Neo-sex chromosomes of Ronderosia bergi: insight into the evolution of sex chromosomes in grasshoppers

Abstract

Sex chromosomes have evolved many times from morphologically identical autosome pairs, most often presenting several recombination suppression events, followed by accumulation of repetitive DNA sequences. In Orthoptera, most species have an X0♂ sex chromosome system. However, in the subfamily Melanoplinae, derived variants of neo-sex chromosomes (neo-XY♂ or neo-X1X2Y♂) emerged several times. Here, we examined the differentiation of neo-sex chromosomes in a Melanoplinae species with a neo-XY♂/XX♀ system, Ronderosia bergi, using several approaches: (i) classical cytogenetic analysis, (ii) mapping via fluorescent in situ hybridization of some selected repetitive DNA sequences and microdissected sex chromosomes, and (iii) immunolocalization of distinct histone modifications. The microdissected sex chromosomes were also used as sources for Polymerase chain reaction (PCR) amplification of RNA-coding multigene families, to study variants related to the sex chromosomes. Our data suggest that the R. bergi neo-Y has become differentiated after its formation by a Robertsonian translocation and inversions, and has accumulated repetitive DNA sequences. Interestingly, the ex autosomes incorporated into the neo-sex chromosomes retain some autosomal post-translational histone modifications, at least in metaphase I, suggesting that the establishment of functional modifications in neo-sex chromosomes is slower than their sequence differentiation.

Extra Microchromosomes Play Male Determination Role in Polyploid Gibel Carp

“…The first kind of repetitive sequence is 137 bp in length; in it there are five intact repeats and four incomplete repeats in the male-specific 8335 sequence ( Besides its characterized repeats, such as target site repeats (TSR), LTR, primer binding sites, and the polypurine tract (PPT); significantly, the similar LTR retrotransposon sequence even includes two intact repeats of the first repetitive sequence in each of the two LTRs ( Figure 5B and Table S2). Thus, these results indicate that that the microchromosomes contain numerous repetitive sequences and transposable elements, which display a common feature similar to neo-sex chromosomes (Kaiser and Bachtrog 2010;Zhou et al 2013;Palacios-Gimenez et al 2015). In addition, these extra microchromosomes in males, which are closely related to male determination, might evolve to sex chromosomes or provide primary material for the origin of sex chromosomes in gibel carp.…”

“…These microchromosomes in males indeed display a common feature similar to neo-sex chromosomes because they contain numerous repetitive sequences and transposable elements ( Figure 5). In insects and fishes, the accumulation of repetitive sequences has been revealed to be the initial stage of neosex chromosome evolution (Zhou and Bachtrog 2012;Zhou et al 2013;Palacios-Gimenez et al 2015), and the expansion of repetitive sequence repeats can trigger heterochromatin formation, restrict recombination, and lead to subsequent chromosomal rearrangements (Kaiser and Bachtrog 2010;Zhou et al 2013;Palacios-Gimenez et al 2015). The current data in polyploid gibel carp indicate that the extra microchromosomes with repetitive sequences and transposable elements in males play a male determination role in gibel carp, and they might evolve to sex chromosomes or provide primary material for the origin of sex chromosomes during the reproduction mode transition from unisexual gynogenesis to sexual reproduction (Zhang et al 2015).…”

Neo-sex Chromosomes in the Maculipennis Species Group (Dichroplus: Acrididae, Melanoplinae): The Cases of D. maculipennis and D. vittigerum

“…These properties vary continuously from the conservation of complete homology, full synapsis and chiasma formation in recently emerged systems, to almost complete degeneration and loss of homology of the neo-Y in putative ancient systems. Degeneration involves further chromosomal rearrangements, gene loss, and accumulation of non-coding repetitive sequences (Bidau and Martí, 2001;Mesa et al, 2001;Castillo et al, 2014;Palacios-Gimenez et al, 2013;Palacios-Gimenez et al, 2015). However, complete loss of the neo-Y, transforming the system into a "neo-X0/XX" one, has never occurred as far as the available information indicates .…”

“…However, R. bergii neo-Y shows a marked dispersion of this repetitive DNA fraction throughout the long arm of the neo-Y chromosome (Palacios-Gimenez et al, 2015). Research also suggests different accumulation/diversification patterns of repetitive DNAs of neo-Y chromosomes in this closely related species; such empirical data could be evidence for the loss of selection pressure in chromosomal regions in which recombination is abolished, leading to a high rate of genetic diversification (Palacios-Gimenez et al, 2013;Castillo et al, 2014;Palacios-Gimenez et al, 2015).…”

“…Recently, the molecular mapping of C0t-1 DNA fraction evidenced in melanopline species (i.e., Eurotettix minor, Dichromatos lilloanus, and D. schrottkyi) points to a relatively restricted spreading of this repetitive DNA in neo-sex chromosomes, which contrasts with the repetitive DNA accumulation expected after recombination restriction (Palacios-Gimenez et al, 2013). However, R. bergii neo-Y shows a marked dispersion of this repetitive DNA fraction throughout the long arm of the neo-Y chromosome (Palacios-Gimenez et al, 2015). Research also suggests different accumulation/diversification patterns of repetitive DNAs of neo-Y chromosomes in this closely related species; such empirical data could be evidence for the loss of selection pressure in chromosomal regions in which recombination is abolished, leading to a high rate of genetic diversification (Palacios-Gimenez et al, 2013;Castillo et al, 2014;Palacios-Gimenez et al, 2015).…”