Chromosomal Inversion Polymorphism Leads to Extensive Genetic Structure

Abstract

The adaptive character of inversion polymorphism in Drosophila subobscura is well established. The OST and O3+4 chromosomal arrangements of this species differ by two overlapping inversions that arose independently on O3 chromosomes. Nucleotide variation in eight gene regions distributed along inversion O3 was analyzed in 14 OST and 14 O3+4 lines. Levels of variation within arrangements were quite similar along the inversion. In addition, we detected (i) extensive genetic differentiation between arrangements in all regions, regardless of their distance to the inversion breakpoints; (ii) strong association between nucleotide variants and chromosomal arrangements; and (iii) high levels of linkage disequilibrium in intralocus and also in interlocus comparisons, extending over distances as great as ∼4 Mb. These results are not consistent with the higher genetic exchange between chromosomal arrangements expected in the central part of an inversion from double-crossover events. Hence, double crossovers were not produced or, alternatively, recombinant chromosomes were eliminated by natural selection to maintain coadapted gene complexes. If the strong genetic differentiation detected along O3 extends to other inversions, nucleotide variation would be highly structured not only in D. subobscura, but also in the genome of other species with a rich chromosomal polymorphism.