Sexual selection is a mechanism of evolution in which members of one biological sex choose mates of the other sex to mate with (intersexual selection), and compete with members of the same sex for access to members of the opposite sex (intrasexual selection). These two forms of selection mean that some individuals have greater reproductive success than others within a population, for example because they are more attractive or prefer more attractive partners to produce offspring. Successful males benefit from frequent mating and monopolizing access to one or more fertile females. Females can maximise the return on the energy they invest in reproduction by selecting and mating with the best males.
The concept was first articulated by Charles Darwin who wrote of a "second agency" other than natural selection, in which competition between mate candidates could lead to speciation. The theory was given a mathematical basis by Ronald Fisher in the early 20th century. Sexual selection can lead males to extreme efforts to demonstrate their fitness to be chosen by females, producing sexual dimorphism in secondary sexual characteristics, such as the ornate plumage of birds-of-paradise and peafowl, or the antlers of deer. Depending on the species, these rules can be reversed. This is caused by a positive feedback mechanism known as a Fisherian runaway, where the passing-on of the desire for a trait in one sex is as important as having the trait in the other sex in producing the runaway effect. Although the sexy son hypothesis indicates that females would prefer male offspring, Fisher's principle explains why the sex ratio is most often 1:1. Sexual selection is widely distributed in the animal kingdom, and is also found in plants and fungi.
Sexual selection was first proposed by Charles Darwin in On the Origin of Species (1859) and developed in The Descent of Man, and Selection in Relation to Sex (1871), as he felt that natural selection alone was unable to account for certain types of non-survival adaptations. He once wrote to a colleague that "The sight of a feather in a peacock's tail, whenever I gaze at it, makes me sick!" His work divided sexual selection into male–male competition and female choice. [1] [2]
... depends, not on a struggle for existence, but on a struggle between the males for possession of the females; the result is not death to the unsuccessful competitor, but few or no offspring. [3]
... when the males and females of any animal have the same general habits ... but differ in structure, colour, or ornament, such differences have been mainly caused by sexual selection. [4]
These views were to some extent opposed by Alfred Russel Wallace, mostly after Darwin's death. He accepted that sexual selection could occur, but argued that it was a relatively weak form of selection. He argued that male–male competitions were forms of natural selection, but that the "drab" peahen's coloration is itself adaptive as camouflage. In his opinion, ascribing mate choice to females was attributing the ability to judge standards of beauty to animals (such as beetles) far too cognitively undeveloped to be capable of aesthetic feeling. [5]
Darwin's ideas on sexual selection were met with scepticism by his contemporaries and not considered of great importance, until in the 1930s biologists decided to include sexual selection as a mode of natural selection. [7] Only in the 21st century have they become more important in biology; the theory is now seen as generally applicable and analogous to natural selection. [8] A ten-year study, experimentally varying sexual selection on flour beetles with other factors held constant, showed that sexual selection protected even an inbred population against extinction. [6]
Ronald Fisher, the English statistician and evolutionary biologist, developed his ideas about sexual selection in his 1930 book The Genetical Theory of Natural Selection . These include the sexy son hypothesis, which might suggest a preference for male offspring, and Fisher's principle, which explains why the sex ratio is usually close to 1:1. The Fisherian runaway describes how sexual selection accelerates the preference for a specific ornament, causing the preferred trait and female preference for it to increase together in a positive feedback runaway cycle. [9] He remarked that: [10]
... plumage development in the male, and sexual preference for such developments in the female, must thus advance together, and so long as the process is unchecked by severe counterselection, will advance with ever-increasing speed. In the total absence of such checks, it is easy to see that the speed of development will be proportional to the development already attained, which will therefore increase with time exponentially, or in geometric progression. —Ronald Fisher, 1930 [9]
This causes a dramatic increase in both the male's conspicuous feature and in female preference for it, resulting in marked sexual dimorphism, until practical physical constraints halt further exaggeration. A positive feedback loop is created, producing extravagant physical structures in the non-limiting sex. A classic example of female choice and potential runaway selection is the long-tailed widowbird. While males have long tails that are selected for by female choice, female tastes in tail length are still more extreme with females being attracted to tails longer than those that naturally occur. [11] Fisher understood that female preference for long tails may be passed on genetically, in conjunction with genes for the long tail itself. Long-tailed widowbird offspring of both sexes inherit both sets of genes, with females expressing their genetic preference for long tails, and males showing off the coveted long tail itself. [10]
