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Tracking the evolutionary pathway of sex chromosomes among fishes: characterizing the unique XX/XY1Y2 system in Hoplias malabaricus (Teleostei, Characiformes)

de Oliveira, EzequielAguiar, Sember, Alexandr, Bertollo, LuizAntonio Carlos, Yano, CassiaFernanda, Ezaz, Tariq, Moreira-Filho, Orlando, Hatanaka, Terumi, Trifonov, Vladimir, Liehr, Thomas, Al-Rikabi, AhmedBasheer Hamid, Ráb, Petr, Pains, Hugmar, Cioffi, Marcelode Bello
Chromosoma 2018 v.127 no.1 pp. 115-128
Hoplias malabaricus, chromosome banding, chromosome painting, comparative genomic hybridization, evolution, fish, karyotyping, microsatellite repeats, ribosomal DNA, sex chromosomes, telomeres
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.