Quantitative trait loci affecting the difference in pigmentation between Drosophila yakuba and D. santomea

Abstract

Using quantitative trait locus (QTL) mapping, we studied the genetic basis of the difference in pigmentation between two sister species of Drosophila: Drosophila yakuba, which, like other members of the D. melanogaster subgroup, shows heavy black pigmentation on the abdomen of males and females, and D. santomea, an endemic to the African island of São Tomé, which has virtually no pigmentation. Here we mapped four QTL with large effects on this interspecific difference in pigmentation: two on the X chromosome and one each on the second and third chromosomes. The same four QTL were detected in male hybrids in the backcrosses to both D. santomea and D. yakuba and in the female D. yakuba backcross hybrids. All four QTL exhibited strong epistatic interactions in male backcross hybrids, but only one pair of QTL interacted in females from the backcross to D. yabuka. All QTL from each species affected pigmentation in the same direction, consistent with adaptive evolution driven by directional natural selection. The regions delimited by the QTL included many positional candidate loci in the pigmentation pathway, including genes affecting catecholamine biosynthesis, melanization of the cuticle, and many additional pleiotropic effects.

Figure 1.

QTL affecting variation in pigmentation between D. yakuba and D. santomea. (A) F₁ females [from D. yakuba (males) × D. santomea (females)] backcrossed to D. yakuba males. (B) F₁ females [from D. yakuba (females) × D. santomea (males)] backcrossed to D. santomea males. Molecular makers are indicated as triangles on the x-axis. Plots are likelihood-ratio (LR) test statistics for pigmentation differences between males (teal) and females (magenta) as determined by composite interval mapping. Significance thresholds for each cross were determined by permutation and are ∼LR = 10 for each cross, denoted by the dashed horizontal line.

Figure 2.

Pairwise epistasis between markers. The significance of all pairwise interactions between markers for males from the backcross to D. santomea is indicated above the diagonal, and for interactions for males from the backcross to D. yakuba it is shown below the diagonal. (Magenta box) P < 0.0001 (Bonferroni correction); (blue box) 0.0001 < P < 0.001; (teal box) 0.001 < P < 0.01; (light purple box) 0.01 < P < 0.05.

Figure 3.

Significant epistatic interactions between QTL, depicted as reaction norms. Values shown are the mean pigmentation scores (y-axis) for a particular genotype in the background of another genotype. (A) Backcrosses to D. santomea males. (B) Backcrosses to D. yakuba males. Epistatic interactions are shown for the significant markers common to both backcross populations, as shown in Figure 2 (M1 × M9, M8 × M18, M8 × M25, and M18 × M25). See Table 3 for marker definitions. Marker genotypes are indicated as D. santomea (A) or D. yakuba (B) homozygote (blue circle) and D. santomea/D. yakuba heterozygote (purple triangle).

Figure 4.

Mean pigmentation scores (y-axis) of the eight marker haplotypes derived from the four QTL with large effects on pigmentation. The letters denote the genotype of the QTL allele (S, D. santomea; Y, D. yakuba), and the order of the letters indicates the genotype for the QTL at the tip of the X chromosome, the QTL at the base of the X chromosome, the second chromosome QTL, and the third chromosome QTL, respectively. Haplotypes refer to the markers at the peak LR in the respective QTL analyses. See Table 3 for marker descriptions. Haplotypes for male backcross hybrids are hemizygous D. yakuba and/or D. santomea for the two X chromosome QTL. The X chromosome QTL in female backcross hybrids and all autosomal QTL are heterozygous or homozygous; the marker genotype of the nonrecurrent parent is indicated. (A) Males from the backcross to D. santomea. Haplotypes are for markers M1, M7, M15, and M24. (B) Males from the backcross to D. yakuba. Haplotypes are for markers M2, M7, M15, and M24. (C) Females from the backcross to D. yakuba. Haplotypes are for markers M1, M8, M15, and M24. The bar graphs are color coded (increasing ratio of black to yellow) to indicate increasing number of D. yakuba alleles and pigmentation scores.