Molecular evolution of the Sex-Ratio inversion complex in Drosophila pseudoobscura: analysis of the Esterase-5 gene region

The Sex-Ratio chromosome in Drosophila pseudoobscura is subject to meioticdrive. It is associated with a series of three nonoverlapping paracentricinversions on the right arm of the X chromosome. The esterase-5 gene regionhas been localized to section 23 within the subbasal inversion of theSex-Ratio inversion complex, making esterase- 5 a convenient locus formolecular evolutionary analyses of the Sex- Ratio inversion complex and theassociated drive system. A 504-bp fragment of noncoding, intergenic DNAfrom the esterase-5 gene region was amplified and sequenced from 14Sex-Ratio and 14 Standard X chromosomes of D. pseudoobscura, and from 9 Xchromosomes of its two sibling species, Drosophila persimilis andDrosophila miranda. There is extensive sequence differentiation between theSex-Ratio and Standard chromosomal types. The common Standard chromosome ishighly polymorphic, while, as expected from either the neutral mutationtheory or the selective sweep hypothesis, the rarer Sex-Ratio chromosomehas much less within-chromosome nucleotide polymorphism. We estimate thatthe Standard and Sex-Ratio chromosomes in D. pseudoobscura diverged between700,000 and 1.3 Mya, or at least 2 million generations ago. The clusteringof D. pseudoobscura Sex-Ratio chromosomes in a neighbor- joining phylogenyindicates a fairly old, monophyletic origin in this species. It appearsfrom these data that Sex-Ratio genes were present prior to the divergenceof D. pseudoobscura and D. persimilis and that both the Standard andSex-Ratio chromosomes of D. persimilis were derived from the Standardchromosome of D. pseudoobscura after the inversion events that isolated theD. pseudoobscura Sex-Ratio chromosome.