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Contribution of visual and circadian neural circuits to memory for prolonged mating induced by rivals

Nature Neuroscience volume 15, pages 876–883 (2012)Cite this article

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Abstract

Rival exposure causes Drosophila melanogaster males to prolong mating. Longer mating duration (LMD) may enhance reproductive success, but its underlying mechanism is currently unknown. We found that LMD is context dependent and can be induced solely via visual stimuli. In addition, we found that LMD involves neural circuits that are important for visual memory, including central neurons in the ellipsoid body, but not the mushroom bodies or the fan-shaped bodies, and may rely on the rival exposure memory lasting for several hours. LMD is affected by a subset of learning and memory mutants. LMD depends on the circadian clock genes timeless and period, but not Clock or cycle, and persists in many arrhythmic conditions. Moreover, LMD critically depends on a subset of pigment dispersing factor neurons rather than the entire circadian neural circuit. Our study thus delineates parts of the molecular and cellular basis for LMD, a plastic social behavior elicited by visual cues.

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Figure 1: General characteristics of the LMD behavior.
Figure 2: LMD is induced by visual stimuli.
Figure 3: LMD is affected in tim and per mutants, but not in Clk or cyc mutants.
Figure 4: PER, but not CLK, protein in PDF neurons is required to generate LMD.
Figure 5: Neural circuitry mapping for LMD.
Figure 6: LMD requires visual memory.
Figure 7: Neural circuitry important for LMD.

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References

  1. Darwin, C. The Descent of Man, and Selection in Relation to Sex (John Murray, 1871).

  2. Kim, Y.-K. Sexual selection and aggressive behavior in Drosophila. in Handbook of Behavior Genetics (ed. Kim, Y.-K.) 317–330 (Springer New York, 2009).

  3. Ridley, M. Seminal work. Nature 397, 576–577 (1999).

    Article  CAS  Google Scholar 

  4. Parker, G.A. Sperm competition and its evolutionary consequences in insects. Biol. Rev. Camb. Philos. Soc. 45, 525–567 (1970).

    Article  Google Scholar 

  5. Markow, T.A. Evolution of Drosophila mating systems. Evol. Biol. 29, 73–106 (1996).

    Google Scholar 

  6. Koref-Santibáñez, S. Effects of age and experience on mating activity in the sibling species Drosophila pavani and Drosophila gaucha. Behav. Genet. 31, 287–297 (2001).

    Article  Google Scholar 

  7. Lefranc, A. & Bundgaard, J. The influence of male and female body size on copulation duration and fecundity in Drosophila melanogaster. Hereditas 132, 243–247 (2000).

    Article  CAS  Google Scholar 

  8. De Crespigny, F.E.C., Pitt, T.D. & Wedell, N. Increased male mating rate in Drosophila is associated with Wolbachia infection. J. Evol. Biol. 19, 1964–1972 (2006).

    Article  Google Scholar 

  9. Luck, N. & Joly, D. Sexual selection and mating advantages in the giant sperm species, Drosophila bifurca. J. Insect Sci. 5, 10 (2005).

    Article  Google Scholar 

  10. Bretman, A., Fricke, C. & Chapman, T. Plastic responses of male Drosophila melanogaster to the level of sperm competition increase male reproductive fitness. Proc. Biol. Sci. 276, 1705–1711 (2009).

    Article  Google Scholar 

  11. Mazzi, D., Kesaniemi, J., Hoikkala, A. & Klappert, K. Sexual conflict over the duration of copulation in Drosophila montana: why is longer better? BMC Evol. Biol. 9, 132 (2009).

    Article  Google Scholar 

  12. Macbean, I.T. & Parsons, P.A. Directional selection for duration of copulation in Drosophila melanogaster. Genetics 56, 233–239 (1967).

    CAS  PubMed  Google Scholar 

  13. Bretman, A., Fricke, C., Hetherington, P., Stone, R. & Chapman, T. Exposure to rivals and plastic responses to sperm competition in Drosophila melanogaster. Behav. Ecol. 21, 317–321 (2010).

    Article  Google Scholar 

  14. von Lintig, J., Dreher, A., Kiefer, C., Wernet, M.F. & Vogt, K. Analysis of the blind Drosophila mutant ninaB identifies the gene encoding the key enzyme for vitamin A formation in vivo. Proc. Natl. Acad. Sci. USA 98, 1130–1135 (2001).

    CAS  PubMed  Google Scholar 

  15. Cook, T., Pichaud, F., Sonneville, R., Papatsenko, D. & Desplan, C. Distinction between color photoreceptor cell fates is controlled by Prospero in Drosophila. Dev. Cell 4, 853–864 (2003).

