First Report of Sex Chromosomes in Achiridae (Teleostei: Pleuronectiformes) with Inferences About the Origin of the Multiple X₁X₁X₂X₂/X₁X₂Y System and Dispersal of Ribosomal Genes inAchirus achirus

Abstract

American soles (family Achiridae) have been characterized by remarkable chromosomal variation even though several species lack basic cytogenetic information. This trend indicates that chromosomal traits can be useful to taxonomy once the morphological identification of some taxa in this family (e.g., Achirus species) is controversial. In this work, we expand the cytogenetic data in Achiridae by providing the first karyotypic analysis of Achirus achirus. An unusual multiple sex chromosome system (XXXX/XXY) was detected, once males presented 2n = 33 with three unpaired chromosomes (XXY) while females presented 2n = 34 with two acrocentric pairs (XX and XX) found in hemizygosis in males. The 18S rDNA clusters were observed interspersed with GC-rich sites in a single pair. However, the 5S rRNA genes were dispersed through the genome of A. achirus in a sex-specific manner (10 clusters in males and 12 in females), as a result of the presence of ribosomal cistrons in X and X chromosomes. This pattern allowed us to infer that Y chromosome has evolved by partial deletion followed by fusion of proto-X and proto-X homologous chromosomes. The high rate of genomic evolution in Achiridae could have favored their reproductive isolation and speciation even in sympatric conditions.

Deciphering the Origin and Evolution of the X1X2Y System in Two Closely-Related Oplegnathus Species (Oplegnathidae and Centrarchiformes)

“…Although both dinucleotide motifs (GA) 15 and (CA) 15 were present on the Y chromosomes, no exclusive or biased accumulations were observed on the sex chromosomes in comparison with the autosomes of both species (present study, see Figure 2; and [58]). These findings agree with the general patterns found in the majority of fish multiple sex chromosomes, where little or no differential accumulation of heterochromatin and repetitive DNA sequences accompanies their emergence and differentiation [25,32,33,37,38,40,45] and it also corroborates our findings yielded by the CGH method (see below).…”

“…The association between rDNAs and the sex chromosomes has been increasingly evidenced in fishes during the last decade, including taxa with multiple sex chromosomes [31,33,38,49,56,59,60,61,62,63,64]. As analogous examples have repeatedly been documented in other animals, different authors speculated about diverse potential roles for rDNA on standard or neo-sex chromosomes, including the effects on the recombination frequency (which may be lowered in nearby chromosomal regions [45,65,66]), prevention against the complete loss of the degenerating sex chromosome due to the persistent presence of structural genes [66], proper pairing and segregation of sex chromosomes [22,67] or as a boundary that prevents the spreading of inactivation on neo-sex chromosome from the original segment to a newly added pseudo-autosomal material [55].…”

“…Including Oplegnathus , about 60 cases of multiple sex chromosomes have so far been reported across the teleost phylogeny (reviewed in [13], for more recent examples, see [30,31,32,33,34,35,36,37,38,39]). In this context, molecular cytogenetics provides a powerful toolbox for understanding the genome evolution and organization [40,41,42], and many of these approaches have enabled unique insights into the vertebrate sex chromosome evolution.…”

Multiple Sex Chromosomes and Evolutionary Relationships in Amazonian Catfishes: The Outstanding Model of the Genus Harttia (Siluriformes: Loricariidae)

“…Meaningly, a close association between microsatellites, rDNAs and multiple sex chromosomes has been reported for many fish taxa [ 55 , 56 , 57 , 58 , 59 ], which highlights the probable role of these sequences in the genesis of such systems. Despite our CGH data do not reveal any conspicuous Y-specific region, neither in both Y chromosomes of H. duriventris and H. villasboas , nor in the proto/neo-Y of H. rondoni , a slight binding preference for the male-derived probe occur at the pericentromeric region of all these chromosomes ( Figure 5 ).…”

Chromosomal Evolution in Lower Vertebrates: Sex Chromosomes in Neotropical Fishes

“…Nonetheless, both models share some common properties, such as repetitive DNA sequences playing a substantial role in the differentiation processes of heteromorphic sex chromosomes. In contrast, the multiple neo-sex chromosomes, arising through the structural rearrangements, do not undergo progressive heterochromatinization [ 9 ]—a feature also repeatedly documented in other fish groups [ 8 , 20 , 85 , 86 ] that presumably has a large impact on the stabilization of the sex multivalents during meiosis [ 86 , 87 ]. In this sense, it appears to be evident that the highest occurrence of XY-derived multiple sex systems reflects the early stage of differentiation of the XX/XY sex system found in most fishes examined so far.…”