X Chromosome Research Articles

The genome sequence of the springtail, Dicyrtomina minuta (O.Fabricius, 1783)

We present a genome assembly from an individual female Dicyrtomina minuta (springtail; Arthropoda; Collembola; Symphypleona; Dicyrtomidae). The genome sequence is 582.0 megabases in span. Most of the assembly is scaffolded into 5 chromosomal pseudomolecules, including the X1 and X2 sex chromosomes. The mitochondrial genome has also been assembled and is 15.59 kilobases in length.

The genome sequence of the Wasp Spider, Argiope bruennichi (Scopoli, 1772).

We present a genome assembly from an individual female Argiope bruennichi (the Wasp Spider; Arthropoda; Arachnida; Araneae; Araneidae). The genome sequence is 1,778.4 megabases in span. Most of the assembly is scaffolded into 13 chromosomal pseudomolecules, including the X 1 and X 2 sex chromosomes. The mitochondrial genome has also been assembled and is 14.06 kilobases in length.

Homeology of sex chromosomes in Amazonian Harttia armored catfishes supports the X-fission hypothesis for the X1X2Y sex chromosome system origin

The Neotropical monophyletic catfish genus Harttia represents an excellent model to study karyotype and sex chromosome evolution in teleosts. Its species split into three phylogenetic clades distributed along the Brazilian territory and they differ widely in karyotype traits, including the presence of standard or multiple sex chromosome systems in some members. Here, we investigate the chromosomal rearrangements and associated synteny blocks involved in the origin of a multiple X1X2Y sex chromosome system present in three out of six sampled Amazonian-clade species. Using 5S and 18S ribosomal DNA fluorescence in situ hybridization and whole chromosome painting with probes corresponding to X1 and X2 chromosomes of X1X2Y system from H. punctata, we confirm previous assumptions that X1X2Y sex chromosome systems of H. punctata, H. duriventris and H. villasboas represent the same linkage groups which also form the putative XY sex chromosomes of H. rondoni. The shared homeology between X1X2Y sex chromosomes suggests they might have originated once in the common ancestor of these closely related species. A joint arrangement of mapped H. punctata X1 and X2 sex chromosomes in early diverging species of different Harttia clades suggests that the X1X2Y sex chromosome system may have formed through an X chromosome fission rather than previously proposed Y-autosome fusion.

The genome sequence of the Autumn Spider, Metellina segmentata (Clerck, 1757).

We present a genome assembly from an individual male Metellina segmentata (the Autumn spider; Arthropoda; Arachnida; Aranae; Tetragnathidae). The genome sequence is 1,665.1 megabases in span. Most of the assembly is scaffolded into 13 chromosomal pseudomolecules, including the X1 and X2 sex chromosomes. The mitochondrial genome has also been assembled and is 17.8 kilobases in length.

The genome sequence of the Common Yellow Sally, Isoperla grammatica (Poda, 1761)

We present a genome assembly from an individual male Isoperla grammatica (the Common Yellow Sally; Arthropoda; Insecta; Plecoptera; Perlodidae). The genome sequence is 874.6 megabases in span. Most of the assembly is scaffolded into 14 chromosomal pseudomolecules, including the assembled X1 and X2 chromosomes. The mitochondrial genome has also been assembled and is 16.2 kilobases in length.

Chromosomal rearrangements and the first indication of an ♀X1 X1 X2 X2 /♂X1 X2 Y sex chromosome system in Rineloricaria fishes (Teleostei: Siluriformes).

