In his autobiography, Charles Darwin says of sexual selection that it was “a subject which had always greatly interested [him],” and that it was one of the few subjects which he had “been able to write about in full, so as to use all the materials which [he] had collected.”[1] It is no wonder that he felt satisfaction with this idea because it makes such good, logical sense. In one way of thinking, it is easier to make sense of sexual selection than of most other forms of natural selection, since it deals directly with advantages in reproduction. Advantage in reproduction is what drives all of natural selection, Darwin’s mechanism of evolution. Most of us think in terms of “survival of the fittest,” where “fit” means having the means to find food, deal with the weather, and escape from predators. However, survival without reproduction has no effect on the genetic makeup of future generations. Survival is a means of ensuring the final goal of reproduction, and it is differential reproduction that makes the difference between fit and less fit types. The organism who leaves behind more offspring wins the contest.
Natural selection is the mechanism of adaptation, first described by Darwin[2] and Alfred Russel Wallace (1823–1913).[3] Driven by natural selection, populations change over time as certain types survive and reproduce more than other types and are therefore more successful at leaving behind offspring with their genetic characteristics. This can be simply stated as differential reproduction. Although Darwin and others have referred to sexual selection as an alternative to natural selection, the former is probably best understood as a special case of the latter, in which features that enhance an individual’s mating success are favored, rather than or in addition to features that enhance survival. In other forms of natural selection, adaptations for survival are emphasized, but in sexual selection, adaptations for survival are often outweighed by characteristics involving mate acquisition. The principal idea of sexual selection was addressed in Darwin’s early book, On the Origin of Species[4] but was covered more completely in his later book, The Descent of Man, and Selection in Relation to Sex.[5]
In Darwin’s words, “sexual selection depends not on a struggle for existence in relation to other organic beings or to external conditions, but on a struggle between the individuals of one sex, generally the males, for the possession of the other sex.”[6] For some time after he introduced the idea, sexual selection received more opposition than the idea of natural selection. Darwin was accused of inventing the idea because he was unable to explain the evolution of human characteristics through natural selection. Perhaps because of entanglement with the subject of human evolution or because of sex itself—both taboo topics—the idea of sexual selection has been somewhat controversial.
Ernst Mayr (1904–2005) suggested that much of the controversy and confusion has come from Darwin’s sharp distinction between two kinds of selection, natural and sexual.[7] Should we consider the two to be separate phenomena? Darwin apparently did: “Sexual selection depends on the success of certain individuals over others of the same sex in relation to the propagation of the species; whilst natural selection depends on the success of both sexes, at all ages, in relation to the general conditions of life.” There are, however, many cases where natural selection and sexual selection are both implicated and difficult to disentangle.
Mayr considered the distinction to depend on one’s concept of fitness.[8] Many definitions have been proposed. Darwin’s concept of “fit” means well-adapted for existence. Fitness for him had to do with survival of whole organisms, and he considered sexual selection a process that could lead to characteristics that are maladaptive (less fit) in a survival sense but that result in greater reproduction. Early mathematical geneticists redefined fitness in terms of single genes and their contributions to the gene pools of future generations whether from survival advantage or reproductive advantage.[9] Others refer to units of evolution and describe fitness as the “probability of leaving descendants.”[10] Some understand fitness as a property of populations rather than of individuals.[11] It has been said that fitness includes several components, including viability (survival), fecundity (number of offspring), and fertility (probability of producing offspring). If sexual fitness is a component of overall fitness, then natural and sexual selection are not mutually exclusive, and the distinction is merely a point of view. Some have considered sexual selection to be minor compared to natural selection while others have demonstrated the power of sexual selection to mold population changes. The relative roles of survival fitness versus reproductive fitness depend on conditions of the environment in which selection is occurring. In most cases, both operate simultaneously. Although the argument may be mainly semantic, many modern scientists consider sexual selection to be a form of natural selection.
