Sex Chromosome Evolution and Genomic Divergence in the Fish Hoplias malabaricus (Characiformes, Erythrinidae)

Abstract

The Erythrinidae family (Teleostei: Characiformes) is a small Neotropical fish group with a wide distribution throughout South America, where Hoplias malabaricus corresponds to the most widespread and cytogenetically studied taxon. This species possesses significant genetic variation, as well as huge karyotype diversity among populations, as reflected by its seven major karyotype forms (i.e., karyomorphs A-G) identified up to now. Although morphological differences in their bodies are not outstanding, H. malabaricus karyomorphs are easily identified by differences in 2n, morphology and size of chromosomes, as well as by distinct evolutionary steps of sex chromosomes development. Here, we performed comparative genomic hybridization (CGH) to analyse both the intra- and inter-genomic status in terms of repetitive DNA divergence among all but one (E) H. malabaricus karyomorphs. Our results indicated that they have close relationships, but with evolutionary divergences among their genomes, yielding a range of non-overlapping karyomorph-specific signals. Besides, male-specific regions were uncovered on the sex chromosomes, confirming their differential evolutionary trajectories. In conclusion, the hypothesis that H. malabaricus karyomorphs are result of speciation events was strengthened.

Chromosomal Evolution in Lower Vertebrates: Sex Chromosomes in Neotropical Fishes

“…From the cytogenetic standpoint, seven distinct karyotype forms or karyomorphs (A–G) in H. malabaricus and four (A–D) in E. erythrinus have already been identified, respectively, based on major differences in diploid chromosome numbers (2n), chromosome morphology, and sex chromosomes [ 44 ]. Studies employing WCP, CGH, and repetitive DNA distribution patterns have highlighted the differentiation plasticity of the erythrinid sex chromosome systems [ 25 , 45 , 46 , 47 ]. More specifically, it was demonstrated that sex chromosomes could emerge via independent pathways, following distinct patterns of differentiation even within the same type of system and among closely related karyomorphs ( Figure 1 ).…”

“…21 found in karyomorph A [ 25 , 52 ]. Noteworthy, a male-specific region is distally confined to the q arms of Y chromosome, corresponding to a C-positive heterochromatic block occupying the same chromosomal region [ 47 ]. Indeed, the location of this region stands out given that a large nucleolar organizer region (NOR) site in the corresponding region of the X chromosome is responsible for the big size difference between both sex chromosomes [ 48 ].…”

“…Karyomorph C (2n = 40, both sexes), is characterized by morphologically undifferentiated XX/XY sex chromosome system evidenced by a small, but considerable, heterochromatin accumulation on the exclusively proximal region of the X chromosome [ 53 ]. CGH results documented the presence of distinct male-specific sequences in this likely nascent sex-determining region [ 47 ]). As reported for karyomorph B, the preferential accumulation of repetitive DNAs on the X chromosome is also a particular feature for the nascent XY sex system of this karyomorph.…”

Centric Fusions behind the Karyotype Evolution of Neotropical Nannostomus Pencilfishes (Characiforme, Lebiasinidae): First Insights from a Molecular Cytogenetic Perspective

“…Despite CGH and related methods represent rather "rough" molecular tools, they may show patterns of the genomic divergence between species, as they rely on the presence of genome-specific repetitive DNA classes. As repetitive DNA usually evolves rapidly in diverging genomes, such an approach may yield specific patterns of hybridization depending on the compared species, which (within a certain evolutionary timeframe) correlate with the degree of their divergence [31,[96][97][98]. In the present study, rather minor interspecific differences in the composition of repetitive DNA among the compared Nannostomus species were shown.…”

“…The probes were precipitated with 100% ethanol and the air-dried pellets were mixed with a hybridization buffer containing 50% formamide, 10% SDS, 10% dextran sulfate, 2× SSC, and Denhardt's buffer (pH 7.0). The hybridization process took place in a moist chamber at 37 • C for 72 h. The hybridization procedure was performed according to Sember et al [31]. After post-hybridization washes, done twice in 50% formamide in 2× SSC, pH 7.0 (44 • C, 10 min each) and three times in 1× SSC (44 • C, 7 min each), the probes were detected using Anti-Digoxigenin-Rhodamin (Roche, Basel, Switzerland) and Avidin-FITC (Sigma, St. Louis, MO, USA).…”