Whether it's a orangutan or a peafowl, sexual dimorphism can manifest in many fascinating ways. Sexual dimorphism, the differences in appearance between males and females of the same species, such as in colour, shape, size, and structure, that are caused by the inheritance of one or the other sexual pattern in the genetic material. The mountain spiny lizard (Sceloporus. Sexual dimorphism in humans is the subject of much controversy. Human male and female appearances are perceived as different, although Homo sapiens has.
Sexual dimorphism in humans is the subject of much controversy. Human male and female appearances are perceived as different, although Homo sapiens has. Whether it's a orangutan or a peafowl, sexual dimorphism can manifest in many fascinating ways. Sexual dimorphism is the condition where the two sexes of the same species exhibit different characteristics beyond the differences in their sexual organs. The condition occurs in many animals and some plants.
Whether it's a orangutan or a peafowl, sexual dimorphism can manifest in many fascinating ways. Early hominid sexual dimorphism and implications for mating systems Sexual dimorphism in Australopithecus afarensis was similar to that of. In mammals, sex chromosomes start to program autosomal gene expression and epigenetic patterns very soon after fertilization. Yet whether.
Sexual Dimorphism. Sexual dimorphism dimorphism the systematic difference in form between individuals of different dimorphism in dimorpyism sexual species. For example, in some species, including many mammals, the male is larger than the female. In sexual, such as some spiders, the female is larger than sexual male. Other sex-specific differences dimorphisj color most birds sexual, dimorphiam in birdssize or presence of parts of dimorphism body used in struggles for dominance, such as horns, antlers, and tusks; size of the eyes e.
Sexual dimorphism in humans is the subject of much controversy. Human male and female appearances are perceived as different, although Homo sapiens has dimkrphism low level of sexual dimorphism compared with many other species. The sexual in the sizes of male and female human beings is a good example of how nature often does not make clear divisions. To give an accurate picture of male and female size differences one would need to show how many individuals there are dimorphis each size category.
There is a considerable overlap. For example, the body masses of both male and female humans are approximately normally distributed. In the United States, the mean mass of an adult dimorphism is However the standard dimorphjsm of male body mass is Biological aspects of sexual dimorphism The phenomenon of sexual dimorphism is a direct product of evolution by natural selection, in sexual the dimorphism for reproductive success drives many male and female organisms down dimorphiem evolutionary paths.
This can produce forms of dimorphism which, on the face of it, would actually seem to disadvantage organisms. For instance, the bright coloration of male game birds makes them highly visible dimorphism for predators, while the drab females are far better equipped to camouflage themselves.
Likewise, the antlers of deer and other forms of natural weaponry are very expensive to grow and carry in terms of the energy sexual by the animal in the process. The answer to this apparent paradox is that, dimorphism a biological level, the reproductive success of an organism is often more important than its long-term survival.
This sexual particularly apparent in the case of game birds: a male Common Pheasant in sexual wild often lives no more than 10 months, with sezual living twice as long. However, a male pheasant's ability dimorphism reproduce depends not on how long he lives but whether females will select him to sexial their mate. His bright coloration demonstrates to the female that he is fit, healthy and a good choice to father her chicks. In the case of herd animals such dimorphhism deer, a male deer's reproductive success is directly proportional to the number of sexually receptive females with which he can mate.
The males' antlers are an example of cimorphism sexually dimorphic weapon with which the males fight each other to establish breeding rights. Again, although they are expensive in terms of personal survival, they ensure that the largest and strongest males will be the most successful in reproducing and thereby ensure that those characteristics are passed on to the next generation. Access to the opposite sex dmiorphism not the only reason why sexual dimorphism exists.
In insects in particular, females are often larger than the males. It is dimorphism that the reason lies in the huge number of eggs sexual insects lay; a larger body size enables a female insect sexual lay more eggs. In some cases, dimoorphism dimorphism enables males and females to exploit different food resources, thus increasing their collective ability to find food.
Some species of woodpecker have differently-sized and shaped beaks, enabling the sexes to find insects in different layers of a tree's bark. It is also common in birds of prey for the female to be larger than the male, an example of reverse sexual dimorphism. The size difference allows the mated pair to hunt a greater variety of prey for themselves and for their chicks.
