The Genetic Basis of Pigmentation Differences Within and Between Drosophila Species

Abstract

In Drosophila, as well as in many other plants and animals, pigmentation is highly variable both within and between species. This variability, combined with powerful genetic and transgenic tools as well as knowledge of how pigment patterns are formed biochemically and developmentally, has made Drosophila pigmentation a premier system for investigating the genetic and molecular mechanisms responsible for phenotypic evolution. In this chapter, we review and synthesize findings from a rapidly growing body of case studies examining the genetic basis of pigmentation differences in the abdomen, thorax, wings, and pupal cases within and between Drosophila species. A core set of genes, including genes required for pigment synthesis (eg, yellow, ebony, tan, Dat) as well as developmental regulators of these genes (eg, bab1, bab2, omb, Dll, and wg), emerge as the primary sources of this variation, with most genes having been shown to contribute to pigmentation differences both within and between species. In cases where specific genetic changes contributing to pigmentation divergence were identified in these genes, the changes were always located in noncoding sequences and affected cis-regulatory activity. We conclude this chapter by discussing these and other lessons learned from evolutionary genetic studies of Drosophila pigmentation and identify topics we think should be the focus of future work with this model system.

Keywords: Evolution; Gene expression; Melanin; bric-a-brac; cis-Regulation; ebony; tan; wingless; yellow.

Figure 1. Developmental and biochemical control of pigmentation in Drosophila

A simplified version of the biochemical pathway controlling pigment biosynthesis in insects is shown with regulators controlling expression of individual pigment synthesis genes in at least one Drosophila species overlaid. Genes colored red are part of the pigment biosynthesis pathway; metabolites are colored gray; and gray arrows indicate chemical reactions during pigmentation synthesis. Genes colored in blue are part of the regulatory network that directly (solid arrows) or indirectly (broken arrows) modulate enzyme expression during pigmentation development in Drosophila. Pointed and blunt arrows indicate positive and negative regulatory interactions, respectively. The pigment biosynthesis pathway is conserved among all Drosophila, but the regulatory relationships shown often function in only a subset of Drosophila species (Gompel et al. 2005; Arnoult et al. 2013).

Figure 2. Abdominal pigmentation in D. melanogaster

The dorsal abdomen of D. melanogaster is shown for wild-type adult females (left) and males (right). Note the dark pigment stripe visible at the posterior edge of abdominal segments A2-A6 in females and A2-A4 in males as well as the more complete melanization in tergites A5 and A6 of males relative to females.

Figure 3. Phylogeny of Drosophila species used to study the genetic basis of pigmentation evolution

Phylogenetic relationships shown were inferred using the online Interactive Tree of Life (iTOL) (Letunic and Bork 2007; 2011), with branch lengths estimated using data from the online Time Tree website (Hedges et al. 2006).

Figure 4. The loci of pigmentation evolution

A summary of genes implicated in pigmentation differences within and/or between species is shown. Genes labeled in blue are regulators of pigmentation development. Genes labeled in red are involved in the pigment biosynthesis pathway. All genetic changes identified as likely to be contributing to a pigmentation difference either within or between species thus far affect cis-regulatory sequences.