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Original Research Article

A novel sex difference in Drosophila contact chemosensory neurons unveiled using single cell labeling

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Pages 116-124 | Received 02 Aug 2018, Accepted 27 Sep 2018, Published online: 20 Nov 2018

References

  • Awasaki, T., & Kimura, K. (1997). pox-neuro is required for development of chemosensory bristles in Drosophila. Journal of Neurobiology, 32, 707–721. doi:10.1002/(SICI)1097-4695(19970620)32:7<707::AID-NEU6>3.0.CO;2-8
  • Bastock, M., & Manning, A. (1955). The courtship of Drosophila melanogaster. Behaviour, 158, 1569–1595.
  • Billeter, J. C., Atallah, J., Krupp, J. J., Millar, J. G., & Levine, J. D. (2009). Specialized cells tag sexual and species identity in Drosophila melanogaster. Nature, 461, 987–991. doi:10.1038/nature08495
  • Boll, W., & Noll, M. (2002). The Drosophila Pox neuro gene: Control of male courtship behavior and fertility as revealed by a complete dissection of all enhancers. Development, 129, 5667–5681. doi:10.1242/dev.00157
  • Brieger, G., & Butterworth, F. N. (1970). Drosophila melanogaster: Identity of male lipid in reproductive system. Science, 167, 1262. doi:10.1126/science.167.3922.1262
  • Clowney, E. J., Iguchi, S., Bussell, J. J., Scheer, E., & Ruta, V. (2015). Multimodal chemosensory circuits controlling male courtship in Drosophila. Neuron, 87, 1036–1049. doi:10.1016/j.neuron.2015.07.025
  • Coen, P., Clemens, J., Weinstein, A. J., Pacheco, D. A., Deng, Y., & Murthy, M. (2014). Dynamic sensory cues shape song structure in Drosophila. Nature, 507, 233–237. doi:10.1038/nature13131.
  • Dickson, B. J. (2008). Wired for sex: the neurobiology of Drosophila mating decisions. Science, 322, 904–909. doi:10.1126/science.1159276
  • Dweck, H. K., Ebrahim, S. A., Thoma, M., Mohamed, A. A., Keesey, I. W., Trona, F., … Hansson, B. S. (2015). Pheromones mediating copulation and attraction in Drosophila. Proceedings of the National Academy of Sciences of United States of America, 112, E2829–E2835. doi:10.1073/pnas.1504527112
  • Fan, P., Manoli, D. S., Ahmed, O. M., Chen, Y., Agarwal, N., Kwong, S., … Shah, N. M. (2013). Genetic and neural mechanisms that inhibit Drosophila from mating with other species. Cell, 154, 89–102. doi:10.1016/j.cell.2013.06.008
  • Ferveur, J.-F. (1997). The pheromonal role of cuticular hydrocarbons in Drosophila melanogaster. BioEssays, 19, 353–358.
  • Grosjean, Y., Rytz, R., Farine, J. P., Abuin, L., Cortot, J., Jefferis, G. S. X. E., & Benton, R. (2011). An olfactory receptor for food-derived odours promotes male courtship in Drosophila. Nature, 478, 236–240. doi:10.1038/nature10428
  • Jallon, J.-M. (1984). A few chemical words exchanged by Drosophila during courtship and mating. Behavior Genetics, 14, 441–478.
  • Jallon, J.-M., Antony, C., & Benamar, O. (1981). Un anti-aphrodisiaque produit par les males Drosophila melanogaster et transferé aux femelles lors de la copulation. Comptes Rendus de l’Académie des Sciences, Paris, 292, 1147–1149.
  • Kallman, B. R., Kim, H., & Scott, K. (2015). Excitation and inhibition onto central courtship neurons biases Drosophila mate choice. eLife, 4, e11188. doi:10.7554/eLife.11188