Understanding sexual selection requires a critical understanding of fitness. In sexual selection, we see fitness directly in terms of reproduction even when the characteristics seem to be counter-adaptive in terms of survival. Sexual selection explains the evolution of some of the most bizarre, puzzling, and paradoxical features of animals and plants, like the brilliant and gaudy plumage of some birds, the enormous antlers of some deer, and the luxuriously elaborate flower structures of many plants. Odd features for acquiring mates have evolved in many organisms even when those features impair survival by making escape from predators or food gathering more difficult or by requiring more food and energy to be spent in the process of acquiring a mate. Overgrown antlers may be nuisances to their possessors, but if they enable them to mate with more females and sire more offspring, the antlers are promoted by selection. Agonistic displays or actual fights between males require a considerable amount of energy and may result in injury or death but are promoted by selection because of advantages in mate acquisition. Sexual selection has even favored an odd copulatory suicide behavior in male redback spiders.[12] Males position themselves above the mouthparts of female spiders and comply with cannibalism because cannibalized males receive longer copulations, more fertilized eggs, and a greater likelihood that subsequent suitors will be rejected.
Types of Natural Selection
Darwin described two types of sexual selection:
The sexual struggle is of two kinds: in the one it is between the individuals of the same sex, generally the male sex, in order to drive away or kill their rivals, the females remaining passive; whilst in the other, the struggle is likewise between the individuals of the same sex, in order to excite or charm those of the opposite sex, generally the females, which no longer remain passive, but select the more agreeable partners.[13]
We now recognize these two forms of sexual selection as intrasexual selection, involving competition for mates between members of the same sex (usually males), and intersexual selection, involving a preference by one sex for individuals with certain characteristics in the opposite sex. Intrasexual selection has been more easily accepted and has received quite a bit of attention. Even Darwin’s grandfather, Erasmus (1731–1802), recognized male-to-male competition.[14] On the other hand, the suggestion that sexual selection might occur through female choice was received with skepticism and even ridiculed by Wallace who thought the idea to be entirely speculative.[15] Many studies have now proven the existence of Darwin’s female choice. The concept is well understood, although there is still much to discover about the nature of female choice and the criteria upon which females discriminate. Recent attention has been given to the idea of cryptic female choice, a phenomenon in mammals and birds in which a female can get rid of a male’s sperm without his knowledge.[16] The equivalent in male-to-male competition is sperm competition, where even after mating, males may have differential reproductive success because of sperm number, size, speed, or subsequent matings.[17]
Even when there is obvious struggle among males or obvious choice exerted by females, there may be confusion as to whether sexual selection is occurring. Males often fight for territories rather than for possession of females; and females often choose males because of the quality of their territories. If both males and females choose quality territories that result in the well-being of their offspring, then natural selection rather than sexual selection is in operation.
Reproductive Strategies
Part of understanding these interesting phenomena lies in knowing that there is an inherent inequality between the sexes in terms of investment in reproduction and a resulting contrast in reproductive strategies. In most sexually reproducing organisms, there is a huge discrepancy in size of gametes. Eggs, by definition, are many times larger than sperm. Females, therefore, have a greater cost or investment in each egg than males do in each sperm. Females produce a limited number of eggs (which can be thought of as reproduction opportunities) at a relatively high cost for each one. Females may be even further limited in reproduction because of gestation and maternal care. Males, on the other hand, produce an almost unlimited number of sperm at a relatively low cost for each one and often engage in little or no parental care. This discrepancy has led to different strategies being typical of males and females. For males, a sensible strategy is to maximize reproduction opportunities, mate with as many females as possible, and produce as many offspring as possible, while investing relatively little in each one. For males, it is a contest of numbers. Females are more discriminating. A sensible female strategy is to make the most of the limited opportunities available by being selective about mates and therefore choosy in which genes to combine with hers. A female who makes a poor mating choice may have a total failure of reproduction and a total loss of her genes from future generations. Thus, there is strong selection pressure for females to be highly discriminatory in mate selection. Because a female will have few offspring relative to the potential for a male, she is also more likely to spend large amounts of time and energy ensuring the success of her offspring. This is why parental care, when it exists, is usually the responsibility of the female. Relative parental investment has been considered a key factor in sexual selection.[18] When one sex invests more, members of the other sex will compete among themselves to mate with members of the higher-investing sex. When investment is equal, sexual selection should operate similarly on both sexes.
