Augmentation of a wound response element accompanies the origin of a Hox-regulated Drosophila abdominal pigmentation trait

Abstract

A challenge for evolutionary research is to uncover how new morphological traits evolve the coordinated spatial and temporal expression patterns of genes that govern their formation during development. Detailed studies are often limited to characterizing how one or a few genes contributed to a trait's emergence, and thus our knowledge of how entire GRNs evolve their coordinated expression of each gene remains unresolved. The melanic color patterns decorating the male abdominal tergites of Drosophila (D.) melanogaster evolved in part by novel expression patterns for genes acting at the terminus of a pigment metabolic pathway, driven by cis-regulatory elements (CREs) with distinct mechanisms of Hox regulation. Here, we examined the expression and evolutionary histories of two important enzymes in this pathway, encoded by the pale and Ddc genes. We found that while both genes exhibit dynamic patterns of expression, a robust pattern of Ddc expression specifically evolved in the lineage of fruit flies with pronounced melanic abdomens. Derived Ddc expression requires the activity of a CRE previously shown to activate expression in response to epidermal wounding. We show that a binding site for the Grainy head transcription factor that promotes the ancestral wound healing function of this CRE is also required for abdominal activity. Together with previous findings in this system, our work shows how the GRN for a novel trait emerged by assembling unique yet similarly functioning CREs from heterogeneous starting points.

Gene Regulatory Network Homoplasy Underlies Recurrent Sexually Dimorphic Fruit Fly Pigmentation

“…Dorsal abdomens were dissected at various pupal developmental stages between P10 and P15ii (P15ii being newly eclosed adults). Stages were identified by the presence of various morphological markers (Ashburner et al, 2005;Grover et al, 2018) (Supplementary Figure S1). Male and female samples were pooled, and females were distinguished by the removal of their wings.…”

“…The D. melanogaster abdominal pigmentation GRN has received considerable attention, which includes a metabolic pathway of differentiation genes whose expression correlates or anti-correlates with the dimorphic phenotype. Among the first acting genes in this pathway are pale and Ddc, which are expressed monomorphically in the abdominal epidermis (Grover et al, 2018), and their enzyme activities catalyze the production of Dopamine. ebony is expressed in a dimorphic pattern, with prominent expression in the female A5 and A6 segments (Rebeiz et al, 2009), and its encoded enzyme converts Dopamine to NBAD that is used to make yellowcolored sclerotin.…”

“…ebony is expressed in a dimorphic pattern, with prominent expression in the female A5 and A6 segments (Rebeiz et al, 2009), and its encoded enzyme converts Dopamine to NBAD that is used to make yellowcolored sclerotin. NBAD can be converted back into Dopamine by the enzyme encoded by tan, and converting Dopamine into black Dopamine-melanin requires the activity of the protein encoded by yellow (Grover et al, 2018). Both tan and yellow expression is upregulated in the male A5 and A6 segments (Camino et al, 2015).…”

From simplicity to complexity: The gain or loss of spot rows underlies the morphological diversity of threeDrosophilaspecies

“…Investigating how pigmentation develops in D. melanogaster provided the foundation to understand the same processes in other fruit flies. This knowledge, in turn, has facilitated studies of species divergence (Lamb et al, 2020) and positioned Drosophila pigmentation as a model to study how gene-regulatory networks – the regulatory mechanisms responsible for organismal development (Davidson and Levin, 2005) – evolved (Camino et al, 2015; Gibert et al, 2018; Grover et al, 2018; Ordway et al, 2014; Rebeiz and Williams, 2017; Roeske et al, 2018). The Drosophila pigmentation pathway with the enzymes and reactions necessary to produce black, brown, and yellow coloration seen on the bodies of fruit flies, is shown in Figure 1 (Rebeiz and Williams, 2017; True et al, 2005; Wittkopp et al, 2003).…”

The Development of Complex Abdominal Spot Patterns in Three Drosophila Species

“…Studying the evolution of GRNs responsible for Drosophila pigmentation continues to clarify the morphological diversity seen within the genus and allows us to better understand the evolution of complex structures (Camino et al, 2015;Carroll, 2000;Davidson and Levin, 2005;Grover et al, 2018;Jeong et al, 2008;Koshikawa et al, 2015;Ordway et al, 2014;Roeske et al, 2018). From the information presented in this study, we can continue to elucidate the GRN(s) responsible for creating complex spot patterns on the abdomen of D. guttifera, and start to understand this same process in two untouched species -D. palustris and D. subpalustris.…”