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A neuropeptide circuit that coordinates sperm transfer and copulation duration in Drosophila
Open accessAbstract
Innate behaviors are often executed in concert with accompanying physiological programs. How this coordination is achieved is poorly understood. Mating behavior and the transfer of sperm and seminal fluid (SSFT) provide a model for understanding how concerted behavioral and physiological programs are coordinated. Here we identify a male-specific neural pathway that coordinates the timing of SSFT with the duration of copulation behavior in Drosophila. Silencing four abdominal ganglion (AG) interneurons (INs) that contain the neuropeptide corazonin (Crz) both blocked SSFT and substantially lengthened copulation duration. Activating these Crz INs caused rapid ejaculation in isolated males, a phenotype mimicked by injection of Crz peptide. Crz promotes SSFT by activating serotonergic (5-HT) projection neurons (PNs) that innervate the accessory glands. Activation of these PNs in copulo caused premature SSFT and also shortened copulation duration. However, mating terminated normally when these PNs were silenced, indicating that SSFT is not required for appropriate copulation duration. Thus, the lengthened copulation duration phenotype caused by silencing Crz INs is independent of the block to SSFT. We conclude that four Crz INs independently control SSFT and copulation duration, thereby coupling the timing of these two processes.
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“For instance, CRZ signaling coordinates aspects of copulation and fecundity in Drosophila (29, 30) and steroid synthesis in Octopus gonads (31).”
From Corazonin signaling integrates energy homeostasis and lunar phase to regulate aspects of growth and sexual maturation in Platynereis (2020) · cites this paper as [29]
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“and reproduction (sperm transfer) (29, 81)”
From Corazonin signaling integrates energy homeostasis and lunar phase to regulate aspects of growth and sexual maturation in Platynereis (2020) · cites this paper as [29]
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Cites
Spatiotemporal Rescue of Memory Dysfunction in Drosophila
McGuire, S. E., Le, P. T., Osborn, A. J., Matsumoto, K., & Davis, R. L. (2003) · Science · doi:10.1126/science.1089035 · Cited by 1,338
Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging
Akerboom, J., Chen, T., Wardill, T. J., Tian, L., Marvin, J. S., Mutlu, S., Calderón, N. C., Esposti, F., Borghuis, B. G., Sun, X. R., et al. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2601-12.2012 · Cited by 1,289
An internal thermal sensor controlling temperature preference in Drosophila
Hamada, F. N., Rosenzweig, M. R., Kang, K., Pulver, S. R., Ghezzi, A., Jegla, T. J., & Garrity, P. (2008) · Nature · doi:10.1038/nature07001 · Cited by 1,089
Mosaic analysis with a repressible cell marker (MARCM) for Drosophila neural development
Lee, T., & Luo, L. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01791-4 · Cited by 928
Male Accessory Gland Secretions: Modulators of Female Reproductive Physiology and Behavior
Gillott, C. (2002) · Annual Review of Entomology · doi:10.1146/annurev.ento.48.091801.112657 · Cited by 824
Altered Electrical Properties inDrosophilaNeurons Developing without Synaptic Transmission
Baines, R., Uhler, J. P., Thompson, A., Sweeney, S. T., & Bate, M. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-05-01523.2001 · Cited by 618
Tokens of love: Functions and regulation of drosophila male accessory gland products
Wolfner, M. F. (1997) · Insect Biochemistry and Molecular Biology · doi:10.1016/s0965-1748(96)00084-7 · Cited by 584
Neural Circuitry that Governs Drosophila Male Courtship Behavior
Stockinger, P., Kvitsiani, D., Rotkopf, S., Tirián, L., & Dickson, B. J. (2005) · Cell · doi:10.1016/j.cell.2005.04.026 · Cited by 560
fruitless Splicing Specifies Male Courtship Behavior in Drosophila
Demir, E., & Dickson, B. J. (2005) · Cell · doi:10.1016/j.cell.2005.04.027 · Cited by 496
tudor, a gene required for assembly of the germ plasm in Drosophila melanogaster
Boswell, R. E. (1985) · Cell · doi:10.1016/0092-8674(85)90015-7 · Cited by 409
Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour
Manoli, D. S., Foss, M., Villella, A., Taylor, B. J., Hall, J. C., & Baker, B. S. (2005) · Nature · doi:10.1038/nature03859 · Cited by 402
SPERM TRANSFER, STORAGE, DISPLACEMENT, AND UTILIZATION IN DROSOPHILA MELANOGASTER
Lefevre, G., & Jonsson, U.-B. (1962) · Genetics · doi:10.1093/genetics/47.12.1719 · Cited by 376
Isolation and structure of corazonin, a cardioactive peptide from the American cockroach
Veenstra, J. A. (1989) · FEBS Letters · doi:10.1016/0014-5793(89)80727-6 · Cited by 291
Alekseyenko, O. V., Lee, C. M., & Kravitz, E. A. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010806 · Cited by 237
Allatostatin-A neurons inhibit feeding behavior in adult Drosophila
Hergarden, A. C., Tayler, T. D., & Anderson, D. J. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1200778109 · Cited by 214
Self-citationSerotonin‐containing neurons in Drosophila melanogaster: Development and distribution
