that are directly detrimental to survival, but beneficial to mating success. Current theoretical and empirical findings suggest that mate preferences are mainly cued in on health including developmental health. Beautiful and irresistible features have evolved numerous times in plants and animals due to the immense selection pressures mainly caused by females, and such preferences and beauty standards provide evidence for the claim that human beauty and obsession with bodily beauty equals similar tendencies throughout the plant and animal kingdoms. The beauty, cosmetics and plastic surgery industries are therefore only surface phenomena that supports this evolutionary interpretation. Human beauty standards reflect our evolutionary distant and recent past and emphasize the role of health assessment in mate choice. Given these findings, it is extremely unlikely that human sexual behavior or mate preferences will change to any significant degree during the future, even in the presence of totalitarian measures.
It is a widespread notion that humans differ from all other animals. It is also a widespread belief that somewhere in the world it is possible to find a culture where people live in harmony with nature and each other, and were it not for the existence of Western culture we would be able to achieve this Paradisic state. Both claims are erroneous. Humans carry an incredibly large baggage of evolutionary history, and the mere fact that our DNA sequences are similar to those of our nearest relatives among the great apes to more than 99% makes it a highly unlikely claim that we could just step out of our ape dress. Human nature is to a large extent universal. This is also the case with respect to certain beauty standards and the ways in which males and females interact.
Sexual selection theory is concerned with 'the advantages that certain individuals have over others of the same sex and species, in exclusive relation to reproduction' (Darwin 1871). What is sexual selection and why is it important for judgments of human beauty standards? 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 colours of many fish and birds. Darwin in his 1871 treatise was the first person to realize the explanation for the evolution and the 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 contrary, extravagant secondary sexual characters are costly, often reduce survival prospects and can only be maintained by sexual selection. Two mechanisms are involved in sexual selection: 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 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 fishes and many kinds of vocalizations. Humans are not much different from other organisms by having evolved sexual size dimorphism due to male-male competition (remember than 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 oestrogens and male choice.
Extravagant secondary sexual characters are considered to be beautiful by humans and perhaps also by animals in general. If both animals and humans find similar structures attractive, the likely reason is that animal and human psychologies have evolved to perceive and become agitated by these impressions. Sugar is only perceived to be sweet by humans because the pleasant and powerful feeling of sweetness during our evolutionary past has been shaped by the benefits that we obtained in terms of energy and nutrition from eating fruits and other biotic structures with particular chemical properties. In the same way, faces of women and particular proportions of waists and hips are only considered to be beautiful because our ancestors with such preferences left more and more healthy offspring than the average individual in the population.
Sexual selection can work in a number of different ways because sexual signals may provide different kinds of information to potential receivers. Human evolutionary psychological studies across a wide range of cultures have shown that men rank female beauty the highest among a long list of attributes, while women rank male resources as the most important attribute of potential mates (Buss 1994). Female beauty signals youth, fertility and health while male resources signal male competitive ability and health.
The advantages of sexual selection as seen from the point of view of the choosy part may come in either of the following ways (review in 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 such 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 characters, 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 ever 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 although it will work better in mating systems with an extreme skew in mating success.
An alternative model of female mate preferences that gives rise to indirect fitness benefits is the so-called good genes hypothesis with is based on the handicap principle. Since secondary sexual characters are costly, only individuals in prime condition may be able to develop and carry such displays. It is only the differential ability of certain individuals due to their genetic constitution that allow them to develop seriously handicapping and costly traits (Zahavi 1975). The honesty and reliability of such displays is maintained by their costs and their differential cost to low quality individuals. A choosy female will by preferring the most extravagantly ornamented male produce offspring of high viability simply because low quality individuals with an inferior genetic constitution will not be able to cheat and produce an extravagant character. There is a number of studies consistent with this mechanism of sexual selection (Andersson 1994).
Charles Darwin (1871) was the first person to extensively think and write about human beauty standards from a biological point of view. The main problem with Darwin's approach was the he relied extensively on correspondence with missionaries in order to obtain information about the beauty standards in different human cultures. Obviously, when these are collected by persons with a British beauty standard, there appears to be little evidence of generality! Contrary to most other fields of evolutionary biology Darwin actually put studies of human beauty to rest for a century by these claims about lack of general principles. It is only recently that features of human facial and bodily beauty have been cross-culturally validated (Perrett et al. 1994; Singh 1993). Estrogenized female faces with small chins, androgenized male faces with large chins and cheek-bones, and female bodies with optimal waist-to-hip ratios around 0.7 appear to be considered generally attractive. Interestingly, these are features that reflect fertility and general health and thus provide important phenotypic information to mate prospecting individuals (see below).