Dimorphism from web pages: Sexual dimorphism sexual dimorphism.
An example of sexual polymorphism determined by environmental conditions exists in the red-backed fairywren. Red-backed fairywren males can be classified into three categories during breeding season : black breeders, brown breeders, and brown auxiliaries. Migratory patterns and behaviors also influence sexual dimorphisms. This aspect also stems back to the size dimorphism in species. It has been shown that the larger males are better at coping with the difficulties of migration and thusly are more successful in reproducing when reaching the breeding destination.
If these are the result for every migration and breeding season the expected results should be a shift towards a larger male population through sexual selection. Sexual selection is strong when the factor of environmental selection is also introduced. The environmental selection may support a smaller chick size if those chicks were born in an area that allowed them to grow to a larger size, even though under normal conditions they would not be able to reach this optimal size for migration.
When the environment gives advantages and disadvantages of this sort, the strength of selection is weakened and the environmental forces are given greater morphological weight. The sexual dimorphism could also produce a change in timing of migration leading to differences in mating success within the bird population. This timing could even lead to a speciation phenomenon if the variation becomes strongly drastic and favorable towards two different outcomes.
Sexual dimorphism is maintained by the counteracting pressures of natural selection and sexual selection. For example, sexual dimorphism in coloration increases the vulnerability of bird species to predation by European sparrowhawks in Denmark. Reproductive benefits arise in the form of a larger number of offspring, while natural selection imposes costs in the form of reduced survival.
This means that even if the trait causes males to die earlier, the trait is still beneficial so long as males with the trait produce more offspring than males lacking the trait.
This balance keeps the dimorphism alive in these species and ensures that the next generation of successful males will also display these traits that are attractive to the females. Such differences in form and reproductive roles often cause differences in behavior. As previously stated, males and females often have different roles in reproduction.
The courtship and mating behavior of males and females are regulated largely by hormones throughout a bird's lifetime. Sexual dimorphism may also influence differences in parental investment during times of food scarcity.
For example, in the blue-footed booby , the female chicks grow faster than the males, resulting in booby parents producing the smaller sex, the males, during times of food shortage.
This then results in the maximization of parental lifetime reproductive success. Sexual dimorphism may also only appear during mating season, some species of birds only show dimorphic traits in seasonal variation. The males of these species will molt into a less bright or less exaggerated color during the off breeding season. Consequently, sexual dimorphism has important ramifications for conservation. However, sexual dimorphism is not only found in birds and is thus important to the conservation of many animals.
Such differences in form and behavior can lead to sexual segregation , defined as sex differences in space and resource use.
The term sesquimorphism the Latin numeral prefix sesqui - means one-and-one-half, so halfway between mono - one and di - two has been proposed for bird species in which "both sexes have basically the same plumage pattern, though the female is clearly distinguishable by reason of her paler or washed-out colour". In a large proportion of mammal species, males are larger than females. Hormones significantly affect human brain formation, and also brain development at puberty.
A review in Nature Reviews Neuroscience observed that "because it is easier to manipulate hormone levels than the expression of sex chromosome genes, the effects of hormones have been studied much more extensively, and are much better understood, than the direct actions in the brain of sex chromosome genes. Marine mammals show some of the greatest sexual size differences of mammals, because of sexual selection.
Pinnipeds are known for early differential growth and maternal investment since the only nutrients for newborn pups is the milk provided by the mother. The pattern of differential investment can be varied principally prenatally and post-natally. Sexual dimorphism in elephant seals is associated with the ability of a male to defend territories, which correlates with polygynic behavior.
The large sexual size dimorphism is due to sexual selection, but also because females reach reproductive age much earlier than males. In addition the males do not provide parental care for the young and allocate more energy to growth. Top: Stylised illustration of humans on the Pioneer plaque , showing both male left and female right. Bottom: Comparison between male left and female right pelvises.
In humans, sex is determined by five factors present at birth: the presence or absence of a Y chromosome, the type of gonads , the sex hormones , the internal reproductive anatomy such as the uterus in females , and the external genitalia. Sexual ambiguity is rare in humans, but wherein such ambiguity does occur, the individual is biologically classified as intersex. Sexual dimorphism among humans includes differentiation among gonads, internal genitals, external genitals, breasts, muscle mass, height, the endocrine hormonal systems and their physiological and behavioral effects.
