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Melanism:macrophysiology to molecules

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Front. Physiol. | doi: 10.3389/fphys.2019.00518

Pleiotropic effects of ebony and tan on pigmentation and cuticular hydrocarbon composition in Drosophila melanogaster

 Jonathan H. Massey1, 2, Noriyoshi Akiyama3, Tanja Bien4, 5,  Klaus Dreisewerd6, 7,  Patricia J. Wittkopp1, 8*,  Joanne Y. Yew9* and  Aya Takahashi3, 10*
  • 1Department of Ecology and Evolution, University of Michigan, United States
  • 2Howard Hughes Medical Institute, Janelia Research Campus, United States
  • 3Department of Biological Sciences, Tokyo Metropolitan University, Japan
  • 4Institute for Hygiene, University of Münster, Germany
  • 5Interdisziplinären Zentrum für Klinische Forschung, Medizinische Fakultät Münster, Germany
  • 6Institute of Hygiene, University Hospital Münster, Germany
  • 7Interdisciplinary Center for Clinical Research (IZKF), University of Münster, Germany
  • 8Department of Molecular, Cellular, and Developmental Biology, College of Literature, Science, and the Arts, University of Michigan, United States
  • 9Pacific Biosciences Research Center, University of Hawaii, United States
  • 10Research Center for Genomics and Bioinformatics, Tokyo Metropolitan University, Japan

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.

Keywords: Drosophila, pleiotropy, Ebony, TaN, Pigmentation, cuticular hydrocarbons, Trait covariation, Dopamine

Received: 01 Feb 2019; Accepted: 11 Apr 2019.

Edited by:

Geoffrey A. Head, Baker Heart and Diabetes Institute, Australia

Reviewed by:

Jean-Michel Gibert, Centre National de la Recherche Scientifique (CNRS), France
Thomas Williams, University of Dayton, United States  

Copyright: © 2019 Massey, Akiyama, Bien, Dreisewerd, Wittkopp, Yew and Takahashi. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence:
Dr. Patricia J. Wittkopp, University of Michigan, Department of Ecology and Evolution, Ann Arbor, 48109, Michigan, United States, wittkopp@umich.edu
Dr. Joanne Y. Yew, University of Hawaii, Pacific Biosciences Research Center, Honolulu, 1107 2020, Hawaii, United States, jyew@hawaii.edu
Dr. Aya Takahashi, Tokyo Metropolitan University, Department of Biological Sciences, Hachioji, 192-0397, Tōkyō, Japan, ayat@tmu.ac.jp