Sex reversal

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Sex reversal is a biological process whereby the pathway directed towards the already determined-sex fate is flipped towards the opposite sex, creating a discordance between the primary sex fate and the sex phenotype expressed. [1] [2] The process of sex reversal occurs during embryonic development or before gonad differentiation. In GSD species, sex reversal means that the sexual phenotype is discordant with the genetic/chromosomal sex. In TSD species, sex reversal means that the temperature/conditions that usually trigger the differentiation towards one sexual phenotype are producing the opposite sexual phenotype. [1]

Contents

Sex reversal can occur naturally, by mutations, or can be induced artificially. Sex reversal can be genetically or hormonally induced in laboratory. It can also occur artificially by exposure to endocrine disruptors such as pollutants, including herbicides, which can act as estrogen promoters or inhibitors, for instance by altering aromatase expression. [3] [4] [5] [6]

In fish

Gonochoristic Fish

In gonochoristic fish, the sex can be determined genetically, environmentally or by a combination of both. In fish, primary sexual fate can be susceptible to alteration by hormones exposure and multiple environmental factors, such as population density, water pH, or temperature. Those conditions can affect the gonad development and differentiation, which can lead to sex reversal. [7] [8] In medaka fish, where sex reversal has been documented show a shared gene related to normal male development, the dmy gene. In wild populations, genetically female fate can be phenotypically reversed to males if they carry the dmy gene or a mutated dmy gene and genetic males can be reversed to females if they lack the dmy gene. [9]

Hermaphroditic Fish

Within seven teleost fish families, two modes of hermaphrodism can be observed—simultaneous hermaphrodism and sequential hermaphrodism. These cases often arise due to social factors, such as a decline in population or changes in dominance. [10] It is assumed that hermaphroditic sex changing fish have increased plasticity within their gonads compared to the typical gonochoristic fish, allowing for gonadal differentiation. Although it is not a reversal of sex, simultaneous hermaphrodism is beneficial for low-density populations as it allows for an increase in conspecific mating opportunities overall. Simultaneous hermaphrodism occurs when fish are able to produce both mature sperm and eggs within their gonads—while self-fertilization is rare, it has been seen to occur in few low-density populations such as the Kryptolebias marmoratus. [11] Sequential hermaphrodism occurs when gonadal sex redifferentiation takes place, often due to a decrease in the population of a specific sex. This form of hermaphrodism has taken upon three modes—protogyny, protandry, and bi-directional sex change. [12]

Protogynous sex change is the female to male gonadal redifferentiation, and it is often found within species that practice haremic polygyny, or one male reproducing with many females. When socially dominant males disappear, larger initial phase female fish will undergo sex change to become terminal phase males. In this, the ovaries are constructed to mature, functional testis. Protogyny sex change has been found within fish species such as the three-spot wrasse (Halichoreres trimaculatas) and the saddleback wrasse (Thalassoma duperrey) with a decline in plasma estrogen contributing to testis development. [12]

In contrast, protandrous sex change is the male to female gonadal redifferentiation, but it is also triggered by the disappearance of the conspecific dominant, in this case the female. While protogynous fish are found within species dominated by larger males, protandrous fish are within large female dominant species, such as the clown fish (Amphiprion). [12] [13] Within the clown fish populations, males develop bi-sexual gonads—mature testis and immature ovaries—while the dominant females only possess ovaries. In cases of protandrous sex change, the immature ovarian tissues develop and the testicular tissues deteriorate due to changes in the activity of gonadal steroid hormones such as estrogen. [12]

Bi-directional, or serial, sex change occurs when hermaphrodites are capable of changing their sex in either direction, possibly multiple times. Some fish species are capable of this sex change due to the presence of both ovaries and testis, with only one gonad actively producing gametic cells at a time. The activation of a gonad is possible through changes in expression of the gonadotropin receptors. This primarily occurs in cases of male-male and female-female mating pairs, with the smaller male changing to female or the larger female changing to male due to the disappearance of the respective sex. [10] This can be found in the Okinawa rubble gobiid fish (Trimma okinawae) whose mating system consists of a polygynous harem. When the dominant male is removed, the largest female changes its sex to male; if the dominant male is reintroduced, the sex can be reversed back to female. [12]

