Rapid evolution of a Y-chromosome heterochromatin protein underlies sex chromosome meiotic drive

Sex chromosome meiotic drive, the non-Mendelian transmission of sex chromosomes, is the expression of an intragenomic conflict that can have extreme evolutionary consequences. However, the molecular bases of such conflicts remain poorly understood. Here, we show that a young and rapidly evolving X-l...

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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences - PNAS 2016-04, Vol.113 (15), p.4110-4115
Main Authors: Helleu, Quentin, Gérard, Pierre R., Dubruille, Raphaëlle, Ogereau, David, Prud’homme, Benjamin, Loppin, Benjamin, Montchamp-Moreau, Catherine
Format: Article
Language:English
Subjects:
Animals
Biological Sciences
Cells
Cellular Biology
Chromosomes
Development Biology
Drosophila simulans
Drosophila simulans - classification
Drosophila simulans - genetics
Evolution, Molecular
Genes
Heterochromatin
Heterochromatin - metabolism
Life Sciences
Meiosis - genetics
Phylogeny
Proteins
Y Chromosome
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Summary:Sex chromosome meiotic drive, the non-Mendelian transmission of sex chromosomes, is the expression of an intragenomic conflict that can have extreme evolutionary consequences. However, the molecular bases of such conflicts remain poorly understood. Here, we show that a young and rapidly evolving X-linked heterochromatin protein 1 (HP1) gene, HP1D2, plays a key role in the classical Paris sex-ratio (SR) meiotic drive occurring in Drosophila simulans. Driver HP1D2 alleles prevent the segregation of the Y chromatids during meiosis II, causing female-biased sex ratio in progeny. HP1D2 accumulates on the heterochromatic Y chromosome in male germ cells, strongly suggesting that it controls the segregation of sister chromatids through heterochromatin modification. We show that Paris SR drive is a consequence of dysfunctional HP1D2 alleles that fail to prepare the Y chromosome for meiosis, thus providing evidence that the rapid evolution of genes controlling the heterochromatin structure can be a significant source of intragenomic conflicts.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.1519332113