There are interesting exceptions to the general rule of parental investment. In giant water bugs of the family Belostomatidae, for instance, females cement their fertilized eggs onto the backs of males. Males are, therefore, limited in reproduction by the number of eggs they can carry. Females are less limited because they may mate with a number of males. As a consequence, there is a reversal of parental roles as males are responsible for the care of developing eggs. Daddy water bugs fiercely protect their progeny from predators and aerate them at the water surface to prevent fungal growth. Another interesting example is found in sea spiders. Males possess specialized egg-carrying legs called ovigers. After mating, females entrust the care of their eggs to the well-equipped males and head off in search of other males to mate with. In these cases, the nature of the exceptions helps to prove the rule.
Mating Systems
Perhaps as a result of conflicting sexual strategies and varying environmental conditions, a number of different mating systems have evolved. Monogamy describes the mating of one male and one female. In such systems, parental care by both partners is typical and the pair usually mates for life. Both partners are equally limited in the number of offspring that are produced. A noted example is the Wandering Albatross, a large sea bird.
In polygamy there are multiple partners, either simultaneously or in a series. Polygyny, in which there are several females per male, as in a lion pride, is more common than polyandry, in which there are several males per female. Many species have mating systems with multiple females and multiple males, sometimes called promiscuity. Variation in environmental conditions is undoubtedly an important factor responsible for the variety of animal mating systems. For example, in environments with limited food resources, feeding of offspring by both parents, and therefore monogamy, may be most adaptive.
Julian Huxley (1887–1975) was the first to emphasize the important link between sexual selection and the nature of a species’ mating system.[19] He noted that exaggerated male morphology and display behavior are usually associated with polygyny. He also pointed out the importance of such environmental conditions as food resources and predation pressure in determining the adaptiveness of polygyny. Sexual selection is unlikely or even impossible in monogamous populations if the sex ratio is 1:1 and all individuals get paired. A likelihood of sexual selection exists, however, in populations that are polygamous and even in monogamous populations where a considerable proportion of individuals do not mate.
Sexual Dimorphism
In many species of animals, males and females are strikingly dissimilar in morphology. Males are often larger and stronger, more brightly colored, or possess adornments not possessed by females. When the sexes differ in features other than the character of their genitalia, the differences are considered to be secondary sexual characteristics. Primary sexual characteristics are those directly concerned with mating or gamete production. Darwin was interested in secondary sexual characteristics and noted,
“The modifications acquired through sexual selection are often so strongly pronounced that the two sexes have frequently been ranked as distinct species or even as distinct genera. Such strongly marked differences must be in some manner highly important; and we know that they have been acquired in some instances at the cost not only of inconvenience but of exposure to actual danger.”[20]
Much of sexual dimorphism can be explained by sexual selection, but even Darwin recognized that other forces may be involved in the evolution of differences between the sexes. A classical example is that of the extinct Huia, a bird that once lived in New Zealand. In that species, a striking difference in bill structure was the result of differential adaptation for feeding or, in Darwin’s words, “differences in their habits of life.” The Huia male used its thick bill to chisel away at wood for insects and spiders while the female’s longer bill was able to probe deeper areas. Apparently, the bill difference allowed males and females to occupy different sub-niches and, therefore, reduce intersexual competition for food. We must recognize that sexual dimorphic features may be the result of a number of different selection pressures. Some are important in bringing the sexes together, some are related to competition (sexual or ecological), and some are related to sexual differences in rearing of offspring. Only when the differences result in reproductive advantage of certain individuals over others should they be considered to be evidence of sexual selection.
At least three categories of sexual dimorphism have evolved without sexual selection:
1. Characteristics that enhance mate finding or synchronize mating behavior and physiological readiness do not necessarily provide an advantage over other members of the same sex. The mustache markings of male Yellow-shafted Flickers, for example, are understood to enhance sex recognition. These characteristics evolve as a result of regular natural selection but may often be enhanced through sexual selection.