Induced reversal in aquaculture industry

In aquaculture, sex control is important due to the role of sex in growth and reproduction. In fish, growth rates can be different between sexes. These differences can affect their economic value. Producing a monosex fish population can improve product quality and therefore generates higher financial profit. [14]

Hormone-induced sex reversal is the most frequent method used in aquaculture. It consists of exposing sexually undifferentiated fish to sex steroids. [15] [16] There are other methods to induced sex reversal in fish such as chromosomal/genetic manipulation, hybridization, or treatments influencing sex determination or gonad differentiation (e.g. temperature, population density, pH, social factors). [14]

In amphibians

Sex is genetically determined in amphibians. [17] [18] Temperature-induced sex reversal has been documented in some species of anuran and caudate amphibians. Temperature only can have an effect on sex differentiation during a window period called thermosensitive period (TSP) which varies among species. [19] [20] [21] Tadpoles or larvae exposed to specific higher or lower temperatures, depending on the temperature thresholds of the species, can differentiate gonads that do not align with their primary sexual fate. [22]

Amphibian sex reversal can be also induced by exposure to sex steroid and pollutants. Endocrine disruptors can affect gonad differentiation, and therefore induce sex reversal. Exposure to ethylnyl estradiol (EE2) and bisphenol A (BPA) induces feminizing effects. [23] Masculinizing effects can be induced by exposure to the drug trenbolone, used in cattle. [24]

Research [25] in wild populations of the North American green frog has demonstrated that sex reversal is common. This work shows that genetic females sex reverse into phenotypic males and that genetic males sex reverse into phenotypic females, providing evidence that sex reversal can be bidirectional in amphibians. While endocrine disrupting chemical contamination is known from laboratory experiments to cause sex reversal in amphibians, [26] sex reversal in green frogs occurs irrespective of contamination, suggesting sex reversal is a natural process in amphibians [27]

In reptiles

Sex in reptiles can be determined genetically (GSD), environmentally (ESD) or by an interaction of both. [28] Sex reversal has been documented in detail in wild populations of the central bearded dragon Pogona vitticeps, and in the eastern three-lined skink Bassiana duperreyi. In these species, their genetically determined sex is overridden by temperature influence. [29] [28] [30]

Further, there are certain primitive reptiles (some chelonians, some crocodilians, and one lizard species) that undergo Temperature-dependent Sex Determination (TSD) during their egg incubation (a form of ESD). [31] [32] TSD functions within a transitional range of temperature (TRT) that influences the sex of the egg and a pivotal temperature that would give rise to a 50:50 chance of females:males. [32] For these reptiles that exhibit TSD, the egg is sensitive to temperature in the middle-third of incubation. [33] The sex of the eggs could be reversed or "corrected" (shifting from one sex, to another, and back to the original) during later stages of the middle-third of incubation if the temperature is shifted. [32]

Sex reversal in reptiles can be induced by hormonal manipulation, treatments influencing sex determination (e.g. temperature) or by inhibition of the aromatase gene (CYP19A1) which causes sex reversal from female to male phenotype. [30] Further, estradiol-17β has been shown to reverse the sex of turtle species when injected into incubating eggs. These eggs were originally placed in are male producing temperatures, but with the estradiol-17β treatment, they would generate females. [34] However, hormone-based sex reversal would be dependent on the gonadal development stages of the embryo (the middle-third of incubation). [35]

In birds

In birds, sex reversal has been documented in natural and experimental conditions. Sex steroid manipulation (such as hormones including androgens, estrogens, and progestogens [36] ) can induce sex reversal in birds by interacting with vertebrae and hormone receptors. Aromatase inhibitors injected into chicken eggs before the gonadal differentiation stage induce testis development in ZW embryos. [37]

