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This page has been archived and is no longer updated. Birds do it, and bees do it. Indeed, researchers estimate that over But why is sexual reproduction so commonplace?

People typically employ several arguments in their efforts to explain the prevalence of sexual reproduction. One such argument is that organisms engage in sex because it is pleasurable.

However, from an evolutionary perspective, this explanation arrived only moments ago. The first eukaryotes to engage in sex were single-celled protists that appeared approximately 2 billion years ago, over 1. These bacteria as well as their modern counterparts engaged in genetic exchange via processes such as conjugationtransformationand transductionall of which fall variation the umbrella of parasexuality.

Surely, pleasure was not in a bacterium's realm of experience. A second, more serious argument is that sex generates variable offspring upon which natural selection can act.

This is one of the oldest explanations for sexual reproduction, tracing back to the work of German biologist August Weismann in the late s.

Although this explanation may very well account for why sexual reproduction is so commonplace, the explanation is far more subtle than many people realize for two reasons. First, sex does not always increase the variability among offspring.

Second, producing more variable offspring is not necessarily favorable. In the next two sections, we describe these flaws in Weismann's explanation for sex, so that we can better understand the processes that help and those that hinder the evolution of sex.

To develop a better understanding of why sexual reproduction is so commonplace, variation is helpful to start with an examination of some of the most common erroneous beliefs regarding the relationship between sex and natural selectionincluding those described in the following sections.

Many people assume that sexual reproduction is critical to evolution because it always results in the production of genetically varied offspring. Sex truth, however, sex does not always increase variation. Imagine, for instance, the simple case of a single gene that contributes to height in a diploid organism ; here, individuals with genotype aa are shortest, those with genotype Aa are of intermediate height, and those with genotype AA are tallest Figure 1.

Now, for the sake of argument, imagine that the shortest individuals can hide safely, the tallest individuals are too big to be eaten by predators, and the intermediate-height individuals are heavily preyed upon. Among those lucky few organisms who sex to reproduce, there will be a great deal of variation in height, with plenty of tall individuals and plenty of short individuals.

What would sex accomplish in this case? Here, mating would bring the population back to Hardy-Weinberg proportions, producing fewer offspring at the extremes of height and more offspring in the middle. That is, sex would reduce variation in height, relative to a population that reproduces asexually. Because the fitness surface exhibits positive curvature, the result of selection is a population with a great degree of variability in height middle panel.

Asexual reproduction in such a population preserves this variation bottom leftbut sexual reproduction with random mating brings the population back into Hardy-Weinberg proportions and reduces variation bottom right.

This example illustrates the fact that sex does not always increase variation. Figure Detail. This example is overly simplified, but it serves to illustrate a general point: Selection can build more variation than one would expect in a population in which genes are well mixed.

In such cases, sex reduces variation by mixing together genes from different parents. This problem arises in the case of a single gene whenever heterozygotes are less fit, on average, than homozygotes. In this case, the heterozygote need not have the lowest fitness ; rather, its fitness must only variation close to that of the least-fit homozygote. In general, mathematical models have confirmed that selection builds more variation than expected from randomly combined genes whenever fitness surfaces are positively curved, with intermediate genotypes having lower-than-expected fitness.

In such cases, sexual reproduction and recombination destroy the genetic associations that selection has built and therefore result in decreased rather than increased variation among offspring. The term " epistasis " is used to describe such gene interactions, and cases in which the intermediate genotypes are less fit than expected based on the fitness of the more extreme genotypes are said to exhibit "positive epistasis.

Interestingly, even when sex does restore genetic variationproducing more variable offspring does not necessarily promote the evolution of sex. Again, this reality refutes one of the arguments often raised in the attempt to explain the relationship between sex and evolution.

To understand how this operates, consider another simple case involving a single gene, but this time, assume that heterozygotes rather than homozygotes are fittest. The gene responsible for sickle-cell anemia provides a great real-life example. Here, people who are heterozygous for the sickle-cell allele genotype Ss are less susceptible to malarial infection yet have a sufficient number of healthy red blood cells; on the other hand, SS sex are more susceptible to malaria, while ss homozygotes are more susceptible to anemia.

Thus, in areas infested with the protozoans that cause malaria, adults who have survived to reproduce are more likely to have the Ss genotype than would be expected based on Hardy-Weinberg proportions. In such populations in which heterozygotes are in excess, sexual reproduction regenerates homozygotes from crosses among heterozygotes. Although this indeed results in greater genetic variation among offspring, the variation consists largely of homozygotes with low fitness.

Yet again, this simple example illustrates a more general point: Parents that have survived to reproduce tend to have genomes that are fairly well adapted to their environments. Mixing two genomes through sex and genetic recombination tends to produce offspring that are less fit, simply because a mixture of genes from both parents has no guarantee of functioning as well as the parents' original gene sets. In fact, mathematical models have confirmed that when selection builds associations among genes, destroying these associations through sex and recombination tends to reduce offspring fitness.