2. Characteristics that prevent mating with individuals of different species (reproductive isolation) are not typically the result of sexual selection. Hybrids usually have lowered fitness, and characteristics that prevent the formation of hybrids have been favored by natural selection. These include discrimination by females as well as any characteristics that make males more readily identified as members of the same species. The green head of mallards is understood in the context of species recognition. This point was almost missed by Darwin but was recognized by Wallace, who said such things enable “the sexes to recognize their kind and thus avoid the evils of infertile classes.”[21]
3. Characteristics involved in ecological niche separation between the sexes, as previously mentioned, are not the result of sexual selection and were noted by Darwin: “When . . . the two sexes differ in structure in relation to habits of life, they have no doubt been modified through natural selection.”[22]
Birds, Plants, and Primates
Studies of birds have been extremely important in the development of ideas about sexual selection. Darwin cited many bird examples of sexual selection and sexual dimorphism, in part perhaps because secondary sex characteristics may be more conspicuous in birds than in other animals.[23], [24] Birds were also important to Wallace.[25] Sexual selection explains the evolution of bright colors in males of species like the Northern Cardinal. Bright colors are often diet-related and present a relative cost to males in terms of food resources. The disadvantages of diet and of being more easily seen by predators are outweighed by the advantages of acquiring mates. Sexual selection also explains the even more bizarre adornments and behaviors seen in males of other bird species. In the peafowl, the brilliantly colored peacock displays his enormous tail feathers to the cryptically colored peahen, and bowerbird males spend inordinate amounts of time building and decorating bowers to attract females. Males in one group of bowerbirds build an “avenue” bower made of two walls of vertically placed sticks. The male collects hundreds of brightly colored objects—including shells, leaves, flowers, feathers, stones, berries, plastic items, coins, nails, rifle shells, or pieces of glass—and spends hours arranging his collection in and around the bower. Birds continue to inform ecological and ethological research, providing the basis for modern interpretations of sexual selection.[26] Studies of Eastern bluebirds being conducted at Auburn University are revealing the factors upon which female birds make their choices of mates and the benefits of reproduction yielded by their choices.[27]
Not until recently have sexual selection ideas been considered by botanists.[28], [29] Yet competition for mates is probably as important to the evolution of some higher plants as it is to animals. Botanists now refer to scrambles among pollen to reach stigmas and fertilize ovules. The results of male-to-male competition in plants include attraction and reward of pollinators through large showy flowers. Evidence also exists that in some plants female choice dictates which pollen tubes successfully grow down the style to reach and fertilize ovules. A new definition of sexual selection has been proposed in which sexual selection is simply viewed as selection that arises from differences in mating success.[30] This definition can be applied to all organisms and is consistent with Darwin’s writings.
Of all the taxa that interested Darwin, the primates were most important for his ideas about human descent. He discussed the evolution of human secondary sexual characteristics within the context of mammal and, especially, primate evolution.
In primates, differences between the sexes often involve weight and muscular development, body dimensions, and pelage color, as well as such anatomical features as long canines, bulbous noses, gular pouches, shoulder capes, crests, baldness, and skin ridges.[31] Sexual selection in primates, as in most higher animals, is most evident in species with polygynous mating systems. The most marked sexual dimorphism of all primates occurs in the Old World monkeys, including many familiar species such as baboons and macaques. Many of their secondary sexual characteristics are associated with the highly competitive nature of their societies, in which members of both sexes frequently gesture submissively when dominant males display. Adaptations resulting from both environmental selection pressures and social conditions are obvious in the primates. Both have operated together throughout the history of primate evolution. Primate societies provide for cooperation and greater effectiveness in foraging for and protecting the young but also exert selection pressures of a different kind. In most present-day nonhuman primates, a few males produce most of the offspring. There is competition among males but little evidence of female choice.