Rineloricaria is the most diverse genus within the freshwater fish subfamily Loricariinae, and it is widely distributed in the Neotropical region. Despite limited cytogenetic data, records from southern and south-eastern Brazil suggest a high rate of chromosomal rearrangements in this genus, mirrored in remarkable inter- and intraspecific karyotype variability. In the present work, we investigated the karyotype features of Rineloricaria teffeana, an endemic representative from northern Brazil, using both conventional and molecular cytogenetic techniques. We revealed different diploid chromosome numbers (2n) between sexes (33♂/34♀), which suggests the presence of an ♀X1 X1 X2 X2 /♂X1 X2 Y multiple sex chromosome system. The male-limited Y chromosome was the largest and the only biarmed element in the karyotype, implying Y-autosome fusion as the most probable mechanism behind its origination. C-banding revealed low amounts of constitutive heterochromatin, mostly confined to the (peri)centromeric regions of most chromosomes (including the X2 and the Y) but also occupying the distal regions of a few chromosomal pairs. The chromosomal localization of the 18S ribosomal DNA (rDNA) clusters revealed a single site on chromosome pair 4, which was adjacent to the 5S rDNA cluster. Additional 5S rDNA loci were present on the autosome pair 8, X1 chromosome, and in the presumed fusion point on the Y chromosome. The probe for telomeric repeat motif (TTAGGG)n revealed signals of variable intensities at the ends of all chromosomes except for the Y chromosome, where no detectable signals were evidenced. Male-to-female comparative genomic hybridization revealed no sex-specific or sex-biased repetitive DNA accumulations, suggesting a presumably low level of neo-Y chromosome differentiation. We provide evidence that rDNA sites might have played a role in the formation of this putative multiple sex chromosome system and that chromosome fusions originate through different mechanisms among different Rineloricaria species.

Karyotype differentiation and male meiosis in European clades of the spider genus Pholcus (Araneae, Pholcidae).

Haplogyne araneomorphs are a diverse spider clade. Their karyotypes are usually predominated by biarmed (i.e., metacentric and submetacentric) chromosomes and have a specific sex chromosome system, X1X2Y. These features are probably ancestral for haplogynes. Nucleolus organizer regions (NORs) spread frequently from autosomes to sex chromosomes in these spiders. This study focuses on pholcids (Pholcidae), a highly diverse haplogyne family. Despite considerable recent progress in pholcid cytogenetics, knowledge on many clades remains insufficient including the most species-rich pholcid genus, Pholcus Walckenaer, 1805. To characterize the karyotype differentiation of Pholcus in Europe, we compared karyotypes, sex chromosomes, NORs, and male meiosis of seven species [P.alticeps Spassky, 1932; P.creticus Senglet, 1971; P.dentatus Wunderlich, 1995; P.fuerteventurensis Wunderlich, 1992; P.phalangioides (Fuesslin, 1775); P.opilionoides (Schrank, 1781); P.silvai Wunderlich, 1995] representing the dominant species groups in this region. The species studied show several features ancestral for Pholcus, namely the 2n♂ = 25, the X1X2Y system, and a karyotype predominated by biarmed chromosomes. Most taxa have a large acrocentric NOR-bearing pair, which evolved from a biarmed pair by a pericentric inversion. In some lineages, the acrocentric pair reverted to biarmed. Closely related species often differ in the morphology of some chromosome pairs, probably resulting from pericentric inversions and/or translocations. Such rearrangements have been implicated in the formation of reproductive barriers. While the X1 and Y chromosomes retain their ancestral metacentric morphology, the X2 chromosome shows a derived (acrocentric or subtelocentric) morphology. Pairing of this element is usually modified during male meiosis. NOR patterns are very diverse. The ancestral karyotype of Pholcus contained five or six terminal NORs including three X chromosome-linked loci. The number of NORs has been frequently reduced during evolution. In the Macaronesian clade, there is only a single NOR-bearing pair. Sex chromosome-linked NORs are lost in Madeiran species and in P.creticus. Our study revealed two cytotypes in the synanthropic species P.phalangioides (Madeiran and Czech), which differ by their NOR pattern and chromosome morphology. In the Czech cytotype, the large acrocentric pair was transformed into a biarmed pair by pericentric inversion.

Chromosome number, sex determination, and meiotic chromosome behavior in the praying mantid Hierodula membranacea.

Praying mantids are important models for studying a wide range of chromosome behaviors, yet few species of mantids have been characterized chromosomally. Here we show that the praying mantid Hierodula membranacea has a chromosome number of 2n = 27, and X1X1X2X2 (female): X1X2Y (male) sex determination. In male meiosis I, the X1, X2, and Y chromosomes of H. membranacea form a sex trivalent, with the Y chromosome associating with one spindle pole and the X1 and X2 chromosomes facing the opposite spindle pole. While it is possible that such a sex trivalent could experience different spindle forces on each side of the trivalent, in H. membranacea the sex trivalent aligns at the spindle equator with all of the autosomes, and then the sex chromosomes separate in anaphase I simultaneously with the autosomes. With this observation, H. membranacea can be used as a model system to study the balance of forces acting on a trivalent during meiosis I and analyze the functional importance of chromosome alignment in metaphase as a preparatory step for subsequent correct chromosome segregation.