Richard Dawkins presents a non-mathematical explanation of the runaway sexual selection process in his book The Blind Watchmaker . [10] Females that prefer long tailed males tend to have mothers that chose long-tailed fathers. As a result, they carry both sets of genes in their bodies. That is, genes for long tails and for preferring long tails become linked. The taste for long tails and tail length itself may therefore become correlated, tending to increase together. The more tails lengthen, the more long tails are desired. Any slight initial imbalance between taste and tails may set off an explosion in tail lengths. Fisher wrote that:
The exponential element, which is the kernel of the thing, arises from the rate of change in hen taste being proportional to the absolute average degree of taste. —Ronald Fisher, 1932 [12]
The female widowbird chooses to mate with the most attractive long-tailed male so that her progeny, if male, will themselves be attractive to females of the next generation—thereby fathering many offspring that carry the female's genes. Since the rate of change in preference is proportional to the average taste amongst females, and as females desire to secure the services of the most sexually attractive males, an additive effect is created that, if unchecked, can yield exponential increases in a given taste and in the corresponding desired sexual attribute. [10]
It is important to notice that the conditions of relative stability brought about by these or other means, will be far longer duration than the process in which the ornaments are evolved. In most existing species the runaway process must have been already checked, and we should expect that the more extraordinary developments of sexual plumage are not due like most characters to a long and even course of evolutionary progress, but to sudden spurts of change. —Ronald Fisher, 1930 [9]
Since Fisher's initial conceptual model of the 'runaway' process, Russell Lande and Peter O'Donald have provided detailed mathematical proofs that define the circumstances under which runaway sexual selection can take place. [13] [14] Alongside this, biologists have extended Darwin's formulation; Malte Andersson's widely-accepted [15] 1994 definition is that "sexual selection is the differences in reproduction that arise from variation among individuals in traits that affect success in competition over mates and fertilizations". [11] [15] Despite some practical challenges for biologists, the concept of sexual selection is "straightforward". [15]
The reproductive success of an organism is measured by the number of offspring left behind, and by their quality or probable fitness. [17] [18] [19] Sexual preference creates a tendency towards assortative mating or homogamy. The general conditions of sexual discrimination appear to be (1) the acceptance of one mate precludes the effective acceptance of alternative mates, and (2) the rejection of an offer is followed by other offers, either certainly or at such high chance that the risk of non-occurrence is smaller than the chance advantage to be gained by selecting a mate. Bateman's principle states that the sex which invests the most in producing offspring becomes a limiting resource for which the other sex competes, illustrated by the greater nutritional investment of an egg in a zygote, and the limited capacity of females to reproduce; for example, in humans, a woman can only give birth every ten months, whereas a male can become a father numerous times in the same period. [20] More recently, researchers have doubted whether Bateman was correct. [21]
The handicap principle of Amotz Zahavi, Russell Lande and W. D. Hamilton, holds that the male's survival until and through the age of reproduction with seemingly maladaptive traits is taken by the female as a signal of his overall fitness. Such handicaps might prove he is either free of or resistant to disease, or that he possesses more speed or a greater physical strength that is used to combat the troubles brought on by the exaggerated trait. [22] [23] [24] Zahavi's work spurred a re-examination of the field and several new theories. In 1984, Hamilton and Marlene Zuk introduced the "Bright Male" hypothesis, suggesting that male elaborations might serve as a marker of health, by exaggerating the effects of disease and deficiency. [25]
Male–male competition occurs when two males of the same species compete for the opportunity to mate with a female. Sexually dimorphic traits, size, sex ratio, [27] and the social situation [28] may all play a role in the effects male–male competition has on the reproductive success of a male and the mate choice of a female. Larger males tend to win male–male conflicts. [29] Males take many risks in such conflicts, so the value of the resource must be large enough to justify those risks. [30] [31] Winner and loser effects further influence male behaviour. [32] Male–male competition may also affect a female's ability to select the best mates, and therefore decrease the likelihood of successful reproduction. [33]
