Sexual selection



Sexual selection is the theory proposed by Charles Darwin that states that the frequency of traits can increase or decrease depending on the attractiveness of the bearer. Biologists today distinguish between "male to male combat" (it is usually males who fight), "mate choice" (usually female choice of male mates) and "mate coercion" (forced mating). Traits selected for by male combat are called "weapons", and traits selected by mate choice are called "ornaments". Much attention has recently been given to cryptic female choice, a phenomenon in internally fertilising animals such as mammals and birds, where a female may simply dispose of a male's sperm without his knowledge. The equivalent in male-to-male combat is sperm competition.

The exact effect of sexual selection depends on the sex ratio, which is usually slightly biased in favour of the "limiting" sex (typically females).

Male to male combat is also classified as intrasexual competition, while mate choice and mate coercion are also known as intersexual competition.

Females often prefer to mate with males with external ornaments - exaggerated features of morphology. These can plausibly arise because an arbitrary female preference for some aspect of male morphology initially increased by genetic drift, creating, in due course, selection for males with the appropriate ornament. This is known as the sexy son hypothesis. Alternatively, genes that enable males to develop great ornaments may simply show off greater disease resistance or a more efficient metabolism - features that also benefit females. This idea is known as the good genes hypothesis.

Phylogeny of sexual selection and base conditions
The success of an organism is not only measured by the number of offspring left behind, but by the quality or probable success of the offspring: reproductive fitness. Sexual selection is the expansion on the ability of organisms to differentiate each other at the species level, interspecies selection.

The grossest blunder in sexual preference, which we can conceive of an animal making, would be to mate with a species different from its own and with which hybrids are either infertile or, through the mixture of instincts and other attributes appropriate to different courses of life, at so serious a disadvantage as to leave no descendants. ..it is no conjecture that a discriminative mechanism exists, variations in which will be capable of giving rise to a similar discrimination within its own species, should such a discrimination become at any time advantageous. —Ronald Fisher, 1930

The expansion of interspecies selection and intraspecies selection is a driving force behind species fission: the separation of a single contiguous species into multiple non-contiguous variants. Sexual preference creates a specialized tendency towards homogamy that provides a system by which a group constantly invaded by the diffusion of unfavourable genes may suppress ill effects.

Individuals in each region most readily attracted to or excited by mates of the type there favored, in contrast to possible mates of the opposite type, will, in fact, be the better represented in future generations, and both the discrimination and the preference will thereby be enhanced. It appears certainly possible that an evolution of sexual preference due to this cause would establish an effective isolation between two differentiated parts of a species, even when geographical and other factors were least favorable to such separation. —Ronald Fisher, 1930

When it is possible for it to be exercised usefully, 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 will be followed by other offers, either certainly, or at such high chance that the risk of non-occurrence will be smaller than the chance advantage to be gained by selecting a mate.

Intrasexual and intersexual selection
Sexual selection takes two major forms: intrasexual selection (also known as 'male–male competition') in which members of the less limited sex (typically males) compete aggressively among themselves for access to the limiting sex, and intersexual selection (also known as 'mate choice' or 'female choice') in which males compete with each other to be chosen by females.

The sexual struggle is of two kinds: in the one it is between the individuals of the same sex, generally the males, in order to drive away or kill their rivals, the females remaining passive; while in the other, the struggle is likewise between the individuals of the same sex, in order to excite or charm those of the opposite sex, generally the females, which no longer remain passive, but select the more agreeable partners. —Charles Darwin, 1871

With intrasexual selection it should be brought to mind that adorned males will gain reproductive advantage without the intervention of female preference and intersexual selection. This advantage will be conferred by weapons used in the process of resolving disputes, such as those over territorial rights. The use of male sexual ornamentation is primarily used in the search of asymmetries between rival males, contrary to what would seem most obvious (mortally wounding the opponent), since a high number of fatal combats over territory would result in a clear disadvantage. The use of sexual ornamentation is used as a signaling device (signalling theory) amongst males to create a dominance hierarchy, also known as a pecking order, without unneeded detriment and fatality. It is predominantly when two opposing males are so closely matched, as would be found in males not having established themselves in a dominance hierarchy, that asymmetries can not be found and the confrontation escalates to a point where the asymmetries must be proved by aggressive use of ornamentation.