    Article  CAS  Google Scholar 

  16. Bretman, A., Westmancoat, J.D., Gage, M.J. & Chapman, T. Males use multiple, redundant cues to detect mating rivals. Curr. Biol. 21, 617–622 (2011).

    Article  CAS  Google Scholar 

  17. Menne, D. & Spatz, H.C. Color vision in Drosophila melanogaster. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 114, 301–312 (1977).

    Article  Google Scholar 

  18. Yamaguchi, S., Wolf, R., Desplan, C. & Heisenberg, M. Motion vision is independent of color in Drosophila. Proc. Natl. Acad. Sci. USA 105, 4910–4915 (2008).

    Article  CAS  Google Scholar 

  19. Zheng, X. & Sehgal, A. Probing the relative importance of molecular oscillations in the circadian clock. Genetics 178, 1147–1155 (2008).

    Article  CAS  Google Scholar 

  20. Hall, J.C. Systems approaches to biological rhythms in Drosophila. Methods Enzymol. 393, 61–185 (2005).

    Article  CAS  Google Scholar 

  21. Beaver, L.M. & Giebultowicz, J.M. Regulation of copulation duration by period and timeless in Drosophila melanogaster. Curr. Biol. 14, 1492–1497 (2004).

    CAS  PubMed  Google Scholar 

  22. Glaser, F.T. & Stanewsky, R. Temperature synchronization of the Drosophila circadian clock. Curr. Biol. 15, 1352–1363 (2005).

    Article  CAS  Google Scholar 

  23. Emery, P., Stanewsky, R., Hall, J.C. & Rosbash, M. Drosophila cryptochromes: a unique circadian-rhythm photoreceptor. Nature 404, 456–457 (2000).

    Article  CAS  Google Scholar 

  24. Yang, Z. & Sehgal, A. Role of molecular oscillations in generating behavioral rhythms in Drosophila. Neuron 29, 453–467 (2001).

    CAS  PubMed  Google Scholar 

  25. Peschel, N. & Helfrich-Forster, C. Setting the clock—by nature: circadian rhythm in the fruitfly Drosophila melanogaster. FEBS Lett. 585, 1435–1442.

  26. Tanoue, S., Krishnan, P., Krishnan, B., Dryer, S.E. & Hardin, P.E. Circadian clocks in antennal neurons are necessary and sufficient for olfaction rhythms in Drosophila. Curr. Biol. 14, 638–649 (2004).

    Article  CAS  Google Scholar 

  27. Rieger, D., Wulbeck, C., Rouyer, F. & Helfrich-Forster, C. Period gene expression in four neurons is sufficient for rhythmic activity of Drosophila melanogaster under dim light conditions. J. Biol. Rhythms 24, 271–282 (2009).

    Article  CAS  Google Scholar 

  28. Shafer, O.T., Helfrich-Forster, C., Renn, S.C. & Taghert, P.H. Reevaluation of Drosophila melanogaster's neuronal circadian pacemakers reveals new neuronal classes. J. Comp. Neurol. 498, 180–193 (2006).

    Article  Google Scholar 

  29. Zhang, L. et al. DN1(p) circadian neurons coordinate acute light and PDF inputs to produce robust daily behavior in Drosophila. Curr. Biol. 20, 591–599 (2010).

    Article  CAS  Google Scholar 

  30. Nitabach, M.N., Blau, J. & Holmes, T.C. Electrical silencing of Drosophila pacemaker neurons stops the free-running circadian clock. Cell 109, 485–495 (2002).

    Article  CAS  Google Scholar 

  31. Nitabach, M.N. et al. Electrical hyperexcitation of lateral ventral pacemaker neurons desynchronizes downstream circadian oscillators in the fly circadian circuit and induces multiple behavioral periods. J. Neurosci. 26, 479–489 (2006).

    Article  CAS  Google Scholar 

  32. Heisenberg, M. Mushroom body memoir: from maps to models. Nat. Rev. Neurosci. 4, 266–275 (2003).

    Article  CAS  Google Scholar 

  33. Popodi, E. et al. Small X duplications for the stock center collection. FlyBase published online, FBrf0210621 (2 March 2010).

  34. Liu, G. et al. Distinct memory traces for two visual features in the Drosophila brain. Nature 439, 551–556 (2006).

    Article  CAS  Google Scholar 

  35. Pan, Y. et al. Differential roles of the fan-shaped body and the ellipsoid body in Drosophila visual pattern memory. Learn. Mem. 16, 289–295 (2009).