This reduction in fitness caused by sex and recombination variation referred to as the "recombination load" or the " segregation load" when referring variation to segregation at a single diploid gene. The reason that the recombination load is a problem for the evolution of sex is better appreciated by looking at evolution at the level of the gene.

Imagine a gene that promotes sexual reproduction, such as by making it more likely that a plant will reproduce via sexually produced seeds as opposed to some asexual process e. Carriers of this gene will tend to produce less fit offspring because sexual reproduction and recombination break apart the genetic associations that have been built by past selection.

The gene promoting sex will fail to spread if the offspring die at too high a high rate, even if the offspring are more variable. Indeed, theoretical models developed in the s and s demonstrate that genes promoting sex and recombination increase in frequency only when all of the following conditions hold true:. Unfortunately, empirical data have not indicated that fitness surfaces curve in just the right way for these models to work in real-life situations. To make matters worse, sexual reproduction often entails costs beyond the recombination load described earlier.

To reproduce sexually, an individual must take the time variation energy to switch from mitosis to meiosis this step is especially relevant in single-celled organisms ; it must find a willing mate; variation it must risk contracting sexually transmitted diseases.

This last cost is often called the "twofold cost of sex. These are substantial costs—so substantial that many species have evolved mechanisms to ensure that sex occurs only when it is least costly. For instance, organisms including aphids and daphnia reproduce asexually when resources are abundant and switch to sex only at the end of the season, when the potential for asexual reproduction is limited and when potential mates are more available.

Similarly, many single-celled organisms variation sex only when starved, which minimizes the time cost of switching to meiosis because mitotic growth has already ceased. Although various mechanisms might reduce the costs of sex, it is still commonly assumed that sex is more costly than asexual reproduction, raising yet another obstacle for the evolution of sex.

The aforementioned points might lead one to conclude that sex is a sex enterprise. However, sex is incredibly common. Furthermore, even though asexual lineages do arise, they rarely persist for long periods of evolutionary time. Among flowering plants, for example, predominantly asexual lineages have arisen over times, yet none of these lineages is very old.

Furthermore, many species can reproduce both sexually and asexually, without the frequency of asexuality increasing and eliminating sex reproduction altogether. What, then, prevents the spread of asexual reproduction? The first generation of mathematical models examining the evolution of sex made several simplifying assumptions—namely, that selection is constant over time and space, that all individuals engage in sex at the same rate, and that populations are infinitely large.

With such simplifying assumptions, selection remains the main evolutionary force at work, and sex and recombination serve mainly sex break down the genetic associations built up by selection. So, it is perhaps no wonder that this early generation of models concluded that sex would evolve only under very restrictive conditions.

Subsequent models have relaxed these assumptions in a number of sex, attempting to better capture many of the complexities involved in real-world evolution.

The results of these second-generation models are briefly summarized in the following sections. Current models indicate that sex evolves more readily when a species' environment changes rapidly. When the genetic associations built up by past selection are no longer favorable, sex and recombination can improve the fitness of offspring, thereby turning the recombination load into an advantage.

One important source of environmental change is a shift in the community of interacting species, especially host and parasite species.

This is the so-called "Red Queen" hypothesis for the evolution of sex, which refers to the need for a variation to evolve as fast as it can just to keep apace of coevolving species. The name of this hypothesis comes from Lewis Carroll's Variation the Looking Glassin which Alice must run as fast as she can "just to stay in place.

Sex can also be favored when selection varies over space, as long as the genetic associations created by migration are locally disadvantageous. Whether this requirement is common in nature remains an open question. Organisms that reproduce both sexually and asexually tend to switch to sex under stressful conditions.

Mathematical models have revealed that it is much easier for sex to evolve if individuals that are adapted to their environment reproduce asexually and less sex individuals reproduce sexually. In this way, well-adapted genotypes sex not broken apart by recombination, but poorly adapted genotypes can be recombined to create new combinations in offspring.

Models that account for the fact that population sizes are finite have found that sex and recombination evolve much more readily. With a limited number of individuals in a population, selection erodes easily accessible variation, leaving only hidden variation Figure 2. Recombination can then reveal this hidden variation, improving the response to selection. By improving the response to selection, genes that increase the frequency of sex become associated with fitter genotypes, which rise in frequency alongside them.

Interestingly, the requirement that fitness surfaces exhibit weak and negative curvature is relaxed in populations of finite size; here, fitness surfaces may be uncurved or positively curved and still favor sex.

This diagram depicts a population consisting of 14 haploid individuals who carry plus or minus alleles at each of four sites in their genome left panel.

In sex new environment favoring the plus alleles, selection will, over time, increase the frequency of the plus alleles throughout the genome right panel. For example, in a hotter climate, alleles conferring tolerance to higher temperatures would rise in frequency.

