Sexual Selection

Males and females of many species exhibit significant differences in addition to the difference in reproductive organs. The distinction of gender through secondary sex characteristics is known as sexual dimorphism. This is most often expressed as a difference in size, with the males usually larger, but also involves differences such as plumage in male birds, manes on male lions, and antlers on male deer. In most cases, the male is the showier sex of the species.

What It Is and How It Works

Sexual selection is the evolutionary process that arises from competition among members of one sex (the competitive sex) for access to members of the other sex (the limiting sex). According to the theories of Charles Darwin, sexual selection should be distinguished from the process of natural selection because the traits that evolve via sexual selection often appear to have a negative effect on the survival rate of their bearers. There are two basic forms of competition for mates that affect the type of traits that evolve. One is intrasexual selection, which includes overt competition among the members of the competitive sex to gain control or monopoly over the limiting sex. This leads to selection of traits such as weapons, large body size, aggression, strength, and endurance. Intersexual selection is when the limiting sex can exercise a choice of mates, leading to elaboration of structures, displays, vocalizations , and odors in the competitive sex.

Sending and receiving signals is a significant step toward mating as the type and intensity of the signal will determine whether or not a mate is obtained. One process of signal evolution that is involved in the search for a mate is called sensory exploitation. According to this model, signal receivers often have inherent, or built-in, preferences that can be exploited by a manipulative signaler to create new signals. For instance, suppose female birds searched preferentially for red seeds while foraging. Because the only time they encounter red is in seeds, it would be advantageous to evolve a general preference for red objects. A mutant male that adds red to its plumage may then be able to exploit this preference for the color red as long as it can be expressed in the context of mate choice. A new signal can then evolve that had no historical link to mate choice but only to an irrelevant context such as foraging.

It is important to note that there is no new information conveyed to the females by the red males. In fact, there may be predatory risks if red males are easier to spot and thus more likely to be killed. Costs to females may be an adaptation to avoid exploitation such as better discriminating abilities or the decoupling, that is, the separation of behavioral strategies, for foraging and decisions about mating. However, females may be able to find males of the same species, termed conspecific males, more easily if the males bear a red patch. Furthermore, red males may provide additional information not provided by normal males. If the intensity of redness is a good indicator of the males' health, then a preference for red males over nonred ones could be a way for females better to identify a good mate. Whether the signal is costly or beneficial, sensory exploitation by itself is highly unstable. Instead, it is followed by coevolution between sender and receiver.

Male Attraction Signals

Females are more often the choosy sex and males the competitive, advertising sex (though in some animals the roles are reversed). Two significant models for the evolution of mate-attraction signals are the runaway selection model and the good genes model. In both of these there is a simultaneous evolution of a female preference for a particular male trait and evolution of that male trait.

Runaway selection model.

This model best defines polygynous species (one in which a number of mates are taken). Initially, there must be some genetic variability associated with variability in physical characteristics of a male trait such as the brightness of a color spot. Males with the preferred trait will obtain more mates, and because the females will be those who tend to prefer that trait, the genes for the female preference will become linked with the male trait in their offspring. Females with the preference also benefit because their sons will have that trait and so will win more mates, thereby spreading the genes of the female. Under the right conditions, a runaway evolutionary process can occur with the male trait becoming larger and the female preference for it becoming stronger. This process stops when the male trait becomes so large that it imposes a cost on the male that outweighs the benefits. The traits that evolve through this model are termed arbitrary traits, because they can take any type of conspicuous form and not provide any information to the female about the male's fitness.

Although this process requires a certain set of circumstances to get under way, there are several different situations that could bring about the initial trait and the preference for it. One possibility is sensory exploitation, as discussed above. Another factor could be that the male trait is initially favored by natural selection and a female preference for this trait subsequently evolves. A third possibility is that the females evolve a preference for the trait because it helps distinguish conspecific males from those of a closely related species, thereby preventing genetic mixing between different species, a process termed interspecific hybridization.

Good genes model.