More recently, the field has grown to include other areas of study, not all of which fit Darwin's definition of sexual selection. A "bewildering" [34] range of models variously attempt to relate sexual selection not only to the fundamental [34] questions of anisogamy and parental roles, but also to mechanisms such as sex ratios – governed by Fisher's principle, [35] parental care, investing in sexy sons, sexual conflict, and the "most-debated effect", [34] namely mate choice. [34] Elaborated characteristics that might seem costly, like the tail of the Montezuma swordfish ( Xiphophorus montezumae ), do not always have an energetics, performance or even survival cost; this may be because "compensatory traits" have evolved in concert with the sexually selected traits. [36]
Sexual selection may explain how characteristics such as feathers had survival value at an early stage in their evolution. The earliest proto-birds such as Protarchaeopteryx had well-developed feathers but could not fly. The feathers may have served as insulation, helping females incubate their eggs, but if proto-bird courtship combined displays of forelimb feathers with energetic jumps, then the transition to flight could have been relatively smooth. [37]
Sexual selection may sometimes generate features that help cause a species' extinction, as has historically been suggested for the giant antlers of the Irish elk (Megaloceros giganteus) that became extinct in Holocene [38] Eurasia [16] (although climate-induced habitat deterioration and anthropogenic pressure are now considered more likely causes). [39] It may, however, also do the opposite, driving species divergence—sometimes through elaborate changes in genitalia [40] —such that new species emerge. [41] [42]
Sexual selection is widely distributed among the eukaryotes, occurring in plants, fungi, and animals. Since Darwin's pioneering observations on humans, it has been studied intensively among the insects, spiders, amphibians, scaled reptiles, birds, and mammals, revealing many distinctive behaviours and physical adaptations. [43]
Darwin conjectured that heritable traits such as beards, hairlessness, and steatopygia in different human populations are results of sexual selection in humans. [44] Humans are sexually dimorphic; females select males using factors including voice pitch, facial shape, muscularity, and height. [45] [46]
Among the many instances of sexual selection in mammals is extreme sexual dimorphism, with males as much as six times heavier than females, and male fighting for dominance among elephant seals. Dominant males establish large harems of several dozen females; unsuccessful males may attempt to copulate with a harem male's females if the dominant male is inattentive. This forces the harem male to defend his territory continuously, not feeding for as much as three months. [47] [48]
Also seen in mammals is sex-role reversal, as in the highly social meerkats, where a large female is dominant within a pack, and female–female competition is observed. The dominant female produces most of the offspring; the subordinate females are nonbreeding, providing altruistic care to the young. [49] [50]
Sexual selection occurs in a wide range of spider species, both before and after copulation. [51] Post-copulatory sexual selection involves sperm competition and cryptic female choice. Sperm competition occurs where the sperm of more than one male competes to fertilise the egg of the female. Cryptic female choice involves the expelling of a male's sperm during or after copulations. [52]
Many forms of sexual selection exist among the insects. Parental care is often provided by female insects, as in bees, but male parental care is found in belostomatid water bugs, where the male, after fertilizing the eggs, allows the female to glue her eggs onto his back. He broods them until the nymphs hatch 2–4 weeks later. The eggs are large and reduce the ability of the male to fertilise other females and catch prey, and increases its predation risk. [53]
Among the fireflies (Lampyrid beetles), males fly in darkness and emit a species-specific pattern of light flashes, which are answered by perching receptive females. The colour and temporal variation of the flashes contribute to success in attracting females. [54] [55] [56] Among the beetles, sexual selection is common. In the mealworm beetle, Tenebrio molitor, males release pheromones to attract females to mate. [57] Females choose mates based on whether they are infected, and on their mass. [58]
Postcopulatory intersexual selection occurs in Idiosepius paradoxus , the Japanese pygmy squid. Males place their spermatangia on an external location on the female's body. The female physically removes spermatangia of males she is presumed to favour less. [59] [60]
Many amphibians have annual breeding seasons with male–male competition. Males arrive at the water's edge first in large numbers, and produce a wide range of vocalizations to attract mates. Among frogs, the fittest males have the deepest croaks and the best territories; females select their mates at least partly based on the depth of croaking. This has led to sexual dimorphism, with females larger than males in 90% of species, and male fighting to access females. [61] [62] Spikethumb frogs are suggested to engage in male-male competition with their elongated prepollex to maintain their mating site. [63] The prepollex, which serves as a rudimentary digit, contains a projecting spine that may be used during this combat, leaving scars on the head and forelimbs of other males. [64] Some species, like P. bibronii , are polyandrous, with one female mating with multiple males.
