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. [1] [2] [3] 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.
Extreme and (seemingly) maladaptive sexual dimorphism represented a paradox for evolutionary biologists from Charles Darwin's time up to the modern synthesis. Darwin attempted to resolve the paradox by assuming heredity for both the preference and the ornament, and supposed an "aesthetic sense" in higher animals, leading to powerful selection of both characteristics in subsequent generations. [3] Fisher developed the theory further by assuming genetic correlation between the preference and the ornament, that initially the ornament signalled greater potential fitness (the likelihood of leaving more descendants), so preference for the ornament had a selective advantage. Subsequently, if strong enough, female preference for exaggerated ornamentation in mate selection could be enough to undermine natural selection even when the ornament has become non-adaptive. [3] Over subsequent generations this could lead to runaway selection by positive feedback, and the speed with which the trait and the preference increase could (until counter-selection interferes) increase exponentially. [3]
Modern descriptions of the same mechanism using quantitative genetic and population genetic models were mainly established by Russell Lande and Mark Kirkpatrick in the 1980s, and are now more commonly referred to as the sexy son hypothesis. [4] [5]
Charles Darwin published a book on sexual selection in 1871 called The Descent of Man, and Selection in Relation to Sex , [6] which garnered interest upon its release but by the 1880s the ideas had been deemed too controversial and were largely neglected. Alfred Russel Wallace disagreed with Darwin, particularly after Darwin's death, that sexual selection was a real phenomenon. [3]
Ronald Fisher was one of the few other biologists to engage with the question. [3] When Wallace stated that animals show no sexual preference in his 1915 paper, The evolution of sexual preference, Fisher publicly disagreed: [7]
The objection raised by Wallace ... that animals do not show any preference for their mates on account of their beauty, and in particular that female birds do not choose the males with the finest plumage, always seemed to the writer a weak one; partly from our necessary ignorance of the motives from which wild animals choose between a number of suitors; partly because there remains no satisfactory explanation either of the remarkable secondary sexual characters themselves, or of their careful display in love-dances, or of the evident interest aroused by these antics in the female; and partly also because this objection is apparently associated with the doctrine put forward by Sir Alfred Wallace in the same book, that the artistic faculties in man belong to his "spiritual nature", and therefore have come to him independently of his "animal nature" produced by natural selection.
Fisher, in the foundational 1930 book, The Genetical Theory of Natural Selection , [8] first outlined a model by which runaway inter-sexual selection could lead to sexually dimorphic male ornamentation based upon female choice and a preference for "attractive" but otherwise non-adaptive traits in male mates. He suggested that selection for traits that increase fitness may be quite common:
Occasions may not be infrequent when a sexual preference of a particular kind may confer a selective advantage, and therefore become established in the species. Whenever appreciable differences exist in a species, which are in fact correlated with selective advantage, there will be a tendency to select also those individuals of the opposite sex which most clearly discriminate the difference to be observed, and which most decidedly prefer the more advantageous type. Sexual preference originated in this way may or may not confer any direct advantage upon the individuals selected, and so hasten the effect of the Natural Selection in progress. It may therefore be far more widespread than the occurrence of striking secondary sexual characters.
