Most cited article - PubMed ID 36208359
Sex chromosome differentiation via changes in the Y chromosome repeat landscape in African annual killifishes Nothobranchius furzeri and N. kadleci
Sex chromosomes have evolved repeatedly across eukaryotes. The emergence of a sex-determining (SD) locus is expected to progressively restrict recombination, driving convergent molecular differentiation. However, evidence from taxa like teleost fishes, representing over half of vertebrate species with unmatched diversity in SD systems, challenges this model. Teleost sex chromosomes are often difficult to detect as they experience frequent turnovers, resetting the differentiation process. Nothobranchius killifishes, which include the XY system shared by N. furzeri and N. kadleci and X1X2Y systems in six other species, offer a valuable model to study sex chromosome turnovers. We characterised X1X2Y systems in five killifish species and found that sex chromosomes evolved at least four times independently. Sex-determining regions resided near centromeres or predicted chromosome rearrangement breakpoints in N. brieni and N. guentheri, suggesting recombination cold spots may facilitate sex chromosome evolution. Chromosomes representing the XY system in N. furzeri/N. kadleci were sex-linked also in the outgroup Fundulosoma thierryi, with several genes, including gdf6, residing in the region of differentiation. Although the X1X2Y systems of N. guentheri, N. lourensi (both Coastal clade), and N. brieni (Kalahari clade) involved different chromosomes, they shared a potential SD region. We uncovered two sex-linked evolutionary strata of distinct age in N. guentheri. However, its potential SD gene amhr2 was located in the younger stratum and is hence unlikely to be the ancestral SD gene in this lineage. Our findings suggest recombination landscapes shape sex chromosome turnover and that certain synteny blocks are repeatedly co-opted as sex chromosomes in killifishes.
- Keywords
- bacterial artificial chromosome, chromosome fusion, pool‐seq, recombination suppression, sex chromosome differentiation, zoo‐FISH,
- MeSH
- Killifishes * genetics MeSH
- Phylogeny MeSH
- Evolution, Molecular * MeSH
- Sex Chromosomes * genetics MeSH
- Sex Determination Processes * genetics MeSH
- Recombination, Genetic MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
BACKGROUND: Java combtail fish Belontia hasselti (Cuvier, 1831), a member of the Osphronemidae family, inhabits lakes and rivers throughout Southeast Asia and Sri Lanka. Previous cytogenetic research revealed it possesses a diploid chromosome number of 48 chromosomes with a female-heterogametic ZZ/ZW sex chromosome system, where the W chromosome is distinguishable as the only metacentric element in the complement. Female-heterogametic sex chromosome systems seem to be otherwise surprisingly rare in the highly diverse order Perciformes and, therefore, B. hasselti provides an important comparative model to evolutionary studies in this teleost lineage. To examine the level of sex chromosome differentiation in B. hasselti and the contribution of repetitive DNAs to this process we combined bioinformatic analyses with chromosomal mapping of selected repetitive DNA classes, and comparative genomic hybridization. RESULTS: By providing the first satellitome study in Perciformes, we herein identified 13 satellite DNA monomers in B. hasselti, suggesting a very low diversity of satDNA in this fish species. Using fluorescence in situ hybridization, we revealed detectable clusters on chromosomes only for four satellite DNA monomers. Together with the two mapped microsatellite motifs, the repeats primarily accumulated on autosomes, with no distinct clusters located on the sex chromosomes. Comparative genomic hybridization showed no region with accumulated female-specific or enriched repeats on the W chromosome. Telomeric repeats terminated all chromosomes, and no additional interstitial sites were detected. CONCLUSION: These data collectively indicate a low degree of sex chromosome differentiation in B. hasselti despite their considerable heteromorphy. Possible mechanisms that may underlie this pattern are discussed.
