Temperature-dependent sex determination

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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. [1] It is observed in reptiles and teleost fish, with some reports of it occurring in species of shrimp. [2] [3] [4] [5] [6] 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. [7] As sex-determining mechanisms, TSD and genetic sex determination (GSD) should be considered in an equivalent manner, [8] 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. [7]

Contents

While TSD has been observed in many reptile and fish species, the genetic differences between sexes and molecular mechanisms of TSD have not been determined. [7] The cortisol-mediated pathway and epigenetic regulatory pathway are thought to be the potential mechanisms involved in TSD. [7] [9]

The eggs are affected by the temperature at which they are incubated during the middle third of embryonic development. [10] This critical period of incubation is known as the thermosensitive period. [11] The specific time of sex-commitment is known due to several authors resolving histological chronology of sex differentiation in the gonads of turtles with TSD. [10]

Thermosensitive period

The thermosensitive, or temperature-sensitive, period is the period during development when sex is irreversibly determined. It is used in reference to species with temperature-dependent sex determination, such as crocodilians and turtles. [12] The TSP typically spans the middle third of incubation with the endpoints defined by embryonic stage when under constant temperatures. The extent of the TSP varies a little among species, [12] and development within the oviducts must be taken into account in species where the embryo is at a relatively late stage of development on egg laying (e.g. many lizards). Temperature pulses during the thermosensitive period are often sufficient to determine sex, but after the TSP, sex is unresponsive to temperature and sex reversal is impossible. [12]

Types

Patterns of temperature-dependent sex determination (TSD) in reptiles. Pattern I is found in turtles, e.g. Red-eared slider turtles (Trachemys scripta), Olive Ridley sea turtles (Lepidochelys olivacea), or Painted turtles (Chrysemys picta). Pattern II has been found in American alligators (Alligator mississippiensis and Leopard geckos (Eublepharis macularius). Patterns of Temperature-Dependent Sex-Determination in reptiles.png
Patterns of temperature-dependent sex determination (TSD) in reptiles. Pattern I is found in turtles, e.g. Red-eared slider turtles ( Trachemys scripta ), Olive Ridley sea turtles ( Lepidochelys olivacea ), or Painted turtles ( Chrysemys picta ). Pattern II has been found in American alligators ( Alligator mississippiensis and Leopard geckos ( Eublepharis macularius ).
Some reptiles use incubation temperatures to determine sex. In some species, this follows the pattern that eggs in extremely high or low temperatures become male and eggs in medium temperatures become female. Different case of temperature dependent sex determination.png
Some reptiles use incubation temperatures to determine sex. In some species, this follows the pattern that eggs in extremely high or low temperatures become male and eggs in medium temperatures become female.

Within the mechanism, two distinct patterns have been discovered and named Pattern I and Pattern II. Pattern I is further divided into IA and IB.

Pattern IA has a single transition zone, where eggs predominantly hatch males if incubated below this temperature zone, and predominantly hatch females if incubated above it. Pattern IA occurs in most turtles, with the transition between male-producing temperatures and female-producing temperatures occurring over a range of temperatures as little as 1–2°C. [15] Pattern IB also has a single transition zone, but females are produced below it and males above it. Pattern IB occurs in multiple fish species [5] and the tuatara.

Pattern II has two transition zones, with males dominating at intermediate temperatures and females dominating at both extremes. [14] Pattern II occurs in some turtles, lizards, and crocodilians. [16] Mixed sex ratios and (more rarely) intersex individuals have been observed at or near the pivotal temperature of sex determination. [15]

It has been proposed that essentially all modes of TSD are actually Pattern II and those that deviate from the expected female-male-female pattern are species whose viable temperature range does not allow for the extreme temperatures needed to pass the second transition zone. [17]

The distinction between chromosomal sex-determination systems and TSD is often blurred because the sex of some species – such as the three-lined skink Bassiana duperreyi and the central bearded dragon Pogona vitticeps – is determined by sex chromosomes, but this is over-ridden by temperatures that are tolerable but extreme. Also, experiments conducted at the pivotal temperature, where temperature is equivocal in its influence, have demonstrated an underlying genetic predisposition to be one sex or the other.

