Intralocus sexual conflict

Last updated August 19, 2023

Intralocus sexual conflict is a type of sexual conflict that occurs when a genetic locus harbours alleles which have opposing effects on the fitness of each sex, such that one allele improves the fitness of males (at the expense of females), while the alternative allele improves the fitness of females (at the expense of males).^[1] Such "sexually antagonistic" polymorphisms are ultimately generated by two forces: (i) the divergent reproductive roles of each sex, such as conflicts over optimal mating strategy,^[2]^[3] and (ii) the shared genome of both sexes, which generates positive between-sex genetic correlations for most traits.^[4] In the long term, intralocus sexual conflict is resolved when genetic mechanisms evolve that decouple the between-sex genetic correlations between traits. This can be achieved, for example, via the evolution of sex-biased or sex-limited genes.

Intralocus sexual conflict can be considered a form of maladaptation,^[5] as it results in a deviation of both sexes from their fitness optima, with both sexes expressing traits that are sub-optimal for that sex's fitness. Intralocus sexual conflict can also be considered a form of pleiotropy, in which genetic variants have opposing effects on different classes of individual within a population (i.e., males and females), rather than opposing effects on different components of fitness (e.g. survival vs. mating success). Intralocus sexual conflict has important implications for the evolution of sexual dimorphism,^[6] the evolution of sex chromosomes^[7]^[8] and the maintenance of genetic variation.^[9]

Sexual conflict

All sexual conflict between the sexes arises because members of one sex express traits that benefit their ability to successfully survive and reproduce, while the expression of these traits negatively impacts the fitness of the opposite sex. In genetics, a locus refers to the exact location of a gene on a chromosome, and sexual conflict can have different consequences depending on the underlying genetics. Interlocus sexual conflict occurs at different loci in each sex, whereas intralocus sexual conflict occurs at the same loci. An example of interlocus sexual conflict is the expression of accessory gland proteins by males during mating, which negatively affect female fitness. This may result in a counter adaptation at a different locus to reduce harm in females. For example, a female may diminish detrimental consequences of being subjected to male accessory gland proteins during mating by waiting longer to re-mate, or she may develop an opposite physical adaptation of her reproductive tract.^[10]

Alternatively, sexual conflict may occur within the same locus, in which case it is known as intralocus sexual conflict. Intralocus sexual conflict occurs because many phenotypic traits are determined by a common set of genes which are found and expressed in both male and female individuals. For example, phenotypic traits such as body size, diet, development time, longevity, and locomotory activity are typically positively genetically correlated between sexes. These traits have also been suggested to underlie intralocus sexual conflict^[11] because they may be subjected to antagonistic patterns of selection, in which elevated values of one trait result in enhanced fitness in one sex but decreased fitness in the other, generating a negative correlation for fitness between male and female individuals that express a particular trait.^[12]

Development

Bonduriansky and Chenowith proposed a four phase model for the development of intralocus sexual conflict, in which the first phase is stabilizing selection on a trait in both sexes. Intralocus conflict then originates in the second phase when a change in physical or social conditions causes intense selection on that trait in males and/or females, and both sexes are displaced from their optimum. In the third phase, diverging selection continues on both sexes, but is attenuated. In the fourth phase, intralocus conflict is fully resolved and sexual dimorphism has occurred.^[13]

Examples

A good example of intralocus sexual conflict can be seen in humans, regarding the selection pressures on height that varies between sexes. In nature, a negative correlation between the height of a woman and her reproductive success has been seen, with selection favoring relatively shorter women. On the other hand, men of average height are preferred, and have higher reproductive success than men who are shorter or taller in nature.^[14] Studies have been able to produce evidence concluding that higher reproductive success is obtained by females in sibling pairs that were shorter in height, whereas reproductive success in sibling pairs of average height was much higher in males. These findings show that intralocus sexual conflict over a physical trait, such as height, can have an effect on Darwinian fitness in humans.^[14]

Intralocus sexual conflict diminishes the benefits of sexual selection.^[15] Examples of intralocus sexual conflict can be seen all throughout nature.