Human sexual differentiation is effected primarily at the gene level, by the presence or absence of a Y-chromosome, which encodes biochemical modifiers for sexual development in males. The average basal metabolic rate is about 6 percent higher in adolescent males than females and increases to about 10 percent higher after puberty. Females tend to convert more food into fat , while males convert more into muscle and expendable circulating energy reserves.
In Olympic weightlifting, male records vary from 5. Females are taller, on average, than males in early adolescence, but males, on average, surpass them in height in later adolescence and adulthood. There is no comparative evidence of differing levels of sexual selection having produced sexual size dimorphism between human populations. Males typically have larger tracheae and branching bronchi , with about 30 percent greater lung volume per body mass.
On average, males have larger hearts , 10 percent higher red blood cell count, higher hemoglobin , hence greater oxygen-carrying capacity. They also have higher circulating clotting factors vitamin K , pro thrombin and platelets. These differences lead to faster healing of wounds and higher peripheral pain tolerance. Females typically have more white blood cells stored and circulating , more granulocytes and B and T lymphocytes. Additionally, they produce more antibodies at a faster rate than males.
Hence they develop fewer infectious diseases and succumb for shorter periods. Considerable discussion in academic literature concerns potential evolutionary advantages associated with sexual competition both intrasexual and intersexual and short- and long-term sexual strategies. Testosterone is converted to estrogen in the brain through the action of the enzyme aromatase.
The relationship between sex differences in the brain and human behavior is a subject of controversy in psychology and society at large. Thus, the percentage of gray matter appears to be more related to brain size than it is to sex. Haier et al.
Strict graph-theoretical analysis of the human brain connections revealed  that in numerous graph-theoretical parameters e. It was shown  that the graph-theoretical differences are due to the sex and not to the differences in the cerebral volume, by analyzing the data of 36 females and 36 males, where the brain volume of each man in the group was smaller than the brain volume of each woman in the group.
Sexual dimorphism was also described in the gene level and shown to be extend from the sex chromosomes.
Overall, about genes have been found to have sex-differential expression in at least one tissue. Many of these genes are not directly associated with reproduction, but rather linked to more general biological features. In addition, it has been shown that genes with sex specific expression undergo reduced selection efficiency, which lead to higher population frequencies of deleterious mutations and contributing to the prevalence of several human diseases.
Phenotypic differences between sexes are evident even in cultured cells from tissues. In theory, larger females are favored by competition for mates, especially in polygamous species. Larger females offer an advantage in fertility, since the physiological demands of reproduction are limiting in females.
Hence there is a theoretical expectation that females tend to be larger in species that are monogamous. Females are larger in many species of insects , many spiders , many fish , many reptiles, owls , birds of prey and certain mammals such as the spotted hyena , and baleen whales such as blue whale.
As an example, in some species, females are sedentary, and so males must search for them. Fritz Vollrath and Geoff Parker argue that this difference in behaviour leads to radically different selection pressures on the two sexes, evidently favouring smaller males. One example of this type of sexual size dimorphism is the bat Myotis nigricans , black myotis bat where females are substantially larger than males in terms of body weight, skull measurement, and forearm length. Females bear the energetic cost of producing eggs, which is much greater than the cost of making sperm by the males.
The fecundity advantage hypothesis states that a larger female is able to produce more offspring and give them more favorable conditions to ensure their survival; this is true for most ectotherms. A larger female can provide parental care for a longer time while the offspring matures. The gestation and lactation periods are fairly long in M. Smaller male size may be an adaptation to increase maneuverability and agility, allowing males to compete better with females for food and other resources.
Some species of anglerfish also display extreme sexual dimorphism. Females are more typical in appearance to other fish, whereas the males are tiny rudimentary creatures with stunted digestive systems. A male must find a female and fuse with her: he then lives parasitically, becoming little more than a sperm-producing body in what amounts to an effectively hermaphrodite composite organism. A similar situation is found in the Zeus water bug Phoreticovelia disparata where the female has a glandular area on her back that can serve to feed a male, which clings to her note that although males can survive away from females, they generally are not free-living.
Some plant species also exhibit dimorphism in which the females are significantly larger than the males, such as in the moss Dicranum  and the liverwort Sphaerocarpos. Another complicated example of sexual dimorphism is in Vespula squamosa , the southern yellowjacket.
