Abstract
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.
Highlights
In one-hour trials, we found that virgin males homozygous for a null allele of the yellow gene (y1) successfully mated with wild-type virgin females only 3% of the time, whereas wild-type males mated with wild-type virgin females 93% of the time (Fisher’s exact test, p=6Â10À13; Figure 1C)
We found that reducing yellow expression in dsx-expressing cells with either of two different dsxGAL4 drivers (Robinett et al, 2010; Rideout et al, 2010) strongly reduced male mating success (Figure 2C, Fisher’s exact test (FET), p=7Â10À9 and 1 Â 10À7; Figure 2—figure supplement 1A, FET, p=0.002 and 0.002), whereas restoring yellow activity in cells expressing dsxGAL4 in y1 mutants significantly increased male mating success compared with y1 controls (Figure 2D, FET, p=0.001 and 0.0004; Figure 2—figure supplement 1B, FET, p=5Â10À10 and 5 Â 10À10)
We find that the reduced mating success of D. melanogaster yellow mutant males, which was perceived as a behavioral defect for decades, is caused by changes in the morphology of the structures used during mating
Summary
“The form of any behavior depends to a degree on the form of the morphology performing it.” – West-Eberhard (2003). The interaction between Yellow and dopamine might explain the protein’s effects on male mating success because dopamine acts as a modulator of male courtship drive in D. melanogaster (Zhang et al, 2016) These effects of dopamine are mediated by neurons expressing the gene fruitless (fru) (Zhang et al, 2016), which is a master regulator of sexually dimorphic behavior in D. melanogaster that can affect every component of courtship and copulation (reviewed in Villella and Hall, 2008). Consistent with this hypothesis, functional links between the pigment synthesis pathway and behavior mediated by the nervous system have previously been reported for other pigmentation genes (Hotta and Benzer, 1969; Heisenberg, 1971; Borycz et al, 2002; Richardt et al, 2002; True et al, 2005; Suh and Jackson, 2007)
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