Identification of Male-Specific Molecular Markers by Recombination of RhoGEF10 Gene in Spotted Knifejaw (Oplegnathus punctatus).

The spotted knifejaw (Oplegnathus punctatus) is a marine economic fish with high ecological value, food value, and fishing value, and its growth has obvious sex dimorphism. The rapid identification of its sex is beneficial to the development of sex determination and breeding. In this study, the method of comparative genomics and PCR amplification was used to further establish a rapid detection method for the recombinant RhoGEF10 gene in O. punctatus, which can quickly, accurately, and efficiently identify the sex of the O. punctatus to be tested. The homologous comparison results of male and female individuals showed that the DNA fragment length of the RhoGEF10 gene on the X1 chromosome was 326 bp, and the DNA fragment length on the Y chromosome was 879 bp. Therefore, it can be concluded that there is an insert fragment of 553 bp on the Y chromosome. PCR amplification results showed that the two DNA fragments of 879 bp and 326 bp were amplified in the Y chromosome and X1 chromosome of the male O. punctatus (X1X2Y), respectively, and the 879 bp fragment was a unique marker fragment of the recombinant RhoGEF10 gene; The female O. punctatus (X1X1X2X2) only a single DNA fragment of 326 bp was amplified. At the same time, the inserted fragment of the male individual resulted in partial inactivation of the RhoGEF10 protein, which in turn resulted in a slowing of peripheral nerve conduction velocity and thinning of the myelin sheath in male O. punctatus. The method shortens the time for accurate identification of the O. punctatus RhoGEF10 gene recombination and improves the detection efficiency. It is of great significance and application value in the research of nerve conduction and myelin development, male and female sex identification, the preparation of high male seedlings, and family selection based on the RhoGEF10 gene in the O. punctatus.

Evolutionary breakpoint regions and chromosomal remodeling in Harttia (Siluriformes: Loricariidae) species diversification.

The Neotropical armored catfish genus Harttia presents a wide variation of chromosomal rearrangements among its representatives. Studies indicate that translocation and Robertsonian rearrangements have triggered the karyotype evolution in the genus, including differentiation of sex chromosome systems. However, few studies used powerful tools, such as comparative whole chromosome painting, to clarify this highly diversified scenario. Here, we isolated probes from the X1 (a 5S rDNA carrier) and the X2 (a 45S rDNA carrier) chromosomes of Harttia punctata, which displays an X1X1X2X2/X1X2Y multiple sex chromosome system. Those probes were applied in other Harttia species to evidence homeologous chromosome blocks. The resulting data reinforce that translocation events played a role in the origin of the X1X2Y sex chromosome system in H. punctata. The repositioning of homologous chromosomal blocks carrying rDNA sites among ten Harttia species has also been demonstrated. Anchored to phylogenetic data it was possible to evidence some events of the karyotype diversification of the studied species and to prove an independent origin for the two types of multiple sex chromosomes, XX/XY1Y2 and X1X1X2X2/X1X2Y, that occur in Harttia species. The results point to evolutionary breakpoint regions in the genomes within or adjacent to rDNA sites that were widely reused in Harttia chromosome remodeling.

The ISWI chromatin remodelling factor NURF is not required for mitotic male X chromosome organisation.

The nucleosome remodelling factor (NURF) is an ISWI-class ATP-dependent chromatin remodeling enzyme required both for gene expression and higher order chromatin organisation. NURF binds to histone modifications that decorate the Drosophila polytene male X chromosome and is required to maintain correct organisation of this chromosome. NURF mutants exhibit distorted and decondensed polytene male X chromosomes dependent on the presence of the male-specific lethal (MSL) complex. Here we tested whether mitotic chromosomes similarly require NURF to maintain correct morphology. Surprisingly, although the MSL complex remains associated with mitotic male X chromosomes, NURF is not required to maintain morphology. While the ISWI subunit of NURF is known to remain associated with mitotic chromosomes we show that the NURF specificity subunit Nurf301/BPTF dissociates from chromatin during both Drosophila and human mitosis, further illuminating that NURF is dispensable for mitotic chromosome organisation.

