X-chromosome meiotic drive in Drosophila simulans: a QTL approach reveals the complex polygenic determinism of Paris drive suppression

• Published in: Heredity Vol. 122; no. 6; pp. 906 - 915
• Main Authors: Courret, Cécile, Gérard, Pierre R, Ogereau, David, Falque, Matthieu, Moreau, Laurence, Montchamp-Moreau, Catherine
• Format: Journal Article
• Language: English
• Published: England Springer Nature B.V 01.06.2019; Nature Publishing Group; Springer International Publishing
• Subjects: Animals; Chromosome 2; Chromosome 3; Chromosome Mapping; Chromosome Segregation; Chromosomes; Determinism; Drosophila simulans; Drosophila simulans - classification; Drosophila simulans - cytology; Drosophila simulans - genetics; Epistasis; Evolution, Molecular; Female; Gametes; Gene mapping; Inbreeding; Insects; Life Sciences; Male; Mapping; Meiosis; Meiotic drive; Models, Genetic; Natural populations; Natural selection; Phylogeny; Polygenic inheritance; Quantitative Trait Loci; Sex; Sex Ratio; Suppressors; X Chromosome - genetics; Y Chromosome; Y chromosomes; segragation distorted sd; widespread; evolution; sex-ratio trait; systems; incompatilibities
• ISSN: 0018-067X; 1365-2540; 0018-067X
• DOI: 10.1038/s41437-018-0163-1

Meiotic drivers are selfish genetic elements that promote their own transmission into the gametes, which results in intragenomic conflicts. In the Paris sex-ratio system of Drosophila simulans, drivers located on the X chromosome prevent the segregation of the heterochromatic Y chromosome during meiosis II, and hence the production of Y-bearing sperm. The resulting sex-ratio bias strongly impacts population dynamics and evolution. Natural selection, which tends to restore an equal sex ratio, favors the emergence of resistant Y chromosomes and autosomal suppressors. This is the case in the Paris sex-ratio system where the drivers became cryptic in most of the natural populations of D. simulans. Here, we used a quantitative trait locus (QTL) mapping approach based on the analysis of 152 highly recombinant inbred lines (RILs) to investigate the genetic determinism of autosomal suppression. The RILs were derived from an advanced intercross between two parental lines, one showing complete autosomal suppression while the other one was sensitive to drive. The confrontation of RIL autosomes with a reference X chromosome allowed us to identify two QTLs on chromosome 2 and three on chromosome 3, with strong epistatic interactions. Our findings highlight the multiplicity of actors involved in this intragenomic battle over the sex ratio.