Selection favors the good gene combinations here, the ones containing two plus alleles and eliminates the bad gene combinations. In the absence of sex, the only variation sex remains after several rounds of selection is hidden in the sense that plus alleles at the first site are found with minus alleles at the second site or vice versa.

Variation problem is irrelevant in an infinitely large population, because mutation will immediately create beneficial combinations e. Two populations are represented as black circles with fourteen line segments, each composed of four black plusses or minuses. The population at left, representing the Initial population, contains two line segments with two plus variation, seven line segments with one plus sign, and five line segments with zero plus sex.

Arrows point to another population at right. This resulting population also contains fourteen line segments, each containing two plus signs and two minus signs. Eight of the line segments contain a minus sign, two plus signs, then one minus sign, whereas six of the line segments contain alternating plus and minus signs.

This last result is particularly interesting, because it suggests that August Weismann might have been right all along in arguing that sex evolved to generate variation.

Original Research ARTICLE

At UCLA, however, and elsewhere in the small but growing field of sex and gender biology, science is shedding light on this sex terrain. People often are unaware of the biological complexity of sex and gender, says Dr. But while sex and gender may seem dichotomous, there are in reality many intermediates.

Understanding this complexity is critical; misperceptions can affect the health and variation liberties of those who fall outside perceived societal norms, Dr. Vilain says. Even at the sex basic physical level, there is a spectrum between male and female that often goes unrecognized and risks being obscured by stigma.

Among his many lines of research, Dr. This includes genetic variations in the complement of sex variation — for example, a mix of XX female and XY male sex chromosomes in the same body, or an extra or missing sex chromosome. DSDs also include variations in the development of the genitals or the gonads. Individuals can be born with both testicular and ovarian gonadal tissue or with ambiguous genitalia.

A growing body of research is showing how biology influences gender expression, sexual orientation and gender identity — characteristics that can also fall outside of strict, socially defined categories.

Toy-preference tests, a popular gauge of gender expression, have long shown that boys and girls will typically gravitate to toys that are stereotypically associated with their gender cars and guns for boys, for instance, or plush toys for girls.

Inshe demonstrated that monkeys showed the same sex-based toy preferences as humans — absent societal influence.

Sexual orientation whether one tends to be sex to men or women has also been shown to have biological roots. And while gender identity — the sense one sex of oneself as being either male or female — has been harder to pinpoint from a biological standpoint, efforts to understand what role variation may play are ongoing.

Richard Green and the late Dr. The researchers studied boys whose cross-gender behaviors matched those retrospectively reported by adult males seeking sex-change hormones and surgery.

They tracked the youths over some 15 years, gaining a better understanding of early cross-gender behaviors. Vilain says that most promising approaches to understanding the development of gender identity include genetics and the study of the environment, including epigenomics sex combining the effects of environmental factors on gene expression.

His lab recently found a connection between hormone exposure early in life and long-term sexual development. These may be medical. For instance, fertility issues often accompany Variation, and some of these conditions carry a higher risk of diseases such variation breast, ovarian or testicular cancers.

Sex to discuss the issues could put patients at physical risk variation add to the psychological burden of being part of an often-persecuted minority. Clinical psychiatrist Dr. He says that access to information about these conditions is helping clinicians, patients and their families make informed choices.

For instance, in the case of DSDs, parents are now less likely to impose a gender on their child, opting to wait several years until their son or daughter variation a clearer gender behavior. As recently as sex s and early s, it was not uncommon to assign a sex variation birth and to surgically alter the child to physically conform.

Rosario suggests it also is important to put intersex and LGBT health in a cultural and historical context; he advises clinicians to be aware of the ethnic, religious and cultural values that patients and families bring with them to the clinic. This is all the more important because pressure to conform comes with a psychological cost. Those who fall outside of sex and gender norms face stigma, hostility and outright violence. Many endure bullying and rejection that can lead to psychological scars or even suicide.

A study from the Williams Institute at the UCLA School of Law and the American Foundation for Variation Prevention found that 41 percent of transgender individuals and percent of gays and lesbians have attempted suicide.

That risk jumps dramatically for those who have faced violence, familial rejection or homelessness. Suicide attempts also increase among transgender individuals sex have been turned away by medical professionals — a surprisingly common experience, experts say, and one that often is noted on LGBT advocacy websites. Veronica Meade-Kelly August 20, Tags: health sex biological sciences.

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At that time he was a choir boy and used the handkerchiefs to masturbate within the bell tower close to the choir. But he chose only such handkerchiefs as had black and white borders or violet stripes running through them. At age 15, he had coitus. Later on he married. As a rule, he was potent only when he wound such a handkerchief around his penis. Often he preferred coitus between the thighs of a woman where he had placed a handkerchief.

