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. 2020 Sep;125(3):124-137.
doi: 10.1038/s41437-020-0327-7. Epub 2020 Jun 4.

High dynamism for neo-sex chromosomes: satellite DNAs reveal complex evolution in a grasshopper

Ana B S M Ferretti  1 , Diogo Milani  1 , Octavio M Palacios-Gimenez  2   3 , Francisco J Ruiz-Ruano  2   3 , Diogo C Cabral-de-Mello  4
Affiliations

High dynamism for neo-sex chromosomes: satellite DNAs reveal complex evolution in a grasshopper

Ana B S M Ferretti et al. Heredity (Edinb). 2020 Sep.

Abstract

A common characteristic of sex chromosomes is the accumulation of repetitive DNA, which accounts for their diversification and degeneration. In grasshoppers, the X0 sex-determining system in males is considered ancestral. However, in some species, derived variants like neo-XY in males evolved several times independently by Robertsonian translocation. This is the case of Ronderosia bergii, in which further large pericentromeric inversion in the neo-Y also took place, making this species particularly interesting for investigating sex chromosome evolution. Here, we characterized the satellite DNAs (satDNAs) and transposable elements (TEs) of the species to investigate the quantitative differences in repeat composition between male and female genomes putatively associated with sex chromosomes. We found a total of 53 satDNA families and 56 families of TEs. The satDNAs were 13.5% more abundant in males than in females, while TEs were just 1.02% more abundant in females. These results imply differential amplification of satDNAs on neo-Y chromosome and a minor role of TEs in sex chromosome differentiation. We showed highly differentiated neo-XY sex chromosomes owing to major amplification of satDNAs in neo-Y. Furthermore, chromosomal mapping of satDNAs suggests high turnover of neo-sex chromosomes in R. bergii at the intrapopulation level, caused by multiple paracentric inversions, amplifications, and transpositions. Finally, the species is an example of the action of repetitive DNAs in the generation of variability for sex chromosomes after the suppression of recombination, and helps understand sex chromosome evolution at the intrapopulation level.

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Conflict of interest statement

The authors declare that they have no conflict of interest.

Figures

Fig. 1
Fig. 1. Repeat landscapes from male and female genomes showing abundance and divergence for satDNAs and TEs identified in Ronderosia bergii.
Bar color- coded repeat landscapes for the satDNA families in males (a) and females (b), and for the most abundant TE superfamilies in males (c) and females (d). The graphs represent genome coverage (y axis) for each type of repeats (color coded) in the different genomes analyzed, clustered according to Kimura distances to their corresponding consensus sequence (x axis, K value from 0 to 40, for a, b) or BLASTn divergence (x axis, BLASTn from 0 to 30, for c, d). Copies clustering on the left of the graph do not diverge very much from the consensus sequence of the element, and potentially correspond to recent copies, while sequences on the right might correspond to ancient/degenerated copies. Note the higher amount of satDNA for male genomes, while for TEs, there is almost no difference between the landscapes. Bar color-coded comparative quantitative analysis for satDNA families (e) and TE superfamily variants (f) enriched between sexes. Each column represents 100% of the reads of a specific sequence with proportions in male (blue) and female (red) genomes.
Fig. 2
Fig. 2. FISH mapping of 13 satDNAs and telomere probes on neo-Y chromosome.
Each probe was pseudo-colored with the indicated colors (a, b), and in (c) all the probes were merged in an ideogram showing the relative position of each other. The neo-Y chromosome in (a′, b′) is aligned by the centromere, and the arrow points to the middle part of the long arm. As the FISH mapping was done in distinct neo-Y chromosomes from the same embryo, the satDNAs, RbeSat25-166 and RbeSat15-288, were used to anchor the two neo-Y, allowing to precisely define the position of all FISH signals. This neo-Y chromosome represents the most common observed in the population, regarding satDNA distribution. Bar 2.5 µm.
Fig. 3
Fig. 3. Line color-coded landscape showing the temporal accumulation of seven satDNA families exclusively located on neo-Y chromosome detected by FISH analysis.
The graphs represent the Kimura distance-based copy divergence analysis to the consensus on the x axis and the satDNA abundance on the y axis. Copies clustering on the left of the graph do not diverge very much from the consensus sequence of the element, and correspond to recent amplified neo-Y- linked copies (in males), while sequences on the right might correspond to ancient/degenerated copies.
Fig. 4
Fig. 4. Cryptic neo-Y variants of Ronderosia bergii.
FISH mapping of satDNAs revealing variants of neo-Y chromosome of distinct male embryos (a–f). Colored squares next to each neo-Y chromosome indicate the location of the satDNA on the most common neo-Y variant (see Fig. 2). The neo-Y chromosomes are aligned by a centromere, and the arrowhead point to the middle part of the long arm. Bar 2.5 µm.
Fig. 5
Fig. 5. SatDNAs located on neo-X chromosome and its variants found on male embryos.
In (a) satDNAs that presented signals on neo-X of all embryos and in (b) satDNAs that were present or absent on neo-X, depending of the embryo. XL represents ancestral X chromosome and XR is the arm that shares homology with neo-Y. The neo-X chromosomes are aligned by a centromere. Bar 2.5 µm.
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