A strong female choice for the expression alone, as opposed to the function, of a male ornament can oppose and undermine the forces of natural selection and result in the runaway sexual selection that leads to the further exaggeration of the ornament (as well as the preference) until the costs (incurred by natural selection) of the expression become greater than the benefit (bestowed by sexual selection). [7] [8]
The plumage dimorphism of the peacock and peahen of the species within the genus Pavo is a prime example of the ornamentation paradox that has long puzzled evolutionary biologists; Darwin wrote in 1860:
The sight of a feather in a peacock’s tail, whenever I gaze at it, makes me sick! [9]
The peacock's colourful and elaborate tail requires a great deal of energy to grow and maintain. It also reduces the bird's agility, and may increase the animal's visibility to predators. The tail appears to lower the overall fitness of the individuals who possess it. Yet, it has evolved, indicating that peacocks who have longer and more colourfully elaborate tails have some advantage over peacocks who do not. Fisherian runaway posits that the evolution of the peacock tail is made possible if peahens have a preference to mate with peacocks that possess a longer and more colourful tail. Peahens that select males with these tails in turn have male offspring that are more likely to have long and colourful tails and thus are more likely to be sexually successful themselves. Equally importantly, the female offspring of these peahens are more likely to have a preference for peacocks with longer and more colourful tails. However, though the relative fitness of males with large tails is higher than those without, the absolute fitness levels of all the members of the population (both male and female) is less than it would be if none of the peahens (or only a small number) had a preference for a longer or more colourful tail. [7] [8]
Fisher outlined two fundamental conditions that must be fulfilled for the Fisherian runaway mechanism to lead to the evolution of extreme ornamentation:
Fisher argued in his 1915 paper, "The evolution of sexual preference", that the type of female preference necessary for Fisherian runaway could be initiated without any understanding or appreciation for beauty. [7] Fisher suggested that any visible features that indicate fitness, that are not themselves adaptive, that draw attention, and that vary in their appearance amongst the population of males so that the females can easily compare them, would be enough to initiate Fisherian runaway. This suggestion is compatible with his theory, and indicates that the choice of feature is essentially arbitrary, and could be different in different populations. Such arbitrariness is borne out by mathematical modelling, and by observation of isolated populations of sandgrouse, where the males can differ markedly from those in other populations. [7] [1] [2] [10] [11] [12]
Fisherian runaway assumes that sexual preference in females and ornamentation in males are both genetically variable (heritable). [8]
If instead of regarding the existence of sexual preference as a basic fact to be established only by direct observation, we consider that the tastes of organisms ... be regarded as the products of evolutionary change, governed by the relative advantage which such tastes may confer. Whenever appreciable differences exist in a species ... there will be a tendency to select also those individuals of the opposite sex which most clearly discriminate the difference to be observed, and which most decidedly prefer the more advantageous type.
— R. A. Fisher (1930) [8]
Fisher argued that the selection for exaggerated male ornamentation is driven by the coupled exaggeration of female sexual preference for the ornament.
Certain remarkable consequences do, however, follow ... in a species in which the preferences of ... the female, have a great influence on the number of offspring left by individual males. ... development will proceed, so long as the disadvantage is more than counterbalanced by the advantage in sexual selection ... there will also be a net advantage in favour of giving to it a more decided preference.
— R. A. Fisher (1930) [8]
Over time a positive feedback mechanism, one that involves a loop in which an increase in a quantity causes a further increase in the same quantity, will see more exaggerated sons and choosier daughters being produced with each successive generation; resulting in the runaway selection for the further exaggeration of both the ornament and the preference (until the costs for producing the ornament outweigh the reproductive benefit of possessing it).
The two characteristics affected by such a process, namely [ornamental] development in the male, and sexual preference for such development in the female, must thus advance together, and … will advance with ever increasing speed. [I]t 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 a geometric progression.
— R. A. Fisher (1930) [8]
Such a process must soon run against some check. Two such are obvious. If carried far enough … counterselection in favour of less ornamented males will be encountered to balance the advantage of sexual preference; … elaboration and … female preference will be brought to a standstill, and a condition of relative stability will be attained. It will be more effective still if the disadvantage to the males of their sexual ornaments so diminishes their numbers surviving, relative to the females, as to cut at the root of the process, by demising the reproductive advantage to be conferred by female preference.
— R. A. Fisher (1930) [8]
Several alternative hypotheses use the same genetic runaway (or positive feedback) mechanism but differ in the mechanisms of the initiation. Indicator hypotheses suggest that females choose desirably ornamented males because the cost of producing the desirable ornaments is indicative of good genes by way of the individual's vigour; for instance, the handicap principle proposes that females distinguish the best males by the measurable cost of certain visible features which have no other purpose, by analogy with a handicap race, in which the best horses carry the largest weights. [13]
The sensory exploitation hypothesis proposes that sexual preferences for exaggerated traits are the result of sensory biases, such as that for supernormal stimuli. [14]
Sexual selection is a mechanism of evolution in which members of one biological sex choose mates of the other sex to mate with, and compete with members of the same sex for access to members of the opposite sex. 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.
