Independent fusions and recent origins of sex chromosomes in the evolution and diversification of glass knife fishes (Eigenmannia)

Abstract

The genus Eigenmannia comprises several species groups that display a surprising variety of diploid chromosome numbers and sex-determining systems. In this study, hypotheses regarding phylogenetic relationships and karyotype evolution were investigated using a combination of molecular and cytogenetic methods. Phylogenetic relationships were analyzed for 11 cytotypes based on sequences from five mitochondrial DNA regions. Parsimony-based character mapping of sex chromosomes confirms previous suggestions of multiple origins of sex chromosomes. Molecular cytogenetic analyses involved chromosome painting using probes derived from whole sex chromosomes from two taxa that were hybridized to metaphases of their respective sister cytotypes. These analyses showed that a multiple XY system evolved recently (o7 mya) by fusion. Furthermore, one of the chromosomes that fused to form the neo-Y chromosome is fused independently to another chromosome in the sister cytotype. This may constitute an efficient post-mating barrier and might imply a direct function of sex chromosomes in the speciation processes in Eigenmannia. The other chromosomal sexdetermination system investigated is shown to have differentiated by an accumulation of heterochromatin on the X chromosome. This has occurred in the past 0.6 my, and is the most recent chromosomal sex-determining system described to date. These results show that the evolution of sexdetermining systems can proceed very rapidly.

Whole chromosome painting reveals independent origin of sex chromosomes in closely related forms of a fish species

“…In the weakly electric fish Eigenmannia it was demonstrated, by chromosomal painting analysis, an independent origin of the sex chromosome systems present in two closed related species (Henning et al 2008, Henning et al 2011. Similar results were also found in salmonid fishes, in which painting probes, specific to the Y chromosome of Salvelinus namaycush, hybridized to two different autosomal pairs of Oncorhynchus myskiss and O. tshawytscha, supporting the lack of homology between the sex chromosomes of these two closely related genera (Phillips et al 2001).…”

Karyotype Differentiation between Two Stickleback Species (Gasterosteidae)

“…Studies have documented sex chromosome diversity within species of poeciliid fish [Nanda et al, 2000;Volff and Schartl, 2001;Schultheis et al, 2009] and within several species of neotropical fish, including E. virescens [Almeida-Toledo et al, 2002;Henning et al, 2011], Erythrinus erythrinus [Bertollo et al, 2004;, and Hoplias malabaricus [Bertollo et al, 2000;. Sex chromosome systems also differ among populations of other stickleback species.…”

Karyotypic and morphological divergence between two cryptic species of Eigenmannia in the Amazon basin with a new occurrence of XX/XY sex chromosomes (Gymnotiformes: Sternopygidae)

“…Silva et al (2009) suggest that the mechanisms involved in the differentiation of the W chromosome are the result of a pericentric inversion event in the proximal region of the short arm of an acrocentric chromosome, followed by a heterochromatization event. These events would have occurred in a distinct manner in independent populations, derived from an ancestral karyotype without differentiated sex chromosomes (Henning et al, 2011). It is highly possible that the sex chromosomes differentiation also contributed to species differentiation/divergence and worked as a reproductive isolation mechanism.…”

“…In fishes, sex chromosomes are not present in basal taxa and their origin within genera or families is probably convergent. Additional information suggests that the origin of sex chromosomes in Neotropical fishes is recent, with diversification in some taxa approximately 7-10 Ma (Charlesworth et al, 2005;Cioffi et al, 2011;Henning et al, 2011).…”