The evolutionary history ofDrosophila simulansY chromosomes reveals molecular signatures of resistance to sex ratio meiotic drive

Abstract

The recent evolutionary history of the Y chromosome in Drosophila simulans, a worldwide species of Afrotropical origin, is closely linked to that of X-linked meiotic drivers (Paris system). The spread of the Paris drivers in natural populations has elicited the selection of drive resistant Y chromosomes. To infer the evolutionary history of the Y chromosome in relation to the Paris drive, we sequenced 21 iso-Y lines, each carrying a Y chromosome from a different location. Among them, 13 lines carry a Y chromosome that is able to counteract the effect of the drivers. Despite their very different geographical origins, all sensitive Y's are highly similar, suggesting that they share a recent common ancestor. The resistant Y chromosomes are more divergent and segregate in four distinct clusters. The phylogeny of the Y chromosome confirms that the resistant lineage predates the emergence of Paris drive. The ancestry of the resistant lineage is further supported by the examination of Y-linked sequences in the sister species of D. simulans, D. sechellia and D. mauritiana. We also characterized the variation in repeat content among Y chromosomes and identified two simple satellites ((AAACAAT)n and (AATGG)n) associated with resistance. Altogether, the molecular polymorphism allows us to infer the demographic and evolutionary history of the Y chromosome and provides new insights on the genetic basis of resistance.

Genetic conflict and the origin of multigene families: implications for sex chromosome evolution

“…Because of their high repeat content, the structural organization of Y chromosomes is evolutionarily labile and prone to rearrangements (e.g. [61]), even within species [111]. Structural variations might have functional consequences: variation in Y-linked heterochromatin contributes to variation in gene expression genome-wide (e.g.…”

“…Structural variations might have functional consequences: variation in Y-linked heterochromatin contributes to variation in gene expression genome-wide (e.g. [112–114]) and resistance to meiotic drive [111,115]. Beyond the amplification of repeated sequences through unequal exchange, the Y chromosome has unusual mutation properties that can create more dramatic rearrangements.…”

“…One intriguing feature of sex-ratio drive is the difference in the nature of suppression or resistance across systems: while some systems evolved autosomal, in addition to Y-linked, suppressors or resistance (e.g. [111,115,130]), others show no autosomal suppression (see [22]), or suppression is completely absent (e.g. [22,131]).…”