Candidate SNP-markers altering TBP binding affinity for promoters of the Y-linked genes CDY2A, SHOX, and ZFY are lowering many indexes of reproductive potential in men

Репродуктивный потенциал – уровень физического и психического состояния организма, позволяю- щий при достижении социальной зрелости воспроизводить здоровое потомство. В узком биомедицинском смыс- ле определение включает комплекс функциональных показателей репродуктивной системы, но в более широком смысле его можно рассматривать как совокупность физиологических, поведенческих, адаптивных, ментальных, ан- тропометрических и генетических характеристик особи, способствующих размножению. Целью настоящей работы было расширить область применимости созданного ранее Web-сервиса SNP_TATA_Z-tester для поиска кандидатных маркеров однонуклеотидного полиморфизма (SNP) на хромосоме Y человека, связанных с мужским репродуктив- ным потенциалом (МРП). В поиске кандидатных SNP-маркеров для МРП мы сосредоточились на генах хромосомы Y человека. Изучены 35 SNP в промоторах генов CDY2A, SHOX и ZFY, представляющих все три типа генов хромосомы Y человека: уникальный, псевдоаутосомный и паралог гена хромосомы X человека соответственно. Предсказаны 11 кандидатных SNP-маркеров ослабления МРП из-за изменения сродства TATA-связывающего белка (TBP) к этим промоторам. Выборочно верифицированы in vitro величины сродства «TBP-промотор», предсказанные в этой рабо- те. Установлена достоверная корреляция (r = 0.94, p < 0.005) между ними и результатами измерения in vitro сродства ТВР человека к олигонуклеотидам, идентичным сайтам ТВР-связывания исследуемых промоторов. Проведя поиск в базе данных PubMed по ключевым словам, мы нашли клиническое описание патологических состояний человека, соответствующих изменению экспрессии генов, несущих предсказанные нами кандидатные SNP-маркеры. Среди них оказались такие патологии, как нарушение сперматогенеза (ZFY: rs1388535808 и rs996955491), задержка поло- вого созревания (CDY2A: rs200670724), нарушения эмбриогенеза (SHOX: rs28378830) и непропорционально низкий рост с деформациями Маделунга (SHOX: rs1452787381). Они свидетельствуют, что в случае SNP-промоторов генов хромосомы Y человека следует ожидать изменений широкого круга показателей МРП, выходящих далеко за рамки генетического контроля собственно мужской репродуктивной функции.

How a Factor on the X Chromosome May Offer Resilience to Alzheimer's for Women

How a Factor on the X Chromosome May Offer Resilience to Alzheimer's for Women

Clinical features and SLC6A8 gene mutations of cerebral creatine deficiency syndrome I: an analysis of two families

This article reports the clinical and genetic features of two cases of cerebral creatine deficiency syndrome I (CCDSI) caused by SLC6A8 gene mutations. Both children were boys. Boy 1 (aged 2 years and 10 months) and Boy 2 (aged 8 years and 11 months) had the clinical manifestations of delayed mental and motor development, and convulsion. Their older brothers had the same symptoms. The mother of the boy 1 had mild intellectual disability. The genetic analysis showed two novel homozygous mutations, c.200G>A(p.Gly67Asp) and c.626_627delCT(p.Pro209Argfs*87), in the SLC6A8 gene on the X chromosome, both of which came from their mothers. These two novel mutations were rated as possible pathogenic mutations and were not reported in the literature before. This study expands the mutation spectrum of the SLC6A8 gene and has great significance in the diagnosis of boys with delayed development, and epilepsy.

Pathogenic copy number variation and clinical phenotype in children with neurodevelopment disorders