  • Kimura, K-i., Hachiya, T., Koganezawa, M., Tazawa, T., & Yamamoto, D. (2008). Fruitless and Doublesex coordinate to generate male-specific neurons that can initiate courtship. Neuron, 59, 759–769. doi:10.1016/j.neuron.2008.06.007
  • Kimura, K-i., Sato, C., Yamamoto, K., & Yamamoto, D. (2015). From the back or front: The courtship position is a matter of smell and sight in Drosophila melanogaster males. Journal of Neurogenetics, 29, 18–22. doi:10.3109/01677063.2014.968278
  • Koganezawa, M., Haba, D., Matsuo, T., & Yamamoto, D. (2010). The shaping of male courtship posture by lateralized gustatory inputs to male-specific interneurons. Current Biology, 20, 1–8. doi:10.1016/j.cub.2009
  • Koh, T. W., He, Z., Gorur-Shandilya, S., Menuz, K., Larter, N. K., Stewart, S., & Carlson, J. R. (2014). The Drosophila IR20a clade of ionotropic receptors are candidate taste and pheromone receptors. Neuron, 83, 850–865. doi:10.1016/j.neuron.2014.07.012
  • Kohatsu, S., Koganezawa, M., & Yamamoto, D. (2011). Female contact activates male-specific interneurons that trigger stereotypic courtship behavior in Drosophila. Neuron, 69, 498–508. doi:10.1016/j.neuron.2010.12.017
  • Krstic, D., Boll, W., & Noll, M. (2009). Sensory integration regulating male courtship behavior in Drosophila. PLoS One, 4, e4457. doi:10.1371/journal.pone.0004457
  • Kurtovic, A., Widmer, A., & Dickson, B. J. (2007). A single class of olfactory neurons mediates behavioral responses to a Drosophila sex pheromone. Nature, 446, 542–546.
  • Lebreton, S., Boffero-Echeverry, F., Gonzalez, F., Solum, M., Wallin, E. A., Hedenström, E., … Witzgall, P. (2017). A Drosophila female pheromone elicits species-specific long-range attraction via an olfactory channel with dual specificity for sex and food. BMC Biology, 15, 88. doi:10.1186/s12915-017-0427-x
  • Lebreton, S., Grabe, V., Omondi, A. B., Ignell, R., Becher, P. G., Hansson, B. S., … Witzgall, P. (2014). Love makes smell blind: Mating suppresses pheromone attraction in Drosophila females via Or65a olfactory neurons. Scientific Reports, 4, 7119. doi:10.1038/srep07119
  • Lee, T., & Luo, L. (1999). Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron, 22, 451–461.
  • Lin, H., Mann, K. J., Starostina, E., Kinser, R. D., & Pikielny, C. W. (2005). A Drosophila DEG/ENaC channel subunit is required for male response to female pheromones. Proceedings of the National Academy of Sciences of United States of America, 102, 12831–12836.
  • Ling, F., Dahanukar, A., Weiss, L. A., Kwon, J. Y., & Carlson, J. R. (2014). The molecular and cellular basis of taste coding in the legs of Drosophila. Journal of Neuroscience, 34, 7148–7164. doi:10.1523/JNEUROSCI.0649-14.2014
  • Lu, B., LaMora, A., Sun, Y., Welsh, M. J., & Ben-Shahar, Y. (2012). ppk23-dependent chemosensory functions contribute to courtship behavior in Drosophila. PLoS Genetics, 8, e1002587. doi:10.1371/journal.pgen.1002587
  • Mellert, D. J., Knapp, J., Manoli, D. S., Meissner, G. W., & Baker, B. S. (2010). Midline crossing by gustatory receptor neuron axons is regulated by fruitless, doublesex and Roundabout receptors. Development, 137, 323–332.
  • Miyamoto, T., & Amrein, H. (2008). Suppression of male courtship by a Drosophila pheromone receptor. Nature Neuroscience, 11, 874–876. doi:10.1038/nn.2161