Examples

Temperature-dependent sex determination was first described in Agama agama in 1966 by Madeleine Charnier. [18]

A 2015 study found that hot temperatures altered the expression of the sex chromosomes in Australia's bearded dragon lizards. The lizards were female in appearance and were capable of bearing offspring, despite having the ZZ chromosomes usually associated with male lizards. [19]

In 2018, a team of Chinese and American researchers showed that the histone H3 lysine 27 (H3K27) demethylase KDM6B (JMJD3), an epigenetic modifier, activates male development in red-eared slider turtles by binding to the promoter of the dominant male gene [DMRT1]. Knocking down the expression of this modifier at 26 °C triggers male-to-female sex reversal in most of the surviving embryos. [20]

Research from 2020 identified the timing of gonadal commitment in the American alligator to understand the effects of estrogen-signaling in TSD. It was determined that a main factor in gonadal fate is the level of testicular genes and estrogen signaling. The study found that critical commitment in testicular development is during stage 24-26, which is later than a known TSP for promoting males in TSD. Additionally, earlier estrogen signaling induced development of parts of the ovary. [21]

Hormones in TSD systems

Synergism between temperature and hormones has also been identified in these systems. Administering estradiol at male-producing temperatures generates females that are physiologically identical to temperature-produced females. [22] The reverse experiment, males produced at female temperatures, only occurs when a nonaromatizable testosterone or an aromatase inhibitor is administered, indicating that the enzyme responsible for conversion of testosterone to estradiol, aromatase, plays a role in female development. [23] Nonetheless, the mechanisms for TSD are still relatively unknown, but in some ways, TSD resembles genetic sex determination (GSD), particularly in regards to the effects of aromatase in each process. [24] In some fish species, aromatase is in both the ovaries of female organisms who underwent TSD and those who underwent GSD, with no less than 85% of the coding sequences of each aromatase being identical, [25] showing that aromatase is not unique to TSD and suggesting that there must be another factor in addition to it that is also affecting TSD.

Hormones and temperature show signs of acting in the same pathway, in that less hormone is required to produce a sexual shift as the incubation conditions near the pivotal temperature. It has been proposed [26] that temperature acts on genes coding for such steroidogenic enzymes, and testing of homologous GSD pathways has provided a genic starting point. [27] Yet, the genetic sexual determination pathway in TSD turtles is poorly understood and the controlling mechanism for male or female commitment has not been identified. [28]

While sex hormones have been observed to be influenced by temperature, thus potentially altering sexual phenotypes, specific genes in the gonadal differentiation pathway display temperature influenced expression. [29] In some species, such important sex-determining genes as DMRT1 [30] and those involved in the Wnt signalling pathway [29] could potentially be implicated as genes which provide a mechanism (opening the door for selective forces) for the evolutionary development of TSD. Aromatase has also been shown to play a role in certain tumor development. [31]

Adaptive significance

The adaptive significance of TSD is currently not well understood. One possible explanation that TSD is common in amniotes is phylogenetic inertia – TSD is the ancestral condition in this clade and is simply maintained in extant lineages because it is currently adaptively neutral or nearly so. [32] Indeed, recent phylogenetic comparative analyses imply a single origin for TSD in most amniotes around 300 million years, with the re-evolution of TSD in squamates [33] and turtles [34] after they had independently developed GSD. Consequently, the adaptive significance of TSD in all but the most recent origins of TSD may have been obscured by the passage of deep time, with TSD potentially being maintained in many amniote clades simply because it works 'well enough' (i.e. has no overall fitness costs along the lines of the phylogenetic inertia explanation).

Other work centers on a 1977 theoretical model (the Charnov–Bull model), [35] [36] predicted that selection should favour TSD over chromosome-based systems when "the developmental environment differentially influences male versus female fitness"; [2] this theoretical model was empirically validated thirty years later [2] but the generality of this hypothesis in reptiles is questioned. This hypothesis is supported by the persistence of TSD in certain populations of spotted skink (Niveoscincus ocellatus), a small lizard in Tasmania, where it is advantageous to have females early in the season. The warmth early in the season ensures female-biased broods that then have more time to grow and reach maturity and possibly reproduce before they experience their first winter, thereby increasing fitness of the individual. [1]

In support of the Charnov and Bull hypothesis, Warner and Shine (2008) showed confidently that incubation temperature influences males’ reproductive success differently than females in Jacky Dragon lizards ( Amphibolurus muricatus ) by treating the eggs with chemicals that interfere with steroid hormone biosynthesis. These chemicals block the conversion of testosterone to estradiol during development so each sex offspring can be produced at all temperatures. They found that hatching temperatures that naturally produce each sex maximized fitness of each sex, which provides the substantial empirical evidence in support of the Charnov & Bull model for reptiles. [2]

Spencer and Janzen (2014) found further support for the Charnov-Bull model by incubating painted turtles (Chrysemys picta) at different temperatures and measuring various characteristics indicative of fitness. The turtles were incubated at temperatures that produce solely males, both sexes, and solely females. Spencer and Janzen (2014) found that hatchlings from mixed-sex nests were less energy efficient and grew less than their same-sex counterparts incubated in single-sex producing temperatures. Hatchlings from single-sex producing temperatures also had higher first-year survivorship than the hatchlings from the temperature that produces both sexes. TSD may be advantageous and selected for in turtles, as embryo energy efficiency and hatchling size are optimized for each sex at single-sex incubation temperatures and are indicative of first-year survivorship. [37] This suggests that natural selection would favor TSD, as TSD may enhance the fitness of offspring.