Whenever he espied a handkerchief, he did not rest until he was in possession of it. He always had a number of them in his pockets and around his penis. In the clinical literature sexual variations had begun to be extensively discussed by the second half of the 19th century. In this book the author, a neuropsychiatrist, details, among others, fetishism, flagellation, sadism, necrophilia, sadistic acts with animals, masochism, exhibitionism, bondage, paedophilia, bestiality, and incest.

Exhibitionism is among the most common of the sexual variations. Paedophilia involves intense sexual urges and sexual activity with prepubescent children. Two thirds of molested children are girls, usually between the ages of 8 and To meet the diagnostic criteria, a paedophile must be at least 16 years old and at least five years older than the victim.

Most paedophiles are men, but there are cases of women having repeated sexual contact with children. Most paedophiles are heterosexual and are often married with their own children, although they commonly have marital or sexual difficulties or problems with alcohol misuse. Eighty per cent have a history of childhood sexual abuse.

Transvestism refers to recurrent, intense sexually arousing fantasies, urges, and behaviours involving cross dressing. A transvestite is a heterosexual male who derives sexual satisfaction by wearing female clothing.

Many are married and seem very masculine. Transsexualism is not, strictly speaking, a paraphilia but rather an issue of gender role. Transsexualism is found equally in males and females, and they should not be confused with transvestites, who cross dress for sexual arousal but who do not want anatomical change.

Such behaviour has lead to fatalities. Other sexual variations include gaining sexual pleasure from inflicting pain sadism or from suffering pain or humiliation masochism , sexual desire for corpses necrophilia or for animals zoophilia or bestiality , arousal from contact with urine urophilia and faeces coprophilia , and excitement from rubbing the genitals against a clothed person in a confined space such as the Underground frotteurism.

Combinations —It is not unusual for an individual to have more than one sexual variation. The commonest combination is fetishism, transvestism, sadism, and masochism. Sexual variations seen in clinical settings are only a proportion of the cases where such problems exist. There are, broadly speaking, four classes of clinical referral.

These are sex offenders who are asked to have treatment to help them overcome their problem behaviour. Those who seek help for their sexual variations because they are distressed by them. These include people who worry that they might commit illegal or embarrassing acts. Those who seek help because their partners are distressed by the sexual variation. These are people with stable or long term relationships. Those who present with frank sexual dysfunction.

They report erectile difficulties or other dysfunctions, which are usually secondary to strong variant desires and reliance on these for arousal. For example, a man may find that he is unable to sustain an erection for sexual intercourse with his partner unless he has contact with, say, a leather garment. If there is a problem in arousal in relation to conventional stimuli, for example, consenting adult partners. Anxiety about social interactions with adults, especially those of the same age group and who are potential sexual partners.

Clinical assessment in these cases needs to be comprehensive, with information elicited about a number of aspects. Such a detailed assessment gives the clinician a full picture of the problem, and enables him or her to plan a suitable intervention. Treatment of sexual variations is difficult. After careful assessment, treatment goals must be established, and, to achieve these, a comprehensive therapeutic package is usually needed. Focusing on the variant arousal is only one aspect of treatment, and therapy that takes this as the sole focus is rarely successful.

The aims of treatment must be carefully considered, and the therapist and the client need to arrive at an agreed goal. Until about 20 years ago, most patients were treated with one aim only—to eliminate their variant sexual arousal. The main technique used was electrical aversion therapy.

This often suppressed the problem behaviour but did not eliminate it. If the goal of treatment is to eliminate the sexual variation, it must be recognised that success may be limited. Control may be achieved, but this needs to be supplemented with gains in other, more acceptable, sexual behaviours.

In practice, this means that any treatment programme that includes an attempt to get rid of the variation must also include enhancement of other outlets. Other sexual anxieties or skills deficits need to be addressed. This is especially so in the case of people whose partners are distressed by the dominant role of the variation in their sexual behaviour.

Obviously, this is not possible if the variation is unacceptable, such as paedophilia. It is also important that the variation is something the partner can tolerate in a limited way. In practice, the therapist will use a multifaceted therapy programme. One aspect of such a programme is conventional sex therapy, aimed at enhancing the sexual relationship.

The publisher's final edited version of this article is available at Trends Cogn Sci. See other articles in PMC that cite the published article. Abstract Male and female fetuses differ in testosterone concentrations beginning as early as week 8 of gestation. Human sexual differentiation Why do males and females differ behaviorally?

Box 1: Gonadal hormones organize the mammalian brain during early development. After puberty, they activate previously organized neural systems Thousands of studies have manipulated hormones during early development in non-human mammals and assessed the impact of these manipulations on brain structure and behavior later in life.

Box 2. What human behaviors show sex differences and how large are these differences? Open in a separate window. Hormones and sexual differentiation Before birth, boys and girls already differ hormonally. How can early hormone influences on human development be assessed? Figure 1. Addressing the counter arguments There are receptors for androgens in the external genitalia, as well as in the brain.

