Multilocus analysis of introgression between two sympatric sister species of Drosophila: Drosophila yakuba and D. santomea

Abstract

Drosophila yakuba is widely distributed in sub-Saharan Africa, while D. santomea is endemic to the volcanic island of São Tomé in the Atlantic Ocean, 280 km west of Gabon. On São Tomé, D. yakuba is found mainly in open lowland forests, and D. santomea is restricted to the wet misty forests at higher elevations. At intermediate elevations, the species form a hybrid zone where hybrids occur at a frequency of approximately 1%. To determine the extent of gene flow between these species we studied polymorphism and divergence patterns in 29 regions distributed throughout the genome, including mtDNA and three genes on the Y chromosome. This multilocus approach, together with the comparison to the two allopatric species D. mauritiana and D. sechellia, allowed us to distinguish between forces that should affect all genes and forces that should act on some genes (e.g., introgression). Our results show that D. yakuba mtDNA has replaced that of D. santomea and that there is also significant introgression for two nuclear genes, yellow and salr. The majority of genes, however, has remained distinct. These two species therefore do not form a "hybrid swarm" in which much of the genome shows substantial introgression while disruptive selection maintains distinctness for only a few traits (e.g., pigmentation and male genitalia).

Figure 1.

Chromosomal locations of the loci included in the polymorphism survey. Cytological positions were inferred from D. melanogaster and the comparative salivary-gland banding maps of Lemeunier and Ashburner (1976). Solid circles symbolize the centromeric regions of the chromosomes. Loci in regions of reduced crossing over are indicated by asterisks.

Figure 2.

Schematic of the phylogenetic relationships among the nine species of the D. melanogaster subgroup (Kliman et al. 2000; Lachaise et al. 2000; Parsch 2003).

Figure 3.

Gene genealogies from the Y chromosome and mtDNA. The reconstruction was done using the neighbor-joining algorithm (Saitou and Nei 1987). The numbers above the branches are bootstrap values based on 1000 replicates (>50%). Solid squares, D. yakuba; open circles, D. santomea.