Sexual Selection in Humans
Have humans been subject to similar kinds of selection pressures? It is almost certainly a fact that we have; however, the topic has been somewhat controversial and direct evidence is difficult to obtain. Darwin conjectured that the male beard, as well as the relative hairlessness of humans compared to nearly all other mammals, are results of sexual selection.[32] He also hypothesized that sexual selection could have caused the differentiation between human races, as he did not believe that natural selection provided a satisfactory answer. It has been hypothesized that many human behaviors not clearly tied to survival benefits—such as humor, music, visual art, verbal creativity, and some forms of altruism—are courtship adaptations that have been favored through sexual selection.[33] In fact, researchers have proposed that the large size of the human brain may not have been selected for in terms of survival and is probably a sexually selected trait.[34] Human vocabulary on average contains more words than necessary for communication and is believed to be used as a way to demonstrate intelligence and other forms of fitness to potential mates.[35] Even attractiveness of the human face has been investigated in terms of sexual selection and it has been said that a sense of human beauty results at least in part from symmetry because it is an indicator to potential mates of health, immunocompetence, developmental homeostasis, and parasite resistance.[36]
Some consider that our courtship behaviors have much in common with courtship of birds and other mammals. Sexually dimorphic characteristics in humans include size, strength, muscular development, metabolic rate, energy utilization, longevity, sexual maturity, sexual drive, complexion, hair pattern, breast development, and voice.[37] At least some of these correlate with those found in other primates. However, humans differ from other primates in the evolution of hair loss, increased skin sensitivity, a behavioral emphasis on contact comfort, loss of estrus, and female orgasm. These are said to relate to a specifically human grade of social organization.[38] The complex of human courtship and social interaction appears to be the result of long-term adaptation to environmental and social conditions in which man developed a polygamous and later a mainly monogamous mating system with effective rearing of young in social units of small size with a tendency for long-term pair bonding. Almost all of this evolution occurred prior to the emergence of complex civilizations. It is no wonder that we now struggle with the role of sexual differences in modern society.
Models of Sexual Selection
The quest to solve the mysteries of sexual selection seems endless, not because Darwin was wrong but because the details of how the process is driven in different systems continue to elude us. Perhaps also because we are fascinated by our own sexuality, scientists today continue to study the phenomenon of sexual selection in the context of modern understanding of genetics, ecology, behavior, and sociology.
Since Darwin first presented the idea, biologists have recognized the importance of sexual selection but have struggled to understand the precise mechanisms. The evolution by sexual selection of traits with a survival disadvantage has been considered a paradox. Many scientists have asked how the process gets started and how a trait becomes exaggerated. R. A. Fisher’s (1890–1962) hypothesis of runaway selection has been popular to explain this puzzle.[39] His idea is that female preference for a certain trait may start arbitrarily, but once it has become established in a population, the trait and the preference will evolve together in an explosively positive feedback loop. The mechanism involves the fact that females with a strong preference for the particular trait, regardless of any survival handicaps the trait may infer, will have a reproductive advantage because their sons will possess the trait and, therefore, be attractive to other females with the same preference. In runaway selection, the strength of female preference increases over generations as females with a stronger preference fare better because of the reproductive success of their sons. The degree to which the trait is expressed in males also increases over generations as the trait becomes more and more highly preferred and may progress well beyond the point of survival fitness. Any heritable trait may be subject to this process because it is not the trait itself but the fact that females choose the trait that makes it attractive. Both the trait and the preference may continue to advance until at some point they may be counterbalanced by natural selection for survival fitness. An elaboration of this concept was coined the “sexy son hypothesis.”[40] In particular, the sexy son hypothesis implies that any other benefits a potential mate may have to offer, compared to the sexual attractiveness of their sons, are irrelevant to the success of a female’s offspring. Since a conceptual model of the runaway process was proposed, others scientists have modeled mathematical proof of the idea.[41], [42]
As a catchy response to the runaway model, a “chase-away model”[43] of sexual selection proposes that exaggerated male traits evolve as a consequence of an evolutionary arms race between males and females for control of reproduction.