Vallés, A. M., & White, K. (1988) · The Journal of Comparative Neurology · doi:10.1002/cne.902680310 · Cited by 208
Physiology of Ejaculation: Emphasis on Serotonergic Control
Giuliano, F., & Clément, P. (2005) · European Urology · doi:10.1016/j.eururo.2005.05.017 · Cited by 205
Fowler, G. L. (1973) · Advances in genetics · doi:10.1016/s0065-2660(08)60173-x · Cited by 176
Gilchrist, A. S., & Partridge, L. (2000) · Evolution · doi:10.1111/j.0014-3820.2000.tb00056.x · Cited by 164
Linklater, J. R., Wertheim, B., Wigby, S., & Chapman, T. (2007) · Evolution · doi:10.1111/j.1558-5646.2007.00157.x · Cited by 144
Identification and characterization of the major Drosophila melanogaster mating plug protein
Lung, O., & Wolfner, M. F. (2001) · Insect Biochemistry and Molecular Biology · doi:10.1016/s0965-1748(00)00154-5 · Cited by 140
Drosophila female sexual behavior induced by sterile males showing copulation complementation
Xue, L., & Noll, M. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.7.3272 · Cited by 137
Santel, A., Winhauer, T., Blümer, N., & Renkawitz‐Pohl, R. (1997) · Mechanisms of Development · doi:10.1016/s0925-4773(97)00031-2 · Cited by 127
Turning Males On: Activation of Male Courtship Behavior in Drosophila melanogaster
Pan, Y., Robinett, C. C., & Baker, B. S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021144 · Cited by 100
Lee, G. G., Villella, A., Taylor, B. J., & Hall, J. C. (2001) · Journal of Neurobiology · doi:10.1002/neu.1021 · Cited by 96
DIRECTIONAL SELECTION FOR DURATION OF COPULATION IN DROSOPHILA MELANOGASTER
MacBean, I. T., & Parsons, P. A. (1967) · Genetics · doi:10.1093/genetics/56.2.233 · Cited by 95
Lee, G., & Hall, J. C. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-02-00513.2001 · Cited by 89
Choi, Y. J., Lee, G., Hall, J. C., & Park, J. H. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20419 · Cited by 86
A mating plug protein reduces early female remating in Drosophila melanogaster
Bretman, A. J., Lawniczak, M., Boone, J. M., & Chapman, T. (2009) · Journal of Insect Physiology · doi:10.1016/j.jinsphys.2009.09.010 · Cited by 79
Strand, F. L. (1998) · The MIT Press eBooks · doi:10.7551/mitpress/4950.001.0001 · Cited by 48
Gilchrist, A. S., & Partridge, L. (2000) · Evolution · doi:10.1554/0014-3820(2000)054[0534:wiidtm]2.0.co;2 · Cited by 29
Cholinergic Control of Synchronized Seminal Emissions in Drosophila
Acebes, Á., Grosjean, Y., Everaerts, C., & Ferveur, J. (2004) · Current Biology · doi:10.1016/j.cub.2004.04.003 · Cited by 28
Villella, A., Peyre, J., Aigaki, T., & Hall, J. C. (2006) · Journal of Comparative Physiology A · doi:10.1007/s00359-006-0154-1 · Cited by 19
Yonezawa, A., Yoshizumi, M., Ebiko, M., Iwanaga, T., Kimura, Y., & Sakurada, S. (2005) · Pharmacology, Biochemistry and Behavior · doi:10.1016/j.pbb.2005.12.001 · Cited by 15
Research works printed but not linked: 1
- A Bairati, Structure and ultrastructure of the male reproductive system of Drosophila melanogaster Meig. 2. The genital duct and accessory glands. Monit. Zoolog. Ital. 2, 105–182 (1968).
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Recent advances in neuropeptide signaling in Drosophila, from genes to physiology and behavior
Nässel, D. R., & Zandawala, M. (2019) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2019.02.003 · Cited by 373
Tachykinin-Expressing Neurons Control Male-Specific Aggressive Arousal in Drosophila
Asahina, K., Watanabe, K., Duistermars, B. J., Hoopfer, E. D., González, C. R., Eyjólfsdóttir, E., Perona, P., & Anderson, D. J. (2014) · Cell · doi:10.1016/j.cell.2013.11.045 · Cited by 363
Self-citationInagaki, H. K., Jung, Y., Hoopfer, E. D., Wong, A. M., Mishra, N., Lin, J. Y., Tsien, R. Y., & Anderson, D. J. (2014) · Nature Methods · doi:10.1038/nmeth.2765 · Cited by 321
Self-citationNeuropeptides as Regulators of Behavior in Insects
Schoofs, L., LOOF, A. D., & Hiel, M. B. V. (2016) · Annual Review of Entomology · doi:10.1146/annurev-ento-031616-035500 · Cited by 269
Metadata
- Authors
- Tayler, T. D., Pacheco, D. A., Hergarden, A. C., Murthy, M., & Anderson, D. J.
- Affiliations
- Princeton University (US)
- California Institute of Technology (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2012-11-28
- Volume
- 109
- Issue
- 50
- Pages
- 20697-20702
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3528491
- OpenAlex
- W2150959561
- Cited by
- 150
- References
- 33
- Citations by year
- 2026: 11 · 2025: 23 · 2024: 13 · 2023: 6 · 2022: 11 · 2021: 16 · 2020: 15 · 2019: 12 · 2018: 9 · 2017: 3 · 2016: 13 · 2015: 7 · 2014: 5 · 2013: 6
- FWCI
- 2.37
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health (5t32ns007251-22, 5f32ns058132-02)
- National Institute on Drug Abuse (R01DA031389)
- National Institute of Neurological Disorders and Stroke (T32 NS-007251, NS007251, F32 NS058132, 5F32NS058132)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Keywords
- sperm transfer, copulation duration, corazonin, neuropeptides, accessory glands, ejaculation, mating behavior
- MeSH terms
- Animals, Copulation, Drosophila melanogaster, Ejaculation, Female, Ganglia, Interneurons, Male, Models, Biological, Neuropeptides, Sperm Transport, Genes, Insect, Receptors, Neuropeptide, Drosophila Proteins, Animals, Genetically Modified
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