Lek paradox

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Greater sage-grouse at lek, with multiple males displaying for the less conspicuous females Greater Sage-Grouse at Lek (6948123054).jpg
Greater sage-grouse at lek, with multiple males displaying for the less conspicuous females

The lek paradox is the conundrum of how additive or beneficial genetic variation is maintained in lek mating species in the face of consistent sexual selection based on female preferences. While many studies have attempted to explain how the lek paradox fits into Darwinian theory, the paradox remains. Persistent female choice for particular male trait values should erode genetic diversity in male traits and thereby remove the benefits of choice, yet choice persists. [1] This paradox can be somewhat alleviated by the occurrence of mutations introducing potential differences, as well as the possibility that traits of interest have more or less favorable recessive alleles.

The basis of the lek paradox is continuous genetic variation in spite of strong female preference for certain traits. There are two conditions in which the lek paradox arises. The first is that males contribute only genes and the second is that female preference does not affect fecundity. [2] Female choice should lead to directional runaway selection, resulting in a greater prevalence for the selected traits. Stronger selection should lead to impaired survival, as it decreases genetic variance and ensures that more offspring have similar traits. [3] However, lekking species do not exhibit runaway selection.

In a lekking reproductive system, what male sexual characteristics can signal to females is limited, as the males provide no resources to females or parental care to their offspring. [4] This implies that a female gains indirect benefits from her choice in the form of "good genes" for her offspring. [5] Hypothetically, in choosing a male that excels at courtship displays, females gain genes for their offspring that increase their survival or reproductive fitness.

Amotz Zahavi declared that male sexual characteristics only convey useful information to the females if these traits confer a handicap on the male. [6] Otherwise, males could simply cheat: if the courtship displays have a neutral effect on survival, males could all perform equally and it would signify nothing to the females. But if the courtship display is somehow deleterious to the male’s survival—such as increased predator risk or time and energy expenditure—it becomes a test by which females can assess male quality. Under the handicap principle, males who excel at the courtship displays prove that they are of better quality and genotype, as they have already withstood the costs to having these traits. [6] Resolutions have been formed to explain why strong female mate choice does not lead to runaway selection. The handicap principle describes how costly male ornaments provide females with information about the male’s inheritable fitness. [7] The handicap principle may be a resolution to the lek paradox, for if females select for the condition of male ornaments, then their offspring have better fitness.

One potential resolution to the lek paradox is Rowe and Houle's theory of condition-dependent expression of male sexually selected traits. Similar to the handicap principle, Rowe and Houle argue that sexually selected traits depend on physical condition. Condition, in turn, summarizes a large number of genetic loci, including those involved in metabolism, muscular mass, nutrition, etc. Rowe and Houle claim that condition dependence maintains genetic variation in the face of persistent female choice, as the male trait is correlated with abundant genetic variation in condition. [5] This is the genic capture hypothesis, which describes how a significant amount of the genome is involved in shaping the traits that are sexually selected. [4] There are two criteria in the genic capture hypothesis: the first is that sexually selected traits are dependent upon condition and the second is that general condition is attributable to high genetic variance. [5]

Genetic variation in condition-dependent traits may be further maintained through mutations and environmental effects. Genotypes may be more effective in developing condition dependent sexual characteristics in different environments, while mutations may be deleterious in one environment and advantageous in another. [4] Thus genetic variance remains in populations through gene flow across environments or generation overlap. According to the genic capture hypothesis, female selection does not deplete the genetic variance, as sexual selection operates on condition dependence traits, thereby accumulating genetic variance within the selected for trait. [5] Therefore, females are actually selecting for high genetic variance.

In an alternate but non-exclusionary hypothesis, W. D. Hamilton and M. Zuk proposed that successful development of sexually selected traits signal resistance to parasites. [8] Parasites can significantly stress their hosts so that they are unable to develop sexually selected traits as well as healthy males. According to this theory, a male who vigorously displays demonstrates that he has parasite-resistant genes to the females. In support of this theory, Hamilton and Zuk found that male sexual ornaments were significantly correlated with levels of incidence of six blood diseases in North American passerine bird species. The Hamilton and Zuk model addresses the lek paradox, arguing that the cycles of co-adaptation between host and parasite resist a stable equilibrium point. Hosts continue to evolve resistance to parasites and parasites continue to bypass resistant mechanisms, continuously generating genetic variation. [8] The genic capture and parasite resistance hypotheses could logically co-occur in the same population.

One resolution to the lek paradox involves female preferences and how preference alone does not cause a drastic enough directional selection to diminish the genetic variance in fitness. [9] Another conclusion is that the preferred trait is not naturally selected for or against and the trait is maintained because it implies increased attractiveness to the male. [2] Thus, there may be no paradox.

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 mode of natural selection 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">Sexual dimorphism</span> Condition where males and females exhibit different characteristics

Sexual dimorphism is the condition where sexes of the same species exhibit different morphological characteristics, particularly 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. A lek can also indicate an available plot of space able to be utilized 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, and mammals, and arthropods including crustaceans and insects.

<span class="mw-page-title-main">Behavioral ecology</span> Study of the evolutionary basis for animal behavior due to ecological pressures

Behavioral ecology, also spelled behavioural ecology, is the study of the evolutionary basis for animal behavior due to ecological pressures. Behavioral ecology emerged from ethology after Niko Tinbergen outlined four questions to address when studying animal behaviors: What are the proximate causes, ontogeny, survival value, and phylogeny of a behavior?