In this wasp species, the female workers are the smallest, the male workers are slightly larger, and the female queens are significantly larger than her female worker and male counterparts.
Sexual dimorphism by size is evident in some extinct species such as the velociraptor. In , Charles Darwin advanced the theory of sexual selection , which related sexual dimorphism with sexual selection. It has been proposed that the earliest sexual dimorphism is the size differentiation of sperm and eggs anisogamy , but the evolutionary significance of sexual dimorphism is more complex than that would suggest.
This intensifies male competition for mates and promotes the evolution of other sexual dimorphism in many species, especially in vertebrates including mammals. However, in some species, the females can be larger than males, irrespective of gametes, and in some species females usually of species in which males invest a lot in rearing offspring and thus no longer considered as so redundant compete for mates in ways more usually associated with males.
In many non-monogamous species, the benefit to a male's reproductive fitness of mating with multiple females is large, whereas the benefit to a female's reproductive fitness of mating with multiple males is small or nonexistent.
The male may therefore come to have different traits from the female. These traits could be ones that allow him to fight off other males for control of territory or a harem , such as large size or weapons;  or they could be traits that females, for whatever reason, prefer in mates.
Females may choose males that appear strong and healthy, thus likely to possess "good alleles " and give rise to healthy offspring. The sexy son hypothesis states that females may initially choose a trait because it improves the survival of their young, but once this preference has become widespread, females must continue to choose the trait, even if it becomes harmful.
Those that do not will have sons that are unattractive to most females since the preference is widespread and so receive few matings. The handicap principle states that a male who survives despite possessing some sort of handicap thus proves that the rest of his genes are "good alleles". If males with "bad alleles" could not survive the handicap, females may evolve to choose males with this sort of handicap; the trait is acting as a hard-to-fake signal of fitness.
From Wikipedia, the free encyclopedia. For sex differences in humans, see Sex differences in humans. This section needs expansion.
You can help by adding to it. April Main article: Sexual dimorphism in non-human primates. Main articles: Sex differences in humans and Sex differences in human psychology. See also: Sexual selection and Mate choice. Retrieved 3 November The Journal of Experimental Biology.
Journal of Theoretical Biology. Bibcode : PNAS.. Journal of Zoology. Senar, J. Pascual Johnsen, K. Delhey, S. Kempenaers Proceedings of the Royal Society B. Lozano Sexual dichromatism in frogs: natural selection, sexual selection and unexpected diversity. Behavioral Ecology. The Differences Between the Sexes. Cambridge University Press. Retrieved 3 November — via Google Books. Biology Letters.
American Journal of Botany. Bibcode : Sci University of Massachusetts. Read More on This Topic. Certain tissues are set aside for the production…. Subscribe today for unlimited access to Britannica. Learn More in these related Britannica articles:. Certain tissues are set aside for the production of sexual reproductive cells, male or female as the case may be. Whether they are testes or ovaries or, as in some animals and plants, both together in the….
The differential effects on the growth of bone, muscle, and fat at puberty increase considerably the difference in body composition between the sexes. Boys have a greater increase not only in stature but especially in breadth of shoulders; girls have a greater relative….
The male is generally smaller in size some exceptions are found in sunfishes, gobies, and blennies and has brighter coloration of the fins and body. Black, white, green, red, blue, and silver are colours characteristic of the brightly…. Detailed molecular information on the ontogeny of sex biases would also elucidate the sex-specific selective pressures operating on embryos and how compensatory mechanisms evolved to resolve sexual conflict.
In the age of genomics, it has become ever more obvious that the long-known differences between males and females in health, longevity, disease risk and presentation, and response to therapy have genetic and epigenetic foundations Yang et al.
It is now clear that every adult somatic cell, to a greater or lesser degree, exhibits sex biases in gene expression and epigenetic profile in human and non-human primates, rodents, and bovines Yang et al. There is also a growing realization that sex differences are the result of complex interactions between the sex hormones, genetic variability, and the environment, all of which operate on the background of the intrinsic effects of the sex chromosome composition, i.