Darwin's claims about the lack of a general beauty standard were at odds with the mere magnitude of the beauty industry. Although feminist claims may suggest that this obsession with beauty is an outcome of male-initiated capitalist activities, there is plenty of evidence for females putting lots of time an effort into their looks as long as archaeological and historical information dates back. Human obsession with beauty in modern Western societies is not much different from similar efforts in other societies, and the mere success of the industry is a reflection of the immense strength of our psychological adaptations and mate preferences. The strong beliefs among women in the wonders of cosmetics and their ability to provide eternal youth obviously is based on the presence of the same psychological adaptations. Any book on the use of cosmetics is a manual of how to accentuate the features that are known to be reliable health and fertility indicators: estrogenized faces and symmetric facial features. With the development of plastic surgery these much desired and admired features of human female beauty can be acquired in a more permanent state as compared to the temporary state of cosmetics. Not surprisingly almost all plastic surgery attempts to correct asymmetries and exaggerate traits that are considered to be generally beautiful and reliable indicators of health and fertility.
Parasites and diseases have played an important role in human evolution, and perhaps even more so than in many of our close relatives. Parasites exert tremendous selection pressures on their hosts by reducing their longevity and reproductive success. It has been known for a long time that individuals differ in their susceptibility to parasites because of genetically determined host resistance, and sexual selection for healthy partners would obviously provide choosy individuals with potentially important fitness benefits (Hamilton and Zuk 1982). Parasite-mediated sexual selection may benefit choosy individuals by preventing them from obtaining mates with contagious parasites that could spread both to themselves and their offspring, obtaining mates that were efficient parents, and obtaining mates that were genetically resistant to parasites (Møller 1990). There is considerable evidence for secondary sexual characters in a wide variety of organisms reliably reflecting levels of parasite infections (Møller 1990), and studies of a diverse array of plants and animals show that parasites render their hosts more asymmetric and hence less attractive than unparasitized individuals (Møller 1996). This is also the case in humans: Men throughout the cultures of the world value female beauty higher than any other attribute, but the importance of beauty is the highest in cultures with serious impact of parasites such as malaria, schistosomiasis and similarly virulent parasites (Gangestad and Buss 1993).
Hosts may reliably avoid the debilitating effects of parasites by evolving efficient immune defenses, and the immune system in humans is one of the most costly activities only equalled by the brain. Immune defense may play a role in host sexual selection because secondary sexual characters reliably may reflect the immunocompetence of individuals (Folstad and Karter 1992). Many secondary sexual characters develop under the influence of testosterone and other sex hormones. However, hormones have antagonistic effects of the functioning of the immune system, and only individuals in prime condition may be able to develop the most extravagant secondary sexual characters without compromising their ability to raise efficient immune defenses. An alternative version of this model just assumes that both secondary sexual characters and immune defenses develop in response to condition, and the reliability of the signaling system is therefore not based on negative interactions between androgens and immunocompetence (Møller 1995). There is some empirical experimental support for the immune system being involved in reliable sexual signaling in birds, but tests for humans are still unavailable (Saino and Møller 1996).
Developmental stability reflects the ability of individuals to maintain stable development of their morphology under given environmental conditions (Møller and Swaddle 1997). While developmental noise and various developmental upsets tend to destabilize development, developmental control mechanisms have the opposite effects on the phenotype. Developmental stability cannot really be measured, but that is not the case for developmental instability or deviations from the ideal developmental outcome. Measures of developmental instability include fluctuating asymmetry and the frequency of phenodeviants, but also other measurements. A character demonstrates fluctuating asymmetry when symmetry is the norm and deviations from symmetry are randomly distributed with respect to side (Ludwig 1932). In other words, characters that demonstrate fluctuating asymmetry have frequency distributions of signed left-minus-right characters values that are normal with a mean value of zero. Most morphological features of plants and animals demonstrate fluctuating asymmetry. Phenodeviants are relative large deviations from normal phenotypes such as a position of the heart in the right side of the body cavity or the presence of an even number of fingers on a hand.
