Tracking the evolutionary pathway of sex chromosomes among fishes: characterizing the unique XX/XY1Y2system in Hoplias malabaricus (Teleostei, Characiformes)

Ezequiel Aguiar de Oliveira, Alexandr Sember, Luiz Antonio C. Bertollo, Cassia Fernanda Yano, T. Ezaz, Orlando Moreira-Filho, Terumi Hatanaka, Vladimir Trifonov, Thomas Liehr, Ahmed Basheer Hamid Al-Rikabi, Petr Ráb, Hugmar Pains, Marcelo de Bello Cioffi

Research output: Contribution to journalArticle

12 Citations (Scopus)

Abstract

The Neotropical fish, Hoplias malabaricus, is one of the most cytogenetically studied fish taxon with seven distinct karyomorphs (A–G) comprising varying degrees of sex chromosome differentiation, ranging from homomorphic to highly differentiated simple and multiple sex chromosomes. Therefore, this fish offers a unique opportunity to track evolutionary mechanisms standing behind the sex chromosome evolution and differentiation. Here, we focused on a high-resolution cytogenetic characterization of the unique XX/XY1Y2 multiple sex chromosome system found in one of its karyomorphs (G). For this, we applied a suite of conventional (Giemsa-staining, C-banding) and molecular cytogenetic approaches, including fluorescence in situ hybridization FISH (with 5S and 18S rDNAs, 10 microsatellite motifs and telomeric (TTAGGG)n sequences as probes), comparative genomic hybridization (CGH), and whole chromosome painting (WCP). In addition, we performed comparative analyses with other Erythrinidae species to discover the evolutionary origin of this unique karyomorph G-specific XY1Y2 multiple sex chromosome system. WCP experiments confirmed the homology between these multiple sex chromosomes and the nascent XX/XY sex system found in the karyomorph F, but disproved a homology with those of karyomorphs A–D and other closely related species. Besides, the putative origin of such XY1Y2 system by rearrangements of several chromosome pairs from an ancestral karyotype was also highlighted. In addition, clear identification of a male-specific region on the Y1 chromosome suggested a differential pattern of repetitive sequences accumulation. The present data suggested the origin of this unique XY1Y2 sex system, revealing evidences for the high level of plasticity of sex chromosome differentiation within the Erythrinidae.
Original languageEnglish
Pages (from-to)115-128
Number of pages14
JournalChromosoma
Volume127
Issue number1
DOIs
Publication statusPublished - Mar 2018

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Characiformes
Sex Chromosomes
Fishes
Sex Differentiation
Chromosome Painting
Cytogenetics
Chromosomes
Comparative Genomic Hybridization
Nucleic Acid Repetitive Sequences
Ribosomal DNA
Fluorescence In Situ Hybridization
Karyotype
Microsatellite Repeats
Staining and Labeling

Cite this

de Oliveira, Ezequiel Aguiar ; Sember, Alexandr ; Bertollo, Luiz Antonio C. ; Yano, Cassia Fernanda ; Ezaz, T. ; Moreira-Filho, Orlando ; Hatanaka, Terumi ; Trifonov, Vladimir ; Liehr, Thomas ; Al-Rikabi, Ahmed Basheer Hamid ; Ráb, Petr ; Pains, Hugmar ; de Bello Cioffi, Marcelo. / Tracking the evolutionary pathway of sex chromosomes among fishes: characterizing the unique XX/XY1Y2system in Hoplias malabaricus (Teleostei, Characiformes). In: Chromosoma. 2018 ; Vol. 127, No. 1. pp. 115-128.
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title = "Tracking the evolutionary pathway of sex chromosomes among fishes: characterizing the unique XX/XY1Y2system in Hoplias malabaricus (Teleostei, Characiformes)",
abstract = "The Neotropical fish, Hoplias malabaricus, is one of the most cytogenetically studied fish taxon with seven distinct karyomorphs (A–G) comprising varying degrees of sex chromosome differentiation, ranging from homomorphic to highly differentiated simple and multiple sex chromosomes. Therefore, this fish offers a unique opportunity to track evolutionary mechanisms standing behind the sex chromosome evolution and differentiation. Here, we focused on a high-resolution cytogenetic characterization of the unique XX/XY1Y2 multiple sex chromosome system found in one of its karyomorphs (G). For this, we applied a suite of conventional (Giemsa-staining, C-banding) and molecular cytogenetic approaches, including fluorescence in situ hybridization FISH (with 5S and 18S rDNAs, 10 microsatellite motifs and telomeric (TTAGGG)n sequences as probes), comparative genomic hybridization (CGH), and whole chromosome painting (WCP). In addition, we performed comparative analyses with other Erythrinidae species to discover the evolutionary origin of this unique karyomorph G-specific XY1Y2 multiple sex chromosome system. WCP experiments confirmed the homology between these multiple sex chromosomes and the nascent XX/XY sex system found in the karyomorph F, but disproved a homology with those of karyomorphs A–D and other closely related species. Besides, the putative origin of such XY1Y2 system by rearrangements of several chromosome pairs from an ancestral karyotype was also highlighted. In addition, clear identification of a male-specific region on the Y1 chromosome suggested a differential pattern of repetitive sequences accumulation. The present data suggested the origin of this unique XY1Y2 sex system, revealing evidences for the high level of plasticity of sex chromosome differentiation within the Erythrinidae.",
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de Oliveira, EA, Sember, A, Bertollo, LAC, Yano, CF, Ezaz, T, Moreira-Filho, O, Hatanaka, T, Trifonov, V, Liehr, T, Al-Rikabi, ABH, Ráb, P, Pains, H & de Bello Cioffi, M 2018, 'Tracking the evolutionary pathway of sex chromosomes among fishes: characterizing the unique XX/XY1Y2system in Hoplias malabaricus (Teleostei, Characiformes)', Chromosoma, vol. 127, no. 1, pp. 115-128. https://doi.org/10.1007/s00412-017-0648-3

