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Visual attraction in Drosophila larvae develops during a critical period and is modulated by crowding conditions

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Abstract

The development of social behavior is poorly understood. Many animals adjust their behavior to environmental conditions based on a social context. Despite having relatively simple visual systems, Drosophila larvae are capable of identifying and are attracted to the movements of other larvae. Here, we show that Drosophila larval visual recognition is encoded by the movements of nearby larvae, experienced during a specific developmental critical period. Exposure to moving larvae, only during a specific period, is sufficient for later visual recognition of movement. Larvae exposed to wild-type body movements, during the critical period, are not attracted to the movements of tubby mutants, which have altered morphology. However, exposure to tubby, during the critical period, results in tubby recognition at the expense of wild-type recognition indicating that this is true learning. Visual recognition is not learned in excessively crowded conditions, and this is emulated by exposure, during the critical period, to food previously used by crowded larvae. We propose that Drosophila larvae have a distinct critical period, during which they assess both social and resource conditions, and that this irreversibly determines later visually guided social behavior. This model provides a platform towards understanding the regulation and development of social behavior.

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Acknowledgments

We thank Bloomington Stock Center for providing fly stocks, C. Deppmann, A. Guler, D. B. Bone and T. Dobrzelewski for reading and commenting on the manuscript, and J. Levine (U. Toronto) for initially encouraging these experiments. Special thanks to Jeremy Louissaint for making the initial observations. Fly strains were obtained from Bloomington Stock Center (NSF Grant No. DBI-0,841,154).

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Correspondence to Barry Condron.

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The authors declare no competing interest.

Funding

This work was supported by NSF Grants CRCNS 1010333, ABI 1062433, and the University of Virginia.

Additional information

Z. Slepian, K. Sundby, S. Glier and J. McDaniels contributed equally to this work.

Electronic supplementary material

359_2015_1034_MOESM1_ESM.tiff

Supplementary Figure S1. S1A. Specificity of visual attraction Same as 4B except that tracks of larvae were digitized as described for Fig. 3a. Twenty samples were used for each data point and heat-plot. S1B. Heat plots and representative traces are shown for each sample. Responses were compared between the different targets at 0 and at 80 % tubby (**p < 0.01; ***p < 0.001). Statistical analysis was performed using one-way ANOVA, followed by Tukey’s multiple-comparison posttest. (TIFF 1141 kb)

359_2015_1034_MOESM2_ESM.tiff

Supplementary Figure S2. S2AB. A more complete plot of times and group sizes with attraction to larval targets S2A and plastic targets S2B. (TIFF 987 kb)

Supplementary videos. S3- L3F2 attraction to a white plastic control (MOV 898 kb)

Supplementary videos. S4- L3F2 attraction to a tethered larval target (MOV 761 kb)

Supplementary videos. S5- L3F1 grouped 10x6 h in old food from a 20x8 h grouping. No attraction is seen. (MOV 674 kb)

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Slepian, Z., Sundby, K., Glier, S. et al. Visual attraction in Drosophila larvae develops during a critical period and is modulated by crowding conditions. J Comp Physiol A 201, 1019–1027 (2015). https://doi.org/10.1007/s00359-015-1034-3

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  • DOI: https://doi.org/10.1007/s00359-015-1034-3

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