This model actually proposes that costly and conspicuous male traits become the trait of choice by females because they indicate some aspect of male quality. Females will benefit from mating with these males because the offspring will have higher survivorship or viability. The male traits are called indicator traits, and the costs to males are deemed necessary costs when in pursuit of a mate. Coevolution of the male indicator trait, intrinsic male viability, and female preference for the trait is the basis for the genetic model of this process. One example of how this may work is the classic handicap model, in which males acquire a trait such as a heavy set of antlers, which obviously imposes a survivorship cost. Low-quality males cannot support the cost of this trait, and so it is seen as a handicap, whereas high-quality males survive and their genes dominate. However, the handicap is balanced out by the higher net fitness of males without this trait and its cost. Another theory is the condition-dependent indicator model, in which males vary the expression of the preferred trait, such as the speed at which the call is performed (termed call rate) so as to optimize their mating success and survival. High-quality males can afford to expend more energy on expression than can low-quality males and so trait magnitude is a good indicator of male quality. Last, in the revealing indicator model all males attempt to develop the trait to the same magnitude and pay the same cost, but the condition of the trait is lower in low-quality males. For instance, call frequency (the number of times a call is repeated) or feather condition are good examples of such traits.

Signalling for a Mate

Many aspects are taken into account when an animal signals for and chooses a mate. Anatomical traits play a role in the attraction of a potential mate. Non-weapon body structures such as color patches, elongated tails, and fins and feather plumes are termed ornaments. Many ornaments appear to be good indicators of the quality of the male. They often come into play when the male performs visual displays to attract the attention of a female. Vigorous displays are indicative of a male's high energy, and thus that male is likely to win out over the less vigorous male.

Auditory signals.

In birds, insects, mammals, and fish, these are also obvious targets of female choice. In all of these groups, the females tend to prefer males with greater calling rates, sound intensity, and call duration. These features actually increase the stimulation value of the signal, so it is possible that the preference arose from the sensory bias of the female receivers and that the traits themselves are just arbitrary. These call characteristics are all energetically expensive, and it seems that females prefer the most costly calling. For example, female grey tree frogs prefer calls that have a long duration and are repeated at a slow rate over a call that is brief and at a high rate though it has the same acoustic "on" time, meaning the calls are heard for the same amount of time. Studies have shown that the long duration calls require a lot more energy than the shorter calls. Such findings suggest that display vigor is an accurate indicator of male quality. It has also been found that costly call characteristics are correlated with age, size, dominance, or parasite load. In addition, they provide females with good gene benefits such as faster growing and more viable offspring. Finally, in some species, call rate is a good index of benefits the females can expect to receive, such as large sperm or territory rich in resources.

Vocal signals.

Another type of call is the copulation call. These are usually vocal signals and may be given by the male, female, or both sexes. In most cases it is difficult to determine the function of the signal and the intended receiver. However, copulation signals are unlikely to be incidental as they are highly structured and individually distinctive. In monogamous species, female copulation signals may be for synchronization of orgasm with the male, as there is usually no other possible intended receiver in the vicinity at that time. In socially mating species, the intended receiver could be external to the copulating pair. The female signals could be intended for other females and to increase dominance status in the group. The signals could also serve as a recruiting call for other male mates and incite competition among them so that the female can choose the dominant male as father of her offspring.

Male copulation signals could serve to transmit information about the male's mating success to other females. It has been found that males who make these calls are more likely to get attacked by other males, but they are also more likely to obtain more matings compared to males that 'do not call. Alternatively, the intended recipient of male copulatory signals could be other males. For example, postcopulatory male rats repeatedly emit vocalizations that are similar to the ultrasonic whistles signaling an alarm situation or a defensive threat. The male rats often appear lethargic and inactive at this time but will aggressively attack any other male that tries to approach the mated female. The signal then seems to be indicating mate-guarding intentions.

The nuptial gift.

This is a slightly different tactic in the search for a mate. Males of some insect and bird species will offer prey items as nuptial gifts during courtship. The females may base their decision on the size, or quality of these items, as well as the rate at which these items are provided. Females that are egg-producing would clearly benefit from receiving food as a nuptial gift. If provisioning rate is correlated with offspring feeding rate in paternal care species, the behavior is an obvious indicator with direct benefits. Another consideration is that if the cost to the male increases with gift magnitude, then it could be an indicator of heritable fitness. However, there is a risk of "false advertisement." In the marsh hawk, provision of the nuptial gifts is a good indicator of the male's nesting provisional ability. But the males sometimes use this signal deceptively in order to attract females into polygynous matings, a disadvantageous position for the female hawk.