  • Moon, S. J., Lee, Y., Jiao, Y., & Montell, C. (2009). A Drosophila gustatory receptor essential for aversive taste and inhibiting male-to-male courtship. Current Biology, 19, 1623–1627. doi:10.1016/j.cub.2009.07.061
  • Nottebohm, E., Usui, A., Therianos, S., Kimura, K-i., Dambly-Chaudière, C., & Ghysen, A. (1994). The gene poxn controls different steps of the formation of chemosensory organs in Drosophila. Neuron, 12, 25–34.
  • von Philipsborn, A. C., Liu, T., Yu, J. Y., Masser, C., Bidaye, S. S., & Dickson, B. J. (2011). Neuronal control of Drosophila courtship song. Neuron, 69, 509–522. doi:10.1016/j.neuron.2011.01.011
  • Possidente, D. R., & Murphey, R. K. (1989). Genetic control of sexually dimorphic axon morphology in Drosophila sensory neurons. Developmental Biology, 132, 448–457.
  • Shankar, S., Chua, J. Y., Tan, K. J., Calvert, M. E., Weng, R., Ng, W. C., … Yew, J. Y. (2015). The neuropeptide tachykinin is essential for pheromone detection in a gustatory neural circuit. eLife, 4, e06914. doi:10.7554/eLife.06914
  • Spieth, H.T. (1952). Mating behavior within the genus Drosophila (Diptera). Bulletin of the American Museum of Natural History, 99, 399–474.
  • Stockinger, P., Kvitsiani, D., Rotkopf, S., Tirian, L., & Dickson, B.J. (2005). Neural circuitry that governs Drosophila male courtship behavior. Cell, 121, 795–807. doi:10.1016/j.cell.2005.04.026
  • Sung, H. Y., Jeong, Y. T., Lim, J. Y., Kim, H., Oh, S. M., Hwang, S. W., … Moon, S. J. (2017). Heterogeneity in the Drosophila gustatory receptor complexes that detect aversive compounds. Nature Communications, 8, 1484. doi:10.1038/s41467-017-01639-5
  • Thistle, R., Cameron, P., Ghorayshi, A., Dennison, L., & Scott, K. (2012). Contact chemoreceptors mediate male-male repulsion and male-female attraction during Drosophila courtship. Cell, 149, 1140–1151. doi:10.1016/j.cell.2012.03.045
  • Toda, H., Zhao, X., & Dickson, B. J. (2012). The Drosophila female aphrodisiac pheromone activates ppk23(+) sensory neurons to elicit male courtship behavior. Cell Reports, 1, 599–607. doi:10.1016/j.celrep.2012.05.007
  • Vijayan, V., Thistle, R., Liu, T., Starostina, E., & Pikielny, C. W. (2014). Drosophila pheromone-sensing neurons expressing the ppk25 ion channel subunit stimulate male courtship and female receptivity. PLoS Genetics, 10, e1004238.
  • Wang, L., Han, X., Mehren, J., Hiroi, M., Billeter, J. C., Miyamoto, T., … Anderson, D. J. (2011). Hierarchical chemosensory regulation of male-male social interactions in Drosophila. Nature Neuroscience, 14, 757–762. doi:10.1038/nn.2800
  • Watanabe, K., Toba, G., Koganezawa, M., & Yamamoto, D. (2011). Gr39a, a highly diversified gustatory receptor in Drosophila, has a role in sexual behavior. Behavior Genetics, 41, 746–753. doi:10.1007/s10519-011-9461-6
  • Yamamoto, D., & Koganezawa, M. (2013). Genes and circuits of courtship behaviour in Drosophila males. Nature Reviews Neuroscience, 14, 681–692. doi:10.1038/nrn3567
  • Yasukawa, J., Tomioka, S., Aigaki, T., & Matsuo, T. (2010). Evolution of expression patterns of two odorant-binding protein genes, Obp57d and Obp57e, in Drosophila. Gene, 467, 25–34. doi:10.1016/j.gene.2010.07.006
  • Yew, J. Y., & Chung, H. (2017). Drosophila as a holistic model for insect pheromone signaling and processing. Current Opinion in Insect Science, 24, 15–20. doi:10.1016/j.cois.2017.09.003

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