The genetic basis of adaptive pigmentation variation in Drosophila melanogaster

Abstract

In a broad survey of Drosophila melanogaster population samples, levels of abdominal pigmentation were found to be highly variable and geographically differentiated. A strong positive correlation was found between dark pigmentation and high altitude, suggesting adaptation to specific environments. DNA sequence polymorphism at the candidate gene ebony revealed a clear association with the pigmentation of homozygous third chromosome lines. The darkest lines sequenced had nearly identical haplotypes spanning 14.5 kb upstream of the protein-coding exons of ebony. Thus, natural selection may have elevated the frequency of an allele that confers dark abdominal pigmentation by influencing the regulation of ebony.

Figure 1. The diversity of female abdominal pigmentation observed in isofemale lines of D. melanogaster derived from natural populations

The upper left image depicts the specific location within the fourth abdominal segment where pigmentation was quantified (as grayscale darkness). The remaining images illustrate the range of A4 pigmentation values observed in our sample.

Figure 2. Geographic analysis of female abdominal pigmentation

(A) Location and mean A4 pigmentation for each population sample. Elevation range is indicated using the symbols listed above. The three samples from the western highlands of Cameroon are listed together and marked with an arrow. Kenya-N is marked with an open triangle – this sample was collected from multiple locations which range in altitude from 1070 to 2086 m. (B) The relationship between elevation and mean A4 pigmentation for 16 non-admixed sub-Saharan samples (Pool and Aquadro 2006). This correlation was found to be statistically significant (P = 5.10 × 10⁻⁴), with elevation accounting for the majority of variation in mean A4 pigmentation (R² = 0.590).

Figure 3. Gene features and haplotype identity in the ebony gene region

At the top, exons of ebony and neighboring genes are depicted (black exons are protein-coding, gray are non-coding). On the left, the sequenced lines are listed, each identified by its population (Uganda or Kenya) and its A4 pigmentation score. Identical haplotypes among two or more lines that extend more than 1 kb are illustrated with colored boxes. A red box indicates the 14.5 kb region of highly similar haplotypes among the darkest four lines. Green X’s represent putative gene conversion events, blue asterisks represent unique substitutions, and purple asterisks represent unique insertions or deletions that interrupt sequence identity among the darkest lines. Vertical lines indicate derived substitutions unique to the darkest four (red) or darkest five (orange) lines.