Sex reversal in chickens form almost identical phenotypes, which characteristics of an expression of the individual genotype with the environment and the genotype being the presentation or its makeup. The sex reversal of bird's ties into mammals as well. However, the sex chromosomes are different: males have ZZ while females have ZW sex chromosomes. The sex orientation in birds is a mix of direct genetic and hormonal mechanisms. Birds show the most amazing sexually dimorphism that are seen in vertebrates. These birds can come from the same species having two different forms. The male bird is bright colored while the female bird is drab or "dull" in color with no radiant or vibrant color to it at all.

In mammals

Sex reversal in mammals has been documented in domestic species such as cattle, water buffalo, horses, dogs, cats, pigs, goats, etc. Sex reversal in these species usually relates to genetic changes and the resulting phenotype is often associated with gonadal malformation. [38] Natural sex reversal without disruptive effects on fertility has been documented in several rodents, including Myopus schisticolor, Dicrostonyx torquatus, Akodon, Mus minutoides, Microtus cabrerae. In these species some individuals genetically determined as males develop typical ovarian structure. [39] In these rodents species, sex reversal mainly occurs after mutational events. [38]

In mammals, sex reversal occurs when the gonadal or sexual phenotype does not align with the genetic sex determined by the XX/XY or ZZ/ZW chromosomal system. The development of an ovary and female phenotype in an individual with XY chromosomes represents the instance of sex reversal in mammals. Research has identified various genes involved in mammalian sex determination and differentiation. SRY (Sex-determining Region Y) in humans and mice is one of the sex-determination genes that plays a significant function in initiating male development. Mutations or anomalies can affect these sex-determining genes resulting in sex reversal phenotypes. [40]

Additionally, hormonal factors play a significant role in sex reversal among mammals. Estrogen and ovarian hormones facilitate female development whereas testosterone and anti-Müllerian hormone (AMH) produced by the testes promote male development. [41] However, disruptions in hormone signaling pathways can lead to sex reversal. For instance, exposure to estrogen during critical periods of development can interfere with normal hormone levels and can cause sex reversal phenotypes. [42]

Sex reversal in mammals can be impacted by ecological factors such as habitat destruction, and resource availability. Changes in environmental conditions may influence the frequency of sex reversal within mammalian populations, ultimately affecting population dynamics and ecosystem functioning. Understanding sex reversal in mammals is crucial for wildlife conservation efforts, particularly in species facing threats such as habitat loss, and pollution. Sex reversal can potentially influence the long-term viability of populations by altering population demographics, reproductive success, and genetic diversity. [43]

Furthermore, sex reversal can lead to behavioral adaptations within mammalian populations as individuals navigate their altered reproductive roles and social dynamics. Research findings have demonstrated changes in mating behaviors, dominance hierarchies, and social interactions among individuals with sex reversal phenotypes. The evolutionary significance of sex reversal and its impact on population dynamics and social structure can be studied by understanding the mechanism of behavioral adaptations. [44]

See also

Related Research Articles

<span class="mw-page-title-main">Sex</span> Trait that determines an organisms sexually reproductive function

Sex is the biological trait that determines whether a sexually reproducing organism produces male or female gametes. During sexual reproduction, a male and a female gamete fuse to form a zygote, which develops into an offspring that inherits traits from each parent. By convention, organisms that produce smaller, more mobile gametes are called male, while organisms that produce larger, non-mobile gametes are called female. An organism that produces both types of gamete is hermaphrodite.

<span class="mw-page-title-main">XY sex-determination system</span> Method of determining sex

The XY sex-determination system is a sex-determination system present in many mammals, including humans, some insects (Drosophila), some snakes, some fish (guppies), and some plants.

