The generation of acoustic communication signals is widespread across the animal kingdom1,2, and males of many species, including Drosophilidae, produce patterned courtship songs to increase their chance of success with a female. For some animals, song structure can vary considerably from one rendition to the next3; neural noise within pattern generating circuits is widely assumed to be the primary source of such variability, and statistical models that incorporate neural noise are successful at reproducing the full variation present in natural songs4. In direct contrast, here we demonstrate that much of the pattern variability in Drosophila courtship song can be explained by taking into account the dynamic sensory experience of the male. In particular, using a quantitative behavioural assay combined with computational modelling, we find that males use fast modulations in visual and self-motion signals to pattern their songs, a relationship that we show is evolutionarily conserved. Using neural circuit manipulations, we also identify the pathways involved in song patterning choices and show that females are sensitive to song features. Our data not only demonstrate that Drosophila song production is not a fixed action pattern5,6, but establish Drosophila as a valuable new model for studies of rapid decision-making under both social and naturalistic conditions.
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We thank B. Arthur and D. Stern for assistance in establishing the song recording system; P. Andolfatto for wild-type fly strains; S. Kamal and V. Cheng for assistance with selecting and maintaining fly strains; G. Guan for technical assistance; T. Tayler for help with injections; J. Shaevitz for help with the fly tracker; R. da Silveira for early discussions on reverse correlation; and G. Laurent, C. Brody, D. Aronov, I. Fiete, M. Ryan, and the entire Murthy lab for thoughtful feedback and comments on the manuscript. Figure 1a was illustrated by K. Ris-Vicari. P.C. is funded by an HHMI International Predoctoral Fellowship and M.M. is funded by the Alfred P. Sloan Foundation, the Human Frontiers Science Program, an NSF CAREER award, the McKnight Endowment Fund, and the Klingenstein Foundation.
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The video shows two flies (WT1 male (grey) and PIBL female (magenta)) interacting in the behavioural chamber, and tracked with our software. Male and female centres are indicated by the larger circles. Dots mark 3 positions along the body axis, with head direction indicated by the larger circles. Lines indicate 3 seconds of tracking history for each fly.
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