An alternative hypothesis of adaptive significance was proposed by Bulmer and Bull in 1982 [38] and supported by the work of Pen et al. (2010). They conjectured that disruptive selection produced by variation in the environment could result in an evolutionary transition from ESD to GSD. [38] Pen et al. (2010) addresses evolutionary divergence in SDMs via natural selection on sex ratios. Studying the spotted skink, they observed that the highland population was not affected by temperature, yet, there was a negative correlation between annual temperature and cohort sex ratios in the lowlands. The highlands are colder with a higher magnitude of annual temperature fluctuation and a shorter activity season, delaying maturity, thus GSD is favored so sex ratios are not skewed. However, in the lowlands, temperatures are more constant and a longer activity season allows for favorable conditions for TSD. They concluded that this differentiation in climate causes divergent selection on regulatory elements in the sex-determining network allowing for the emergence of sex chromosomes in the highlands. [39]

Climate change effects

Climate change presents a unique threat in species influenced by temperature-dependent sex determination by skewing sex ratios and population decline. [40] The warming of the habitats of species exhibiting TSD are beginning to affect their behavior and may soon start affecting their physiology. [41] Many species (with Pattern IA and II) have begun to nest earlier and earlier in the year to preserve the sex ratio. [42] The three traits of pivotal temperature (the temperature at which the sex ratio is 50%), maternal nest-site choice, and nesting phenology have been identified as the key traits of TSD that can change, and of these, only the pivotal temperature is significantly heritable, this would have to increase by 27 standard deviations to compensate for a 4 °C temperature increase. [43] It is likely that climate change will outpace the ability of many TSD animals to adapt, [44] [45] and many will likely go extinct. However, there is evidence that during climatic extremes, changes in the sex determining mechanism itself (to GSD) are selected for, particularly in the highly-mutable turtles. [46] It has also been proposed that sea turtles may be able to use TSD to their advantage in a warming climate. When the offspring viability is decreased due to increased temperatures, they are able to use the coadaptation between sex ratio and survivability to increase the production of female offspring. This allows sea turtles to maintain populations and could increase their resiliency to climate change. [47]

See also

Related Research Articles

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

Sex is the 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 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 used to classify many mammals, including humans, some insects (Drosophila), some snakes, some fish (guppies), and some plants. In this system, the sex of an individual is determined by a pair of sex chromosomes. In most cases, females have two of the same kind of sex chromosome (XX), and are called the homogametic sex. Males have two different kinds of sex chromosomes (XY), and are called the heterogametic sex.

<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">Viviparity</span> Development of the embryo inside the mother

In animals, viviparity is development of the embryo inside the body of the mother, with the maternal circulation providing for the metabolic needs of the embryo's development, until the mother gives birth to a fully or partially developed juvenile that is at least metabolically independent. This is opposed to oviparity, where the embryos develop independently outside the mother in eggs until they are developed enough to break out as hatchlings; and ovoviviparity, where the embryos are developed in eggs that remain carried inside the mother's body until the hatchlings emerge from the mother as juveniles, similar to a live birth.

<span class="mw-page-title-main">Sex ratio</span> Ratio of males to females in a population

A sex ratio is the ratio of males to females in a population. As explained by Fisher's principle, for evolutionary reasons this is typically about 1:1 in species which reproduce sexually. However, many species deviate from an even sex ratio, either periodically or permanently. Examples include parthenogenic species, periodically mating organisms such as aphids, some eusocial wasps, bees, ants, and termites.

<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">Spotted turtle</span> Species of turtle

The spotted turtle, the only species of the genus Clemmys, is a small, semi-aquatic turtle that reaches a carapace length of 8–12 cm (3.1–4.7 in) upon adulthood. Their broad, smooth, low dark-colored upper shell, or carapace, ranges in its exact colour from black to a bluish black with a number of tiny yellow round spots. The spotting patterning extends from the head, to the neck and out onto the limbs. Sexually mature males have a concave plastron and a long, thick tail. By contrast, sexually mature females possess a flat plastron and have a tail that is noticeably shorter and thinner than that of mature males. Mature males also have a dark iris and face; females typically have a yellow or orange iris and a similarly coloured face that is distinctly lighter than the males'. Juveniles appear female-like in this regard, and at maturity males begin to develop darker features.

