Oligogenic Adaptation, Soft Sweeps, and Parallel Melanic Evolution inDrosophila melanogaster

Unraveling the genetic architecture of adaptive phenotypic divergence is a fundamental quest in evolutionary biology. In Drosophila melanogaster, high-altitude melanism has evolved in separate mountain ranges in sub-Saharan Africa, potentially as an adaptation to UV intensity. We investigated the genetic basis of this melanism in three populations using a new bulk segregant analysis mapping method. Although hundreds of genes are known to affect cuticular pigmentation in D. melanogaster, we identified only 19 distinct QTLs from 9 mapping crosses, with several QTL peaks being shared among two or all populations. Surprisingly, we did not find wide signals of genetic differentiation ( F st ) between lightly and darkly pigmented populations at these QTLs, in spite of the pronounced phenotypic difference in pigmentation. Instead, we found small numbers of highly differentiated SNPs at the probable causative genes. A simulation analysis showed that these patterns of polymorphism are consistent with selection on standing genetic variation (leading to “soft sweeps“). Our results thus support a role for oligogenic selection on standing genetic variation in driving parallel ecological adaptation.