Although the driver of sex differences in mammals has traditionally been considered to be the so-called sex determination pathway, sex-specific transcriptional and epigenomic profiles are present in the embryo very soon after fertilization in a range of mammals, i. Moreover, male and female embryos exhibit different susceptibilities to environmental factors during early gestation Jenkins et al.
These differences reflect the early sexual identity of the embryo Hansen et al. Long before sex hormones appear, the primary sex-determining factor is the imbalance in sex chromosome composition Blecher and Erickson, ; Arnold, If sex differences at the molecular level begin at such an early stage, the question is, do those differences matter and what are their contributions to sex differences that become apparent later in life?
Do these sex biases matter more for some tissues than for others? Do expression and epigenetic sex biases wax and wane over the course of embryogenesis? How does the sex-specific molecular skewing inform on compensatory mechanisms that operate on males and females during embryogenesis from an evolutionary standpoint?
The goal of this article is to identify gaps in our knowledge that impede us from answering these questions. Two observations justify how sex-biased expression in pre-implantation embryos could establish male and female-specific transcriptional and epigenetic legacies that become apparent at later stages in development.
First, a number of dosage-dependent regulatory factors are expressed in a sex-biased manner in pre-implantation embryos, some of which are encoded on the X and Y chromosomes. Many transcription factors TFs and epigenetic regulators must be expressed at the appropriate levels for proper activation or repression of their downstream target genes.
In fact, TFs are overrepresented in haploinsufficiency disorders McKusick, ; Seidman and Seidman, 1 , in which mutations inactivating one allele produce a reduction by half in the protein levels of the TF. Second, there are precedents for epigenetic marks present after fertilization to persist after implantation. For example, genomic imprints from each parental genome are maintained throughout the genome-wide pre- and post-implantation reprograming processes Barlow and Bartolomei, ; Engel, In principle, variations in TF levels can change the response of their target genes or alter their affinity to their cognate sites Chen et al.
Promoters and enhancers are more or less sensitive to TF concentrations depending on the number of binding sites for specific TFs Badis et al.
In addition, TFs often act synergistically or in multimers, so higher or lower levels can result in changes in downstream effects Jolma et al. Dosage also affects epigenetic factors EFs , such as DNA-methyltransferases and histone modification enzymes. Because these usually act in large complexes, changes in the levels of protein components of these complexes can alter their stoichiometry and function Veitia and Birchler, ; Ori et al. In turn, some TFs are sensitive to the chromatin environment Blattler and Farnham, ; Inukai et al.
Unfortunately, there is a dearth of experimental data to determine how dosage differences in TFs and EFs shift transcriptomes, much less phenotypes, in mammalian model systems. ChIP data showing that sex-biased TFs are distributed differentially across the genome or that they activate their targets differentially would go a long way toward understanding dosage effects of regulatory factors.
Making ChIP more quantitative and more sensitive, and expanding the availability of ChIP-grade antibodies for regulatory factors is a pre-requisite. Perhaps technology that allows us to tag TFs by genetic engineering will solve some of these issues Savic et al.
The ability to finely tune the levels of TFs is also necessary to determine if subtle variations have downstream consequences. One of the best-studied events distinguishing male and female pre-implantation embryos is that females undergo X chromosome inactivation XCI.
XCI in placental mammals is a dosage compensation mechanism that transcriptionally silences the majority of genes on one of the X chromosomes in females. Because males have a single X chromosome, this ensures dosage equivalence between males and females. The long non-coding RNA Xist becomes highly expressed on one X chromosome, coating the entire chromosome and triggering the accumulation of DNA methylation and condensing histone modifications, ultimately resulting in heterochromatinization Disteche and Berletch, ; Sahakyan et al.
Two consequences result from this massive epigenetic overhaul of an entire chromosome. First, female embryos are developmentally delayed relative to male embryos until XCI is complete Thornhill and Burgoyne, ; Schulz et al.
It is well-established that XCI is intimately tied to cell differentiation, at least in the mouse Lessing et al. Thus, in addition to the effects of sex-biased expression of TFs, the delay in XX embryos opens a window of opportunity for TFs and EFs to act on the female genome in a sex-specific manner, even if they are not expressed in a sex-biased manner.
On the other hand, the male genome may undergo specific modifications as a consequence of not needing to inactivate an X chromosome. Another consequence of XCI that has been hypothesized is that the inactive X is a sink for epigenetic factors, altering their relative concentrations between males and female, with possible consequences for autosomal regulation Wijchers et al.