- Keywords
- Fishes, Isochromosome, Molecular cytogenetics, Satellitome, Sex chromosome evolution, Teleostei,
- MeSH
- In Situ Hybridization, Fluorescence MeSH
- Chromosome Mapping MeSH
- Microsatellite Repeats MeSH
- Perciformes * genetics MeSH
- Sex Chromosomes * genetics MeSH
- Repetitive Sequences, Nucleic Acid * MeSH
- DNA, Satellite genetics MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- DNA, Satellite MeSH
BACKGROUND/OBJECTIVES: Arachnids are a megadiverse arthropod group. The present study investigated the chromosomes of pedipalpid tetrapulmonates (orders Amblypygi, Thelyphonida, Schizomida) and two arachnid orders of uncertain phylogenetic placement, Ricinulei and Solifugae, to reconstruct their karyotype evolution. Except for amblypygids, the cytogenetics of these arachnid orders was almost unknown prior to the present study. METHODS: Chromosomes were investigated using methods of standard (Giemsa-stained preparations, banding techniques) and molecular cytogenetics (fluorescence in situ hybridization, comparative genomic hybridization). RESULTS AND CONCLUSIONS: New data for 38 species, combined with previously published data, suggest that ancestral arachnids possessed low to moderate 2n (22-40), monocentric chromosomes, one nucleolus organizer region (NOR), low levels of heterochromatin and recombinations, and no or homomorphic sex chromosomes. Karyotypes of Pedipalpi and Solifugae diversified via centric fusions, pericentric inversions, and changes in the pattern of NORs and, in solifuges, also through tandem fusions. Some solifuges display an enormous amount of constitutive heterochromatin and high NOR number. It is hypothesized that the common ancestor of amblypygids, thelyphonids, and spiders exhibited a homomorphic XY system, and that telomeric heterochromatin and NORs were involved in the evolution of amblypygid sex chromosomes. The new findings support the Cephalosomata clade (acariforms, palpigrades, and solifuges). Hypotheses concerning the origin of acariform holocentric chromosomes are presented. Unlike current phylogenetic hypotheses, the results suggest a sister relationship between Schizomida and a clade comprising other tetrapulmonates as well as a polyploidization in the common ancestor of the clade comprising Araneae, Amblypygi, and Thelyphonida.
- Keywords
- Ricinulei, heterochromatin, holocentric, nucleolus organizer region, polyploidy, sex chromosome, solifuge, somatic pairing, spider, telomere,
- MeSH
- Phylogeny MeSH
- In Situ Hybridization, Fluorescence MeSH
- Karyotype * MeSH
- Karyotyping MeSH
- Evolution, Molecular * MeSH
- Arachnida * genetics classification MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
Zoraptera (also called "angel insects") is one of the most unexplored insect orders. However, it holds promise for understanding the evolution of insect karyotypes and genome organization given its status as an early branching group of Polyneoptera and Pterygota (winged insects) during the Paleozoic. Here, we provide karyotype descriptions of three Zorapteran species: Brazilozoros huxleyi (2n♂; ♀ = 42; 42), B. kukalovae (2n♂; ♀ = 43; 44) and Latinozoros cacaoensis (2n♂; ♀ = 36; 36). These species represent two of the four recently recognized Zorapteran subfamilies. Contrary to an earlier suggestion that Zoraptera has holocentric chromosomes, we found karyotypes that were always monocentric. Interestingly, we detected both X0 (B. kukalovae) and XY (B. huxleyi, L. cacaoensis) sex chromosome systems. In addition to conventional karyotype descriptions, we applied fluorescent in situ hybridization for the first time in Zoraptera to map karyotype distributions of 18S rDNA, histone H3 genes, telomeres and (CAG)n and (GATA)n microsatellites. This study provides a foundation for cytogenetic research in Zoraptera.
- Keywords
- Karyotype, Microsatellites, Sex chromosomes, Telomere, rDNA,
- MeSH
- Chromosomes, Insect * genetics MeSH
- Cytogenetics methods MeSH
- Histones genetics MeSH
- Insecta genetics classification MeSH
- In Situ Hybridization, Fluorescence MeSH
- Karyotype * MeSH
- Microsatellite Repeats genetics MeSH
- Evolution, Molecular MeSH
- Sex Chromosomes genetics MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Comparative Study MeSH
- Names of Substances
- Histones MeSH
Multiple sex chromosomes usually arise from chromosomal rearrangements which involve ancestral sex chromosomes. There is a fundamental condition to be met for their long-term fixation: the meiosis must function, leading to the stability of the emerged system, mainly concerning the segregation of the sex multivalent. Here, we sought to analyze the degree of differentiation and meiotic pairing properties in the selected fish multiple sex chromosome system present in the wolf-fish Hoplias malabaricus (HMA). This species complex encompasses seven known karyotype forms (karyomorphs) where the karyomorph C (HMA-C) exhibits a nascent XY sex chromosomes from which the multiple X1X2Y system evolved in karyomorph HMA-D via a Y-autosome fusion. We combined genomic and cytogenetic approaches to analyze the satellite DNA (satDNA) content in the genome of HMA-D karyomorph and to investigate its potential contribution to X1X2Y sex chromosome differentiation. We revealed 56 satDNA monomers of which the majority was AT-rich and with repeat units longer than 100 bp. Seven out of 18 satDNA families chosen for chromosomal mapping by fluorescence in situ hybridization (FISH) formed detectable accumulation in at least one of the three sex chromosomes (X1, X2 and neo-Y). Nine satDNA monomers showed only two hybridization signals limited to HMA-D autosomes, and the two remaining ones provided no visible FISH signals. Out of seven satDNAs located on the HMA-D sex chromosomes, five mapped also to XY chromosomes of HMA-C. We showed that after the autosome-Y fusion event, the neo-Y chromosome has not substantially accumulated or eliminated satDNA sequences except for minor changes in the centromere-proximal region. Finally, based on the obtained FISHpatterns, we speculate on the possible contribution of satDNA to sex trivalent pairing and segregation.
