Interlocus sexual conflict

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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. [1] 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. [2] 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. [3]

Contents

As the sexes demonstrate a significant investment discrepancy for reproduction, interlocus sexual conflict can arise. To achieve reproductive success, a species member will display reproductive characteristics that enhance their ability to reproduce, regardless of whether the fitness of their mate is negatively affected. [4] Sperm production by males is substantially less biologically costly than egg production by females, and sperm are produced in much greater quantities. Consequently, males invest more energy into mating frequency, while females are choosier with mates and invest their energy into offspring quality. [5]

The evolutionary pathways resulting from interlocus sexual conflict form part of interlocus contest evolution, a theory describing the coevolution of different loci in a species through the process of intergenomic conflict. [6] This has led to the proposal that sexual antagonistic coevolution is fueled by interlocus sexual conflict. [6]

Well-evidenced examples come exclusively from the insect world, with the majority of research being conducted in yellow dung flies, Scathophaga stercoraria , and fruit flies, Drosophila melanogaster. Examples outside of these taxa are theoretical, though currently not well studied. [7]

Interlocus sexual conflict differs from intralocus sexual conflict, a similar theory in which a set of antagonistic alleles resides on the same locus in both sexes.

Theory development

Models

The first model of interlocus sexual conflict, the genetic threshold model, was developed by Parker to explain sexual conflict among yellow dung flies. [2] Further investigation of sexual conflict theory remained relatively untouched until Rice predicted that genes for sexually antagonistic traits exist at the same loci of the sex chromosomes in both sexes, which led to the development of intralocus sexual conflict. Rice's genetic model of X-linkage influencing sexual dimorphism demonstrated that alleles for reproductive traits will persist if they increase the fitness of one sex, regardless of the associated cost for their mate. [8]

An expansion of Parker's genetic threshold model was later used to examine how sex-linked harming alleles, or mutant alleles that cause males to harm females during reproduction, proliferate within a population and initiate interlocus sexual conflict. [9] In a population of fruit flies where a Y-linked harming allele decreases the fitness of a female mate, an indirect cost is imposed on the male's fitness. Consequently, the harming allele is only favored in circumstances where the difference between offspring sired by harming males and normal males is greater for harming males, or harming males are at a fitness advantage.

The chase-away sexual selection model, proposed by Holland and Rice, enabled the prediction that mating discrimination by females will drive the evolution of male display features toward extreme phenotypes. As a result, an arms race develops where female mate choice drives male morphology. [10] A model of antagonistic coevolution by Arnqvist and Rowe highlighted the example of abdominal spines in female water striders, Gerris incognitus , to demonstrate how this arms race leads to evolutionary adaptations in females. Female water striders achieve control over copulatory acts by using their spines as defense against aggressive males. [11]

Interlocus contest evolution

Interlocus sexual conflict forms the basis for interlocus contest evolution (ICE), characterized by the coevolution of genes at different loci in a species through intergenomic conflict. [6] In other words, a disequilibrium forms as alleles for reproductive traits are substituted at different loci in opposing sexes, resulting in rapid evolution of the trait at the locus, which further fuels an arms race between the sexes.

The Red Queen hypothesis postulates that evolution of a trait in one species will drive antagonistic coevolution in an opposing species and can be used to explain coevolution in cases of predatory behaviour, host-parasite relationships, and sexual selection. [12] Of interest to interlocus sexual conflict, the Red Queen hypothesis allows for the evolution of traits that enhance reproductive fitness. [6] ICE extends from this hypothesis, proposing that antagonistic coevolution does not require opposing species, but can be applied to genes at different loci in a single species.

Versus intralocus sexual conflict

The genetic basis of the distinction between interlocus sexual conflict and intralocus sexual conflict is the location of the interacting antagonistic alleles. Conflict in which the antagonistic alleles are located at the same locus is termed intralocus sexual conflict. [9] This occurs when males and females undergo different selective pressures at the same locus, resulting in either sex limiting the fitness of the other sex. [13]

Importantly, many examples of sexual conflict are not categorized into interlocus sexual conflict or intralocus sexual conflict, as the genetic locations of the interacting alleles for these traits are not known or specified. It is critical to note when interpreting information regarding sexual conflict that these terms are sometimes used interchangeably, despite this being incorrect. [14]

Antagonistic coevolution

Sexual antagonistic coevolution is characterized by an arms race between the sexes in which one sex experiences changes in morphology or behaviour to compensate for the negative effects of the reproductive traits of the opposite sex. Both sexes strive to maintain an optimal fitness level, but do so at the expense of their mate's fitness. For interlocus sexual conflict to be a valid cause of antagonistic coevolution, the harm induced by the males across all loci has to outweigh the indirect benefits that the females gain by interacting with males. [15]