Tracking the evolutionary pathway of sex chromosomes among fishes: characterizing the unique XX/XY1Y2system in Hoplias malabaricus (Teleostei, Characiformes). / de Oliveira, Ezequiel Aguiar; Sember, Alexandr; Bertollo, Luiz Antonio C.; Yano, Cassia Fernanda; Ezaz, T.; Moreira-Filho, Orlando; Hatanaka, Terumi; Trifonov, Vladimir; Liehr, Thomas; Al-Rikabi, Ahmed Basheer Hamid; Ráb, Petr; Pains, Hugmar; de Bello Cioffi, Marcelo.

In: Chromosoma, Vol. 127, No. 1, 03.2018, p. 115-128.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Tracking the evolutionary pathway of sex chromosomes among fishes: characterizing the unique XX/XY1Y2system in Hoplias malabaricus (Teleostei, Characiformes)

AU - de Oliveira, Ezequiel Aguiar

AU - Sember, Alexandr

AU - Bertollo, Luiz Antonio C.

AU - Yano, Cassia Fernanda

AU - Ezaz, T.

AU - Moreira-Filho, Orlando

AU - Hatanaka, Terumi

AU - Trifonov, Vladimir

AU - Liehr, Thomas

AU - Al-Rikabi, Ahmed Basheer Hamid

AU - Ráb, Petr

AU - Pains, Hugmar

AU - de Bello Cioffi, Marcelo

N1 - cited By 1; Article in Press

PY - 2018/3

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N2 - The Neotropical fish, Hoplias malabaricus, is one of the most cytogenetically studied fish taxon with seven distinct karyomorphs (A–G) comprising varying degrees of sex chromosome differentiation, ranging from homomorphic to highly differentiated simple and multiple sex chromosomes. Therefore, this fish offers a unique opportunity to track evolutionary mechanisms standing behind the sex chromosome evolution and differentiation. Here, we focused on a high-resolution cytogenetic characterization of the unique XX/XY1Y2 multiple sex chromosome system found in one of its karyomorphs (G). For this, we applied a suite of conventional (Giemsa-staining, C-banding) and molecular cytogenetic approaches, including fluorescence in situ hybridization FISH (with 5S and 18S rDNAs, 10 microsatellite motifs and telomeric (TTAGGG)n sequences as probes), comparative genomic hybridization (CGH), and whole chromosome painting (WCP). In addition, we performed comparative analyses with other Erythrinidae species to discover the evolutionary origin of this unique karyomorph G-specific XY1Y2 multiple sex chromosome system. WCP experiments confirmed the homology between these multiple sex chromosomes and the nascent XX/XY sex system found in the karyomorph F, but disproved a homology with those of karyomorphs A–D and other closely related species. Besides, the putative origin of such XY1Y2 system by rearrangements of several chromosome pairs from an ancestral karyotype was also highlighted. In addition, clear identification of a male-specific region on the Y1 chromosome suggested a differential pattern of repetitive sequences accumulation. The present data suggested the origin of this unique XY1Y2 sex system, revealing evidences for the high level of plasticity of sex chromosome differentiation within the Erythrinidae.

AB - The Neotropical fish, Hoplias malabaricus, is one of the most cytogenetically studied fish taxon with seven distinct karyomorphs (A–G) comprising varying degrees of sex chromosome differentiation, ranging from homomorphic to highly differentiated simple and multiple sex chromosomes. Therefore, this fish offers a unique opportunity to track evolutionary mechanisms standing behind the sex chromosome evolution and differentiation. Here, we focused on a high-resolution cytogenetic characterization of the unique XX/XY1Y2 multiple sex chromosome system found in one of its karyomorphs (G). For this, we applied a suite of conventional (Giemsa-staining, C-banding) and molecular cytogenetic approaches, including fluorescence in situ hybridization FISH (with 5S and 18S rDNAs, 10 microsatellite motifs and telomeric (TTAGGG)n sequences as probes), comparative genomic hybridization (CGH), and whole chromosome painting (WCP). In addition, we performed comparative analyses with other Erythrinidae species to discover the evolutionary origin of this unique karyomorph G-specific XY1Y2 multiple sex chromosome system. WCP experiments confirmed the homology between these multiple sex chromosomes and the nascent XX/XY sex system found in the karyomorph F, but disproved a homology with those of karyomorphs A–D and other closely related species. Besides, the putative origin of such XY1Y2 system by rearrangements of several chromosome pairs from an ancestral karyotype was also highlighted. In addition, clear identification of a male-specific region on the Y1 chromosome suggested a differential pattern of repetitive sequences accumulation. The present data suggested the origin of this unique XY1Y2 sex system, revealing evidences for the high level of plasticity of sex chromosome differentiation within the Erythrinidae.

KW - Comparative genomic hybridization

KW - Fish cytogenetics

KW - Male-specific region

KW - Repetitive sequences

KW - Whole chromosome painting

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UR - http://www.mendeley.com/research/tracking-evolutionary-pathway-sex-chromosomes-among-fishes-characterizing-unique-xxxy-1-y-2-system-h

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