Other hypotheses have been developed to explain sexually attractive traits with survival impairment in which females receive survival benefits for their offspring as a result of their choosiness. The “handicap hypothesis”suggests that a male’s ability to survive in spite of a handicap indicates overall fitness and good genes to contribute to offspring.[44] The so-called “good genes model”also considers genetic benefits received by choosy females but still assumes a dichotomy between mating success and survival success.[45] The “truth-in-advertising model”proposes that sexual selection favors the evolution of costly and variable traits, whether they are handicaps or not, because their expression reflects the survivorship, vigor, and overall genetic quality of males who possess them.[46] Females choose males with exaggerated expression of preferred traits because they truthfully advertise desirable attributes that can be passed on to offspring. Others have emphasized the role of parasites in sexual selection by suggesting that females prefer to mate with males with showy sexual displays because they are the healthiest and the most resistant to parasites.[47] By avoiding infected males, choosy females can reduce their risk of contracting contagious diseases, obtain more parental investment, and increase the resistance of their progeny to parasites. The idea of “fluctuating asymmetry”is based on observations that healthier specimens have more left-to-right-sided symmetry than less healthy specimens.[48] Studies with rodents and humans now suggest that chemosensory signals in an individual’s scent reveal a male’s disease resistance and genetic compatibility.[49] Recently an approach has been encouraged that incorporates multiple sexual selection mechanisms, considers a continuum of reproductive and survival fitness, and exploits advances in physiology and molecular biology to understand the mechanisms through which both males and females achieve reproductive success.[50], [51] None of these new models of sexual selection contradict the model as originally proposed by Darwin. It is remarkable that 150 years since his first publication on the idea, modern science has just refined the basic idea.
In contemplation of his life’s work and having listed each of his books, Darwin says in his autobiography, “I think that I have become a little more skillful in guessing right explanations and in devising experimental tests; but this may probably be the result of mere practice, and of a larger store of knowledge.” This is a humble statement from a man so highly revered by biologists since his time. Many scientists have considered Darwin’s idea of sexual selection to be one the most profound insights in all biology. This idea, possibly a favorite of Darwin’s and still popular today, has allowed us to understand the evolution of some of biology’s most interesting phenomena and continues to stimulate investigations into the complexities of life.
Notes
1 - Darwin, C. 1887. The Autobiography of Charles Darwin 1809–1882. ed. N. Barlow. New York: Norton, 1958. This book was edited by Charles’s granddaughter, Nora, with original omissions restored, and includes notes and letters.
2 - Darwin, C. 1859. On the Origin of Species By Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. London: John Murray.
3 - Alfred Russel Wallace independently conceived of an idea very similar to Darwin’s natural selection and wrote a letter about it to Darwin. Darwin’s friends arranged for a simultaneous announcement of their idea at the Linnaean Society in London in 1858. Wallace’s 1858 essay was entitled, “On the tendency of varieties to depart indefinitely from the original type.”
4 - Darwin, 1859.
5 - Darwin, C. 1871. The Descent of Man, and Selection in Relation to Sex. London: John Murray.
6 - Ibid.
7 - Mayr, E. 1972. Sexual Selection and Natural Selection. In Sexual Selection and the Descent of Man: The Darwinian Pivot. ed. B. Campbell. New Brunswick: Aldine Transactions.
8 - Ibid.
9 - J.B.S. Haldane, R.A. Fisher, and S. Wright were mathematical geneticists who published works in the early 1930s involving models of evolution.
10 - Thoday, J. 1953. “Components of Fitness.” Symp. Soc. Exptl. Biol. 7: 96–113.
11 - Fisher, R. 1930. The Genetical Theory of Natural Selection. Oxford: Clarendon Press.
12 - Andrade, M. 1996. “Sexual Selection for Male Sacrifice in the Australian Redback Spider.” Science 271: 70–72.
13 - Darwin, 1871.
14 - Darwin, C. 1794. Zoonomia. London: J. Johnson.
15 - Wallace, A. 1889. Darwinism: An Exposition of the Theory of Natural Selection and Its Applications. London: Macmillan.
16 - Eberhard, W. 1996. Female Control: Sexual Selection by Cryptic Female Choice. Princeton: Princeton University Press.
17 - Parker, G. 1970. “Sperm Competition and its Evolutionary Consequences in the Insects.” Biological Reviews 45: 525–67.
18 - Trivers, R. 1972. Parental Investment and Sexual Selection. In Sexual Selection and the Descent of Man: The Darwinian Pivot. ed. B. Campbell. New Brunswick: Aldine Transaction.
19 - Huxley, J. 1938. “Darwin’s Theory of Sexual Selection and the Data Subsumed by It.” The Light of Recent Research. American Naturalist 72 (742): 416–33.
20 - Darwin, 1871.