As a propagandist the cock behaves as though he knew that it was advantageous to impress the males as the females of his species, and a sprightly bearing with fine feathers and triumphant song are quite as well adapted for war-propaganda as for courtship. —Ronald Fisher, 1930

How often males will physically engage each other, and in what manner, can best be understood by applying game theory developed for biology, most notably by John Maynard Smith.

In addition to conventional aggression, male–male competition may take the form of sperm competition.



However, 'sexual selection' typically refers to the process of choice (the limiting factor, which is typically females) over members of the opposite sex (the non-limited factor, typically males). This process is known as intersexual selection. Fisher pointed out that preference could be under genetic control and therefore subject to a combination of natural and sexual selection just as much as the qualities of the ornamentation 'preferred'.

The conditions determining which sex is the limiting factor in intersexual selection can be best understood by way of Bateman's principle which states that the sex which invests the most in producing offspring becomes a limiting resource over which the other sex will compete. This can be most easily illustrated by the contrast in nutritional investment into a zygote between egg and sperm, and the limited reproductive capacity of females compared to males.

The stochastic process of sexual selection, the combined effects of its subsets (intra and intersexual selection), create assortative mating and linkage disequilibrium.

Koinophilia is a specific form of mate selection, with, potentially, major evolutionary consequences.

Since natural selection causes beneficial (or "fit") features to replace their disadvantageous counterparts, the beneficial features become increasingly more common with each generation, while the disadvantageous features become increasingly rare. A sexual creature, therefore, wishing to mate with a fit partner, would be expected to avoid individuals sporting unusual features, while being especially attracted to those individuals with a predominance of common or average features. This is termed Koinophilia. Koinophilia has, as an important side effect, that mates displaying mutant features (the result of a genetic mutations) are also avoided. This, in itself, is also advantageous, since the vast majority of mutations are disadvantageous. Since it is impossible to judge whether a new mutation is beneficial or not, koinophilic creatures will avoid them all with equal determination, even if this means avoiding the very occasional beneficial mutation. Thus, koinophilia, while not perfect or infallible in its ability to distinguish fit from unfit mates, remains far and away the best bet strategy when choosing a mate: it will be right far more often than it will be wrong. And, even when it is wrong, a koinophilic choice always ensures that the offspring will inherit a suite of tried and tested features.

Koinophilia provides very simple and obvious explanations for such evolutionary conundrums as the process of speciation, evolutionary stasis and punctuated equilibria, sex and the affordability of males,  and the evolution of cooperation,  and ritualistic behavior. Most of the answers to these evolutionary problems stem from the evolutionary conservatism (i.e. resistance to change) that is the inevitable result of koinophilia. Evolutionary change can still take place, but generally not in large groups. It is presumably only when small groups of individuals become isolated from the main group that genetic drift will induce changes, which, as the isolate grows, become the new set of norms according to which the desirability of potential mates will be judged. If the new set of norms is inherently disadvantageous the isolate will die out. If, on the other hand, the isolate survives and comes into contact with other isolates with other norms, competition between the groups will determine which set of norms survives, and therefore what the new "species" will look like, and how it will behave.

The koinophilia model assumes that sexual creatures have senses with which they evaluate the various individual features of potential mates; and that they are capable of judging which features are common or usual, and which are unusual. Commonness is the only universally appropriate sign of fitness, or, at the very least, of an evolutionarily tried and tested phenotype. The link between all other mate attractants and fitness is both cirumstance-dependent, and ultimately fakable (i.e. the link between the mate attractant and fitness fades, or might even reverse). Commonness cannot be faked, nor is it circumstance-dependent in the way that the other mate attractants are. (Thus, rats and peacocks can both use commoness to judge the desirability of a potential mate, but a gaudy tail cannot be used likewise.) Fitness, by definition, causes commonness, and drives less fit traits into rarity. Koinophilia is therefore evolutionarily robust and likely to be widespread amongst sexual creatures.

Geometric progression
In species which the reproductive success of one sex depends heavily on winning the concession of the other, as is evident with many polygamous birds, sexual selection will act by increasing the degree of preference to which it is due, with the consequence that both the trait preferred and the intensity of preference will be increased together with ever-increasing velocity. This process causing a fervent and rapid evolution of both the conspicuous ornamentation and the preference for such, until so arrested directly or indirectly by bionomic Natural Selection reasons. Thus, in many cases a positive feedback loop of sexual selection is created, resulting with exorbitant physical structures in the non-limited sex, the most notorious example being the peacock (shown above). It is important to note that while a Peacock may have exorbitant plumage, the Peahen has equally exorbitant taste for such.

