Sexual selection

Darwin

Sexual selection was first proposed by Charles Darwin in The Origin of Species (1859) and developed in The Descent of Man and Selection in Relation to Sex (1871), as he felt that natural selection alone was unable to account for certain types of non-survival adaptations. He once wrote to a colleague that "The sight of a feather in a peacock's tail, whenever I gaze at it, makes me sick!" His work divided sexual selection into male-male competition and female choice.

... depends, not on a struggle for existence, but on a struggle between the males for possession of the females; the result is not death to the unsuccessful competitor, but few or no offspring.

... when the males and females of any animal have the same general habits ... but differ in structure, colour, or ornament, such differences have been mainly caused by sexual selection.

These views were to some extent opposed by Alfred Russel Wallace, mostly after Darwin's death. He accepted that sexual selection could occur, but argued that it was a relatively weak form of selection. He argued that male-male competitions were forms of natural selection, but that the "drab" peahen's coloration is itself adaptive as camouflage. In his opinion, ascribing mate choice to females was attributing the ability to judge standards of beauty to animals (such as beetles) far too cognitively undeveloped to be capable of aesthetic feeling.

Ronald Fisher

Ronald Fisher, the English statistician and evolutionary biologist developed a number of ideas about sexual selection in his 1930 book The Genetical Theory of Natural Selection including the sexy son hypothesis and Fisher's principle. The Fisherian runaway describes how sexual selection accelerates the preference for a specific ornament, causing the preferred trait and female preference for it to increase together in a positive feedback runaway cycle. In a remark that was not widely understood for another 50 years he said:

... 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

This causes a dramatic increase in both the male's conspicuous feature and in female preference for it, until practical, physical constraints halt further exaggeration. A positive feedback loop is created, producing extravagant physical structures in the non-limiting sex. A classic example of female choice and potential runaway selection is the long-tailed widowbird. While males have long tails that are selected for by female choice, female tastes in tail length are still more extreme with females being attracted to tails longer than those that naturally occur. Fisher understood that female preference for long tails may be passed on genetically, in conjunction with genes for the long tail itself. Long-tailed widowbird offspring of both sexes will inherit both sets of genes, with females expressing their genetic preference for long tails, and males showing off the coveted long tail itself.

Richard Dawkins presents a non-mathematical explanation of the runaway sexual selection process in his book The Blind Watchmaker. Females that prefer long tailed males tend to have mothers that chose long-tailed fathers. As a result, they carry both sets of genes in their bodies. That is, genes for long tails and for preferring long tails become linked. The taste for long tails and tail length itself may therefore become correlated, tending to increase together. The more tails lengthen, the more long tails are desired. Any slight initial imbalance between taste and tails may set off an explosion in tail lengths. Fisher wrote that:

The exponential element, which is the kernel of the thing, arises from the rate of change in hen taste being proportional to the absolute average degree of taste. —Ronald Fisher, 1932

The female widow bird will desire to mate with the most attractive long-tailed male so that her progeny, if male, will themselves be attractive to females of the next generation - thereby fathering many offspring who will carry the female's genes. Since the rate of change in preference is proportional to the average taste amongst females, and as females desire to secure the services of the most sexually attractive males, an additive effect is created that, if unchecked, can yield exponential increases in a given taste and in the corresponding desired sexual attribute.

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 Fisher's initial conceptual model of the 'runaway' process, Russell Lande and Peter O'Donald have provided detailed mathematical proofs that define the circumstances under which runaway sexual selection can take place.

Reproductive success

The reproductive success of an organism is measured by the number of offspring left behind, and their quality or probable fitness.

Sexual preference creates a tendency towards assortative mating or homogamy. The general conditions of sexual discrimination appear to be (1) the acceptance of one mate precludes the effective acceptance of alternative mates, and (2) the rejection of an offer 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.

The conditions determining which sex becomes the more limited resource 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", illustrated by the greater nutritional investment of an egg in a zygote, and the limited capacity of females to reproduce; for example in humans a woman can only give birth every ten months whereas in theory a male can become a father every day.

Modern interpretation

The sciences of evolutionary psychology, human behavioural ecology, and sociobiology study the influence of sexual selection in humans.

Darwin's ideas on sexual selection were met with scepticism by his contemporaries and not considered of great importance in the early 20th century, until in the 1930s biologists decided to include sexual selection as a mode of natural selection. Only in the 21st century have they become more important in biology. The theory however is generally applicable and analogous to natural selection.

New theories highlight intrinsically useful qualities of such traits. Antlers, horns and the like can be used in physical defence from a predator, and also in competition among males in a tournament species. The winner, which 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.

Research published in 2015 indicates that sexual selection, including mate choice, "improves population health and protects against extinction, even in the face of genetic stress from high levels of inbreeding" and "ultimately dictates who gets to reproduce their genes into the next generation - so it's a widespread and very powerful evolutionary force." The study involved the flour beetle over a ten-year period where the only changes were in the intensity of sexual selection.

Another theory, the handicap principle of Amotz Zahavi, Russell Lande and W. D. Hamilton, holds that the fact that the male is able to survive until and through the age of reproduction with such a seemingly maladaptive trait is taken 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 that he 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 tungara frog, proposed the hypothesis of "Sensory Exploitation", where exaggerated male traits may provide a sensory stimulation that females find hard to resist. Subsequently, the theories of the "Gravity Hypothesis" by Jordi Moya-Larano et al. (2002), invoking a simple biomechanical model to account for the adaptive value for smaller male spiders of speed in clmbing vertical surfaces, and "Chase Away" by Brett Holland and William R. Rice have been added. In the late 1970s, 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 other areas of study, not all of which fit 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 homosexual rape in certain male animals.