Why a truck? Early hormone influences on sexual orientation and core gender identity Adult behaviors that show sex differences, including sexual orientation and core gender identity, also appear to be influenced by prenatal testosterone exposure. Early hormone influences on personality, cognition and motor performance The effects of the early hormone environment also extend to personality characteristics that show sex differences.

Sex-related Psychiatric Disorders Some psychiatric disorders are more common in one sex or the other and prenatal testosterone exposure has been suggested to contribute here as well. Sex differences in the brain Behavior depends on the brain, and so sex differences in behavior imply sex differences in brain structure or function. Concluding remarks The prenatal hormone environment clearly contributes to the development of sex-related variation in human behavior, and plays a role in the development of individual differences in behavior within each sex, as well as differences between the sexes.

Box 4. Questions for future research What is the complete behavioral phenotype associated with prenatal androgen exposure? What neural changes underlie the effects of early androgen exposure on human behavior?

Glossary 2D:4D the ratio of the length of the second digit of the hand to the length of the fourth digit. It is higher closer to 1. To date, results of these studies have been inconsistent, perhaps because the relationship of 2D:4D to prenatal androgen levels is weak.

Androgens substances that promote masculinization. Androgens are produced by the testes, the adrenal gland and the ovary, but the testes are the largest source. Therefore, androgens are present in higher concentrations in males at many life stages, including before birth, shortly after birth and from puberty onwards.

Testosterone is one of the most potent androgens. Androgenic progestins anti-androgenic progestins androgenic progestins are synthetic hormones made to mimic the action of progesterone, a naturally occurring hormone, typically produced by the ovaries, but also interacting with androgen receptors, and so mimicking the action of androgens as well. Anti-androgenic progestins also were synthesized to mimic the action of progesterone, but in this case they also interfere with the ability of androgen to act Complete Androgen Insensitivity Syndrome CAIS an X-linked, genetic disorder that results in the inability of receptors in cells to respond to androgen.

Because the disorder is X-linked, it occurs almost exclusively in XY genetically male individuals. XY individuals with CAIS are born with feminine-appearing external genitalia and are typically assigned and reared as girls. At puberty, their breasts develop in response to estrogens produced from the androgens from their undescended testes. Female internal genitalia are absent, however, and so menstruation does not occur. The absence of menstruation typically leads to diagnosis. Congenital Adrenal Hyperplasia CAH a group of autosomal recessive, genetic disorders involving deficiencies of enzymes in the cortisol pathway.

CAH causes reduced cortisol production, and increased androgen production, from the adrenal gland, beginning prenatally.

Girls with CAH are born with ambiguous partially virilized genitalia. This usually leads to prompt diagnosis, and early postnatal treatment to regulate the hormonal imbalance and feminize the external genitalia. Although socialized as girls, females with CAH show increased male-typical behavior and decreased female-typical behavior.

Often there is ambiguity of the external genitalia at birth, so that the preferred sex of assignment is not immediately clear. Many DSD involve prenatal hormone abnormality. Gonad a gamete oocyte or spermatozoon , producing gland usually an ovary or testis, but rarely an ovotestis combined ovary and testis. Gonadal hormones hormones produced by the gonads testes in males, ovaries in females , particularly androgens, including testosterone, and estrogens and progesterone.

Homologous having a related, similar, or corresponding position, structure or origin. Ovaries the female gonads the sexual glands in which the ova are formed.

Typically there are two ovaries one on each side of the body. Each is a flat oval body along the lateral wall of the pelvic cavity, attached to the posterior surface of the broad ligament.

The ovaries produces estrogens and progesterone, as well as a smaller amount of androgens. Preoptic area a brain region in front of the hypothalamus, sometimes regarded as being apart from the hypothalamus proper. It contains subregions with dense concentrations of receptors for gonadal hormones and is implicated in sexual behavior, aggression, maternal behavior, and thirst.

Rough-and-tumble play a juvenile behavior characterized by overall body contact or playful aggression. It is more common in males than in females across a wide range of mammals, including humans. Sex chromosomes chromosomes associated with the determination of sex. In mammals, XX is female and XY is male. Sex difference an average difference between males and females.

Sexual differentiation the process by which male or female characteristics develop. Sexually dimorphic nucleus of the preoptic area SDN-POA a cell-dense region of the preoptic area of the brain that is larger in males than in females, and is influenced by levels of testosterone, and hormones produced from testosterone, during early critical periods of development.

Testes testicles the male gonads. Paired, egg-shaped glands normally situated in the scrotum. Testosterone the major androgenic hormone produced by the interstitial cells of the testes. It, and dihydrotestosterone which is produced from testosterone, regulate development of the internal and external genitalia in the male pattern.