<span class="mw-page-title-main">Aromatase</span> Enzyme involved in estrogen production

Aromatase, also called estrogen synthetase or estrogen synthase, is an enzyme responsible for a key step in the biosynthesis of estrogens. It is CYP19A1, a member of the cytochrome P450 superfamily, which are monooxygenases that catalyze many reactions involved in steroidogenesis. In particular, aromatase is responsible for the aromatization of androgens into estrogens. The enzyme aromatase can be found in many tissues including gonads, brain, adipose tissue, placenta, blood vessels, skin, and bone, as well as in tissue of endometriosis, uterine fibroids, breast cancer, and endometrial cancer. It is an important factor in sexual development.

<span class="mw-page-title-main">Polyphenism</span> Type of polymorphism where different forms of an animal arise from a single genotype

A polyphenic trait is a trait for which multiple, discrete phenotypes can arise from a single genotype as a result of differing environmental conditions. It is therefore a special case of phenotypic plasticity.

<span class="mw-page-title-main">XO sex-determination system</span> Biological system that determines the sex of offspring

The XO sex-determination system is a system that some species of insects, arachnids, and mammals use to determine the sex of offspring. In this system, there is only one sex chromosome, referred to as X. Males only have one X chromosome (XO), while females have two (XX). The letter O signifies the lack of a Y chromosome. Maternal gametes always contain an X chromosome, so the sex of the animals' offspring depends on whether a sex chromosome is present in the male gamete. Its sperm normally contains either one X chromosome or no sex chromosomes at all.

<span class="mw-page-title-main">ZW sex-determination system</span> Chromosomal system

The ZW sex-determination system is a chromosomal system that determines the sex of offspring in birds, some fish and crustaceans such as the giant river prawn, some insects, the schistosome family of flatworms, and some reptiles, e.g. majority of snakes, lacertid lizards and monitors, including Komodo dragons. It is also present in some plants, where it has probably evolved independently on several occasions. The letters Z and W are used to distinguish this system from the XY sex-determination system. In the ZW system, females have a pair of dissimilar ZW chromosomes, and males have two similar ZZ chromosomes.

Sex allocation is the allocation of resources to male versus female reproduction in sexual species. Sex allocation theory tries to explain why many species produce equal number of males and females.

<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">Environmental sex determination</span> Method of sex-determination

Environmental sex determination is the establishment of sex by a non-genetic cue, such as nutrient availability, experienced within a discrete period after fertilization. Environmental factors which often influence sex determination during development or sexual maturation include light intensity and photoperiod, temperature, nutrient availability, and pheromones emitted by surrounding plants or animals. This is in contrast to genotypic sex determination, which establishes sex at fertilization by genetic factors such as sex chromosomes. Under true environmental sex determination, once sex is determined, it is fixed and cannot be switched again. Environmental sex determination is different from some forms of sequential hermaphroditism in which the sex is determined flexibly after fertilization throughout the organism’s life.

Fisher's principle is an evolutionary model that explains why the sex ratio of most species that produce offspring through sexual reproduction is approximately 1:1 between males and females. A. W. F. Edwards has remarked that it is "probably the most celebrated argument in evolutionary biology".

<span class="mw-page-title-main">Eastern three-lined skink</span> Species of lizard

The eastern three-lined skink, also known commonly as the bold-striped cool-skink, is a species of skink, a lizard in the family Scincidae. The species is endemic to Australia. A. duperreyi has been extensively studied in the context of understanding the evolution of learning, viviparity in lizards, and temperature- and genetic-sex determination. A. duperreyi is classified as a species of "Least Concern" by the IUCN.

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. 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.

<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.

Ecological evolutionary developmental biology (eco-evo-devo) is a field of biology combining ecology, developmental biology and evolutionary biology to examine their relationship. The concept is closely tied to multiple biological mechanisms. The effects of eco-evo-devo can be a result of developmental plasticity, the result of symbiotic relationships or epigenetically inherited. The overlap between developmental plasticity and symbioses rooted in evolutionary concepts defines ecological evolutionary developmental biology. Host- microorganisms interactions during development characterize symbiotic relationships, whilst the spectrum of phenotypes rooted in canalization with response to environmental cues highlights plasticity. Developmental plasticity that is controlled by environmental temperature may put certain species at risk as a result of climate change.

<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.

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