Molecular genetic variation in the centromeric region of the X chromosome in three Drosophila ananassae populations. I. Contrasts between the vermilion and forked loci

Abstract

We have surveyed three natural populations of Drosophila ananassae for restriction map variation at the forked (f) and vermilion (v) loci, using 6-cutter restriction enzymes. Both loci are located in the centromeric region of the X chromosome. Two major conclusions can be drawn from the data. First, we found strong evidence for population subdivision, i.e., significant differences in the frequency distributions of polymorphisms and/or haplotypes between the Burma, India, and Brazil populations. Secondly, the pattern of DNA sequence variation between the two loci is unexpectedly different. The level of nucleotide variation in the v locus region is reduced (relative to f), especially in the Burma population. Furthermore, in contrast to v, we found no insertions/deletions larger than 700 bp and no significant linkage disequilibrium at f. The genetic differentiation among subpopulations can readily be attributed to restricted migration as the predominant evolutionary force. According to population genetics theory, the differences in DNA polymorphisms between the two loci are in qualitative agreement with the hypothesis that recombination is reduced in the v locus region ("centromere effect") but not at f. In order to test this hypothesis directly, we determined the cytogenetic positions of several loci in the centromeric region by in situ hybridization and found by comparison with the genetic map that recombination at v is indeed very low, much lower than at f.