In humans, males and females who appear to be more masculine in their physical appearance for their sex report to have brothers that score a higher mate value relative to their sisters.^[16] Similarly, individuals who are of normal weight and have higher levels of estradiol are positively correlated with higher mate values in women, and higher levels of testosterone are positively correlated with higher mate values in men.^[16] Individuals that are physically and hormonally more masculine tend to have brothers that are fairly more attractive than their sisters, while more feminine individuals have sisters that are more attractive than their brothers. This suggests that intralocus sexual conflict can mediate and determine the fitness of an individual. Human hips are another example, where females need larger hips for childbirth as opposed to smaller hips (optimal for walking) for males.^[17] The genes that affect hip size must reach a compromise that is at neither the male optimum nor the female optimum.

In the Ibiza wall lizard (Podarcis pityusensis), intralocus sexual conflict exist over color. In this species, color is used as a signal of male fighting ability. Males that are more brightly colored are perceived as better fighters. As lizards in this species age, they become larger and more colorful. During mating seasons, males will typically compete for females and resources by fighting with each other. Males will select opponents based on the intensity of the color of their opponent's coat. Females of this species also possess brightly colored coats. This trait is detrimental for females, since being colorful makes them more conspicuous to males^{[ clarification needed ]} and predators. However, in males, being colorful helps males win fights and increases their reproductive success.

Another example can be seen in the features of the soay sheep (Ovis aries) horns, and the length of the serin finch's (Serinus serin) tail. Males that possess larger horns or longer tails in these species have higher success during male competition and increased reproductive success. However, these features require a great deal of energy for females to possess and do not benefit females in any significant way.^[10]

Intralocus genetic differences between males and females have been identified in a variety of fish species using RAD sequencing, including gulf pipefish ^[18] and deacon rockfish.^[19] It has been hypothesised that some of the loci in deacon rockfish may be examples of intralocus sexual conflict but their function and evolutionary significance is currently uncertain.^[19]

Resolution

There have been several hypotheses made that attempt to explain possible resolutions for intralocus sexual conflict. In one proposition, it is suggested that intralocus sexual conflict can be minimized through sex-dependent gene regulation. By doing this, genes that are negatively selected may evolve sexually dimorphic traits that encourage sex- specific optima. Sexual dimorphism is thought to be an effective resolution, since it can be made irreversible under short term selection.^[20] As a result, sexual dimorphism could pose as a resolution to intralocus sexual conflict. Another proposed hypothesis suggests that intralocus sexual conflict can be resolved through alternative splicing. In this mechanism, the sex of an organism will ultimately decide the final form of the protein that is created from a shared coding region within a set of genes. Through this posttranscriptional process, RNA that is created by a gene is spliced in various ways that allow it to ultimately join exons in a variety of ways^[20] Genomic imprinting also presents as a possible resolution for intralocus sexual conflict. In genomic imprinting, genes are marked through methylation of DNA with information of its parental origin. In order for genomic imprinting to resolve intralocus sexual conflict, parents would have to imprint their genes in sex- specific matter. For example, males could imprint their genes in a way so that sexually antagonistic alleles that benefit males are not expressed in sperm that is only X-bearing.^[20]

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.

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 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.

Population genetics is a subfield of genetics that deals with genetic differences within and among populations, and is a part of evolutionary biology. Studies in this branch of biology examine such phenomena as adaptation, speciation, and population structure.

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">Pleiotropy</span> Influence of a single gene on multiple phenotypic traits

Pleiotropy occurs when one gene influences two or more seemingly unrelated phenotypic traits. Such a gene that exhibits multiple phenotypic expression is called a pleiotropic gene. Mutation in a pleiotropic gene may have an effect on several traits simultaneously, due to the gene coding for a product used by a myriad of cells or different targets that have the same signaling function.

<span class="mw-page-title-main">Anisogamy</span> Sexual reproduction involving a large, female gamete and a small, male gamete

Anisogamy is a form of sexual reproduction that involves the union or fusion of two gametes that differ in size and/or form. The smaller gamete is male, a sperm cell, whereas the larger gamete is female, typically an egg cell. Anisogamy is predominant among multicellular organisms. In both plants and animals gamete size difference is the fundamental difference between females and males.

