Pleiotropic Effects of ebony and tan on Pigmentation and Cuticular Hydrocarbon Composition in Drosophila melanogaster.

Jonathan H Massey,Noriyoshi Akiyama,Aya Takahashi,Klaus Dreisewerd,Patricia J Wittkopp,Tanja Bien,Joanne Y Yew

doi:10.3389/fphys.2019.00518

Abstract

Pleiotropic genes are genes that affect more than one trait. For example, many genes required for pigmentation in the fruit fly Drosophila melanogaster also affect traits such as circadian rhythms, vision, and mating behavior. Here, we present evidence that two pigmentation genes, ebony and tan, which encode enzymes catalyzing reciprocal reactions in the melanin biosynthesis pathway, also affect cuticular hydrocarbon (CHC) composition in D. melanogaster females. More specifically, we report that ebony loss-of-function mutants have a CHC profile that is biased toward long (>25C) chain CHCs, whereas tan loss-of-function mutants have a CHC profile that is biased toward short (<25C) chain CHCs. Moreover, pharmacological inhibition of dopamine synthesis, a key step in the melanin synthesis pathway, reversed the changes in CHC composition seen in ebony mutants, making the CHC profiles similar to those seen in tan mutants. These observations suggest that genetic variation affecting ebony and/or tan activity might cause correlated changes in pigmentation and CHC composition in natural populations. We tested this possibility using the Drosophila Genetic Reference Panel (DGRP) and found that CHC composition covaried with pigmentation as well as levels of ebony and tan expression in newly eclosed adults in a manner consistent with the ebony and tan mutant phenotypes. These data suggest that the pleiotropic effects of ebony and tan might contribute to covariation of pigmentation and CHC profiles in Drosophila.

Highlights

When organisms adapt to novel environments, genetic changes often cause multiple traits to evolve
We found that ebonyCRISPR(1,2) flies tended to show lower levels of short chain cuticular hydrocarbon (CHC) (25C), suggesting that disrupting the function of ebony causes a CHC lengthening effect (Figure 1D, Spearman’s ρ = 0.83, P < 1.0 × 10−5)
Our results suggest (1) that ebony and tan have a previously undescribed role in CHC synthesis and/or deposition and (2) that pleiotropy of both genes might influence the covariation of pigmentation and CHC composition

Summary

Introduction

When organisms adapt to novel environments, genetic changes often cause multiple traits to evolve. For example, marine populations independently invading freshwater lake habitats have repeatedly evolved similar changes in defensive armor, behavior, Pleiotropic Effects of ebony and tan and body shape (Walker and Bell, 2000; Schluter et al, 2004; Wark et al, 2011). Such correlated evolution might result from (i) selection favoring a particular suite of traits (i.e., selection targeting multiple unlinked loci), (ii) selection favoring a trait that is genetically linked to genes affecting other traits, or (iii) selection favoring a trait that varies due to genetic variation at a pleiotropic gene affecting multiple traits. Studies in various other plant and animal species support the hypothesis that pleiotropy contributes to the coevolution of correlated traits (e.g., McKay et al, 2003; McLean et al, 2011; Duveau and Félix, 2012; Nagy et al, 2018)

Methods

Results

Conclusion