- Keywords
- FISH, Meiosis, Multiple sex chromosomes, Satellitome, Sex trivalent,
- MeSH
- Characiformes * genetics MeSH
- Y Chromosome genetics MeSH
- In Situ Hybridization, Fluorescence * MeSH
- Karyotype MeSH
- Meiosis genetics MeSH
- Evolution, Molecular MeSH
- Sex Chromosomes * genetics MeSH
- DNA, Satellite * genetics MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- DNA, Satellite * MeSH
Satellite DNA (satDNA) is a rapidly evolving class of tandem repeats, with some monomers being involved in centromere organization and function. To identify repeats associated with (peri)centromeric regions, we investigated satDNA across Southern and Coastal clades of African annual killifishes of the genus Nothobranchius. Molecular cytogenetic and bioinformatic analyses revealed that two previously identified satellites, designated here as NkadSat01-77 and NfurSat01-348, are associated with (peri)centromeres only in one lineage of the Southern clade. NfurSat01-348 was, however, additionally detected outside centromeres in three members of the Coastal clade. We also identified a novel satDNA, NrubSat01-48, associated with (peri)centromeres in N. foerschi, N. guentheri, and N. rubripinnis. Our findings revealed fast turnover of satDNA associated with (peri)centromeres and different trends in their evolution in two clades of the genus Nothobranchius.
- Keywords
- Centromere drive, Constitutive heterochromatin, RepeatExplorer, Repetitive sequences, satDNA,
- MeSH
- Centromere genetics MeSH
- Killifishes * genetics MeSH
- Fundulidae * genetics MeSH
- Evolution, Molecular MeSH
- DNA, Satellite MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- DNA, Satellite MeSH
The remarkable fish biodiversity encompasses also great sex chromosome variability. Harttia catfish belong to Neotropical models for karyotype and sex chromosome research. Some species possess one of the three male-heterogametic sex chromosome systems, XY, X1X2Y or XY1Y2, while other members of the genus have yet uncharacterized modes of sex determination. Particularly the XY1Y2 multiple sex chromosome system shows a relatively low incidence among vertebrates, and it has not been yet thoroughly investigated. Previous research suggested two independent X-autosome fusions in Harttia which led to the emergence of XY1Y2 sex chromosome system in three of its species. In this study, we investigated evolutionary trajectories of synteny blocks involved in this XY1Y2 system by probing six Harttia species with whole chromosome painting (WCP) probes derived from the X (HCA-X) and the chromosome 9 (HCA-9) of H. carvalhoi. We found that both painting probes hybridize to two distinct chromosome pairs in Amazonian species, whereas the HCA-9 probe paints three chromosome pairs in H. guianensis, endemic to Guyanese drainages. These findings demonstrate distinct evolutionary fates of mapped synteny blocks and thereby elevated karyotype dynamics in Harttia among the three evolutionary clades.
- Keywords
- WCP, chromosomal rearrangements, evolution, karyotype, microdissection,
- Publication type
- Journal Article MeSH
The karyotype differentiation of the twelve known members of the Nothobranchiusugandensis Wildekamp, 1994 species group is reviewed and the karyotype composition of seven of its species is described herein for the first time using a conventional cytogenetic protocol. Changes in the architecture of eukaryotic genomes often have a major impact on processes underlying reproductive isolation, adaptation and diversification. African annual killifishes of the genus Nothobranchius Peters, 1868 (Teleostei: Nothobranchiidae), which are adapted to an extreme environment of ephemeral wetland pools in African savannahs, feature extensive karyotype evolution in small, isolated populations and thus are suitable models for studying the interplay between karyotype change and species evolution. The present investigation reveals a highly conserved diploid chromosome number (2n = 36) but a variable number of chromosomal arms (46-64) among members of the N.ugandensis species group, implying a significant role of pericentric inversions and/or other types of centromeric shift in the karyotype evolution of the group. When superimposed onto a phylogenetic tree based on molecular analyses of two mitochondrial genes the cytogenetic characteristics did not show any correlation with the phylogenetic relationships within the lineage. While karyotypes of many other Nothobranchius spp. studied to date diversified mainly via chromosome fusions and fissions, the N.ugandensis species group maintains stable 2n and the karyotype differentiation seems to be constrained to intrachromosomal rearrangements. Possible reasons for this difference in the trajectory of karyotype differentiation are discussed. While genetic drift seems to be a major factor in the fixation of chromosome rearrangements in Nothobranchius, future studies are needed to assess the impact of predicted multiple inversions on the genome evolution and species diversification within the N.ugandensis species group.
- Keywords
- 2n uniformity, chromosome evolution, chromosome inversion, chromosomes, cytogenetics, karyotype variability,
- Publication type
- Journal Article MeSH