<span class="mw-page-title-main">Sex-determination system</span> Biological system that determines the development of an organisms sex

A sex-determination system is a biological system that determines the development of sexual characteristics in an organism. Most organisms that create their offspring using sexual reproduction have two common sexes and a few less common intersex variations.

<span class="mw-page-title-main">Germ cell</span> Gamete-producing cell

A germ cell is any cell that gives rise to the gametes of an organism that reproduces sexually. In many animals, the germ cells originate in the primitive streak and migrate via the gut of an embryo to the developing gonads. There, they undergo meiosis, followed by cellular differentiation into mature gametes, either eggs or sperm. Unlike animals, plants do not have germ cells designated in early development. Instead, germ cells can arise from somatic cells in the adult, such as the floral meristem of flowering plants.

<span class="mw-page-title-main">XY gonadal dysgenesis</span> Medical condition

XY complete gonadal dysgenesis, also known as Swyer syndrome, is a type of defect hypogonadism in a person whose karyotype is 46,XY. Though they typically have normal vulvas, the person has underdeveloped gonads, fibrous tissue termed "streak gonads", and if left untreated, will not experience puberty. The cause is a lack or inactivation of an SRY gene which is responsible for sexual differentiation. Pregnancy is sometimes possible in Swyer syndrome with assisted reproductive technology. The phenotype is usually similar to Turner syndrome (45,X0) due to a lack of X inactivation. The typical medical treatment is hormone replacement therapy. The syndrome was named after Gerald Swyer, an endocrinologist based in London.

<span class="mw-page-title-main">Sexual differentiation</span> Embryonic development of sex differences

Sexual differentiation is the process of development of the sex differences between males and females from an undifferentiated zygote. Sex determination is often distinct from sex differentiation; sex determination is the designation for the development stage towards either male or female, while sex differentiation is the pathway towards the development of the phenotype.

<span class="mw-page-title-main">Virilization</span> Biological development of male sex characteristics

Virilization or masculinization is the biological development of adult male characteristics in young males or females. Most of the changes of virilization are produced by androgens.

<span class="mw-page-title-main">Sex-determining region Y protein</span> Protein that initiates male sex determination in therian mammals

Sex-determining region Y protein (SRY), or testis-determining factor (TDF), is a DNA-binding protein encoded by the SRY gene that is responsible for the initiation of male sex determination in therian mammals. SRY is an intronless sex-determining gene on the Y chromosome. Mutations in this gene lead to a range of disorders of sex development with varying effects on an individual's phenotype and genotype.

<span class="mw-page-title-main">Male reproductive system</span> Reproductive system of the human male

The male reproductive system consists of a number of sex organs that play a role in the process of human reproduction. These organs are located on the outside of the body, and within the pelvis.

<span class="mw-page-title-main">XX male syndrome</span> Congenital condition where an individual with a 46,XX karyotype is male

XX male syndrome, also known as de la Chapelle syndrome, is a rare intersex condition in which an individual with a 46,XX karyotype develops a male phenotype. Synonyms for XX male syndrome include 46,XX testicular difference of sex development

<span class="mw-page-title-main">Iberian ribbed newt</span> Species of amphibian

The Iberian ribbed newt, gallipato or Spanish ribbed newt is a newt endemic to the central and southern Iberian Peninsula and Morocco. It is the largest European newt species and it is also known for its sharp ribs which can puncture through its sides, and as such is also called the sharp-ribbed newt.

<span class="mw-page-title-main">Sex cords</span> Structures that develop from the genital ridges that further differentiate based on an embryos sex

Sex cords are embryonic structures which eventually will give rise (differentiate) to the adult gonads. They are formed from the genital ridges - which will develop into the gonads - in the first 2 months of gestation which depending on the sex of the embryo will give rise to male or female sex cords. These epithelial cells penetrate and invade the underlying mesenchyme to form the primitive sex cords. This occurs shortly before and during the arrival of the primordial germ cells (PGCs) to the paired genital ridges. If there is a Y chromosome present, testicular cords will develop via the Sry gene : repressing the female sex cord genes and activating the male. If there is no Y chromosome present the opposite will occur, developing ovarian cords. Prior to giving rise to sex cords, both XX and XY embryos have Müllerian ducts and Wolffian ducts. One of these structures will be repressed to induce the other to further differentiate into the external genitalia.