Many different tactics are used by snakes to acquire mates. Ritual combat between males for the females they want to mate with includes topping, a behavior exhibited by most viperids in which one male will twist around the vertically elevated fore body of its opponent and forcing it downward. It is common for neck biting to occur while the snakes are entwined. [65] [66]
Birds have evolved a wide variety of mating behaviours and many types of sexual selection. These include intersexual selection (female choice) and intrasexual competition, where individuals of the more abundant sex compete with each other for the privilege to mate. Many species, notably the birds-of-paradise, are sexually dimorphic; the differences such as in size and coloration are energetically costly attributes that signal competitive breeding. Conflicts between an individual's fitness and signalling adaptations ensure that sexually selected ornaments such as coloration of plumage and courtship behaviour are honest traits. Signals must be costly to ensure that only good-quality individuals can present these exaggerated sexual ornaments and behaviours. Males with the brightest plumage are favoured by females of multiple species of bird. [67] [68] [69]
Many bird species make use of mating calls, the females preferring males with songs that are complex and varied in amplitude, structure, and frequency. Larger males have deeper songs and increased mating success. [70] [71] [72] [73]
Flowering plants have many secondary sexual characteristics subject to sexual selection including floral symmetry if pollinators visit flowers assortatively by degree of symmetry, [74] nectar production, floral structure, and inflorescences, as well as sexual dimorphisms. [75] [76] [77]
Fungi appear to make use of sexual selection, although they also often reproduce asexually. In the Basidiomycetes, the sex ratio is biased towards males, implying sexual selection there. Male–male competition to fertilise occurs in fungi including yeasts. Pheromone signaling is used by female gametes and by conidia, implying male choice in these cases. Female–female competition may also occur, indicated by the much faster evolution of female-biased genes in fungi. [43] [78] [79] [80]
Sexual dimorphism is the condition where sexes of the same species exhibit different morphological characteristics, including characteristics not directly involved in reproduction. The condition occurs in most dioecious species, which consist of most animals and some plants. Differences may include secondary sex characteristics, size, weight, color, markings, or behavioral or cognitive traits. Male-male reproductive competition has evolved a diverse array of sexually dimorphic traits. Aggressive utility traits such as "battle" teeth and blunt heads reinforced as battering rams are used as weapons in aggressive interactions between rivals. Passive displays such as ornamental feathering or song-calling have also evolved mainly through sexual selection. These differences may be subtle or exaggerated and may be subjected to sexual selection and natural selection. The opposite of dimorphism is monomorphism, when both biological sexes are phenotypically indistinguishable from each other.
A lek is an aggregation of male animals gathered to engage in competitive displays and courtship rituals, known as lekking, to entice visiting females which are surveying prospective partners with which to mate. It can also refer to a space used by displaying males to defend their own share of territory for the breeding season. A lekking species is characterised by male displays, strong female mate choice, and the conferring of indirect benefits to males and reduced costs to females. Although most prevalent among birds such as black grouse, lekking is also found in a wide range of vertebrates including some bony fish, amphibians, reptiles, mammals, and arthropods including crustaceans and insects.
Behavioral ecology, also spelled behavioural ecology, is the study of the evolutionary basis for animal behavior due to ecological pressures. Behavioral ecology emerged from ethology after Niko Tinbergen outlined four questions to address when studying animal behaviors: What are the proximate causes, ontogeny, survival value, and phylogeny of a behavior?
The handicap principle is a disputed hypothesis proposed by the Israeli biologist Amotz Zahavi in 1975. It is meant to explain how "signal selection" during mate choice may lead to "honest" or reliable signalling between male and female animals which have an obvious motivation to bluff or deceive each other. The handicap principle suggests that secondary sexual characteristics are costly signals which must be reliable, as they cost the signaller resources that individuals with less of a particular trait could not afford. The handicap principle further proposes that animals of greater biological fitness signal this through handicapping behaviour, or morphology that effectively lowers overall fitness. The central idea is that sexually selected traits function like conspicuous consumption, signalling the ability to afford to squander a resource. Receivers then know that the signal indicates quality, because inferior-quality signallers are unable to produce such wastefully extravagant signals.