Objective To analyze the microdeletion and microduplication characteristics of pathogenic copy number variations (pCNVs) and clinical phenotypes in children with neurodevelopmental disorders, and to clarify the genetic pathogenic cause of children with neurodevelopmental disorders. Methods Children who were identified as neurodevelopment disorders such as global developmental delay and mental disorder, by next generation sequencing-based whole genomic copy number variation testing from January 2017 to November 2019 at the First Affiliated Hospital of Anhui Medical University were enrolled, and the clinical phenotypes and pCNVs were reviewed analyzed. Results There were 36 pCNVs in total 31 children, consisting of 24 microdeletion segments (66.67%)and 12 microduplication segments (33.33%), with sizes ranging from 320.00 kb to 93.26 Mb (mean 11.33 Mb). pCNVs frequently occurred in chromosome 15 , chromosome 8 and chromosome X, there were 9 children with 9 pCNVs in chromosome 15(25.00%), 3 children with 5 pCNVs in chromosome 8(13.89%)and 3 children with 4 pCNVs in chromosome X(11.11%) .The mainly clinical manifestations were motor disorder (30 children, 96.77%), mental disorder (22 children, 70.97%), speech development delay(22 children, 70.97% )accompanied by the malformation(11 children, 35.48%), abnormal face(11 children, 35.48%) and epilepsy(8 children, 25.81%), multisystem abnormalities generally exist in one individual. Conclusion This study demonstrates the clinical utility of whole genome CNVs testing in the genetic diagnosis of children with neurodevelopment disorders.Genetic pathogenesis of children with neurodevelopmental disorders can be revealed by the analysis of pCNVs. Key words: Neurodevelopmental disorder; Pathogenic copy number variation; Child

First detection of the hemizygote frameshift variant of the DMD gene in a 13-year-old patient affected by dystrophinopathy (Duchenne DMD and Becker BMD) at Saint Camille Hospital of Ouagadougou, Burkina Faso: Case report

Genetic diseases are poorly reported in sub-Saharan Africa, especially in Burkina Faso. The reasons for this reality are multifactorial including, the difficulty of diagnostic confirmation, financial accessibility and even the difficulty with referral of cases by medical staff. Genetic diseases, although relatively rare, exist in families and deserve special attention in our paraclinical assessments. Few cases can be diagnosed in sub-Saharan Africa. The clinical case we are reporting here is a dystrophynopathy by mutation of the Duchenne muscular dystrophy (DMD) gene. This is the first confirmed detection of a frameshift mutation in the DMD gene in a boy received at Saint Camille Hospital in Ouagadougou, Burkina Faso. This is a 13-year-old MR boy, from a family of four siblings, all male, from the eastern region of Burkina Faso. The boy had a clinical picture of myopathy with difficulty in walking, frequent falls, myogenic syndrome with stool sign, Gowers sign and scapula alata, all leading to a suspicion of dystrophinopathy with a request for genetic analysis. The DMD gene responsible for the disease is located on the X chromosome (Xp21.2-p21.1). The study of the dystrophin gene (DMD) was done using three methods, namely MLPA, high throughput sequencing and Sanger sequencing. The results led to the identification of a frameshift mutation of exon 71 in the DMD gene: it is a hemizygotic variant with ribosomal shift of the DMD gene NM_004006.2 (DMD): c.10258del p.(Ser3420Leufs*25). This clinical case led for the first time in Burkina Faso to the confirmed diagnosis of hereditary muscular dystrophy resulting from a mutation with a frameshift in exon 71 of the DMD gene in the hemizygotic state in a 13-year-old boy, a student and the eldest sibling of 4 boys, three of whom have myopathy. Key words: Mutation, Duchenne muscular dystrophy (DMD) gene, dystrophinopathy, duchenne versus becker, case report.

Development of a PCR-based genetic sex identification method in spinyhead croaker (Collichthys lucidus)

Spinyhead croaker (Collichthys lucidus) is a commercially important marine sciaenid fish, exhibiting sexual dimorphism in growth, and being of a special multiple sex system X1X1X2X2/X1X2Y. In the present study, we developed the first PCR-based method for identifying the genetic sex in spinyhead croaker with a next generation sequencing (NGS)-based approach. After whole genome resequencing was performed on 10 individuals and 2 pools for each sex, approximately 404 G clean data and 2,857,406 high quality SNPs were obtained. With genome-wide association analysis (GWAS), 420 SNPs on 8 chromosomes were identified as sex significantly associated loci. Most of the sex associated loci aggregated on Chr. 1 and Chr. 7, suggesting that they might be the X1 and X2 chromosome. On the segment of Chr. 7 that aggregated sex associated SNPs, three candidate male specific deletions were detected by comparing the sequencing depth between sexes. Based on one of the putative male specific deletions (68 bp), a pair of primers for sex identification were designed and validated with PCR. The primers were applicable to ND and JR populations belonging to the southern group, but not to ZS population belonging the northern group. The methods for sex identification developed in the present study along with its limited versatility provided a necessary tool and important clues for deciphering the sex determination mechanism in spinyhead croaker.