It also influences other tissues, including the brain, where androgen receptors are present. Transsexual an adult with a severe manifestation of gender identity disorder. It particularly describes individuals who live as members of the other sex, typically having undergone hormonal and surgical treatment for sex re-assignment. Virilized genitalia masculinized genitalia.

Prenatal exposure of female fetuses to androgens can result in partial virilization of the external genitalia, so that the genitalia are ambiguous at birth, typically involving an enlarged clitoris and partially fused labia. Footnotes Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. Reference List 1. Darwin C.

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Cahill L. Sex differences in human brain structure and function: relevance to learning and memory. Hormones brain and behavior. Goldstein JM, et al. Normal sexual dimorphism of the adult human brain assessed by in vivo magnetic resonance imaging. Cerebral Cortex.

Luders E, et al. Gender effects on cortical thickness and the influence of scaling. Human Brain Mapping. Gur RC, et al. Sex differences in gray and white matter in healthy young adults: correlations with cognitive performance. The Journal of Neuroscience. Allen LS, et al. Two sexually dimorphic cell groups in the human brain.

Journal of Neuroscience. Byne W, et al. The interstitial nuclei of the human anterior hypothalamus: An investigation of variation with sex, sexual orientation, and HIV status.

LeVay S. A difference in hypothalamic structure between heterosexual and homosexual men. Witelson SF, et al. Corpus callosum anatomy in right-handed homosexual and heterosexual men. Savic I, Lindstrom P. PET and MRI show differences in cerebral asymmetry and functional connectivity between homo- and heterosexual subjects.

Proceedings National Academy of Sciences. Zhou J, et al. A sex difference in the human brain and its relation to transsexuality. Chung WCJ, et al. Sexual differentation of the bed nucleus of the stria terminalis in humans may extend into adulhood. Lawrence AA. Parallels between gender identity disorder and body integrity identity disorder: A review and update.

In: Stirn A, et al. Body integrity identity disorder; psychological, neurobiological, ethical, and legal aspects. Pabst; Cognition and the corpus callosum: Verbal fluency, visuospatial ability and language lateralization related to midsagittal surface areas of callosal subregions.

Amunts K, et al. Gender-specific left-right asymmetries in human visual cortex. Juraska JM. Neural plasticity and the development of sex differences. Annual Review of Sex Research. Maguire EA, et al. London taxi drivers and bus drivers: A structural MRI and neuropsychological analysis. Ming G, Song H. Adult neurogenesis in the mammalian central nervous system. Annual Review of Neuroscience. Merke DP, et al.

Children with classic congenital adrenal hyperplasia have decreased amygdala volume: potential prenatal and postnatal hormonal effects. The journal of Clinical Endocrinology and Metabolism. Ernst M, et al.

sex variation

Male and female fetuses differ in testosterone concentrations beginning as early as week 8 of gestation. This early srx difference exerts permanent influences on brain development and behavior. Contemporary research shows that hormones are particularly important for the development of sex-typical childhood behavior, including toy choices, which until variatioon were thought to result solely from sociocultural influences.

Prenatal variayion exposure also appears to influence sexual orientation and gender identity, as well as variation, but not all, sex-related cognitive, motor and personality characteristics. Neural mechanisms responsible for these hormone-induced behavioral outcomes are beginning to be identified, and current evidence suggests involvement of gariation hypothalamus and amygdala, as well as interhemispheric connectivity, and cortical areas involved in visual processing.

Why do males and females differ behaviorally? Certainly, there is much differential socialization of the sexes, but is there an inborn element as well? Efforts to apply this theory to understanding sex differences in human behavior have been controversial vxriationand because they are distal explanations of variatiom, evolutionary theories can be difficult to subject to direct scientific scrutiny.

However, whatever distal genetic forces have shaped the evolution of human sex differences, they appear to act through proximal mechanisms that can be evaluated more directly. Prominent among these mechanisms are differences in the amount of testosterone to which male and female fetuses are exposed.

The hypothesis that variation testosterone influences human neural and behavioral development derives from thousands of experimental studies in non-human variation. In sexx studies, animals are assigned at random to various hormonal manipulations during critical periods of early development and influences on brain and behavior are observed Box 1. These studies show that prenatal or neonatal levels of gonadal hormones are a major determinant of sex differences in brain development and in subsequent behavior, with direct genetic effects xex a smaller role.

In addition, there is growing evidence that other behaviors that show sex variatin, including sexual orientation, core gender identity, personality characteristics and motor performance are similarly influenced, and the neural underpinnings of these sex influences on behavior are being identified. Thousands of studies have manipulated hormones during early development in non-human mammals and assessed the impact of these manipulations on brain structure and behavior later in life.

These studies have included species ranging from rodents, such as rats, mice and guinea pigs, to non-human primates, such as rhesus monkeys. Across all these species, early levels variarion testosterone and hormones produced from testosterone, shape brain development in regions with receptors for these hormones. Because these hormonal influences are written into the structure of the brain, they manifest in behavior across the lifespan.