<span class="mw-page-title-main">Handicap principle</span> Hypothesis in evolutionary biology

The handicap principle is a disputed hypothesis proposed by the Israeli biologist Amotz Zahavi in 1975. It is meant to explain how sexual selection may lead to "honest" or reliable signalling between male and female animals which have an obvious motivation to bluff or deceive each other. The handicap principle suggests that secondary sexual characteristics are costly signals which must be reliable, as they cost the signaller resources that individuals with less of a particular trait could not afford. The handicap principle further proposes that animals of greater biological fitness signal this through handicapping behaviour, or morphology that effectively lowers overall fitness. The central idea is that sexually selected traits function like conspicuous consumption, signalling the ability to afford to squander a resource. Receivers then know that the signal indicates quality, because inferior-quality signallers are unable to produce such wastefully extravagant signals.

<span class="mw-page-title-main">Fisherian runaway</span> Sexual selection mechanism

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. 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.

<span class="mw-page-title-main">Stalk-eyed fly</span> Family of dipteran insects with antennae located on eyestalks

Stalk-eyed flies are insects of the fly family Diopsidae. The family is distinguished from most other flies by most members of the family possessing "eyestalks": projections from the sides of the head with the eyes at the end. Some fly species from other families such as Drosophilidae, Platystomatidae, Richardiidae, and Tephritidae have similar heads, but the unique character of the Diopsidae is that their antennae are located on the stalk, rather than in the middle of the head as in all other flies. Stalked eyes are present in all members of the subfamily Diopsinae, but are absent in the Centrioncinae, which retain unstalked eyes similar to those of other flies. The stalked eyes are usually sexually dimorphic, with eyestalks present but shorter in females.

<span class="mw-page-title-main">Sexual conflict</span> Term in evolutionary biology

Sexual conflict or sexual antagonism occurs when the two sexes have conflicting optimal fitness strategies concerning reproduction, particularly over the mode and frequency of mating, potentially leading to an evolutionary arms race between males and females. In one example, males may benefit from multiple matings, while multiple matings may harm or endanger females, due to the anatomical differences of that species. Sexual conflict underlies the evolutionary distinction between male and female.

<span class="mw-page-title-main">Mate choice</span> One of the primary mechanisms under which evolution can occur

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">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">Antagonistic pleiotropy hypothesis</span> Proposed evolutionary explanation for senescence

The antagonistic pleiotropy hypothesis was first proposed by George C. Williams in 1957 as an evolutionary explanation for senescence. Pleiotropy is the phenomenon where one gene controls more than one phenotypic trait in an organism. A gene is considered to possess antagonistic pleiotropy if it controls more than one trait, where at least one of these traits is beneficial to the organism's fitness early on in life and at least one is detrimental to the organism's fitness later on due to a decline in the force of natural selection. The theme of G.C. William's idea about antagonistic pleiotropy was that if a gene caused both increased reproduction in early life and aging in later life, then senescence would be adaptive in evolution. For example, one study suggests that since follicular depletion in human females causes both more regular cycles in early life and loss of fertility later in life through menopause, it can be selected for by having its early benefits outweigh its late costs.

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.

<span class="mw-page-title-main">Major histocompatibility complex and sexual selection</span> Adaptive immune gene selection

The major histocompatibility complex in sexual selection concerns how major histocompatibility complex (MHC) molecules allow for immune system surveillance of the population of protein molecules in a host's cells. In 1976, Yamazaki et al. demonstrated a sexual selection mate choice by male mice for females of a different MHC.

The theoretical foundations of evolutionary psychology are the general and specific scientific theories that explain the ultimate origins of psychological traits in terms of evolution. These theories originated with Charles Darwin's work, including his speculations about the evolutionary origins of social instincts in humans. Modern evolutionary psychology, however, is possible only because of advances in evolutionary theory in the 20th century.

Genic capture is a hypothesis explaining the maintenance of genetic variance in traits under sexual selection. A classic problem in sexual selection is the fixation of alleles that are beneficial under strong selection, thereby eliminating the benefits of mate choice. Genic capture resolves this paradox by suggesting that additive genetic variance of sexually selected traits reflects the genetic variance in total condition. A deleterious mutation anywhere in the genome will adversely affect condition, and thereby adversely affect a condition-dependent sexually selected trait. Genic capture therefore resolves the lek paradox by proposing that recurrent deleterious mutation maintains additive genetic variance in fitness by incorporating the entire mutation load of an individual. Thus any condition-dependent trait "captures" the overall genetic variance in condition. Rowe and Houle argued that genic capture ensures that good genes will become a central feature of the evolution of any sexually selected trait.

<span class="mw-page-title-main">Marlene Zuk</span> American evolutionary biologist

Marlene Zuk is an American evolutionary biologist and behavioral ecologist. She worked as professor of biology at the University of California, Riverside (UCR) until she transferred to the University of Minnesota in 2012. Her studies involve sexual selection and parasites.

<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.

<span class="mw-page-title-main">Parasite-stress theory</span> Theory of human evolution

Parasite-stress theory, or pathogen-stress theory, is a theory of human evolution proposing that parasites and diseases encountered by a species shape the development of species' values and qualities, proposed by researchers Corey Fincher and Randy Thornhill.

In humans, males and females differ in their strategies to acquire mates and focus on certain qualities. There are two main categories of strategies that both sexes utilize: short-term and long-term. Human mate choice, an aspect of sexual selection in humans, depends on a variety of factors, such as ecology, demography, access to resources, rank/social standing, genes, and parasite stress.

References

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