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

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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Fig. 1: Repeat landscapes from male and female genomes showing abundance and divergence for satDNAs and TEs identified in Ronderosia bergii.
Fig. 2: FISH mapping of 13 satDNAs and telomere probes on neo-Y chromosome.
Fig. 3: Line color-coded landscape showing the temporal accumulation of seven satDNA families exclusively located on neo-Y chromosome detected by FISH analysis.
Fig. 4: Cryptic neo-Y variants of Ronderosia bergii.
Fig. 5: SatDNAs located on neo-X chromosome and its variants found on male embryos.

Data availability

The sequencing data are deposited in GenBank under accession numbers MT501156-MT5001208, SRX8370569, and SRX8370570.

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Acknowledgements

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES), by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (process numbers 2015/16661-1, 2014/11763-8), and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). We thank Julie Blommaert for the English corrections. We are grateful to the anonymous reviews for providing insightful peer reviews of this paper. OMPG and FJRR acknowledge the scholarship obtained from the Lawski Foundation (Sweden). ABSMF and DM acknowledge the scholarship from CAPES. DCCM is a recipient of a research productivity fellowship from the Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq (process number 304758/2014-0). Computing ran on resources provided by the Swedish National Infrastructure for Computing (SNIC) through Uppsala Multidisciplinary Center for Advanced Computational Science (UPPMAX).

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Correspondence to Diogo C. Cabral-de-Mello.

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Ferretti, A.B.S.M., Milani, D., Palacios-Gimenez, O.M. et al. High dynamism for neo-sex chromosomes: satellite DNAs reveal complex evolution in a grasshopper. Heredity (2020). https://doi.org/10.1038/s41437-020-0327-7

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