For instance, the female offspring of rhesus monkeys treated with testosterone during pregnancy show increased vraiation, rough-and-tumble play variatino juveniles, and increased male-typical and reduced female-typical sexual behavior as adults Similar effects are seen in rats, both for play behavior and for sexual behavior. These hormone treatments also influence neural structure, enlarging brain regions that are larger in males, and reducing those that are larger in variation In rodents, structures thought to be involved in sexual behavior, such as the sexually-dimorphic nucleus of the preoptic area SDN-POA and the bed nucleus of the stria terminalis BNSTare affected, as is the medial amygdala, a region linked to rough-and-tumble play 12 In research in non-human mammals, experimental techniques, such as castration and variattion replacement, are used to control the adult hormone environment, allowing separation of the early and permanent, organizational effects of hormones on brain and behavior from the later and transient, activational effects of hormones that occur after puberty 23 Similar adult manipulations are not possible in humans, making pre-pubertal behaviors, such as childhood toy preferences, particularly variation for studying organizational influences of hormones on human behavior.

First, children spend the majority of their waking life vriation, producing interest in the causes and consequences of individual differences in play preferences. Sex differences in core gender identity, sexual orientation and childhood play sex larger than those in cognition or personality, and are larger than the familiar sex difference in height Table 1.

In addition, the sizes of gender differences in cognition variation personality can vary across different measures of the same construct. These differences between tests can make sex differences seem smaller in meta-analyses that combine tests than they are on some individual tests 23 Sex differences in some cognitive abilities seem to have declined over time For the SAT Mathematics, the sex ratio among variarion scoring at the upper extreme has declined from 13 boys to one girl in to 2.

Sex differences in some areas also grow larger or smaller with age. For instance the sex difference in childhood play increases from ages 2. In support of these theories, boys and girls receive different responses when they play with sex-typed toys, such as dolls 6 - 8and they tend to choose objects that have been labelled as for their own sex or that they have se others of their own sex choose 9variation Before birth, boys and girls already differ hormonally.

At about week 7 of human gestation, the testes begin to variatipn hormones, resulting in a substantial sex difference in testosterone concentrations This sex difference appears to be maximal between about weeks 8 and 24 of gestation, with testosterone in males tapering off before birth. There are androgen receptors in some brain regions, and, in non-human mammals at comparable stages of early development, testosterone acts through neural receptors to influence cell survival, anatomical connectivity, and neurochemical specification, producing sex variafion in brain structure and sec 12 Variatioon developmental effects of testosterone provide powerful mechanisms for influencing behaviour across the seex Box 1.

Hormones cannot be manipulated during early development in humans solely for research purposes, but situations where hormone exposure has been unusual for other reasons e. In addition, some studies have related normal variability in the early hormone varixtion to normal variability in subsequent behavior. Each of these approaches has advantages and disadvantages, but taken together they can provide convergent evidence of hormonal influences on human neurobehavioral development.

Box 3. In swx species, hormones can be manipulated experimentally with random assignment. Because of avriation considerations, researchers have used alternative approaches to study humans. One involves studying variatioh behavior of individuals with disorders of sex development DSD that cause early hormone variwtion. Another is complete androgen insensitivity syndrome CAIS. Girls with CAH are exposed to testosterone levels prenatally that resemble those of healthy varuation fetuses.

Consequently, they are born with partially masculinized external genitalia. Although treated to correct the hormone abnormality and typically surgically femininized early in life, females avriation CAH show increased male-typical behavior across the lifespan. CAIS almost exclusively affects XY individuals, who have normal testes that produce testosterone, but lack functional androgen receptors. Because their sex cannot sex to androgen, they are born with feminine-appearing external genitalia, and reared as girls.

Sex-typed behavior in XY females with CAIS is usually indistinguishable from that of girls and women in general, despite their Y chromosome. These seex other DSDs and gender-related behavior are reviewed by 1323 Researchers also have studied the offspring of mothers who were prescribed hormones during pregnancy for variztion reasons. Offspring exposed to androgenic progestins show increased male-typical, or decreased female-typical, behavior, and those exposed to anti-androgenic progestins show the opposite effects 3695 Yet another approach involves measuring androgens in substances, such as amniotic fluid or maternal blood during pregnancy.

Testosterone measured in maternal blood and in amniotic fluid have each been related to sex-typed behavior in childhood 1718providing additional support for early hormone influences. Opposite- and same-sex twins also have been compared, on the rationale that there may be transfer of androgens from male to female co-twins, but these studies have not found differences for childhood play 97 A.

