Rates and patterns of chromosomal evolution in Drosophila pseudoobscura and D. miranda

Abstract

Comparisons of gene orders between species permit estimation of the rate of chromosomal evolution since their divergence from a common ancestor. We have compared gene orders on three chromosomes of Drosophila pseudoobscura with its close relative, D. miranda, and the distant outgroup species, D. melanogaster, by using the public genome sequences of D. pseudoobscura and D. melanogaster and approximately 50 in situ hybridizations of gene probes in D. miranda. We find no evidence for extensive transfer of genes among chromosomes in D. miranda. The rates of chromosomal rearrangements between D. miranda and D. pseudoobscura are far higher than those found before in Drosophila and approach those for nematodes, the fastest rates among higher eukaryotes. In addition, we find that the D. pseudoobscura chromosome with the highest level of inversion polymorphism (Muller's element C) does not show an unusually fast rate of evolution with respect to chromosome structure, suggesting that this classic case of inversion polymorphism reflects selection rather than mutational processes. On the basis of our results, we propose possible ancestral arrangements for the D. pseudoobscura C chromosome, which are different from those in the current literature. We also describe a new method for correcting for rearrangements that are not detected with a limited set of markers.

Figure 1.

Southern blotting results for determining the banding patterns of gek in D. miranda males and females. Lane L, kilobase ladder; lanes 1–5, digests of male genomic DNA. The enzymes used were ApaI (1), BamHI (2), EcoRI (3), HindIII (4), and Nde (5). Lanes 6–10, digests of female genomic DNA using the same set.

Figure 2.

Schematic of the relative order of markers and chromosomal rearrangements between D. miranda and two other species (D. pseudoobscura and D. melanogaster). The solid circle represents the centromere; the position of the markers shows only their relative order along the chromosomes. The locations of the genes and the sizes of Muller elements are not scaled. The arrangements depicted correspond to the Standard–D. miranda and the Arrowhead–D. pseudoobscura arrangements.

Figure 3.

This shows the most parsimonious interpretation of the relations between the major rearrangements in D. pseudoobscura and the D. miranda–Standard arrangement. Double arrows indicate putative inversions between arrangements: 1, inversions D. miranda–ST; 2, inversion ST–AR; 3, inversion ST–HY. The exact location of the genes in D. miranda is shown in Table 1; the locations of the genes in the ST, HY, and TL arrangements were inferred from their approximate position in the D. pseudoobscura Genome Project (AR).

Figure 4.

Neighbor-joining tree obtained by concatenating six random samples of each arrangement from the Schaeffer et al. (2003) data set. It includes seven genes (en, exu1, vg, Amy1, eve, mef2, and EcR) and an intergenic region (F6). AR, Arrowhead; ST, Standard; CH, Chiricaua; SC, Santa Cruz; TL, Tree Line; OL, Olympic.