21 - Wallace, 1889.
22 - Darwin, 1871.
23 - Ibid.
24 - Selander, R. 1972. Sexual Selection and Dimorphism in Birds. In Sexual Selection and the Descent of Man: The Darwinian Pivot. ed. B. Campbell. New Brunswick: Aldine Transaction.
25 - Wallace, 1889.
26 - Selander, 1972.
27 - Liu, M., L. Sieferman, H. Mays Jr., J. Steffen and G. Hill. 2009. “A Field Test of Female Mate Preference for Male Plumage Coloration in Eastern Bluebirds.” Animal Behaviour 78 (4): 879–85. Geoff Hill and students at Auburn University have studied Eastern bluebirds for several years. Much of their research deals with sexual selection.
28 - Willson, M. 1994. “Sexual Selection in Plants: Perspective and Overview.” American Naturalist 144: S13–S39.
29 - Andersson, M. and Y. Iwasa. 1966. “Sexual Selection.” Trends in Ecol. & Evol. 11 (2): 53–8.
30 - Arnold, S. 1994. “Is There a Unifying Concept of Sexual Selection that applies to both Plants and Animals?” American Naturalist 144: S1–S12.
31 - Crook, J. 1972. Sexual Selection, Dimorphism, and Social Organization in the Primates. In Sexual Selection and the Descent of Man: The Darwinian Pivot. ed. B. Campbell. New Brunswick: Aldine Transaction.
32 - Darwin, 1871.
33 - Miller, G. 2000. The Mating Mind: How Sexual Choice Shaped the Evolution of Human Nature. London: Heinemann.
34 - Schillaci, M. 2006. “Sexual Selection and the Evolution of Brain Size in Primates.” PloS One 1(1). http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1762360.
35 - Miller, 2000.
36 - Grammer, K. and R. Thornhill. 1994. “Human (Homo sapiens) Facial Attractiveness and Sexual Selection: The Role of Symmetry and Averageness.” Jour. Comp. Psychology 108 (3): 233–42.
37 - Caspari, E. 1972. Sexual Selection in Human Evolution. In Sexual Selection and the Descent of Man: The Darwinian Pivot. ed. B. Campbell. New Brunswick: Aldine Transaction.
38 - Ibid.
39 - Fisher, 1930.
40 - Weatherhead P. and Robertson R. 1979. “Offspring Quality and the Polygyny Threshold: ‘The Sexy Son Hypothesis.’” American Naturalist 113 (2): 201–08.
41 - Lande, R. 1981. “Models of Speciation by Sexual Selection on Polygenic Traits.” PNAS 78: 3721–25.
42 - Kirkpatrick, M. 1982. “Sexual Selection and the Evolution of Female Choice.” Evolution 36 (1): 1–12.
43 - Holland, B. and W. Rice. 1998. “Perspective: Chase-Away Sexual Selection: Antagonistic Seduction versus Resistance.” Evolution 52 (1): 1–7.
44 - Zahavi, A. 1975. “Mate Selection –A Selection for a Handicap.” Journal of Theoretical Biology 53: 205–14.
45 - Hamilton, W., and M. Zuk. 1982. “Heritable True Fitness and Bright Birds: a role for Parasites?” Science 218, 384–87
46 - Kodric-Brown, A. and J. Brown. 1984. “Truth in Advertising: The Kinds of Traits Favored by Sexual Selection.” American Naturalist 124 (3): 309–23.
47 - Hamilton and Zuk, 1982.
48 - Moller, A. and A. Pomiankowski. 1993. “Fluctuating Asymmetry and Sexual Selection.” Genetica 89 (1–3): 267–79.
49 - Penn, D. and W. Potts. 1998. “Chemical Signals and Parasite-Mediated Sexual Selection.” Trends in Ecol. & Evol. 13 (10): 391–96.
50 - Kokko, H., R. Brooks, J. McNamara, and A. Houston. 2002. “The Sexual Selection Continuum.” Biological Sciences 269: 1331–40.
51 - Zeh, J. and D. Zeh. 2003. “Toward a new Sexual Selection Paradigm: Polyandry, Conflict and Incompatibility.” Ethology 109: 929–50.