In some species there is a sex-role reversal in terms of competing for mates. The sex-role reversal results from evolution of male parental investment, although not all paternal care species display complete reversal of courtship roles. A determining factor is the extent to which the male cares for the offspring. If the males can care for the offspring of several females simultaneously, the sex ratio is still skewed in favor of males. In those circumstances, males are still the competitive gender and will perform aggressive or persuasive courtship behaviors. However, if the males can care for the offspring of only one female, then males become a limiting resource for females. The females will then compete for males and develop aggressive behaviors, ornaments, and mate-attraction displays most often associated with the male gender.

see also Reproduction, Asexual and Sexual; Sexual Dimorphism.

Danielle Schnur

Bibliography

Andersson, M. Sexual Selection. Princeton, NJ: Princeton University Press, 1994.

Bradbury, Jack W., and Sandra L. Vehrencamp. Principles of Animal Communication. Sunderland, MA: Sinauer, 1998.

Campbell, Neil A. Biology, 3rd ed. Berkeley, CA: Benjamin/Cummings Publishing Company, 1993.

Parker, G. A. Mate Choice. Cambridge, U.K.: Cambridge University Press, 1983.

Sexual Selection

English naturalist Charles Darwin revolutionized scientific thinking when he proposed that species evolve over time to become adapted to their environments by means of natural selection in his On the Origin of Species (1859). He was initially puzzled, though, by the seemingly useless exaggerated characters often found in animals, particularly males. The long and colorful tail of the peacock, for example, seemed to hinder rather than help its bearer survive. In his later work, The Descent of Man, and Selection in Relation to Sex (1871), Darwin proposed that some characters do not increase survival, but instead increase reproductive success. He called this sexual selection, which refers to the process that produces traits that affect an individual's reproductive success as a result of competition over mates.

While both sexual selection and natural selection are evolutionary processes that increase an organism's fitness, they differ in several important ways. Environmental, physical, or biological factors often drive natural selection, whereas sexual rivals and mates are the exclusive agents of sexual selection. Furthermore, the evolutionary effects of sexual selection differ markedly from those of natural selection. Sexual selection frequently produces sexual dimorphism and exaggerated male traits, often in opposition to the forces of natural selection.

For example, male widowbirds have extraordinarily long tails (more than twice their body length) that make flight more difficult. When researchers manipulated the tail length of several males, they found that female widowbirds preferred males with longer tails to males with short or normal length tails. Thus, while the long tails of widowbirds may be selected against by natural selection, they are favored by sexual selection.

There are two broad categories of sexual selection: intrasexual selection (members of one sex compete among themselves for reproductive opportunities with individuals of the other sex) and intersexual selection (members of one sex choose among members of the other sex).

Intrasexual Selection

Many examples of intrasexual selection are readily observable. Males of many species fight, display, vocalize, and otherwise compete for the opportunity to mate with available females. Male deer fight with their antlers and enormous male elephant seals fight with their bulk to establish dominance and consequently the right to mate with females. Male red-winged blackbirds display and sing to establish their territories, the quality of which determines the number of mates they will attract.

Post-mating competition also occurs. Male dragonflies often guard their mates after copulation to ensure that the female lays her clutch of eggs before remating. Male fruit flies sometimes transfer a substance to their mate that inhibits courtship by subsequent males. Male dunnocks (a small European bird) often peck the cloaca of their mate until she everts it, sometimes ejecting sperm.

Once the male has successfully rid the female of the sperm from a previous mate he will proceed to reinseminate her. Some male parasitic worms cement the genitalia of their mates after copulation to form a copulatory plug. These male worms take intraspecific competition one step further by occasionally "mating" with rival males and cementing the genitalia of their rivals to prevent subsequent sperm transfer.

Intersexual Selection

For several decades after Darwin presented his theory of sexual selection, most naturalists discounted the importance of intersexual selection, or mate choice. However, in the 1950s a few scientists began to revisit this subject, and by the 1980s mate choice had gained wide popularity as a topic of study.

Many exaggerated male traits are now thought to have evolved as a result of female mate choice, although several competing hypotheses exist to explain the origin and maintenance of these female preferences. Ronald A. Fisher proposed an explanation called "runaway sexual selection" in The Genetical Theory of Natural Selection (1930). Fisher suggested that as females began to evolve a preference for a particular male trait, such as tail feather length, these females would be more likely to mate with males who displayed the preferred trait. The offspring of these matings would inherit the genes for both the male trait and the female preference, resulting in a genetic correlation between the preference and the trait. Consequently, as the male trait spreads because females prefer it, the female preference itself also spreads because it is linked with the male trait. This is called a self-reinforcing choice, and is one way that exaggerated male traits can evolve without conferring any direct benefits on the females who prefer them.