Fisherian runaway or runaway selection is a sexual selection mechanism proposed by the mathematical biologist Ronald Fisher in the early 20th century, to account for the evolution of ostentatious male ornamentation by persistent, directional female choice. An example is the colourful and elaborate peacock plumage compared to the relatively subdued peahen plumage; the costly ornaments, notably the bird's extremely long tail, appear to be incompatible with natural selection. Fisherian runaway can be postulated to include sexually dimorphic phenotypic traits such as behavior expressed by a particular sex.
Anisogamy is a form of sexual reproduction that involves the union or fusion of two gametes that differ in size and/or form. The smaller gamete is male, a sperm cell, whereas the larger gamete is female, typically an egg cell. Anisogamy is predominant among multicellular organisms. In both plants and animals, gamete size difference is the fundamental difference between females and males.
Monogamous pairing in animals refers to the natural history of mating systems in which species pair bond to raise offspring. This is associated, usually implicitly, with sexual monogamy.
Sexual conflict or sexual antagonism occurs when the two sexes have conflicting optimal fitness strategies concerning reproduction, particularly over the mode and frequency of mating, potentially leading to an evolutionary arms race between males and females. In one example, males may benefit from multiple matings, while multiple matings may harm or endanger females due to the anatomical differences of that species. Sexual conflict underlies the evolutionary distinction between male and female.
Mate choice is one of the primary mechanisms under which evolution can occur. It is characterized by a "selective response by animals to particular stimuli" which can be observed as behavior. In other words, before an animal engages with a potential mate, they first evaluate various aspects of that mate which are indicative of quality—such as the resources or phenotypes they have—and evaluate whether or not those particular trait(s) are somehow beneficial to them. The evaluation will then incur a response of some sort.
The sexy son hypothesis in evolutionary biology and sexual selection, proposed by Patrick J. Weatherhead and Raleigh J. Robertson of Queen's University in Kingston, Ontario in 1979, states that a female's ideal mate choice among potential mates is one whose genes will produce males with the best chance of reproductive success. This implies that other benefits the father can offer the mother or offspring are less relevant than they may appear, including his capacity as a parental caregiver, territory and any nuptial gifts. Fisher's principle means that the sex ratio is always near 1:1 between males and females, yet what matters most are her "sexy sons'" future breeding successes, more likely if they have a promiscuous father, in creating large numbers of offspring carrying copies of her genes. This sexual selection hypothesis has been researched in species such as the European pied flycatcher.
A courtship display is a set of display behaviors in which an animal, usually a male, attempts to attract a mate; the mate exercises choice, so sexual selection acts on the display. These behaviors often include ritualized movement ("dances"), vocalizations, mechanical sound production, or displays of beauty, strength, or agonistic ability.
Sexual selection in humans concerns the concept of sexual selection, introduced by Charles Darwin as an element of his theory of natural selection, as it affects humans. Sexual selection is a biological way one sex chooses a mate for the best reproductive success. Most compete with others of the same sex for the best mate to contribute their genome for future generations. This has shaped human evolution for many years, but reasons why humans choose their mates are not fully understood. Sexual selection is quite different in non-human animals than humans as they feel more of the evolutionary pressures to reproduce and can easily reject a mate. The role of sexual selection in human evolution has not been firmly established although neoteny has been cited as being caused by human sexual selection. It has been suggested that sexual selection played a part in the evolution of the anatomically modern human brain, i.e. the structures responsible for social intelligence underwent positive selection as a sexual ornamentation to be used in courtship rather than for survival itself, and that it has developed in ways outlined by Ronald Fisher in the Fisherian runaway model. Fisher also stated that the development of sexual selection was "more favourable" in humans.
Sexual antagonistic co-evolution is the relationship between males and females where sexual morphology changes over time to counteract the opposite's sex traits to achieve the maximum reproductive success. This has been compared to an arms race between sexes. In many cases, male mating behavior is detrimental to the female's fitness. For example, when insects reproduce by means of traumatic insemination, it is very disadvantageous to the female's health. During mating, males will try to inseminate as many females as possible, however, the more times a female's abdomen is punctured, the less likely she is to survive. Females that possess traits to avoid multiple matings will be more likely to survive, resulting in a change in morphology. In males, genitalia is relatively simple and more likely to vary among generations compared to female genitalia. This results in a new trait that females have to avoid in order to survive.
