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. 2018 Jan 8;18(1):2.
doi: 10.1186/s12862-017-1113-x.

Uncovering the Evolutionary History of neo-XY Sex Chromosomes in the Grasshopper Ronderosia Bergii (Orthoptera, Melanoplinae) Through Satellite DNA Analysis

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Free PMC article

Uncovering the Evolutionary History of neo-XY Sex Chromosomes in the Grasshopper Ronderosia Bergii (Orthoptera, Melanoplinae) Through Satellite DNA Analysis

Octavio M Palacios-Gimenez et al. BMC Evol Biol. .
Free PMC article

Abstract

Background: Neo-sex chromosome systems arose independently multiple times in evolution, presenting the remarkable characteristic of repetitive DNAs accumulation. Among grasshoppers, occurrence of neo-XY was repeatedly noticed in Melanoplinae. Here we analyzed the most abundant tandem repeats of R. bergii (2n = 22, neo-XY♂) using deep Illumina sequencing and graph-based clustering in order to address the neo-sex chromosomes evolution.

Results: The analyses revealed ten families of satDNAs comprising about ~1% of the male genome, which occupied mainly C-positive regions of autosomes. Regarding the sex chromosomes, satDNAs were recorded within centromeric or interstitial regions of the neo-X chromosome and four satDNAs occurred in the neo-Y, two of them being exclusive (Rber248 and Rber299). Using a combination of probes we uncovered five well-defined cytological variants for neo-Y, originated by multiple paracentric inversions and satDNA amplification, besides fragmented neo-Y. These neo-Y variants were distinct in frequency between embryos and adult males.

Conclusions: The genomic data together with cytogenetic mapping enabled us to better understand the neo-sex chromosome dynamics in grasshoppers, reinforcing differentiation of neo-X and neo-Y and revealing the occurrence of multiple additional rearrangements involved in the neo-Y evolution of R. bergii. We discussed the possible causes that led to differences in frequency for the neo-Y variants between embryos and adults. Finally we hypothesize about the role of DNA satellites in R. bergii as well as putative historical events involved in the evolution of the R. bergii neo-XY.

Keywords: Chromosomal rearrangements; Evolution; FISH; Satellite DNA; Sex chromosome.

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Figures

Fig. 1
Fig. 1
Fluorescent in situ hybridization in male embryo mitotic metaphase for the ten satDNAs recovered from R. bergii genome (a-f). Note the divergent pattern of location depending of the repeat (a-f) and the exclusive occurrence of Rber248 (c) and Rber299 (b) in the neo-Y chromosome. The sex chromosomes are directly indicated in each panel, as the specific satDNA family mapped
Fig. 2
Fig. 2
Neo-Y five chromosomes variants revealed by physical mapping of the two satDNAs exclusive of neo-Y chromosome, i.e. Rber248 (green) and Rber299 (red). Note in (a-c, e) that the Rber248 is maintained in the same position while the Rber299 is involved in the paracentric inversion, that involved distinct sizes of the neo-Y. In d note the enlargement of the neo-Y and that the Rber248 and Rber299 are maintained near each other, but in inverted order in comparison to the other neo-Y variants. The percentages indicate the proportion of individuals harboring the distinct variants of neo-Y in embryos (mitosis) and adults (meiosis)
Fig. 3
Fig. 3
a Selected neo-XY chromosomes showing the differences in size for neo-X and neo-Y for the four variants observed in mitosis. b FISH using three distinct satDNAs families in the neo-Y variant IV
Fig. 4
Fig. 4
Male metaphase I probed for Rber248 and Rber299 showing the fragmented neo-Y chromosome. The inset shows the sex bivalent in early anaphase, highlighting the fragmentation of the neo-Y chromosome
Fig. 5
Fig. 5
Hypothesis on the R. bergii neo-XY sex chromosome evolution based on satDNAs distribution patterns. a First the de novo origin of the neo-sex chromosomes involved an X-A centric fusion. After the neo-XY arisen, the neo-X and neo-Y presents conserved homology (indicated in blue) and recombining events are still able to occur between the XR arm and the neo-Y. A pericentric inversion has become established on the neo-Y involving more than 90% of its length followed by heterochromatinization (indicated in black) and recombination suppression between neo-XY. These rearrangements and recombination suppression could favored the accumulation of the satDNAs on the neo-Y and generate the different neo-Y variants as indicated in (b), as follows: (i) three large and independent paracentric inversions involving Rber299 displacing this satDNAs towards interstitial or distal regions originating the variants II, III and V; (ii) a paracentric inversion involving both Rber248 and Rber299 and (iii) amplifications of Rber1 and Rber59 (not observed in the variant I, probably by low copy number and FISH resolution) generating the pattern IV, in which the neo-Y is enlarged. Each satDNAs mapped on the neo-Y chromosome are indicated by colors directly on the images

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