Distinct genetic architectures underlie divergent thorax, leg, and wing pigmentation between Drosophila elegans and D. gunungcola

Abstract

Understanding the genetic basis of species differences is a major goal in evolutionary biology. Pigmentation divergence between Drosophila species often involves genetic changes in pigmentation candidate genes that pattern the body and wings, but it remains unclear how these changes affect pigmentation evolution in multiple body parts between the same diverging species. Drosophila elegans and D. gunungcola show pigmentation differences in the thorax, legs, and wings, with D. elegans exhibiting male-specific wing spots and D. gunungcola lacking wing spots with intensely dark thoraces and legs. Here, we performed QTL mapping to identify the genetic architecture of these differences. We find a large effect QTL on the X chromosome for all three body parts. QTL on Muller Element E were found for thorax pigmentation in both backcrosses but were only marginally significant in one backcross for the legs and wings. Consistent with this observation, we isolated the effects of the Muller Element E QTL by introgressing D. gunungcola alleles into a D. elegans genetic background and found that D. gunungcola alleles linked near the pigmentation candidate gene ebony caused intense darkening of the thorax, minimal darkening of legs, and minimal shrinking of wing spots. D. elegans ebony mutants showed changes in pigmentation consistent with Ebony having different effects on pigmentation in different tissues. Our results suggest that multiple genes have evolved differential effects on pigmentation levels in different body regions.