Fisherian runaway

The peacock tail in flight, the classic example of a Fisherian runaway

File:R. A. Fischer.jpg

Ronald Fisher

Fisherian or Fisher's runaway, first proposed by Ronald Fisher in the early 20th century, is a hypothesized genetic sexual selection mechanism for the evolution of exaggerated male ornamentation (a subtype secondary sexual characteristic) observed in numerous species that produce offspring through sexual reproduction; based upon female choice, the preference or attraction of females for ornamented male mates.

The evolution of male ornamentation, an example being the colourful and elaborate peacock plumage compared to the relatively subdued peahen plumage, represented a paradox for evolutionary biologists in the period following Charles Darwin and leading up to the modern evolutionary synthesis; the selection for costly ornaments appeared to biologists at the time as being incompatible with natural selection. Fisherian runaway was an attempt to resolve this paradox using an assumed genetic basis for both the preference and the ornament, and through the powerful forces of sexual selection. Fisherian runaway hypothesizes that females choose "attractive" males with the most exaggerated ornaments based solely upon the males' possession of that ornament. According to Fisher, if strong enough, female preference for exaggerated ornamentation in mate selection could be enough to undermine natural selection if the ornament under sexual selection is otherwise non-adaptive. Fisher hypothesized this counteraction would result in the next generation's male offspring being more likely to possess the ornament and female offspring more likely to possess the preference for the ornament than the previous generation. Over subsequent generations this would lead to the runaway selection via a positive feedback mechanism for males who possess the most exaggerated ornaments.

Fisherian runaway sought to explain the paradox of male ornamentation but neither the mechanism nor the secondary sexual characteristic or preference is restricted to this system: Fisherian runaway can be applied to include sexually dimorphic phenotypic traits and character structures such as behaviour and structural displays expressed by either sex.

Fisherian runaway has been difficult to demonstrate empirically, despite being theoretically plausible, due in part to the difficulty of detecting the genetic mechanism and the process by which it is initiated.

Historical context

Female (left) and male (right) common pheasant, a sexually dimorphic species by which morphological traits vary between sexes

R.A. Fisher was, like Charles Darwin before him, fascinated by the mechanics of sexual selection."

[of] the branches of biological science to which Charles Darwin's life-work has given us the key, few, if any, are as attractive as the subject of Sexual Selection ... Fisher, R.A. (1915) The evolution of sexual preference. Eugenics Review (7) 184:192

Darwin published a book on sexual selection in 1871 called The Descent of Man, and Selection in Relation to Sex, which garnered interest upon its release but by the 1880s the ideas had been deemed too controversial and largely neglected. The interest Fisher and a few others had in sexual selection was not shared, however, by the vast majority of his peers in the early developments of the modern evolutionary synthesis, being ignored by biologists until the second half of the 20th century.

When Alfred Russel Wallace stated that animals show no sexual preference in his 1915 paper, The evolution of sexual preference Fisher publicly disagreed.

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, R.A. (1915) The evolution of sexual preference. Eugenics Review (7) 184:192

Fisher, in the foundational 1930 book, The Genetical Theory of Natural Selection, 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.

[O]ccasions 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. Fisher, R.A. (1930) The Genetical Theory of Natural Selection. ISBN 0-19-850440-3

Overview

Fisherian runaway is a hypothesized genetic inter-sexual selection mechanism for the paradoxical evolution of elaborate and exaggerated male ornaments that neither play a role in intra-sexual selection nor serve increase the fitness in an obvious way. Fisherian runaway is an attempt to resolve this paradoxical evolution within the context of evolutionary theory. Originally hypothesized during the beginning of the modern evolutionary synthesis, Fisherian runaway suggests that male ornamentation is the result of a positive feedback ("runaway") mechanism that is driven by the "intersexual" preference of females for males that express the most exaggerated ornaments in mate choice. 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) indefinitely until the costs (incurred by natural selection) of the expression become greater than the benefit (bestowed by sexual selection).

Peacocks and sexual dimorphism

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 Pavo genus are the de facto example of the ornamentation paradox that has long puzzled evolutionary biologists. The peacock's colorful and elaborate tail requires a great deal of energy to grow and maintain. It also reduces the bird's agility, and may even 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 with longer and more colorfully elaborate tails have some advantage over peacocks who don’t, and that the expression of the costly tail serves to increase overall fitness. 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 because of the preference for them by peahens. Equally importantly the female offspring of these peahens are more likely to produce peahen offspring that have a preference for peacocks with longer and more colourful tails. Given this, having a preference for longer and more colorful tails bestows an advantage to peahens just as having a longer and more colorful tail bestows an advantage upon peacocks.