Fluctuating asymmetry is a particularly useful measure of developmental control ability for several reasons. First, we know the optimal solution a priori: it is symmetry. This is a particularly unique situation in biology because optima usually have to be determined before the research can start, and the optimum will even then only be specific to particular circumstances. Second, fluctuating asymmetry develops in response to an enormous range of genetic and environmental factors that tend to upset developmental processes (review in Møller and Swaddle 1997). These include genetic factors such as inbreeding, hybridization, mutation and to some extent homozygosity, and environmental factors such as quality and quantity of nutrients, pollutants, radiation, population density, parasites, predators, noise, and light regime. Simple asymmetry measures therefore integrate an enormous range of internal genetic and external environmental factors that each contribute to destabilization of development. Third, fluctuating asymmetry is very easy to measure and we can investigate plants, insects, birds and humans using the same simple and uncostly tool, a precise ruler. Fourth, we cannot investigate how plants and animals feel about or perceive their environment, but we can answer this question indirectly by measuring their asymmetry because asymmetry reliably integrates the consequences of all disruptive effects of the environment. Since the optimal phenotype is the symmetric one because it promotes performance, any deviation from perfect symmetry can be considered a sub-optimal solution to a design problem that will result in performance problems in the future. It was probably difficult for a pre-historic human to escape from a lion, but it was even more difficult to escape with two legs of unequal length. Indeed, skeletal remains from pre-historic Indians have shown that individuals that were old had more symmetric bones than individuals that died as young (Ruff and Jones 1984). This finding is particularly interesting because continuous re-modeling of bones during life generally gives rise to increasing asymmetry among older humans.
It is perhaps not surprising that asymmetry has been found to be extremely important for plants and animals including humans when faced with the realities of life, the struggle for survival, mates and reproduction (Møller and Swaddle 1997). The continuous selection against asymmetry starts already among sperm and eggs within females of species with internal fertilization: Only a small fraction of gametes ever makes it, and it is mainly those with deviant phenotypes that are disadvantaged (Møller 1997). Developmental selection against deviant gametes and zygotes appears to be a very widespread phenomenon. Fruit and seed abortion is extremely common in plants. Experimental work has demonstrated that in the flowering plant fireweed (Epilobium angustifolium) around three quarters of all embryos are aborted during the first few cell divisions because of irregular developmental patterns (Møller 1996b). Interestingly, the abortion frequency is directly related to the symmetry of the flowers of both the pollen donor and the pollen recipient. This finding implies that a similar developmental mechanism is involved in the generation of symmetry in embryos and flowers. Similar phenomena have been described among a wide range of organisms spanning invertebrates and vertebrates including humans (Møller 1997). For example, a study of the scorpion (Pandanus imperator) has shown that the new-born offspring have to climb to the back of their mother during their first day of life. Some offspring are born with deformities and are therefore unable to perform this task. The mother eats these offspring after a while, and this act makes sense because malformed offspring that were reared away from their mother together with siblings with normal phenotypes always performed poorly even as adults (D. Mahsberg in Møller 1997). Infanticide has been and is still a common practice in many human societies mainly directed towards children with deviant phenotypes. This behaviour has obviously been adaptive by avoiding wastage of costly resources on offspring with poor survival prospects. Evolutionary psychological studies of parental reactions to newborns have demonstrated that modern human beings still carry psychological adaptations towards this end by reacting with strongly negative feelings that best can be described as disgust and aggression when confronted with children with increasingly deviant appearances.
Asymmetry also matters tremendously when its comes to the mating game. Developmental stability and sexual selection are closely associated in a wide variety of organisms ranging from plants, flies, grasshoppers and fish to birds and mammals (Møller and Thornhill 1997). For example, barn swallow (Hirundo rustica) females prefer males with symmetric tails over males with asymmetric tails (Møller 1992). Similarly, women prefer men with symmetric faces and bodies (Grammer and Thornhill 1994; Thornhill and Gangestad 1994), and the number of sexual partners during life is directly related to skeletal asymmetry in men (Thornhill and Gangestad 1994). Since symmetry relates to performance in general, choosy females that prefer symmetric males will obtain mates that are better able to provide resources, but also able to provide genes for developmental health to the offspring. Given the intense developmental selection against asymmetric offspring, females will also benefit in terms of increased fecundity.
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 that 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 chauvinism 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 behaviour 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.
My research was supported by grants from the Danish and Swedish Natural Science Research Councils. I am grateful for the invitation by Third Culture Copenhagen to participate in the summer activities of 1996.
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