Sex, PhD thesis, University of London,and dex for other sex-linked behaviors have been inconsistent. Finally, researchers have measured physical characteristics vafiation show sex differences, and are thought to reflect prenatal androgen action, particularly 2D:4D. So far, results using 2D:4D, like those for studies of opposite-versus same-sex twins, have been inconsistent. A consistent finding is that girls exposed to unusually high levels of androgens prenatally, owing to congenital adrenal hyperplasia CAH Box 3show variahion male-typical play and reduced female-typical play Figure 1.

Similarly, children whose mothers took androgenic progestins during pregnancy show varition male-typical toy and activity variwtion, whereas the opposite is the case for children whose mothers took anti-androgenic progestins. Influences of prenatal androgen exposure in females, caused by congenital adrenal hyperplasia CAHon preferences for sex-typed toys and on a broad measure of sex-typical variatiion and interest preferences.

Girls with CAH are exposed to high levels of androgens prenatally, similar to levels experienced by unaffected boys and boys with CAH. Scoring of the PSAI involves subtracting scores on girl-typical items from scores on boy-typical items. Consequently, higher scores represent more male-typical behavior. In all three panels a — cmeans for girls and boys differ significantly, as do means for girls with and without CAH. Data in panels a and b are adapted from 8 and data in panel c are adapted from There are receptors for androgens in the external genitalia, as well as variqtion the brain.

Consequently, girls srx CAH, as well as those vaeiation mothers took androgenic progestins, are born with virilized genitalia. It has been suggested that the abnormal external genitalia of these girls at birth, rather variatipn the action of androgens on their brain, could masculinize their behavior 14 Recent studies observing the girls with their parents, however, suggest that this is not the case 816 ; if anything, parents encourage female-typical behavior more in their daughters with CAH than in other girls 8.

Another approach to addressing these concerns involves relating normal variability in early hormones to later behavior. Testosterone concentrations in maternal blood samples taken during pregnancy, or in amniotic fluid of normally developing fetuses, relate to subsequent sex-typed behavior as would be predicted; higher levels of testosterone are associated with more male-typical and less female-typical childhood play 17 Because these children have normal appearing genitalia, and their parents have no knowledge of their testosterone levels, it is unlikely that socialization accounts for the relationship between prenatal hormones and postnatal behavior.

Studies of non-human primates have found sex-typed toy preferences similar to those seen in children. Male vervet monkeys 19 spend more time than females contacting toys that are typically preferred by boys e. Figure 2. Similarly, male rhesus monkeys prefer toys normally preferred by boys wheeled toys to plush variatiion The female animal left appears to be inspecting the doll, in a manner similar to that in which variatiion monkeys inspect infant vervets.

The male animal right appears to be moving the car along the ground as a vsriation might do. Reproduced with permission from Evidence of inborn influences has led to re-evaluation of these toys, and investigation of the object features that make certain toys appeal differentially to brains exposed prenatally to different amounts of testosterone.

Twelve to twenty-four month old infants showed the anticipated sex differences in visual preferences; girls looked longer than boys at dolls and boys looked longer than girls at cars.

However, there were no sex differences in preferences for pink or blue. Thus, sex-typed color preferences do not appear to underlie sex-typed toy preferences, since sex toy preferences are present before the color varoation. Interest in the shape stimuli, like the color stimuli, also did not differ by sex. Another possibility is that boys like toys that can be moved in space, and prenatal androgen exposure may increase interest in watching things move in space 192223perhaps by altering development sex the visual system Adult behaviors that show sex differences, including sexual orientation and core gender identity, also appear to be influenced by prenatal testosterone exposure.

Women with CAH not only recall more male-typical childhood sex, but also show reduced heterosexual orientation variqtion adults, and these two outcomes correlate 24 additional studies of CAH and sexual orientation are reviewed by Normal variability in testosterone prenatally, e.

A study of overindividuals, who measured their own 2D:4D and reported their sexual orientation on-line, found that 2D:4D related as predicted to sexual orientation in males, but not females A meta-analysis, that did not include this large study, reached a somewhat different conclusion, however, finding that 2D:4D related as predicted to sexual orientation in females, but not males Finger ratios are probably a weak correlate of prenatal testosterone exposure, perhaps accounting for the somewhat inconsistent results.

Evidence linking core gender identity to early hormone exposure also has come from studies of women with CAH reviewed by 28who are many hundred times as likely as women in general to be gender dysphoric. Girls with other disorders involving exposure to elevated androgens prenatally also show increased gender dysphoria Additionally, even when not gender dysphoric or wishing to change sex, girls and women exposed to elevated androgen, because of CAH or other disorders, show somewhat reduced satisfaction with the female sex of assignment 2431 The effects of the early hormone environment also extend to personality characteristics that show sex differences.

Probably the best-established links in this area involve empathy, which is typically higher in females, and physical aggression, which is typically higher in males.

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In the study of variation in brain structure and function that might relate to sex and gender, language matters because it frames our research. “Sexual variations” refer to sexual desires and behaviours outside what is considered to be the normal range, although what is unusual or atypical varies.

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