Focusing on the effect of sexual conflict, as hypothesized by William Rice, Locke Rowe et Göran Arnvist, Thierry Lodé underlines that the divergence of interest constitutes a key for evolutionary process. Sexual conflict leads to an antagonistic co-evolution in which one sex tends to control the other, resulting in a tug of war. Besides, the sexual propaganda theory only argued that mate were opportunistically lead, on the basis of various factors determining the choice such as phenotypic characteristics, apparent vigour of individual, strength of mate signals, trophic resources, territoriality etc. and could explain the maintenance of genetic diversity within populations.

Several workers have brought attention to the fact that elaborated characters that ought to be costly in one way or another for their bearers (e.g., the tails of some species of Xiphophorus fish) do not always appear to have a cost in terms of energetics, performance or even survival. One possible explanation for the apparent lack of costs is that "compensatory traits" have evolved in concert with the sexually selected traits.

Toolkit of natural selection

Sexual selection may explain how certain characteristics (such as feathers) had distinct survival value at an early stage in their evolution. Geoffrey Miller proposes that sexual selection might have contributed by creating evolutionary modules such as Archaeopteryx feathers as sexual ornaments, at first. The earliest proto-birds such as China's Protarchaeopteryx, discovered in the early 1990s, had well-developed feathers but no sign of the top/bottom asymmetry that gives wings lift. Some have suggested that the feathers served as insulation, helping females incubate their eggs. But perhaps the feathers served as the kinds of sexual ornaments still common in most bird species, and especially in birds such as peacocks and birds-of-paradise today. If proto-bird courtship displays combined displays of forelimb feathers with energetic jumps, then the transition from display to aerodynamic functions could have been relatively smooth.

Sexual selection sometimes generates features that may help cause a species' extinction, as has been suggested for the giant antlers of the Irish elk (Megaloceros giganteus) that became extinct in Pleistocene Europe. However, sexual selection can also do the opposite, driving species divergence - sometimes through elaborate changes in genitalia - such that new species emerge.

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 colour patterns. Sexual dimorphisms abound in nature. Examples include the possession of antlers by only male deer, the brighter coloration of many male birds in comparison with females of the same species, or even more distinct differences in basic morphology, such as the drastically increased eye-span of the male stalk-eyed fly. The peacock, with its elaborate and colourful tail feathers, which the peahen lacks, is often referred to as perhaps the most extraordinary example of a dimorphism. Male and female black-throated blue warblers and Guianan cock-of-the-rocks also differ radically in their plumage. Early naturalists even believed the females to be a separate species. 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. Many other fish such as guppies also exhibit sexual dimorphism. Extreme sexual size dimorphism, with females larger than males, is quite common in spiders and birds of prey.

In different taxa

Sexual selection has been observed to occur in plants, animals and fungi. In certain hermaphroditic snail and slug species of molluscs the throwing of love darts is a form of sexual selection. Certain male insects of the lepidoptera order of insects cement the vaginal pores of their females.

Today, biologists say that certain evolutionary traits can be explained by intraspecific competition - competition between members of the same species - distinguishing between competition before or after sexual intercourse.

Before copulation, intrasexual selection - usually between males - may take the form of male-to-male combat. Also, intersexual selection, or mate choice, occurs when females choose between male mates. Traits selected by male combat are called secondary sexual characteristics (including horns, antlers, etc.), which Darwin described as "weapons", while traits selected by mate (usually female) choice are called "ornaments". Due to their sometimes greatly exaggerated nature, secondary sexual characteristics can prove to be a hindrance to an animal, thereby lowering its chances of survival. 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 colourations 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. 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. However, one must also consider that intersexual selection can occur with an emphasis on resources that one sex possesses rather than morphological and physiological differences. For example, males of Euglossa imperialis, a non-social bee species, form aggregations of territories considered to be leks, to defend fragrant-rich primary territories. The purpose of these aggregations is only facultative, since the more suitable fragrant-rich sites there are, the more habitable territories there are to inhabit, giving females of this species a large selection of males with whom to potentially mate.

After copulation, male–male competition distinct from conventional aggression may take the form of sperm competition, as described by Parker in 1970. More recently, interest has arisen in cryptic female choice, a phenomenon of internally fertilised animals such as mammals and birds, where a female will get rid of a male's sperm without his knowledge.

Finally, sexual conflict is said to occur between breeding partners, sometimes leading to an evolutionary arms race between males and females. Sexual selection can also occur as a product of pheromone release, such as with the stingless bee, Trigona corvina.

Female mating preferences are widely recognized as being responsible for the rapid and divergent evolution of male secondary sexual traits. Females of many animal species prefer to mate with males with external ornaments - exaggerated features of morphology such as elaborate sex organs. These preferences may arise when an arbitrary female preference for some aspect of male morphology — initially, perhaps, a result of genetic drift — creates, in due course, selection for males with the appropriate ornament. One interpretation of this is known as the sexy son hypothesis. Alternatively, genes that enable males to develop impressive ornaments or fighting ability 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.

Darwin conjectured that heritable traits such as beards and hairlessness in different human populations are results of sexual selection in humans. Geoffrey Miller has hypothesized that many human behaviours not clearly tied to survival benefits, such as humour, music, visual art, verbal creativity, and some forms of altruism, are courtship adaptations that have been favoured through sexual selection. In that view, many human artefacts could be considered subject to sexual selection as part of the extended phenotype, for instance clothing that enhances sexually selected traits. Some argue that the evolution of human intelligence is a sexually selected trait, as it would not confer enough fitness in itself relative to its high maintenance costs.