<span class="mw-page-title-main">Genital ridge</span> Developmental precursor to the gonads in an embryo

In embryology, the genital ridge is the developmental precursor to the gonads. The genital ridge initially consists mainly of mesenchyme and cells of underlying mesonephric origin. Once oogonia enter this area they attempt to associate with these somatic cells. Development proceeds and the oogonia become fully surrounded by a layer of cells.

Gonadal dysgenesis is classified as any congenital developmental disorder of the reproductive system characterized by a progressive loss of primordial germ cells on the developing gonads of an embryo. One type of gonadal dysgenesis is the development of functionless, fibrous tissue, termed streak gonads, instead of reproductive tissue. Streak gonads are a form of aplasia, resulting in hormonal failure that manifests as sexual infantism and infertility, with no initiation of puberty and secondary sex characteristics.

<span class="mw-page-title-main">Sex chromosome</span> Chromosome that differs from an ordinary autosome in form, size, and behavior

Sex chromosomes are chromosomes that carry the genes that determine the sex of an individual. The human sex chromosomes are a typical pair of mammal allosomes. They differ from autosomes in form, size, and behavior. Whereas autosomes occur in homologous pairs whose members have the same form in a diploid cell, members of an allosome pair may differ from one another.

<span class="mw-page-title-main">Sexual differentiation in humans</span> Process of development of sex differences in humans

Sexual differentiation in humans is the process of development of sex differences in humans. It is defined as the development of phenotypic structures consequent to the action of hormones produced following gonadal determination. Sexual differentiation includes development of different genitalia and the internal genital tracts and body hair plays a role in sex identification.

<span class="mw-page-title-main">Temperature-dependent sex determination</span> Environmental sex determination by temperature during development

Temperature-dependent sex determination (TSD) is a type of environmental sex determination in which the temperatures experienced during embryonic/larval development determine the sex of the offspring. It is observed in reptiles and teleost fish, with some reports of it occurring in species of shrimp. TSD differs from the chromosomal sex-determination systems common among vertebrates. It is the most studied type of environmental sex determination (ESD). Some other conditions, e.g. density, pH, and environmental background color, are also observed to alter sex ratio, which could be classified either as temperature-dependent sex determination or temperature-dependent sex differentiation, depending on the involved mechanisms. As sex-determining mechanisms, TSD and genetic sex determination (GSD) should be considered in an equivalent manner, which can lead to reconsidering the status of fish species that are claimed to have TSD when submitted to extreme temperatures instead of the temperature experienced during development in the wild, since changes in sex ratio with temperature variation are ecologically and evolutionally relevant.

<span class="mw-page-title-main">David Crews</span> American zoologist

David Pafford Crews is the Ashbel Smith Professor of Zoology and Psychology at the University of Texas at Austin. He has been a pioneer in several areas of reproductive biology, including evolution of sexual behavior and differentiation, neural and phenotypic plasticity, and the role of endocrine disruptors on brain and behavior.

<span class="mw-page-title-main">Evolution of sex-determining mechanisms</span>

The evolution of sex-determining mechanisms, characterized by the evolutionary transition to genetic sex determination or temperature-dependent sex determination from the opposite mechanism, has frequently and readily occurred among multiple taxa across a transitionary continuum.

Cynoglossus semilaevis, commonly known as the Chinese tongue sole, is a popular aquaculture flatfish species. They are native to China's northern coast but have experienced overfishing these past three decades. Tongue sole farming began in 2003, and they have since become a popular, expensive seafood. Farmers in this practice encounter issues related to the tongue sole's pathogen susceptibility and uneven sex ratio.

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