Copulation in Scathophaga stercoraria Mating Dung Flies - Scatophaga stercoraria.jpg
Copulation in Scathophaga stercoraria

In Scathophaga stercoraria

Through Parker's genetic threshold model, it was discovered that female yellow dung flies can be injured in battles between male suitors. Males are selected to evolve traits for competitive ability that would increase their reproductive success, but females would evolve a set of antagonistic adaptations to reduce their chances of being injured during these interactions. [2] Male yellow dung flies use pheromones, seminal fluid proteins (SPFs), and aggressive behaviour attributable to their size to manipulate females during courtship. As yellow dung flies are a polyandrous species, females obtain sperm from multiple males which is stored for fertilization. Larger males have a competitive advantage in displacing the sperm of other males, enhancing the likelihood of their sperm fertilizing the eggs. [16] This phenomenon is termed sperm competition. In response, females have evolved larger spermathecae, spermicides, and an enhanced ability to select sperm based on the fitness of male suitors.

Scathophaga stercoraria displaying either polyandry or monogamy differ in female fitness. When females are placed in enforced polyandrous or monogamous mating conditions, females from polyandrous conditions exhibit substantially reduced fitness, displaying decreased egg production, decreased number of offspring, and a shortened life span compared to monogamous females after only one mating experience. [17] Initially, it was suggested that the sexy son hypothesis was enough to compensate for the direct impact of antagonistic coevolution on female fitness. [9] However, the detrimental fitness impact in females singly-mated with a polyandrous male suggests adaptations to resist harm by males requires competition, and is therefore better explained by interlocus sexual conflict. [17]

In Drosophila melanogaster

Copulation in Drosophila melanogaster Drosophila.melanogaster.couple.2.jpg
Copulation in Drosophila melanogaster

Drosophila melanogaster are a promiscuous species in which mate choice is a recurring event, fostering the development of interlocus sexual conflict. [18]

The ejaculate of male fruit flies contains seminal fluid proteins (SFPs) that play a significant role in determining female fitness. [18] SPFs are capable of influencing processes such as oogenesis, [19] sperm storage, [20] and the onset of ovulation. [21] This ultimately leads to a decrease in female fitness, as increasing behaviours such as egg-laying can decrease the success of fertilization, [22] delay remating, [19] and impact the female's life span. [23] In response to the negative effects of SPFs, female fruit flies have evolved resistance tactics to hyperactive males and refractoriness, resulting in interlocus sexual conflict. This has been supported in studies revealing the rapid evolution of SPF genes. [24]

In a study examining fruit flies under polygamous and monogamous conditions, it was discovered that antagonistic coevolution decreases in monogamy, as the organisms mate with only one opposite-sex member and there is no competition among males to mate with the female. [18]

In another laboratory study, a mutation that reduces the attractiveness of females was introduced into the genome of the experimental females. By reducing the attractiveness of the females expressing the trait, the mutation provided females with resistance to the direct costs of re-mating and male courtship. These results show that the resistance allele significantly accumulated in the experimental group, suggesting that the direct costs of male-courtship are greater than the indirect benefits of male-courtship. [15]

Reciprocal crosses of Drosophila melanogaster have been used to investigate the evolution of sexual traits under allopatric conditions. In divergent populations, organisms will respond adaptively to local mates but not foreign mates. As a result, the female remating rate decreased significantly upon introduction of foreign males. Females are most resistant to males they coevolved with in local conditions, but show limited defense against foreign males. [25]

See also

Related Research Articles

<i>Drosophila</i> Genus of flies

Drosophila is a genus of flies, belonging to the family Drosophilidae, whose members are often called "small fruit flies" or pomace flies, vinegar flies, or wine flies, a reference to the characteristic of many species to linger around overripe or rotting fruit. They should not be confused with the Tephritidae, a related family, which are also called fruit flies ; tephritids feed primarily on unripe or ripe fruit, with many species being regarded as destructive agricultural pests, especially the Mediterranean fruit fly.

<i>Drosophila melanogaster</i> Species of fruit fly

Drosophila melanogaster is a species of fly in the family Drosophilidae. The species is often referred to as the fruit fly or lesser fruit fly, or less commonly the "vinegar fly", "pomace fly", or "banana fly". In the wild, D. melanogaster are attracted to rotting fruit and fermenting beverages, and are often found in orchards, kitchens and pubs.

<span class="mw-page-title-main">Sperm competition</span> Reproductive process

Sperm competition is the competitive process between spermatozoa of two or more different males to fertilize the same egg during sexual reproduction. Competition can occur when females have multiple potential mating partners. Greater choice and variety of mates increases a female's chance to produce more viable offspring. However, multiple mates for a female means each individual male has decreased chances of producing offspring. Sperm competition is an evolutionary pressure on males, and has led to the development of adaptations to increase male's chance of reproductive success. Sperm competition results in a sexual conflict between males and females. Males have evolved several defensive tactics including: mate-guarding, mating plugs, and releasing toxic seminal substances to reduce female re-mating tendencies to cope with sperm competition. Offensive tactics of sperm competition involve direct interference by one male on the reproductive success of another male, for instance by mate guarding or by physically removing another male's sperm prior to mating with a female. For an example, see Gryllus bimaculatus.

