A portrait of copy-number polymorphism in Drosophila melanogaster

Abstract

Thomas Hunt Morgan and colleagues identified variation in gene copy number in Drosophila in the 1920s and 1930s and linked such variation to phenotypic differences [Bridges CB (1936) Science 83:210]. Yet the extent of variation in the number of chromosomes, chromosomal regions, or gene copies, and the importance of this variation within species, remain poorly understood. Here, we focus on copy-number variation in Drosophila melanogaster. We characterize copy-number polymorphism (CNP) across genomic regions, and we contrast patterns to infer the evolutionary processes acting on this variation. Copy-number variation in D. melanogaster is nonrandomly distributed, presumably because of a mutational bias produced by tandem repeats or other mechanisms. Comparisons of coding and noncoding CNPs, however, reveal a strong effect of purifying selection in the removal of structural variation from functionally constrained regions. Most patterns of CNP in D. melanogaster suggest that negative selection and mutational biases are the primary agents responsible for shaping structural variation.

Fig. 1.

Average and standard error of log-intensity ratios in self–self hybridization (A) and male–female hybridization (B) (±0.3 threshold is in blue). Red, X chromosome; green, chromosome 2L; orange, chromosome 2R;purple, chromosome 3L; yellow, chromosome 3R; gray, chromosome 4.

Fig. 2.

Distribution of probes (black = coding, gray = noncoding + intergenic) and copy-number polymorphisms (red) on chromosome arm 3R. (Inset) Approximately 1 Mb of 3R is shown that illustrates clustering and noncoding bias.