Initially to start the process, there would be a correlation between the trait and higher fitness. Two previously isolated species, A and B, could come to inhabit the same area resulting in some hybridization. In this situation reproductive isolation will be favored. If the mean value of a trait i.e. tails, in species A, is larger than those of species B, selection would favor females of species A with preference for large tails. Once started the process could continue past the need for species isolation.

The peahen will desire to copulate with the most attractive Peacock so that her progeny, if male, will be attractive to females in the next generation. Additionally the Peacock will desire to copulate with a Peahen that finds him attractive so that if the progeny is female, preference for his degree of ornamentation remains present in the next generation. Since the rate of change in preference is proportioned according to the highest average degree of taste amongst females, and that females desire to best other members of the sex, it creates an additive effect in the cyclical process that will yield exponential increases, in both sexes, if unchecked.

R.A.Fisher in The Genetical Theory of Natural Selection was the first to articulate this process in a game theoretic style treatment.

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

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

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

Since R.A.Fishers initial conceptual model of the 'run-away' process, various others have continued the work on modeling an accurate mathematical proof. Notably R.Lande & P.O'Donald.

Sexual dimorphism
Sex differences directly related to reproduction and serving no direct purpose in courtship are called primary sexual characteristics. Traits amenable to sexual selection, which give an organism an advantage over its rivals (such as in courtship) without being directly involved in reproduction, are called secondary sex characteristics.

In most sexual species the males and females have different equilibrium strategies, due to a difference in relative investment in producing offspring. As formulated in Bateman's principle, females have a greater initial investment in producing offspring (pregnancy in mammals or the production of the egg in birds and reptiles), and this difference in initial investment creates differences in variance in expected reproductive success and bootstraps the sexual selection processes. Classic examples of reversed sex-role species include the pipefish, and Wilson's phalarope. Also, unlike a female, a male (except in monogamous species) has some uncertainty about whether or not he is the true parent of a child, and so will be less interested in spending his energy helping to raise offspring that may or may not be related to him. As a result of these factors, males are typically more willing to mate than females, and so females are typically the ones doing the choosing (except in cases of forced copulations, which can occur in certain species of primates, ducks, and others). The effects of sexual selection are thus held to typically be more pronounced in males than in females.

Differences in secondary sexual characteristics between males and females of a species are referred to as sexual dimorphisms. These can be as subtle as a size difference (sexual size dimorphism, often abbreviated as SSD) or as extreme as horns and color patterns. Sexual dimorphisms abound in nature. Examples include the possession of antlers by only male deer, and the brighter coloration of many male birds, in comparison with females of the same species. The peacock, with its elaborate and colorful tail feathers, which the peahen lacks, is often referred to as perhaps the most extraordinary example of a dimorphism. The largest sexual size dimorphism in vertebrates is the shell dwelling cichlid fish Neolamprologus callipterus in which males are up to 30 times the size of females. Extreme sexual size dimorphism, with females larger than males, is quite common in spiders.

Viability and variations of the theory
Due to their sometimes greatly exaggerated nature, secondary sexual characteristics can prove to be a hindrance to an animal, thereby lowering its fitness. For example, the large antlers of a moose are bulky and heavy and slow the creature's flight from predators; they also can become entangled in low-hanging tree branches and shrubs, and undoubtedly have led to the demise of many individuals. Bright colorations and showy ornamenations, such as those seen in many male birds, in addition to capturing the eyes of females, also attract the attention of predators; when a male peacock spreads its tail, it is beautiful, but very obvious (though this may actually be advantageous to the survival of the male's offspring and the breeding population as a whole; see below). Some of these traits also represent energetically costly investments for the animals that bear them. Because traits held to be due to sexual selection often conflict with the survival fitness of the individual, the question then arises as to why, in nature, in which survival of the fittest is considered the rule of thumb, such apparent liabilities are allowed to persist.

