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This could certainly explain why a particular synteny group is associated with sex in distantly related lineages, since genes that are physically linked to one of these repeatedly chosen sex-determining genes will hitchhike with it, especially since sex chromosomes tend to be rearranged infrequently. However, this does not explain why 2 synteny groups, hitchhiking to form sex chromosomes in different lineages, would be found together in an ancestor.
Another possibility is that a second potentially sex-determining gene has a advantage in the same sex which is designated by the sex-determining gene. At least some of the sex-determining genes, such as DMRT1 and AMH , are involved in the sex determination pathway even where they are not the head of it. It is possible, therefore, that there has been selection for a male or female- specific allele on the chromosome that carries the gene that specifies that sex.
These genes could have acted as the sex-specific gene that drove selection for the loss of recombination with the sex-specific member of the sex pair Rice ; Charlesworth Another hypothesis is that these chromosomes happen to occupy adjacent positions in the interphase nucleus in all amniotes. This could make their physical fusion and translocation more likely, as seems to be the case for translocations in cancer Othman et al. Chromosome painting shows that chromosomes occupy highly conserved territories both in somatic cells of mammals and birds Tanabe et al.
The positions of these territories are related to the gene content of chromosomes, and sex chromosomes, having a low gene density, are more frequently at the periphery. The paucity of genes on sex chromosomes appears to remain a property of ex-sex chromosomes, as we have discussed. It is also apparent that the interphase position of chromosomes is related to their epigenetic state, which may have relevance to dosage compensation of sex chromosomes, at least in therian mammals, although evidently not for snakes and birds McQueen et al.
Cremer and M. Cremer ; Wolf and Bryk ; Vicoso et al. The original bird-like sex chromosome of a mammal ancestor may have undergone serial translocations with the chromosomes in closest proximity, forming X 1 , X 2 , and X 3 in a monotreme ancestor. It is interesting that platypus chromosome 6, the homologue of the mammalian XCR, lies adjacent to the sex chromosome chain at meiosis Cortez et al. Perhaps this relationship was also important for the choice of this autosome as the therian sex chromosome MYA.
We know that there are several genes that are sex determining in one species, but not in others. The expectation is that these genes have been independently recruited to head the sex-determining pathway in different species, where each is necessary and sufficient for sex determination.
Is there an alternative whereby 2 sex-determining genes must act in concert? Most genes that are sex determining in one species are part of the conserved sex-determining network in all lineages. For instance, DMRT1 , although it does not initiate sex determination in mammals or snakes, is essential for testis stabilization, and AMH , although it is not sex determining in therian mammals or birds, is essential for male development.
Other sex-determining genes arose from transcription factors or growth factors that were recruited to a novel sex-determining role. Is it possible that the biochemical interaction of the products of these genes to bring about sex determination is facilitated by their physical proximity? There is no evidence that this is so. Indeed, transgenesis and knockouts imply the exact opposite; that SRY , by itself is male determining in mammals Koopman et al.
There are many changes that occur to gene content once an autosomal pair becomes a sex chromosome pair. Not only is there mass deletion, and selection of sex-specific traits on the sex-specific chromosome Y or W , but there are also changes in the gene content of the partner sex chromosome X or Z that reflect its hemizygous state in one sex. For instance, the mammal X has accumulated and amplified testis antigen genes and other genes involved in reproduction as well as intelligence.
The chicken Z has also accumulated genes involved in female reproduction Mank As we have discussed, this altered gene content remains a property of ex-sex chromosomes for millions of years. It is hard to see how such changes in gene content of an ancestral sex chromosome predispose regions of it to become sex chromosomes in different lineages.
However, particular sequences such as ribosomal RNA genes may play some part in sex chromosome regulation. Several mammalian sex chromosome pairs e. It has been observed that platypus sex chromosomes are frequently arrayed around the nucleolus during meiosis, which brings them into close proximity to the NOR-bearing chromosome 6, the homologue of the human XCR. The NOR may also be important in rearrangements that create novel sex chromosomes.
Our 2 color fluorescence in situ hybridization mapping of the NOR along with bacterial artificial chromosome BAC clones derived from ZW sex microchromosomes in bearded dragon lizard revealed that the sex chromosome-derived BAC clone contains repeats shared with the region adjacent to NOR repeat location in chromosome 2. This led us to hypothesize that the sex microchromosomes in this species may have arisen by fission adjacent to NOR near the telomere of chromosome 2 and later fusion with a proto microchromosome.
These rearrangements provide evidence that the bearded dragon ZW pair once shared a common ancestry with squamate chromosome 2 Ezaz et al. Another possibility is that the behavior of sex chromosomes may relate to their content of repetitive sequence. Human and mouse X chromosomes have been enriched with long interspersed nuclear elements LINEs that are thought to act in transmitting epigenetic silencing on the inactive X Lyon CTCF sequences are highly conserved epigenetic regulators Hore et al.
Rather than look for an explanation for shared synteny in novel sex-determining genes, or in the altered gene or repeat content of sex chromosomes, perhaps we must look more generally at the properties of sex chromosomes as a whole. Are there changes in properties of chromosomes, for instance reduction of recombination, altered 3D conformation and dosage compensation that make parts of them more likely to become sex-determining regions in descendants?
Recent examination of the 3D architecture of human chromosomes using in situ Hi-C Rao et al. Such 3D interactions appear to be critical for gene expression along chromosomes Dekker and Mirny Although the active X chromosome has a structure similar to that of the autosomes, the inactive X chromosome has a bipartite structure in both human and mouse; 2 massive domains that are separated by a similar hinge sequence Rao et al.