A biological ornament is a characteristic of an animal that appears to serve a decorative function rather than a utilitarian function. Many are secondary sexual characteristics, and others appear on young birds during the period when they are dependent on being fed by their parents. Ornaments are used in displays to attract mates, which may lead to the evolutionary process known as sexual selection. An animal may shake, lengthen, or spread out its ornament in order to get the attention of the opposite sex, which will in turn choose the most attractive one with which to mate. Ornaments are most often observed in males, and choosing an extravagantly ornamented male benefits females as the genes that produce the ornament will be passed on to her offspring, increasing their own reproductive fitness. As Ronald Fisher noted, the male offspring will inherit the ornament while the female offspring will inherit the preference for said ornament, which can lead to a positive feedback loop known as a Fisherian runaway. These structures serve as cues to animal sexual behaviour, that is, they are sensory signals that affect mating responses. Therefore, ornamental traits are often selected by mate choice.
Interlocus sexual conflict is a type of sexual conflict that occurs through the interaction of a set of antagonistic alleles at two or more different loci, or the location of a gene on a chromosome, in males and females, resulting in the deviation of either or both sexes from the fitness optima for the traits. A co-evolutionary arms race is established between the sexes in which either sex evolves a set of antagonistic adaptations that is detrimental to the fitness of the other sex. The potential for reproductive success in one organism is strengthened while the fitness of the opposite sex is weakened. Interlocus sexual conflict can arise due to aspects of male–female interactions such as mating frequency, fertilization, relative parental effort, female remating behavior, and female reproductive rate.
Intralocus sexual conflict is a type of sexual conflict that occurs when a genetic locus harbours alleles which have opposing effects on the fitness of each sex, such that one allele improves the fitness of males, while the alternative allele improves the fitness of females. Such "sexually antagonistic" polymorphisms are ultimately generated by two forces: (i) the divergent reproductive roles of each sex, such as conflicts over optimal mating strategy, and (ii) the shared genome of both sexes, which generates positive between-sex genetic correlations for most traits. In the long term, intralocus sexual conflict is resolved when genetic mechanisms evolve that decouple the between-sex genetic correlations between traits. This can be achieved, for example, via the evolution of sex-biased or sex-limited genes.
Sexual swelling, sexual skin, or anogenital tumescence refers to localized engorgement of the anus and vulva region of some female primates that vary in size over the course of the menstrual cycle. Thought to be an honest signal of fertility, male primates are attracted to these swellings; preferring, and competing for, females with the largest swellings.
Sexual selection in birds concerns how birds have evolved a variety of mating behaviors, with the peacock tail being perhaps the most famous example of sexual selection and the Fisherian runaway. Commonly occurring sexual dimorphisms such as size and color differences are energetically costly attributes that signal competitive breeding situations. Many types of avian sexual selection have been identified; intersexual selection, also known as female choice; and intrasexual competition, where individuals of the more abundant sex compete with each other for the privilege to mate. Sexually selected traits often evolve to become more pronounced in competitive breeding situations until the trait begins to limit the individual's fitness. Conflicts between an individual fitness and signaling adaptations ensure that sexually selected ornaments such as plumage coloration and courtship behavior are "honest" traits. Signals must be costly to ensure that only good-quality individuals can present these exaggerated sexual ornaments and behaviors.
Sexual selection in mammals is a process the study of which started with Charles Darwin's observations concerning sexual selection, including sexual selection in humans, and in other mammals, consisting of male–male competition and mate choice that mold the development of future phenotypes in a population for a given species.
Sexual selection in amphibians involves sexual selection processes in amphibians, including frogs, salamanders and newts. Prolonged breeders, the majority of frog species, have breeding seasons at regular intervals where male-male competition occurs with males arriving at the waters edge first in large number and producing a wide range of vocalizations, with variations in depth of calls the speed of calls and other complex behaviours to attract mates. The fittest males will have the deepest croaks and the best territories, with females making their mate choices at least partly based on the males depth of croaking. This has led to sexual dimorphism, with females being larger than males in 90% of species, males in 10% and males fighting for groups of females.
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