Another explanation for the evolution of female choice is called the handicap hypothesis. In his study "Mate Selection—A Selection for a Handicap" (1975), Amotz Zahavi suggested that exaggerated male traits indicate to females that the male is healthy enough to survive despite his substantial handicap. The exaggerated trait is a signal through which females can assess a male's genetic quality, and therefore is often called a good genes hypothesis. This is another way that exaggerated male traits can evolve without directly benefiting the females who prefer them.

Other explanations of the evolution of female mate choice include sensory bias (for example, female frogs prefer males who call loudly or in a low pitch because they can hear them better) and direct benefits (for example, females might prefer males who provide superior resources, defense, or parental care).

Experimental Techniques

The refinement of several genetic analyses in the late 1980s and the 1990s have contributed greatly to the study of sexual selection. Using deoxyribonucleic acid (DNA) fingerprinting, microsatellite DNA typing, and related techniques, researchers can confidently assign paternity to offspring using genetic markers, whereas in the past they had to rely on behavioral cues. These techniques are particularly well used in avian studies, where scientists are learning that many birds thought to be monogamous actually have a high frequency (30 to 95 percent) of promiscuity. Using molecular techniques to definitively assign paternity has and will continue to further the study of sexual selection, particularly mate choice and sperm competition.

see also Behavior, Genetic Basis of; Darwin, Charles; Evolution; Mating Systems; Natural Selection; Sexual Reproduction

Michelle J. Solensky

Bibliography

Andersson, Malte. Sexual Selection. Princeton, NJ: Princeton University Press, 1994.

——. "Female Choice Selects for Extreme Tail Length in a Widowbird." Nature 299 (1982): 818–820.

Darwin, Charles. On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. London: John Murray, 1859.

——. The Descent of Man, and Selection in Relation to Sex. London: John Murray, 1871.

Fisher, Ronald A. The Genetical Theory of Natural Selection. Oxford: Clarendon Press, 1930.

Zahavi, Amotz, and Avishag Zahavi. The Handicap Principle: A Missing Piece of Darwin's Puzzle. New York: Oxford University Press, 1997.

Sexual Selection Theory

BIBLIOGRAPHY

Although Charles Darwin is best known for his theory of evolution by natural selection, he was also fascinated by the differences between males and females in all species. His 1871 book, The Descent of Man and Selection in Relation to Sex, documented these differences and suggested an explanation for them. Darwin pointed out that traits such as peacock tails that occur in only one sex could be of two types: The primary sexual characters enable males to produce sperm and females to produce and nurture eggs; the evolution of these traits is easy to explain via natural selection. The secondary sexual characters, such as the long tails and bright colors of many male birds or antlers on male deer, are often detrimental to survival, either because they make males more conspicuous to predators, or because they are physiologically costly to produce.

Darwin said that secondary sexual characters could evolve in one of two ways. First, they could be useful to one sex, usually males, in fighting for access to members of the other sex. Weapons like the antlers on male ungulates or horns on male beetles are advantageous because better fighters get more mates and have more offspring. The second way was more problematic. Noting that females often pay attention to traits like long tails and elaborate plumage during courtship, Darwin concluded that the traits evolved because the females preferred them. The sexual selection process, then, consisted of two components: male-male competition, which results in weapons, and female choice, which results in ornaments.

Although competition among males for females seemed reasonable to Darwin’s Victorian contemporaries, the idea that females could do anything as complex as discriminate between males with different degrees of development of a character like colorful plumage was one they could not swallow. Alfred Russel Wallace, who independently arrived at some of the same conclusions about evolution and natural selection as Darwin, was particularly vehement in his objections.

Largely because of this opposition to the idea of female choice, sexual selection as a theory lay dormant for several decades. It was not until the 1960s that evolutionary biologists began to reconsider the portrait they had painted of animal social life. Probably the most important new insight came from work by Robert Trivers, who pointed out that females and males differ in how they put resources and effort into the next generation, which he termed parental investment. Females are limited by the number of offspring they can successfully produce and rear. Because they are the sex that supplies the nutrient-rich egg and often the sex that cares for the young, they leave the most genes in the next generation by having the highest quality young they can. Which male they mate with is important because a mistake in the form of poor genes or no help with the young could mean that they lose their whole breeding effort for an entire year.