A secondary sex characteristic is a physical characteristic of an organism that is related to or derived from its sex, but not directly part of its reproductive system. In humans, these characteristics typically start to appear during puberty—and include enlarged breasts and widened hips of females, facial hair and Adam's apples on males, and pubic hair on both. In non-human animals, they can start to appear at sexual maturity—and include, for example, the manes of male lions, the bright facial and rump coloration of male mandrills, and horns in many goats and antelopes.
Peafowl is a common name for two bird species of the genus Pavo and one species of the closely related genus Afropavo within the tribe Pavonini of the family Phasianidae. Male peafowl are referred to as peacocks, and female peafowl are referred to as peahens.
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.
The Genetical Theory of Natural Selection is a book by Ronald Fisher which combines Mendelian genetics with Charles Darwin's theory of natural selection, with Fisher being the first to argue that "Mendelism therefore validates Darwinism" and stating with regard to mutations that "The vast majority of large mutations are deleterious; small mutations are both far more frequent and more likely to be useful", thus refuting orthogenesis. First published in 1930 by The Clarendon Press, it is one of the most important books of the modern synthesis, and helped define population genetics. It had been described by J. F. Crow as the "deepest book on evolution since Darwin".
The Indian peafowl, also known as the common peafowl or blue peafowl, is a peafowl species native to the Indian subcontinent. While it originated in the Indian subcontinent, it has since been introduced to many other parts of the world. Male peafowl are referred to as peacocks, and female peafowl are referred to as peahens, although both sexes are often referred to colloquially as a "peacock".
Within evolutionary biology, signalling theory is a body of theoretical work examining communication between individuals, both within species and across species. The central question is when organisms with conflicting interests, such as in sexual selection, should be expected to provide honest signals rather than cheating. Mathematical models describe how signalling can contribute to an evolutionarily stable strategy.
Geoffrey Franklin Miller is an American evolutionary psychologist, author, and associate professor of psychology at the University of New Mexico. He is known for his research on sexual selection in human evolution.
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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.
The long-tailed widowbird is a species of bird in the family Ploceidae. The species are found in Angola, Botswana, the Democratic Republic of the Congo, Kenya, Lesotho, South Africa, Eswatini, and Zambia. The long-tailed widowbird is a medium-sized bird and one of the most common in the territories it inhabits. Adult breeding males are almost entirely black with orange and white shoulders (epaulets), long, wide tails, and a bluish white bill. Females are rather inconspicuous, their feathers streaked tawny and black with pale patches on the chest, breast and back, narrow tail feathers, and horn-colored bills.
Fisher's principle is an evolutionary model that explains why the sex ratio of most species that produce offspring through sexual reproduction is approximately 1:1 between males and females. A. W. F. Edwards has remarked that it is "probably the most celebrated argument in evolutionary biology".
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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.
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Evolutionary aesthetics refers to evolutionary psychology theories in which the basic aesthetic preferences of Homo sapiens are argued to have evolved in order to enhance survival and reproductive success.
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The Evolution of Beauty: How Darwin's Forgotten Theory of Mate Choice Shapes the Animal World—and Us is a 2017 book by the ornithologist and evolutionary biologist Richard O. Prum about the power of aesthetic mate choice, arguing it to be an important independent agent in evolution. Prum indicates that while Charles Darwin made this argument in The Descent of Man, published in 1871, the concept was sidelined and forgotten and the notion of natural selection being the sole driver of evolution took over. As an ornithologist, Prum describes many examples in avian evolution where aesthetics are preeminent. Prum proceeds to apply the principle of aesthetic evolution as an independent force in human evolution.