    Article  Google Scholar 

  36. Stocker, R.F. The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res. 275, 3–26 (1994).

    Article  CAS  Google Scholar 

  37. Renn, S.C. et al. Genetic analysis of the Drosophila ellipsoid body neuropil: organization and development of the central complex. J. Neurobiol. 41, 189–207 (1999).

    Article  CAS  Google Scholar 

  38. Shang, Y., Griffith, L.C. & Rosbash, M. Light-arousal and circadian photoreception circuits intersect at the large PDF cells of the Drosophila brain. Proc. Natl. Acad. Sci. USA 105, 19587–19594 (2008).

    Article  CAS  Google Scholar 

  39. Kent, C., Azanchi, R., Smith, B., Formosa, A. & Levine, J.D. Social context influences chemical communication in D. melanogaster males. Curr. Biol. 18, 1384–1389 (2008).

    Article  CAS  Google Scholar 

  40. Krupp, J.J. et al. Social experience modifies pheromone expression and mating behavior in male. Drosophila melanogaster. Curr. Biol. 18, 1373–1383 (2008).

    CAS  PubMed  Google Scholar 

  41. Gong, Z., Xia, S., Liu, L., Feng, C. & Guo, A. Operant visual learning and memory in Drosophila mutants dunce, amnesiac and radish. J. Insect Physiol. 44, 1149–1158 (1998).

    Article  CAS  Google Scholar 

  42. Guo, A. & Gotz, K.G. Association of visual objects and olfactory cues in Drosophila. Learn. Mem. 4, 192–204 (1997).

    Article  CAS  Google Scholar 

  43. Choi, C. & Nitabach, M.N. Circadian biology: environmental regulation of a multi-oscillator network. Curr. Biol. 20, R322–324 (2010).

    Article  CAS  Google Scholar 

  44. Keene, A.C. et al. Clock and cycle limit starvation-induced sleep loss in Drosophila. Curr. Biol. 20, 1209–1215 (2010).

    Article  CAS  Google Scholar 

  45. Parisky, K.M. et al. PDF cells are a GABA-responsive wake-promoting component of the Drosophila sleep circuit. Neuron 60, 672–682 (2008).

    Article  CAS  Google Scholar 

  46. Krstic, D., Boll, W. & Noll, M. Sensory integration regulating male courtship behavior in Drosophila. PLoS ONE 4, e4457 (2009).

    Article  Google Scholar 

  47. Preuss, F. et al. Drosophila doubletime mutations which either shorten or lengthen the period of circadian rhythms decrease the protein kinase activity of casein kinase I. Mol. Cell. Biol. 24, 886–898 (2004).

    Article  CAS  Google Scholar 

  48. Hasegawa, E. et al. Concentric zones, cell migration and neuronal circuits in the Drosophila visual center. Development 138, 983–993 (2011).

    Article  CAS  Google Scholar 

  49. Yang, C.H. et al. Control of the postmating behavioral switch in Drosophila females by internal sensory neurons. Neuron 61, 519–526 (2009).

    Article  CAS  Google Scholar 

  50. Lee, T. & Luo, L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451–461 (1999).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank S. Zhu for the unpublished fly line GAL414–94. We also thank A. Keene, J. Blau, M. Heisenberg, C. Helfrich-Förster, L. Griffith, R. Allada, M. Noll, J.L. Price, A. Sehgal, M. Young, J.D. Armstrong and M. Sato for kindly providing valuable flies. We are grateful to A. Keene for valuable discussion of this project and J. Berg for assisting with the writing of the manuscript. The work was supported by US National Institutes of Health grant 2R37NS040929 to Y.N.J. L.Y.J. and Y.N.J. are investigators of the Howard Hughes Medical Institute.

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  1. Departments of Physiology, Howard Hughes Medical Institute, Biochemistry and Biophysics, University of California, San Francisco, San Francisco, California, USA

    Woo Jae Kim, Lily Yeh Jan & Yuh Nung Jan

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  1. Woo Jae Kim
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W.J.K. designed and performed the experiments. W.J.K., Y.N.J. and L.Y.J. wrote the manuscript. Y.N.J. and L.Y.J. supervised the project.

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Correspondence to Yuh Nung Jan.

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Kim, W., Jan, L. & Jan, Y. Contribution of visual and circadian neural circuits to memory for prolonged mating induced by rivals. Nat Neurosci 15, 876–883 (2012). https://doi.org/10.1038/nn.3104

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