Fisherian runaway

Last updated
The peacock tail in flight, the classic example of an ornament assumed to be a Fisherian runaway Peacock Flying.jpg
The peacock tail in flight, the classic example of an ornament assumed to be a Fisherian runaway

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.

Contents

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]

Female (left) and male (right) pheasant, a sexually dimorphic species Male and female pheasant.jpg
Female (left) and male (right) pheasant, a sexually dimorphic species
Peacock spider males perform courtship dances that display their boldly patterned chelicerae, legs, and abdomens. Females are cryptic brown. MalePeacockSpider.jpg
Peacock spider males perform courtship dances that display their boldly patterned chelicerae, legs, and abdomens. Females are cryptic brown.

History

From Charles Darwin to Ronald Fisher

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.

R.A. Fisher (1915) [7]

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]

Peacocks and sexual dimorphism

The peacock, on the right, is courting the peahen, on the left. Peacock courting peahen.jpg
The peacock, on the right, is courting the peahen, on the left.

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]

Mechanism

Initiation

Fisher outlined two fundamental conditions that must be fulfilled for the Fisherian runaway mechanism to lead to the evolution of extreme ornamentation:

  1. Sexual preference in at least one of the sexes
  2. A corresponding reproductive advantage to the preference. [8]

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]

Genetic basis

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]

Female choice

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]

Positive feedback

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]

Alternative hypotheses

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]

See also

Related Research Articles

<span class="mw-page-title-main">Sexual selection</span> Mode of natural selection involving the choosing of and competition for mates

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.

<span class="mw-page-title-main">Secondary sex characteristic</span> Features that occur in an organism at sexual maturity

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. In animals, they can start to appear at sexual maturity. In humans, secondary sex characteristics 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, secondary sex characteristics include, for example, the manes of male lions, the bright facial and rump coloration of male mandrills, and horns in many goats and antelopes.

<span class="mw-page-title-main">Peafowl</span> Group of large game birds

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.

<span class="mw-page-title-main">Sexual dimorphism</span> Evolved difference in sex-specific characteristics

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.

<span class="mw-page-title-main">Lek mating</span> Type of animal mating behaviour

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.

<i>The Genetical Theory of Natural Selection</i> Book by Ronald Aylmer Fisher

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".

<span class="mw-page-title-main">Indian peafowl</span> Species of bird

The Indian peafowl, also known as the common peafowl or blue peafowl, is a peafowl species native to the Indian subcontinent. It has been introduced to many other countries. 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".

<span class="mw-page-title-main">Signalling theory</span> Theory in evolutionary biology

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.

<span class="mw-page-title-main">Mate choice</span> Mechanism for evolution

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.

<span class="mw-page-title-main">Sexy son hypothesis</span> Postulate in biology

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.

<span class="mw-page-title-main">Lek paradox</span> Conundrum in sexual selection behaviour

The lek paradox is a conundrum in evolutionary biology that addresses the persistence of genetic variation in male traits within lek mating systems, despite strong sexual selection through female choice. This paradox arises from the expectation that consistent female preference for particular male traits should erode genetic diversity, theoretically leading to a loss of the benefits of choice. The lek paradox challenges our understanding of how genetic variation is maintained in populations subject to intense sexual selection, particularly in species where males provide only genes to their offspring. Several hypotheses have been proposed to resolve this paradox, including the handicap principle, condition-dependent trait expression, and parasite resistance models.

<span class="mw-page-title-main">Long-tailed widowbird</span> Species of bird

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".

<span class="mw-page-title-main">Courtship display</span> Communication to start a relationship with someone or to get sexual contact

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.

<span class="mw-page-title-main">Sexual selection in humans</span> Evolutionary effects of sexual selection on humans

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.

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.

<span class="mw-page-title-main">Sexual selection in birds</span>

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.

<i>The Evolution of Beauty</i> 2017 book by Richard O. Prum

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.

References

  1. 1 2 Andersson, M. (1994). Sexual selection. Princeton University Press. ISBN   0-691-00057-3.
  2. 1 2 Andersson, M.; Simmons, L.W. (2006). "Sexual selection and mate choice". Trends in Ecology and Evolution. 21 (6): 296–302. CiteSeerX   10.1.1.595.4050 . doi:10.1016/j.tree.2006.03.015. PMID   16769428.
  3. 1 2 3 4 5 6 Gayon, J. (2010). "Sexual selection: Another Darwinian process". Comptes Rendus Biologies. 333 (2): 134–144. doi:10.1016/j.crvi.2009.12.001. PMID   20338530.
  4. Kirkpatrick, Mark (1982). "Sexual Selection and the Evolution of Female Choice". Evolution , 36 (1): 1–12. https://doi.org/10.2307/2407961
  5. Lande, R. (1980). Sexual Dimorphism, Sexual Selection, and Adaptation in Polygenic Characters. Evolution , 34 (2): 292–305. https://doi.org/10.2307/2407393
  6. Darwin, C. (1871). The Descent of Man, and Selection in Relation to Sex. Prometheus Books. ISBN   978-1-57392-176-3.
  7. 1 2 3 4 5 6 Fisher, Ronald A. (1915). "The evolution of sexual preference". Eugenics Review. 7 (3): 184–192. PMC   2987134 . PMID   21259607.
  8. 1 2 3 4 5 6 7 8 9 10 Fisher, Ronald A. (1930). The Genetical Theory of Natural Selection. Oxford, UK: Clarendon Press. ISBN   978-0-19-850440-5. "[online archived copy]". At The Clarendon Press. 1930.
  9. Darwin, C. (3 April 1860). "Darwin Project letter 2743". Letter to Asa Gray.
  10. Rodd, F.H.; Hughs, K.A.; Grether, G.F.; Baril, C.T. (2002). "A possible non-sexual origin of mate preference: Are male guppies mimicking fruit?". Proceedings of the Royal Society B: Biological Sciences. 269 (1490): 571–577. doi:10.1098/rspb.2001.1891. PMC   1690917 . PMID   11886639.
  11. Pomiankowski, A.; Iwasa, Y. (1998). "Runaway ornament diversity caused by Fisherian sexual selection". Proceedings of the National Academy of Sciences. 95 (9): 5106–5111. Bibcode:1998PNAS...95.5106P. doi: 10.1073/pnas.95.9.5106 . PMC   20221 . PMID   9560236.
  12. Mead, L.S.; Arnold, S.J. (2004). "Quantitative genetic models of sexual selection". Trends in Ecology and Evolution. 19 (5): 264–271. doi:10.1016/j.tree.2004.03.003. PMID   16701266.
  13. Zahavi, Amotz (1975). "Mate selection—A selection for a handicap". Journal of Theoretical Biology. 53 (1). Elsevier BV: 205–214. Bibcode:1975JThBi..53..205Z. CiteSeerX   10.1.1.586.3819 . doi:10.1016/0022-5193(75)90111-3. ISSN   0022-5193. PMID   1195756.
  14. Ryan, Michael (2018). A taste for the beautiful: The evolution of attraction. Princeton University Press. pp. 3, 32, 41, 43–44, 155. ISBN   9780691167268.