An often-cited theory, published by R.A. Fisher in 1930, that attempts to resolve the paradox, posits that such traits are the results of explosive positive feedback loops that have as their starting points particular sexual preferences for features that confer a survival advantage and thus "become established in the species." Fisher argued that such features advance in the direction of the preference even beyond the optimal level for survival, until the selection pressure of female choice is precisely counterbalanced by the resultant disadvantage for survival. Fisher further argued that the strength of the female preference tends to grow exponentially (leading to 'explosive' evolution of the characteristic) until finally checked by ecological selection, since the offspring of those females with the strongest preference typically fare better in reproducing than the offspring of females with weaker preferences. Any mutations for the preference opposite to the given characteristic, though tending to promote survival against ecological selection, nevertheless tend not to survive in the gene pool because male offspring that result from matings based on the preference are less sexually attractive to the majority of the females in the population, and thus infrequently chosen as mates. An equivalent way of expressing this is that if most females are looking, for example, for long-tailed males, then each female individually does better to select a long-tailed male, since then her male children are more likely to succeed. (The females do not actually have this thought process; this kind of "decision" is an evolutionarily stable strategy.)

Other theories highlight intrinsically useful qualities of such traits. Antlers, horns and the like can be used in physical defense from a predator, and also in show jousting or competition among males in a species. The winner, who typically becomes the dominant animal in the population, is granted access to females, and therefore increases his reproductive output. Antlers are not the only mechanism that can be used to counteract predation. Predators typically look for the eyes of their prey so they can attack that end of the creature. The conspicuousness of eyespots on many species of butterflies and fishes confuses predators and helps to prevent the prey from suffering serious damage.

Another, more recently developed theory, the Handicap principle due to Amotz Zahavi, Russell Lande and W. D. Hamilton, holds that the fact that the male of the species is able to survive until and through the age of reproduction with such a seemingly maladaptive trait is effectively considered by the female to be a testament to his overall fitness. Such handicaps might prove he is either free of or resistant to disease, or it might demonstrate that this animal possesses more speed or a greater physical strength that is used to combat the troubles brought on by the exaggerated trait.

Zahavi's work spurred a re-examination of the field, which has produced an ever-accelerating number of 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. In 1990, Michael Ryan and A.S. Rand, working with the túngara frog, proposed the hypothesis of "Sensory Exploitation", where exaggerated male traits may provide a sensory stimulation that females find hard to resist. In 1991, Anders Pape Møller, working with the tails of male barn swallows, introduced fluctuating asymmetry to the field. Fluctuating asymmetry, a concept previously invoked under natural selection, is based on the observations that healthier specimens have more left-to-right sided symmetry than less healthy specimens. Subsequently the theories of the "Gravity Hypothesis" by Jordi Moya-Larano et al. and "Chase Away" by Brett Holland and William R. Ricehave have also been added. In addition, in the late 1970's Janzen and Mary Willson, noting that male flowers are often larger than female flowers, expanded the field of sexual selection into plants.

In the past few years, the field has exploded to include many additional areas of study, not all of which are clearly included under Darwin's definition of sexual selection. These include cuckoldry, nuptial gifts, sperm competition, infanticide, physical beauty, mating by subterfuge, species isolation mechanisms, male parental care, ambiparental care, mate location, polygamy, and mechanisms that can only be called bizarre, including homosexual rape in certain male animals, cementing of females' vaginal pores by males in some lepidopteran insects, and insect penises specialized to remove any sperm packets from females which may have been deposited by previous suitors.

These theories are not mutually exclusive; combinations of them may also be considered.

Noting, however, that this proliferation of theories and the widening confusion about the definition of the field matches the patterns of a Kuhnian crisis; Joe Abraham published two papers questioning whether the problems of sexual selection might be explained under natural selection. In 1998, he published the Female Sabotage hypothesis, pointing out that mating provides females with the opportunity to sabotage polygamous males, by only mating with males who exhibit life-threatening traits. As males increasingly die as a result of their elaborations, fighting, and mating exertions, their declining numbers leave more food and other resources for females and offspring, and relieve them of predation pressure. In 2005 he published a companion paper looking at sexual dimorphism in flower sizes, resurrecting an older theory by Hermann Müller, that larger male flowers may simply serve to attract pollinators to pollen donors, before they visit pollen acceptors. Abraham's experimental data showed strongly that this is the case, and flower dimorphisms may also be a function under natural selection rather than sexual selection.