However, though the relative fitness of males with 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 colorful tail. In the absence of such a preference, the possession of these tails would be non-adaptive; reduced mobility and increased visibility to predators would no longer be incentivized by a sexual preference. The sexual preference of peahens to mate with peacocks that possess long and colourful tails in this case undermines the seemingly non-adaptiveness of these tails according to Fisherian runaway, giving rise to the sexually dimorphic peacocks and peahens of the Pavo genus.

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

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

Genetic basis

For any hypothesis to be resolved within the context of evolutionary biology there must be a genetic basis. In order for traits and characters to be passed along to offspring and in order for more exaggerated expressions to be sexually selected for, Fisherian runaway assumes that sexual preference in females and ornamentation in males is both genetically variable and heritable.

Fisher alluded to this need for a genetic basis when outlining Fisherian runaway in the The Genetical Theory of Natural Selection (1930).

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. Fisher, R.A. (1930) The Genetical Theory of Natural Selection. ISBN 0-19-850440-3

Female choice

Fisher argues that the selection for exaggerated male ornamentation is driven by the coupled exaggeration of female sexual preference for the ornament (with the degree/intensity of expression positively correlating with the degree/intensity of the preference). This coupled preference makes more exaggerated ornaments more desirable (preferred) based upon the degree of expression alone; even though outside of the forces of sexual selection the ornament appears non-adaptive. Fisher suggests that this sexual selection process is pivotal in undermining the direction of natural selection.

Certain remarkable consequences do, however, follow if some sexual preferences of this kind … are developed in a species in which the preferences of … the female, have a great influence on the number of offspring left by individual males. In such cases… an additional advantage conferred by female preference, which will be proportional to the intensity of the preference. The selective agencies other than sexual preference may be opposed to … yet … 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. Fisher, R.A. (1930) The Genetical Theory of Natural Selection. ISBN 0-19-850440-3

Positive feedback

A Preference intensity that is genetically coupled with the degree of ornament expression consequently makes an exaggerated preference advantageous. Females that instinctively choose males with the most exaggerated ornament increase the likelihood that their offspring will express a higher degree of preference intensity (daughters) and ornament exaggeration (sons). Over time this genetic coupling is further reinforced by a positive feedback mechanism that 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. Given time, this type of runaway selection facilitates the continued exaggeration at a rate exponentially, 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. Fisher, R.A. (1930) The Genetical Theory of Natural Selection. ISBN 0-19-850440-3

Fisher makes special note of two possible outcomes when the costs of ornamentation equal or outweigh the reproductive benefit. The first outcome is a counterselection for less ornamented males that will cease the further elaboration of the ornament condition until the advantage attained from sexual preference balances with the costs of ornamentation halting the further exaggeration of both the ornament and the preference to create a condition of relative stability and, (ii) a severing of the entire process if the costs associated with the ornament reduce the number of surviving and reproducing offspring which in turn makes the preference disadvantageous along with the ornamentation.

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. Fisher, R.A. (1930) The Genetical Theory of Natural Selection. ISBN 0-19-850440-3

Initiation

Fisher made a case for how the type of female preference necessary for Fisherian runaway could be initiated without any understanding or appreciation for beauty and only a limited facultative sense in his 1915 paper, The evolution of sexual preference. Fisher suggested that points on an organism that draw attention and vary in their appearance amongst the population of males so as to be easily compared by the females may be enough to initiate Fisherian runaway if somehow the most developed of the points coincides with vigour and vitality but is non-adaptive itself. If a disproportionate amount of females choose the males with the developed point and high vitality based upon the attention drawing of the point, a female preference may be initiated. This hypothesis for the initiation is compatible with Fisherian runaway in that it establishes an arbitrary attractiveness based upon a trait that is not necessarily correlated with fitness outside of the initiated preference.

Alternative hypotheses

Fisherian runaway suggests that the genetically coupled runaway selection for seemingly non-adaptive exaggerated ornaments in males by the exaggerated preference for them in females is due to an arbitrary attraction. Several alternative hypotheses use the same genetic runaway (or positive feedback) mechanism but differ in the mechanisms of the initiation. The alternative sexy sons hypothesis (also proposed by Fisher) suggests that females choose desirably ornamented males with the a priori intention of having desirably ornamented (or sexy) sons. Indicator hypotheses (for example the good genes hypothesis) suggest females choose desirably ornamented males because the cost of producing the desirable ornaments is indicative of good genes by way of the individuals vigour. Both of these hypotheses use the same mechanism as Fisherian runaway but assume female choice is motivated by an assessment of a potential male mate that is beyond arbitrary attraction.

Other hypotheses for the evolution of male ornamentation include: sensory bias hypothesis, compatibility hypothesis and the handicap principle.

See also

• Sexual selection
• Mate choice
• Secondary sex characteristic
• Sexy sons hypothesis
• Handicap principle
• Good genes hypothesis
• Modern evolutionary synthesis