The decrease in availability of EFs in females would introduce differences in the chromatin status of regulatory sequences.
In turn, this would introduce a variation in how the genome is read and regulated in the female embryo. Both of these scenarios require experimental validation with sensitive genomic and proteomic tools that allow interrogation of single sexed embryos before and after XCI to determine whether females are on a different developmental clock and whether specific epigenetic factors are indeed substantially diminished relative to male embryos.
The process of XCI is stochastic in the embryo and the choice of the X chromosome to be inactivated is heritable. This means that female placental mammals are mosaics because in some cells the paternally inherited X chromosome is inactive whereas in other cells it is the maternally inherited X which is inactive Migeon, As a result, expression of X-linked allelic variants will vary in different cell lineages Wu et al.
If the alleles exhibit variation in their expression levels, female cells in which the maternal X is active can have expression levels of X-linked genes that differ from those in male cells. Although the majority of genes are silenced on the inactive X chromosome, a number of genes escape XCI and remain more highly expressed in female cells after implantation, contributing to sex biases in gene expression throughout the lifespan of the organism Disteche and Berletch, ; Balaton and Brown, Implantation signals a major reprograming of the genome, concomitant with lineage determination.
If sex-biased epigenetic landscapes can weather the de novo DNA methylation and chromatin re-structuring that ensues, it remains to be determined which specific epigenetic marks identify the cell as male or female. If, on the other hand, implantation erases all sex biases between XX and XY embryos, there are still genes encoded on the sex chromosomes that are differentially expressed before the appearance of sex hormones that could lead to sex-biased autosomal gene expression.
Such is the case of Y-linked genes, absent in female cells, X-linked allelic variants and genes that escape XCI altogether Disteche and Berletch, Therefore, we need a detailed, lineage-specific catalog of what genes escape XCI over the course of development and how they affect transcriptional outcomes.
Studies in multiple non-mammalian models have revealed sex-biased expression of many genes not necessarily related to sexual function throughout embryogenesis Mank et al. Such detailed characterization of the fluctuations in transcriptional and epigenetic sex biases during development is lacking for mammals.
Therefore, tissue-specific developmental time-series data are needed to begin to answer these questions experimentally. Evolutionary conflict arises between the sexes when their fitness interests diverge. Because males and females share most of their genomes, genes common to both sexes encode many of their shared traits Cox and Calsbeek, ; Hosken et al.
Sexually antagonistic selection emerges when optimal fitness for traits differs, leading to intra-locus sexual conflict. For example, intra-locus conflict arises when expression of a gene is beneficial in one sex but detrimental in the other.
Contradictory selection pressures can lead to sub-optimal expression levels for each sex, with subsequent regulatory mechanisms evolving to offset the less-than-optimal expression level. Thus, sex-biased gene expression can be indicative of ongoing or resolved intra-locus sexual conflict Parsch and Ellegren, ; Rowe et al.
Forces generating expression differences are expected to be maximal in the adults, because this is when reproductive interests diverge. However, if we envision sexual differentiation as a progressive developmental process, with independent and combined contributions from the sex chromosomes and sex hormones, it is possible that expression patterns of early embryos are also under sex-specific selection pressures and that sex-biased expression during development indicates sexual antagonism Ingleby et al.
Because we lack detailed sex-stratified data across the whole life cycle in mammals, we do not know how sex-biased transcription contributes to the male and female phenotypes, much less all of the genes involved. For example, some sex biases may need to be expressed continuously throughout development, while others may be transient, setting the stage for later sexual dimorphism.
A different mechanism of uncoupling the genetic architecture between males and females involves gene duplication and the evolution of sex-specific regulatory mechanisms for each duplicate Wyman et al. Especially in the case of mammals, with their greatly expanded families of TFs, it would be interesting to investigate if different paralogs enable conflict resolution by harboring divergent regulatory sequences that direct sex-specific expression.
Although the majority of genes that contribute to sexually dimorphic traits are autosomal and shared between the sexes, the sex chromosomes are a separate solution to sexual conflict, expanding the range of sexual differences at the level of expression that can exist Hosken et al.
