Global patterns of sequence evolution in Drosophila

Abstract

Background: Sequencing of the genomes of several Drosophila allows for the first precise analyses of how global sequence patterns change among multiple, closely related animal species. A basic question is whether there are characteristic features that differentiate chromosomes within a species or between different species.

Results: We explored the euchromatin of the chromosomes of seven Drosophila species to establish their global patterns of DNA sequence diversity. Between species, differences in the types and amounts of simple sequence repeats were found. Within each species, the autosomes have almost identical oligonucleotide profiles. However, X chromosomes and autosomes have, in all species, a qualitatively different composition. The X chromosomes are less complex than the autosomes, containing both a higher amount of simple DNA sequences and, in several cases, chromosome-specific repetitive sequences. Moreover, we show that the right arm of the X chromosome of Drosophila pseudoobscura, which evolved from an autosome 10 - 18 millions of years ago, has a composition which is identical to that of the original, left arm of the X chromosome.

Conclusion: The consistent differences among species, differences among X chromosomes and autosomes and the convergent evolution of X and neo-X chromosomes demonstrate that strong forces are acting on drosophilid genomes to generate peculiar chromosomal landscapes. We discuss the relationships of the patterns observed with differential recombination and mutation rates and with the process of dosage compensation.

Figure 1

Oligonucleotide profiles (word size k = 13) detailing the relative word frequencies between the X and 2L chromosomes (A) or the 3R and 2L chromosomes (B) of D. melanogaster. Results for 2 Mb of the X or the 3R chromosomes (x-axis) are shown. The y-axis reflects the relative frequency of words in the two chromosomes after size correction. Details in panel A show the repetitious internal structure characteristic of an X-specific satellite.

Figure 2

Average values for relative word frequencies in comparisons among D. melanogaster chromosomes. To draw panel A, the frequency of all words present in the X chromosome was establish in both the X and autosomes. The histograms show, in the y-axis, the values of the X/autosome ratio, once corrected for chromosome sizes. Values from k = 1 to k = 13 are depicted from left to right for each comparison. Panel B is similar, but the words were obtained from the 2L chromosomal arm.

Figure 3

Relative X/2L and 3R/2L values for 5 10⁵ words randomly obtained from X (black) or 3R (red). For simplicity, ratios above 20 are not shown. The blue line indicate a value of 2.

Figure 4

Average values for relative word frequencies in chromosomes of seven Drosophila species. As in Figure 2, values from k = 1 to k = 13 are shown from left to right for each comparison between chromosomes.

Figure 5

Typical X/autosome profiles for 1 Mb of chromosome X sequences in the seven drosophilid species. Again, the y-axis reflects the relative frequency of the words in the pairs of chromosomes.

Figure 6

Comparison of the frequencies of 5 10⁵ words randomly taken from the chromosomes shown in the x-axis in both the chromosome from which the sequences were obtained (x-axis values) and a second chromosome (y-axis values). Panels A) and B) show intraspecific comparisons for D. melanogaster chromosomes. Panels C) and D) show comparisons between D. melanogaster and D. simulans chromosomes. Panels E) and F) show comparisons between D. melanogaster and D. virilis chromosomes.

Figure 7

Average values for relative word frequencies in comparisons involving the XR chromosomal arm of D. pseudoobscura. Again, values from k = 1 to k = 13 are shown for each comparison.

Figure 8

Comparisons of frequencies for 5 10⁵ words obtained from different D. pseudoobscura chromosomes. Details as in Figure 6.