Neural Changes Underlying Rapid Fly Song Evolution

Abstract

11The neural basis for behavioural evolution is poorly understood. Functional comparisons 12 of homologous neurons may reveal how neural circuitry contributes to behavioural 13 evolution, but homologous neurons cannot be identified and manipulated in most taxa.14 Here, we compare the function of homologous courtship song neurons by exporting 15 neurogenetic reagents that label identified neurons in Drosophila melanogaster to D. 16 yakuba. We found a conserved role for a cluster of brain neurons that establish a 17 persistent courtship state. In contrast, a descending neuron with conserved 18 electrophysiological properties drives different song types in each species. Our results 19suggest that song evolved, in part, due to changes in the neural circuitry downstream of 20 this descending neuron. This experimental approach can be generalized to other neural 21 circuits and therefore provides an experimental framework for studying how the nervous 22 system has evolved to generate behavioural diversity. 24peer-reviewed) is the author/funder. All rights reserved. No reuse allowed without permission.The copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/238147 doi: bioRxiv preprint first posted online Dec. 21, 2017; 2 however, do not sing sine song, but they produce two distinct modes of pulse song: thud 54 peer-reviewed) is the author/funder. All rights reserved. No reuse allowed without permission. Main textThe copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/238147 doi: bioRxiv preprint first posted online Dec. 21, 2017; 3 song and clack song 11 . Thud song is generated by unilateral wing vibration; while clack 55 song is generated when males vibrate both wings behind them (Fig. 1a) moving faster than when males sing pulse song (Fig. 1e, f). Additionally, males sing 68 pulse song mostly when they are located directly behind females, whilst they sing clack 69 song across a wide range of distances and positions relative to females (Fig. 1g) 11 . 70Consistent with these observations, removing motion signals by providing males with a 71 motionless decapitated female eliminated clack song but not pulse song (Fig. 1h, i shown to reduce wing extension during courtship 15 . We found that pIP10 inhibition in D.144 peer-reviewed) is the author/funder. All rights reserved. No reuse allowed without permission.The copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/238147 doi: bioRxiv preprint first posted online Dec. 21, 2017; 6 melanogaster using our new split-GAL4 line caused almost complete elimination of 145 pulse song and a small reduction in sine song produced during normal courtship (Fig. 146 2a). In contrast, pIP10 inhibition in D. yakuba eliminated clack song consistently across 147 different split-GAL4 drivers and neuronal inhibitors (Fig. 2b and Extended Data Fig. 5a-148 c). In addition, in some treatments, pIP10 inhibition resulted in a quantitative reduction 149 of pulse song (Extended Data Fig. 5a, c). Th...

How to Build a Behavior

“…This tunability has been previously suggested in game theoretic models of aggression (e.g., ‘‘badges of dominance’’), where continuously tunable threat signals are used to explain variability in a population (Maynard Smith and Harper, 1988). In addition, the observed threshold dependence in the neural control of behavior is reminiscent of recent results in Drosophila courtship behavior, where different levels of activation were found to drive species-specific song outputs (Ding et al, 2017), as well as previous results showing that activating the same set of neurons could engender either aggressive or courtship behavior in flies (Hoopfer et al, 2015).…”

Discovery of a New Song Mode in Drosophila Reveals Hidden Structure in the Sensory and Neural Drivers of Behavior

“…The most parsiminous explanation for this pattern is that the existence of these two pulse types predates the species split and that D. sechellia has lost the ancestral P fast type. Interestingly, D. yakuba —a member of the melanogaster group outside of the branch considered here (Figure 2G)—produces two pulse types termed “thud” and “clack” that are produced at different distances to the female [40, 41], just as with P slow and P fast in D. melanogaster . Notably, pIP10 activation in D. yakuba [41] and in D. melanogaster (Figure 4B3) biases the song toward the louder and higher frequency pulse type.…”

Neural control of sexually dimorphic social behaviors

“…Although the overall displays of sexually dimorphic social behaviors are often conserved at a coarse level, many features of these behaviors can differ even between closely related species. Ding and colleagues have recently shown that qualitative differences in the courtship songs of two species, D. melanogaster and D. yakuba, are not due to changes in central song-command neurons (P1 neurons), but instead may be caused by changes in circuitry downstream of descending neurons that drive song [11]. In a separate study, Ding and colleagues found that strain- and species-specific differences in sine song characteristics have arisen from mutations at the locus encoding the slowpoke ion channel, although the neural site of action of this widely expressed gene is presently unknown [12].…”