Abstract
BackgroundNeo-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.ResultsThe 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.ConclusionsThe 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.
Highlights
Neo-sex chromosome systems arose independently multiple times in evolution, presenting the remarkable characteristic of repetitive DNAs accumulation
The analysis of clusters generated by RepeatExplorer and using Tandem Repeats Finder (TRF) algorithm, besides dotplots confirmed that 10 of the 551 clusters were resolved to be satDNAs sequences, with repeat units ranging from 5 to 285 bp long
General organization of satDNAs in R. bergii genome In grasshoppers RepeatExplorer satDNAs analysis was successfully applied in three species, revealing clues about organization of satDNAs in chromosomes of Schistocerca gregaria [52], general patterns of evolution of satDNAs using in Locusta migratoria [45] and the origin of the B chromosome in Eumigus monticola [46]
Summary
Neo-sex chromosome systems arose independently multiple times in evolution, presenting the remarkable characteristic of repetitive DNAs accumulation. Common hallmarks of sex chromosome evolution include the partial or complete loss of recombination between them; abundant gene inactivation or loss (i.e., genetic degeneration); progressive accumulation/expansion of repetitive DNAs; and heterochromatinization of the Y or W chromosomes [6, 7, 9,10,11,12,13,14]. In Orthoptera the X0♂/XX♀ sex chromosome system is a conserved pattern found in most species. This modal system results from the loss of the Y chromosome in an Palacios-Gimenez et al BMC Evolutionary Biology (2018) 18:2 ancestral XY♂/XX♀ species [15, 16]. The establishment of inversions, for example, is typically associated with recombination suppression and has been detected in the Y chromosome of the grasshopper Ronderosia bergii [20], mammals [23], the three-spine stickleback fish [26], and the plant Silene latifolia (Nicolas et al [11])
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