Males, on the other hand, can leave the most genes in the next generation by fertilizing as many females as possible. Because each mating requires relatively little investment, a male mating with many females sires many more young than a male mating with only one female. Hence males are expected to compete among themselves for access to females, and females are expected to be choosy and to mate with the best possible male they can.

A classic example is the elephant seal. These animals spend most of the year at sea. In late fall males arrive at isolated beaches and establish a dominance hierarchy, often by vicious fighting and throwing around of their weight, which can exceed three tons. Female elephant seals, about a third the size of males, arrive later, already pregnant. Males herd them when they get to shore; after having her pup, a female is sexually receptive and mates with (usually) the male who has herded her and controls her movements. Males that can sequester more females have a chance for enormous payoffs: A study of an elephant seal colony showed that, in one year, a single male fathered about 90 percent of the pups in the colony. It thus pays to compete with other males because males that do so leave more genes in succeeding generations. Females, on the other hand, have one pup regardless of how many males they mate with. This species is oriented more toward male-male competition than female choice, and the best fighter wins.

In other species female choice predominates. For example, satin bowerbirds are members of a family in which males build elaborate structures during the breeding season. The male collects objects and carefully places them around the bower, after which he waits by it for a female to appear. If she does, he begins a species-specific display that may involve song, complicated courtship dances, or other enticements. Sometimes the female is won over, stays with the male, and mates. Sometimes she watches for a while and leaves. Either way, her choice determines the outcome.

In a handful of species the usual pattern is reversed: Males provide a large contribution to females and offspring, while females benefit by mating with many different males. Katydid males, for instance, sing to attract females for mating. But once a female arrives, she stands to gain much more than a fertilization of her eggs. The males of many katydids produce a gelatinous, nutrient-rich structure called a spermatophylax, which is given to females along with a packet of sperm and which the female eats while the sperm is fertilizing her eggs. It supplies her with protein she often does not get in her usual diet, which enables her to lay more eggs. Females with larger nuptial gifts, as they are called, have more offspring.

But the gifts have an even bigger return if the female recipient is herself relatively large, because larger females lay more eggs. A male cannot give many spermatophylaxes to females in a season, as they can average up to 30 percent of his weight. Therefore, in many species of katydids, male choice rather than female choice occurs, with males seeming to gauge the size of prospective mates and rejecting them if they are too light. Male competition in katydids is much less important than male mate choice; instead, female competition may be a major force, and males choose from among available females. This further supports the notion that the crucial factor is which sex limits the reproductive capacity of the opposite sex.

SEE ALSO Alpha-male; Darwin, Charles; Fertility, Human; Hierarchy; Natural Selection

BIBLIOGRAPHY

Andersson, Malte. 1994. Sexual Selection. Princeton, NJ: Princeton University Press.

Andersson, M., and Simmons, L. W. 2006. Sexual Selection and Mate Choice. Trends in Ecology and Evolution 21 (6): 296-302.

Darwin, Charles. [1871.] 1989. The Descent of Man and Selection in Relation to Sex. New York: New York University Press.

Trivers, R. L. 1972. Parental Investment and Sexual Selection. In Sexual Selection and the Descent of Man 1871-1971, ed. Bernard Campbell, 136-179. Chicago: Aldine.

Marlene Zuk

sexual selection A theory proposed by Darwin, that in some species males compete for mates and that characteristics enhancing their success in mating would have value and be perpetuated irrespective of their overall value in the struggle for existence. Such characters would be used either in male display to attract females (inter-sexual selection) or in combat between rival males (intra-sexual selection), and both could act at the same time. See also handicap principle and runaway hypothesis.

sexual selection The theory, proposed by Darwin, that in some species males compete for mates and that characteristics enhancing their success in mating would have value and be perpetuated irrespective of their overall value in the struggle for existence. Such characters would be used either in male display to attract females (inter-sexual selection) or in combat between rival males (intra-sexual selection), and both could act at the same time.

sexual selection The means by which it is assumed that certain secondary sexual characteristics, particularly of male animals, have evolved. Females presumably choose to mate with the male that gives the best courtship display and therefore has the brightest coloration, etc.: these features would be inherited by its male offspring and would thus tend to become exaggerated down the generations.

sexual selection see selection .