In humans
Charles Darwin conjectured that the male beard, as well as the relative hairlessness of humans compared to nearly all other mammals, are results of sexual selection. He reasoned that since, compared to males, the bodies of females are more nearly hairless, hairlessness is one of the atypical cases due to its selection by males at a remote prehistoric time, when males had overwhelming selective power, and that it nonetheless affected males due to genetic correlation between the sexes. He also hypothesized that sexual selection could also be what had differentiated between different human races, as he did not believe that natural selection provided a satisfactory answer.

Geoffrey Miller, drawing on some of Darwin's largely neglected ideas about human behavior, has hypothesized that many human behaviors not clearly tied to survival benefits, such as humor, music, visual art, verbal creativity, and some forms of altruism, are courtship adaptations that have been favored through sexual selection. In that view, many human artefacts could considered subject to sexual selection as part of the extended phenotype, for instance clothing that enhance sexually selected traits.

Some hypothesises about the evolution of the human brain argues that is a sexually selected trait, as it would not confer enough fitness in itself relative to its high maintenance costs (a quarter to a fifth of the energy and oxygen consumed by a human).

The zoologist Richard Dawkins pointed out in 1989 that the loss of the penis bone in humans, when it is present in our nearest related species the chimpanzee demands some form of evolutionary explanation. He speculates that its loss is probably a form of sexual selection by females looking for signs of good health in prospective mates. The reliance of the human penis solely on hydraulic means to achieve a rigid state makes it particularly vulnerable to blood pressure variation. Poor erectile function betrays, not only physical states such as diabetes and neurological disorders, but mental states such as stress and depression.

History and application of the theory
The theory of sexual selection was first proposed by Charles Darwin in his book The Origin of Species, though it was primarily devoted to natural selection. A later work, The Descent of Man and Selection in Relation to Sex dealt with the subject of sexual selection exhaustively, in part because Darwin felt that natural selection alone was unable to account for certain types of apparently non-competitive adaptations, such as the tail of a male peacock. 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 two primary categories: male-male competition (which would produce adaptations such as a Bighorn Sheep's horns, which are used primarily in sparring with other males over females), and cases of female choice (which would produce adaptations like beautiful plumage, elaborate songs, and other things related to impressing and attracting).

Darwin's views on sexual selection were opposed strongly by his "co-discoverer" of natural selection, Alfred Russel Wallace, though much of his "debate" with Darwin took place after Darwin's death. Wallace argued that the aspects of it which were male-male competition, while real, were simply forms of natural selection, and that the notion of "female choice" was attributing the ability to judge standards of beauty to animals far too cognitively undeveloped to be capable of aesthetic feeling (such as beetles). Historians have noted that Wallace had previously had his own problem with "female choice": he had been left at the altar by a woman of a higher social class.

Wallace also argued that Darwin too much favored the bright colors of the male peacock as adaptive without realizing that the "drab" peahen's coloration is itself adaptive, as camouflage. Wallace more speculatively argued that the bright colors and long tails of the peacock were not adaptive in any way, and that bright coloration could result from non-adaptive physiological development (for example, the internal organs of animals, not being subject to a visual form of natural selection, come in a wide variety of bright colors). This has been questioned by later scholars as quite a stretch for Wallace, who in this particular instance abandoned his normally strict "adaptationist" agenda in asserting that the highly intricate and developed forms such as a peacock's tail resulted by sheer "physiological processes" that were somehow not at all subjected to adaptation.

Though Darwin considered sexual and natural selection to be two separate processes of equal importance, most of his contemporaries were not convinced, and sexual selection is usually de-emphasized as being a lesser force than, or simply a part of, natural selection.

The sciences of evolutionary psychology, human behavioral ecology, and sociobiology study the influence of sexual selection in humans, though these are often controversial fields. The field of epigenetics is broadly concerned with the competence of adult organisms within a given sexual, social, and ecological niche, which includes the development of mating competences, e.g., by mimicking adult behavior.

Criticism
A group of authors led by Joan Roughgarden have criticised sexual selection theory, claiming there was evidence that individuals did not compete strongly for mating opportunities, but that the function of sex was mostly social. The evidence used in the paper, however, was heavily criticised by many other notable authors for its factual inaccuracy.