The special nature of the sex chromosomes is related to evolutionary forces that have driven their differentiation and the compensatory mechanisms that allow male cells to tolerate the presence of a single X chromosome Skaletsky et al. These forces are independent, but can interact with those related to the divergent niches of males and females in reproduction.
Offsetting the imbalance in the sex chromosomes is necessary either because genes on the sex chromosomes participate in complex regulatory networks or because they encode components of dosage-sensitive protein complexes Bellott et al. Compensation is partially achieved by XCI in female cells. However, very little is known about the adjustments of the autosomes to the imbalance of sex chromosomes in males and females, which in principle could give rise to sex-biased expression of autosomal genes at any point in development Veitia et al.
Detailed molecular information across all stages of development for males and females would allow us to test the major hypotheses on the ontogeny and evolutionary significance of sex biases by integrating functional studies of individual genes with systems-level analyses and identifying similarities and differences across a range of species. Some genes are expressed with less than a twofold difference between the sexes Arnold et al. These differences may be considered trivial, but the systems biology revolution has highlighted that genes are interconnected in complex networks and that small differences in multiple genes can shift transcriptional and phenotypic outcomes.
Considering that some sexually dimorphic traits are extremely complex, many small-effect loci are likely to underlie these traits. Expression variation quantitative trait locus eQTL mapping of sex-biased expression in mice support this expectation Yang et al. A recent mandate from the NIH to include sex as a biological variable in all studies has adrenalized the interest in sex differences in disease risk and susceptibility Clayton and Collins, Significant inroads have been made in characterizing sex biases in gene expression and epigenetic features in a variety of adult tissues.
Modeling of regulatory networks in adult human and mouse tissues have shown surprising differences in regulatory architecture between males and females Chen et al. The range of continuously evolving analytical tools opens the possibility of looking at the aggregate pattern of sex-biased expression to reveal sex-specific modules within the global networks that specify cellular types. There is a high degree of plasticity in developmental pathways, with a variety of intermediate states leading to the same phenotypic space Briggs et al.
It is conceivable, then, that sex skews some parts of a network encoding a cellular phenotype, while not affecting others. It is also possible that some cell types may require a greater degree of molecular convergence between the sexes than others. Sex-stratified transcriptional and epigenetic data from embryos would also allow a more complete understanding of how the appearance of sex hormones affect developmental processes beyond the reproductive system.
Figure 1. Sex-specific transcriptional networks and phenotype maps. Schematic representation of the relationships between genotype, transcriptional networks, and final phenotype during development. Male and female genotypes, represented as XY and XX produce distinct epigenotypes, with effects on and counter-effects from the autosomes A.
Modifications of the epigenotype on the autosomes lead to transcriptional changes that in turn influence expression from the sex chromosomes. Different transcription factor TF networks can either determine distinct phenotypes space A or converge to an equivalent phenotype spaces B, C. We propose that genes encoded on the sex chromosomes act on autosomal genes to generate a differential regulatory and epigenetic landscape upon which later factors, such as hormones, act to counter or compound sex biases.
Because the epigenome does not necessarily affect transcription until stage-specific TFs appear, epigenetic sex biases established in early development could persist and contribute to sex-specific phenotypes at later time points Figure 2. Testing this hypothesis will first require identifying the nature of sex-biased epigenetic marks, with DNA methylation an obvious candidate.
Then, we must gather and integrate dynamic, sex-stratified epigenetic, expression, and proteomic data throughout embryogenesis. The degree to which molecular sex differences are compensated for between the sexes are likely to be tissue-specific, with some cell types requiring greater molecular convergence than others for proper functionality.
This can be revealed with detailed tissue-specific analyses, a time-consuming but certainly worthwhile effort. The role of sex hormones in these processes can then be inferred and validated with in vivo manipulations in animal models. This will pave the way for connecting sex biases during development to adult phenotypes. Figure 2. Schematic of our hypothesis.
A Sex biases have different origins depending on the developmental stage of the organism. Before gonadogenesis, sex chromosomes are the primary determinants of sex differences. Sex hormones influence the transcriptome and epigenome independently of and in combination with sex chromosome effects. B Soon after fertilization, male and female cells have sex-specific transcriptomes, epigenomes, and phenotypes for example, male embryos grow faster than female embryos.