Thus, the 3D structure of the inactive X results from long-range interactions between sequences of the inactive X chromosome. It may be, therefore, that evolution of control sequences such as LINEs and CTCF on sex chromosomes that must be dosage compensated, remain on decommissioned sex chromosomes and predispose regions to become sex chromosomes in other lineages.
The diversity of sex chromosomes among amniotes can be understood as the product of independent evolution of different systems in different lineages, defined by novel sex-determining genes. It is also easy to understand the numerous instances of convergent evolution of sex chromosomes across distantly related taxa if certain genes are particularly adept at taking on a sex-determining role.
However, it is more challenging to explain why nonhomologous regions that are sex determining in one lineage or another are found to share synteny in several different lineages. Although the first example of shared synteny mammal X and bird Z lay on the same chromosome in a salamander Smith and Voss could be dismissed as sheer coincidence, comparative gene mapping and more recently whole genome sequencing, have now turned up other surprising relationships among mammals, birds, turtles, snakes, and lizards.
Does this, after all, constitute evidence that these regions were once linked in a super-sex chromosome that was broken up in different ways in different amniote lineages? The advances in genomics technologies, particularly low-cost next generation sequencing, provide unparalleled opportunities for in-depth analysis of sex chromosomes—and recently decommissioned ex-sex chromosomes—in other amniotes that have recently undergone sex chromosome turnover.
It will be valuable to compare maps and sequences and explore homologies across wider evolutionary distances. It will also be crucial to examine sequences involved in conformation, recombination, and epigenetic regulation of gene dosage of sex chromosomes, and of ex-sex chromosomes.
Combinations of short- and long-read sequencing can also provide chromosome-scale descriptions of repeat landscape of sex chromosomes, providing insights into the origin and degeneration of sex chromosomes, as well evidence of conservation of repetitive sequences on sex chromosomes across taxa.
With ever more genomes being sequenced, these technologies can also provide opportunities to explore and investigate the epigenetic landscape of young and cryptic sex chromosomes, to determine their evolutionary origin as well as explore their stability and functions.
These new sequence information will then provide basis for a high resolution phylogenetic reconstruction, which will combine existing databases such as Ensembl Flicek et al.
This will indeed be required to test the alternative hypotheses raised in this paper. There is particular value in examining animals—reptiles, amphibians, and fish as well as mammals—with atypical sex chromosomes and sex determination, and it is heartening to see the rapid accumulation of data from sex chromosomes from whole groups such as the birds Zhou et al. Oxford University Press is a department of the University of Oxford.
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Sex Chromosome Evolution. Relationships Between Amniote Sex Chromosomes. Sex Chromosome Turnover in Amniotes. Conflict of Interest. Tariq Ezaz. Oxford Academic. Google Scholar. Kornsorn Srikulnath. Jennifer A. Marshall Graves. Address correspondence to Tariq Ezaz at the address above, or e-mail: Tariq. Ezaz canberra. Corresponding editor: Catherine Peichel.
Cite Citation. Permissions Icon Permissions. Abstract The diversity of sex chromosomes among amniotes is the product of independent evolution of different systems in different lineages, defined by novel sex-determining genes. Open in new tab Download slide. The genome of the green anole lizard and a comparative analysis with birds and mammals. Search ADS. Mammalian Y chromosomes retain widely expressed dosage-sensitive regulators.
Evidence for avian cell autonomous sex identity CASI and implications for the sex-determination process? DMRT gene cluster analysis in the platypus: new insights into genomic organization and regulatory regions.
Sequence and gene content of a large fragment of a lizard sex chromosome and evaluation of candidate sex differentiating gene R-spondin 1. The ZW sex microchromosomes of an Australian dragon lizard share no homology with those of other reptiles or birds. Molecular marker suggests rapid changes of sex-determining mechanisms in Australian dragon lizards.
Sex chromosome evolution in lizards: independent origins and rapid transitions. An SRY -related sequence on the marsupial X chromosome: implications for the evolution of the mammalian testis-determining gene. The origin and function of the mammalian Y chromosome and Y-borne genes—an evolving understanding. Are homologies in vertebrate sex determination due to shared ancestry or to limited options? Conservation of chromosome arrangement and position of the X in mammalian sperm suggests functional significance.
In the platypus a meiotic chain of ten sex chromosomes shares genes with the bird Z and mammal X chromosomes. Sex reversal triggers the rapid transition from genetic to temperature-dependent sex. The origin and differentiation process of X and Y chromosomes of the black marsh turtle Siebenrockiella crassicollis , Geoemydidae, Testudines. The ZW micro-sex chromosomes of the Chinese soft-shelled turtle Pelodiscus sinensis , Trionychidae, Testudines have the same origin as chicken chromosome The Staurotypus turtles and aves share the same origin of sex chromosomes but evolved different types of heterogametic sex determination.
In the Super Bowl stings, men who are 31 to 40 led the pack, followed by men who are 21 to When police started Operation Guardian Angel four years ago, most of the arrested men were white. In the Super Bowl stings, about 44 percent of the men were white and the rest were from various ethnic groups, Snyder said.
In recent years, there have been various campaigns online, on billboards and in schools about not buying sex. The group also analyzed whether there was a change in how many people were posting ads selling sex during the Super Bowl. During the 11 days around the Super Bowl, there were 9, ads on multiple sites, compared with 8, during the same time last year. Crazy Credits. Alternate Versions. Rate This. Director: Matthew Modine. Writer: Matthew Modine. Added to Watchlist.
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