Sex chromosome diversity in Armenian toad grasshoppers (Orthoptera, Acridoidea, Pamphagidae)

Abstract

Although previous cytogenetic analysis of Pamphagidae grasshoppers pointed to considerable karyotype uniformity among most of the species in the family, our study of species from Armenia has discovered other, previously unknown karyotypes, differing from the standard for Pamphagidae mainly in having unusual sets of sex chromosomes. Asiotmethis turritus (Fischer von Waldheim, 1833), Paranocaracris rubripes (Fischer von Waldheim, 1846), and Nocaracris cyanipes (Fischer von Waldheim, 1846) were found to have the karyotype 2n♂=16+neo-XY and 2n♀=16+neo-XX, the neo-X chromosome being the result of centromeric fusion of an ancient acrocentric X chromosome and a large acrocentric autosome. The karyotype of Paranothrotes opacus (Brunner von Wattenwyl, 1882) was found to be 2n♂=14+X1X2Y and 2n♀=14+X1X1X2X2., the result of an additional chromosome rearrangement involving translocation of the neo-Y and another large autosome. Furthermore, evolution of the sex chromosomes in these species has involved different variants of heterochromatinization and miniaturization of the neo-Y. The karyotype of Eremopeza festiva (Saussure, 1884), in turn, appeared to have the standard sex determination system described earlier for Pamphagidae grasshoppers, 2n♂=18+X0 and 2n♀=18+XX, but all the chromosomes of this species were found to have small second C-positive arms. Using (FISH)fluorescent in situ hybridization with 18S rDNA and telomeric (TTAGG)n DNA repeats to yield new data on the structural organization of chromosomes in the species studied, we found that for most of them, clusters of repeats homologous to 18S rDNA localize on two, three or four pairs of autosomes and on the X. In Eremopeza festiva, however, FISH with labelled 18S rDNA painted C-positive regions of all autosomes and the X chromosome; clusters of telomeric repeats localized primarily on the ends of the chromosome arms. Overall, we conclude that the different stages of neo-Y degradation revealed in the Pamphagidae species studied make the family a very promising and useful model for studying sex chromosome evolution.

Comparative analysis of chromosomal localization of ribosomal and telomeric DNA markers in three species of Pyrgomorphidae grasshoppers

“…In single cases, clusters of rDNA were revealed in the pericentric heterochromatin of all chromosomes in the set (Jetybayev et al 2012). In contrast to Pyrgomorphidae and Acrididae grasshoppers, multiple localization of rDNA clusters on one chromosome in the Pamphagidae family has been shown (Bugrov et al 2016, Jetybayev et al 2017). Perhaps, the revealed differences in the localization of rDNA in Pyrgomorphidae and Acrididae on the one hand, and Pamphagidae on the other hand, may contain a certain phylogenetic signal.…”

“…For instance, recently, a new model of the Y-chromosome evolution was proposed based on studies in Pamphagidae grasshoppers. It was shown that in Pamphagidae grasshoppers centric fusion of the X chromosome and autosome occurred independently in two phylogenetic branches, and due to further evolution the neo-Y chromosome exhibited different stages of degradation process (Bugrov et al 2016, Jetybayev et al 2017). …”

“…Analysis of chromosome sets within such Orthoptera groups, which have never been studied before, in conjunction with the use of new techniques for chromosome research, may therefore potentially lead to many new insights. As an example, using molecular cytogenetic methods, in-depth research of the family Pamphagidae has recently revealed new evolutionary pathways of autosomes and sex chromosomes previously unknown in this family (Bugrov et al 2016, Jetybayev et al 2017). …”

Origin and Evolution of the Neo-Sex Chromosomes in Pamphagidae Grasshoppers through Chromosome Fusion and Following Heteromorphization

“…The Pamphagidae family is one of the few taxa among grasshoppers, which includes phylogenetic lineages characterized by the neo-sex chromosome systems. Recently species of this family were karyotyped and the neo-sex chromosomes were described with C-banding of mitotic and meiotic chromosomes and FISH of 28S rDNA and telomeric repeats [ 23 , 24 , 32 , 33 ]. However, understanding of the neo-sex chromosome evolution requires identification of the autosomes fused with the ancestral X, description of their degradation process and characterization of newly arisen clusters of DNA repeats.…”

“…The neo-Y is similar to original autosome according to the size. In the second lineage (Nocarodeini tribe of Pamphaginae subfamily), the neo-sex chromosomes exhibit advanced stages of heteromorphization with significant degradation of the neo-Y [ 23 , 24 ]. This study is devoted to the comparative analysis of the neo-sex chromosomes in both evolutionary lineages in Pamphagidae by the generation of microdissected DNA probes from neo-sex chromosomes or their regions, followed by in situ hybridization with chromosomes of different species of Pamphagidae.…”