The regulation of a pigmentation gene in the formation of complex color patterns in Drosophila abdomens

Abstract

Changes in cis-regulatory modules (CRMs) that control developmental gene expression patterns have been implicated in the evolution of animal morphology1-6. However, the genetic mechanisms underlying complex morphological traits remain largely unknown. Here we investigated the molecular mechanisms that induce the pigmentation gene yellow (y) in a complex spot and shade pattern on the abdomen of the quinaria group species Drosophila guttifera. We show that the y expression pattern is controlled by only one CRM, which contains a stripe-inducing CRM at its core. We identified several developmental genes that may collectively interact with the CRM to orchestrate the patterning in the pupal abdomen of D. guttifera. We further show that the core CRM is conserved among D. guttifera and the closely related quinaria group species Drosophila deflecta, which displays a similarly spotted abdominal pigment pattern. Our data suggest that besides direct activation of patterns in distinct spots, abdominal spot patterns in Drosophila species may have evolved through partial repression of an ancestral stripe pattern, leaving isolated spots behind. Abdominal pigment patterns of extant quinaria group species support the partial repression hypothesis and further emphasize the modularity of the D. guttifera pattern.