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.

The mechanisms of reproductive isolation are a collection of evolutionary mechanisms, behaviors and physiological processes critical for speciation. They prevent members of different species from producing offspring, or ensure that any offspring are sterile. These barriers maintain the integrity of a species by reducing gene flow between related species.

<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">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.

<i>Drosophila pseudoobscura</i> Species of fly

Drosophila pseudoobscura is a species of fruit fly, used extensively in lab studies of speciation. It is native to western North America.

<i>Scathophaga stercoraria</i> Species of fly

Scathophaga stercoraria, commonly known as the yellow dung fly or the golden dung fly, is one of the most familiar and abundant flies in many parts of the Northern Hemisphere. As its common name suggests, it is often found on the feces of large mammals, such as horses, cattle, sheep, deer, and wild boar, where it goes to breed. The distribution of S. stercoraria is likely influenced by human agriculture, especially in northern Europe and North America. The Scathophaga are integral in the animal kingdom due to their role in the natural decomposition of dung in fields. They are also very important in the scientific world due to their short life cycles and susceptibility to experimental manipulations; thus, they have contributed significant knowledge about animal behavior.

Bateman's principle, in evolutionary biology, is that in most species, variability in reproductive success is greater in males than in females. It was first proposed by Angus John Bateman (1919–1996), an English geneticist. Bateman suggested that, since males are capable of producing millions of sperm cells with little effort, while females invest much higher levels of energy in order to nurture a relatively small number of eggs, the female plays a significantly larger role in their offspring's reproductive success. Bateman's paradigm thus views females as the limiting factor of parental investment, over which males will compete in order to copulate successfully.

<span class="mw-page-title-main">Female sperm storage</span>

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.

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, while the alternative allele improves the fitness of females. 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, and (ii) the shared genome of both sexes, which generates positive between-sex genetic correlations for most traits. 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.

A behaviour mutation is a genetic mutation that alters genes that control the way in which an organism behaves, causing their behavioural patterns to change.

Cryptic female choice is a form of mate choice which occurs both in pre and post copulatory circumstances when females in certain species use physical or chemical mechanisms to control a male's success of fertilizing their ova or ovum; i.e. by selecting whether sperm are successful in fertilizing their eggs or not. It occurs in internally-fertilizing species and involves differential use of sperm by females when sperm are available in the reproductive tract.

<i>Prochyliza xanthostoma</i> Species of fly

Prochyliza xanthostoma, the waltzing fly, is a species of carrion-feeding cheese skipper, insects in the family Piophilidae and the order Diptera. P. xanthostoma is a member of the genus Prochyliza, which contains eleven species. The adult flies are found through North America and are brown-bodied, with orange and black coloring. Mating occurs on animal carcasses and male perform mating rituals; females engage in ejaculate feeding. The waltzing fly is known for its exaggerated sexual dimorphism and has thus become a prominent model for sexual dimorphism and larval behavior. These organisms are known as cheese skippers because when startled, the larvae can leap several inches into the air. P. xanthostoma is an important model organism for sexual selection, larval behavior, and adult reproductive success and survivability.

<span class="mw-page-title-main">Seminal fluid protein</span> Non-sperm component of semen

Seminal fluid proteins (SFPs) or accessory gland proteins (Acps) are one of the non-sperm components of semen. In many animals with internal fertilization, males transfer a complex cocktail of proteins in their semen to females during copulation. These seminal fluid proteins often have diverse, potent effects on female post-mating phenotypes. SFPs are produced by the male accessory glands.

Mariana Federica Wolfner is the Goldwin Smith Professor of molecular biology and genetics at Cornell University. Her research investigates sexual conflict in the fruit fly Drosophila melanogaster. She was elected a member of the National Academy of Sciences (NAS) in 2019 in recognition of her distinguished and continuing achievements in original research.

Derocephalus angusticollis is a fly in the family Neriidae. They are typically found on the east coast of Australia near rotting vegetation. Aggregating on the rotting bark of trees such as Acacia longifolia and other trees in New South Wales and southern Queensland. D. angusticollis flies found in the wild have accelerated speeds of development and age of mortality when compared to those in captivity. Derocephalus One characteristic of the neriid fly is that it demonstrates sexual dimorphism. Males have a larger build as well as exaggerated physical characteristics such as wider heads and longer limbs. Certain phenotypic characteristics are dependent on the diet of the parents.

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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