Highly conserved Z and molecularly diverged W chromosomes in the fish genus Triportheus (Characiformes, Triportheidae)

Abstract

The main objectives of this study were to test: (1) whether the W-chromosome differentiation matches to species' evolutionary divergence (phylogenetic concordance) and (2) whether sex chromosomes share a common ancestor within a congeneric group. The monophyletic genus Triportheus (Characiformes, Triportheidae) was the model group for this study. All species in this genus so far analyzed have ZW sex chromosome system, where the Z is always the largest chromosome of the karyotype, whereas the W chromosome is highly variable ranging from almost homomorphic to highly heteromorphic. We applied conventional and molecular cytogenetic approaches including C-banding, ribosomal DNA mapping, comparative genomic hybridization (CGH) and cross-species whole chromosome painting (WCP) to test our questions. We developed Z-and W-chromosome paints from T. auritus for cross-species WCP and performed CGH in a representative species (T. signatus) to decipher level of homologies and rates of differentiation of W chromosomes. Our study revealed that the ZW sex chromosome system had a common origin, showing highly conserved Z chromosomes and remarkably divergent W chromosomes. Notably, the W chromosomes have evolved to different shapes and sequence contents within~15-25 Myr of divergence time. Such differentiation highlights a dynamic process of W-chromosome evolution within congeneric species of Triportheus.

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

“…Chromosomal mapping of rDNA clusters has repeatedly helped to unveil diverse evolutionary issues (e.g., [82,83]). Particularly in fishes, it provided valuable clues about the incidence of cryptic, morphologically indistinguishable sibling species [5,6,8,10,84], polyploidization and interspecific hybridization events [85,86], a geographical gradient of genomic and morphological change [87], patterns of sex chromosome differentiation [80,[88][89][90], and the correlation of genome dynamics in response to environmental cues [91,92]. Among the Nannostomus species investigated here, chromosomal mapping revealed somewhat uniform patterns of distribution for both rDNA classes, with one to few sites of accumulation, as found in most fishes [93,94], as well as in some other lebiasinids [21,22] investigated to date.…”

Genomic Organization of Repetitive DNAs and Differentiation of an XX/XY Sex Chromosome System in the Amazonian Puffer Fish, <b><i>Colomesus asellus </i></b>(Tetraodontiformes)

“…For example, in the characid genus Triportheus (Triportheidae), the W chromosome harbors an 18S rDNA cistron in the terminal region of the q arms, which is missing in the Z chromosome in the majority of the species [Yano et al, 2016a]. In this case, it is likely that these sequences could have been deleted from the Z chromosome after acquisition of a sex-specific allele by the W and the restriction of recombination in the sex chromosome pair [Yano et al, 2016b]. In Hoplias malabaricus (Erythrinidae), which corresponds to a species complex having a conspicuous XX/XY sex chromosome system in one of its karyomorphs, the X chromosome also shows an exclusive heterochromatic segment associated with a NOR region [Cioffi et al, 2010].…”

Contributions to the cytogenetics of the Neotropical fish fauna

“…This way, the significative role of several classes of repetitive DNAs in the differentiation path of the sex pair, both at its inicial stage (Cioffi and Bertollo 2010; Freitas et al in press) or more advanced ones (Cioffi et al 2010, 2011a, b, 2012b; Yano et al 2014a, b), was clearly highlighted. Notably, whole chromosome painting (WCP) and comparative genomic hybridization (CGH) were able to demonstrate that fish sex chromosomes can have an independent origin even among closely related species (Cioffi et al 2011c, d; 2013) or, alternatively, a common origin within particular monophyletic groups (Yano et al 2016). …”