Molecular ecology is a field of evolutionary biology that is concerned with applying molecular population genetics, molecular phylogenetics, and more recently genomics to traditional ecological questions. It is virtually synonymous with the field of "Ecological Genetics" as pioneered by Theodosius Dobzhansky, E. B. Ford, Godfrey M. Hewitt, and others. These fields are united in their attempt to study genetic-based questions "out in the field" as opposed to the laboratory. Molecular ecology is related to the field of conservation genetics.

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Interlocus contest evolution (ICE) is a process of intergenomic conflict by which different loci within a single genome antagonistically coevolve. ICE supposes that the Red Queen process, which is characterized by a never-ending antagonistic evolutionary arms race, does not only apply to species but also to genes within the genome of a species.

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<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.

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.

Sex-limited genes are genes that are present in both sexes of sexually reproducing species but are expressed in only one sex and have no penetrance, or are simply 'turned off' in the other. In other words, sex-limited genes cause the two sexes to show different traits or phenotypes, despite having the same genotype. This term is restricted to autosomal traits, and should not be confused with sex-linked characteristics, which have to do with genetic differences on the sex chromosomes. Sex-limited genes are also distinguished from sex-influenced genes, where the same gene will show differential expression in each sex. Sex-influenced genes commonly show a dominant/recessive relationship, where the same gene will have a dominant effect in one sex and a recessive effect in the other. However, the resulting phenotypes caused by sex-limited genes are present in only one sex and can be seen prominently in various species that typically show high sexual dimorphism.

Female sperm storage is a biological process and often a type of sexual selection in which sperm cells transferred to a female during mating are temporarily retained within a specific part of the reproductive tract before the oocyte, or egg, is fertilized. This process takes place in some species of animals, but not in humans. The site of storage is variable among different animal taxa and ranges from structures that appear to function solely for sperm retention, such as insect spermatheca and bird sperm storage tubules, to more general regions of the reproductive tract enriched with receptors to which sperm associate before fertilization, such as the caudal portion of the cow oviduct containing sperm-associating annexins. Female sperm storage is an integral stage in the reproductive process for many animals with internal fertilization. It has several documented biological functions including:

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.

Interlocus sexual conflict is a type of sexual conflict that occurs through the interaction of a set of antagonistic alleles at two or more different loci, or the location of a gene on a chromosome, in males and females, resulting in the deviation of either or both sexes from the fitness optima for the traits. A co-evolutionary arms race is established between the sexes in which either sex evolves a set of antagonistic adaptations that is detrimental to the fitness of the other sex. The potential for reproductive success in one organism is strengthened while the fitness of the opposite sex is weakened. Interlocus sexual conflict can arise due to aspects of male–female interactions such as mating frequency, fertilization, relative parental effort, female remating behavior, and female reproductive rate.

Sexual selection in scaled reptiles studies how sexual selection manifests in snakes and lizards, which constitute the order Squamata of reptiles. Each of the over three thousand snakes use different tactics in acquiring mates. Ritual combat between males for the females they want to mate with includes topping, a behavior exhibited by most viperids in which one male will twist around the vertically elevated fore body of its opponent and forcing it downward. It is common for neck biting to occur while the snakes are entwined.

Reinforcement is a process of speciation where natural selection increases the reproductive isolation between two populations of species. This occurs as a result of selection acting against the production of hybrid individuals of low fitness. The idea was originally developed by Alfred Russel Wallace and is sometimes referred to as the Wallace effect. The modern concept of reinforcement originates from Theodosius Dobzhansky. He envisioned a species separated allopatrically, where during secondary contact the two populations mate, producing hybrids with lower fitness. Natural selection results from the hybrid's inability to produce viable offspring; thus members of one species who do not mate with members of the other have greater reproductive success. This favors the evolution of greater prezygotic isolation. Reinforcement is one of the few cases in which selection can favor an increase in prezygotic isolation, influencing the process of speciation directly. This aspect has been particularly appealing among evolutionary biologists.

Genetic incompatibility describes the process by which mating yields offspring that are nonviable, prone to disease, or genetically defective in some way. In nature, animals can ill afford to devote costly resources for little or no reward, ergo, mating strategies have evolved to allow females to choose or otherwise determine mates which are more likely to result in viable offspring.

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