Lineage specification and pluripotency revealed by transcriptome analysis from oocyte to blastocyst in pig.

The inner cell mass (ICM) in blastocyst is the origin of all somatic and germ cells in mammals and pluripotent stem cells (PSCs) in vitro. As the conserved principles between pig and human, here we performed comprehensive single-cell RNA-seq for porcine early embryos from oocyte to early blastocyst (EB). We show the specification of the ICM and trophectoderm in morula and the molecular signature of the precursors. We demonstrate the existence of naïve pluripotency signature in morula and ICM of EB, and the specific pluripotent genes and the activity of signalling pathways highlight the characteristics of the naïve pluripotency. We observe the absence of dosage compensation with respect to X-chromosome (XC) in morula, and incomplete dosage compensation in the EB. However, the dynamics of dosage compensation may be independent of the expression of XIST induced XC inactivation. Our study describes molecular landmarks of embryogenesis in pig that will provide a better strategy for derivation of porcine PSCs and improve research in regenerative medicine.

Identification of a deletion variant in exon 9 of iduronate-2-sulfatase gene in patients with type II mucopolysaccharidosis

Objective: Mucopolysaccharidosis type II (MPS II) or Hunter syndrome is a lysosomal storage disorder caused by mutation of the iduronate-2-sulfatase (IDS) gene, which is located on chromosome X. The profile of IDS gene at exon 9 has not been previously studied in Indonesian patients. The objective of this study was to detect and analyze mutations in exon 9 of the IDS gene in MPS II patients from Indonesia. Subjects and Methods: DNA from 10 MPS II patients from Indonesia was analyzed along with 50 healthy individuals, both male and female, which formed the control group. DNA isolation, polymerase chain reaction amplification, electrophoresis, and sequencing were performed for the analysis. Results: The IDS gene was successfully analyzed for all samples. A DNA base deletion at position c.1549delATC was found in an MPS II patient. Conclusions: This IDS gene variant is novel. Further research would be necessary to detect other IDS gene variants, with mutations at other exons, in the Indonesian MPS II patients.

Comparative Cytogenetics and Neo-Y Formation in Small-Sized Fish Species of the Genus Pyrrhulina (Characiformes, Lebiasinidae).

Although fishes have traditionally been the subject of comparative evolutionary studies, few reports have concentrated on the application of multipronged modern molecular cytogenetic techniques (such as comparative genomic hybridization = CGH and whole chromosome painting = WCP) to analyze deeper the karyotype evolution of specific groups, especially the historically neglected small-sized ones. Representatives of the family Lebiasinidae (Characiformes) are a notable example, where only a few cytogenetic investigations have been conducted thus far. Here, we aim to elucidate the evolutionary processes behind the karyotype differentiation of Pyrrhulina species on a finer-scale cytogenetic level. To achieve this, we applied C-banding, repetitive DNA mapping, CGH and WCP in Pyrrhulina semifasciata and P. brevis. Our results showed 2n = 42 in both sexes of P. brevis, while the difference in 2n between male and female in P. semifasciata (♂41/♀42) stands out due to the presence of a multiple X1X2Y sex chromosome system, until now undetected in this family. As a remarkable common feature, multiple 18S and 5S rDNA sites are present, with an occasional synteny or tandem-repeat amplification. Male-vs.-female CGH experiments in P. semifasciata highlighted the accumulation of male-enriched repetitive sequences in the pericentromeric region of the Y chromosome. Inter-specific CGH experiments evidenced a divergence between both species’ genomes based on the presence of several species-specific signals, highlighting their inner genomic diversity. WCP with the P. semifasciata-derived Y (PSEMI-Y) probe painted not only the entire metacentric Y chromosome in males but also the X1 and X2 chromosomes in both male and female chromosomes of P. semifasciata. In the cross-species experiments, the PSEMI-Y probe painted four acrocentric chromosomes in both males and females of the other tested Pyrrhulina species. In summary, our results show that both intra- and interchromosomal rearrangements together with the dynamics of repetitive DNA significantly contributed to the karyotype divergence among Pyrrhulina species, possibly promoted by specific populational and ecological traits and accompanied in one species by the origin of neo-sex chromosomes. The present results suggest how particular evolutionary scenarios found in fish species can help to clarify several issues related to genome organization and the karyotype evolution of vertebrates in general.