The yellow gene influences Drosophila male mating success through sex comb melanization

• Published in: eLife Vol. 8
• Main Authors: Massey, Jonathan H, Chung, Daayun, Siwanowicz, Igor, Stern, David L, Wittkopp, Patricia J
• Format: Journal Article
• Language: English
• Published: England eLife Science Publications, Ltd 15.10.2019; eLife Sciences Publications Ltd; eLife Sciences Publications, Ltd
• Subjects: Animal reproduction; Animals; Behavior; Biological Evolution; Biomechanical Phenomena; Bristles; Copulation; Copulation - physiology; Courtship; DNA-Binding Proteins - genetics; DNA-Binding Proteins - metabolism; Dopamine; Drosophila; Drosophila melanogaster - anatomy & histology; Drosophila melanogaster - genetics; Drosophila melanogaster - metabolism; Drosophila Proteins - deficiency; Drosophila Proteins - genetics; Drosophila Proteins - metabolism; Evolutionary Biology; Extremities - anatomy & histology; Female; Females; Gene expression; Gene Expression Regulation; Genetic aspects; Genetics and Genomics; Genotype & phenotype; Hypotheses; Insects; Male; male mating success; Males; Mating behavior; Mating Preference, Animal - physiology; Mechanical properties; Melanization; Morphology; Mutation; Nerve Tissue Proteins - genetics; Nerve Tissue Proteins - metabolism; Nervous system; Neural networks; Observations; Pigmentation; Pigmentation - genetics; Plasmids; sex comb; Sexual behavior; Song; Success; Transcription Factors - genetics; Transcription Factors - metabolism; Vigor; yellow; Yellow gene; United States; Ann Arbor Michigan; United States > US; India; male mating success; melanization; evolutionary biology; genetics; sex comb; yellow; genomics; D. melanogaster; mating behavior
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/eLife.49388

Drosophila melanogaster males perform a series of courtship behaviors that, when successful, result in copulation with a female. For over a century, mutations in the yellow gene, named for its effects on pigmentation, have been known to reduce male mating success. Prior work has suggested that yellow influences mating behavior through effects on wing extension, song, and/or courtship vigor. Here, we rule out these explanations, as well as effects on the nervous system more generally, and find instead that the effects of yellow on male mating success are mediated by its effects on pigmentation of male-specific leg structures called sex combs. Loss of yellow expression in these modified bristles reduces their melanization, which changes their structure and causes difficulty grasping females prior to copulation. These data illustrate why the mechanical properties of anatomy, not just neural circuitry, must be considered to fully understand the development and evolution of behavior. More than 100 years ago, Nobel-prize winning geneticist Thomas Hunt Morgan and his colleagues discovered that some fruit flies inherited genetic mutations that caused their body color to change. The yellow flies had a mutation in one specific gene and these mutants did not only look different from normal flies, they behaved differently too. Specifically, yellow males were far less successful at mating than normal males, demonstrating for the first time that some behaviors had a genetic basis. Since then it has remained a mystery how the genetic mutations that cause yellow coloration in fruit flies lead to unsuccessful mating attempts. Geneticists have long suggested that mutations in insect pigment genes cause changes in the fly’s brain because these pigments are made from dopamine, a chemical messenger that acts in the brain. They proposed that yellow flies must have altered levels of dopamine in their brains which was causing them to fail at mating. To solve this mystery, Massey et al. used a series of genetic experiments and high speed-videos to assess how mutations in male yellow fruit flies affected their mating behavior. The experiments showed that yellow fruit flies mated poorly not because of changes in their brain but because of changes in specialized structures on their legs called sex combs. The yellow males lack melanin pigments in their sex combs, which changes their structure. As a result, the yellow males would court female flies but were then unable to grab and mount them. This explains why yellow flies often fail to mate and why fruit flies have sex combs in the first place. The study reveals the importance of scientists considering that genes that affect behavior may do so by changing anatomy rather than by altering the brain. The results also may benefit those working to control insect pests. For example, they could help insect pest managers to develop strategies that prevent reproduction in other insects that spread disease or destroy crops.