Abstract
Introduction
In this study, we analyzed gynandromorphs with female terminalia, to dissect mating-related female behaviors in Drosophila. Materials and methods: We used gynandromorphs, experimentally modified wild-type (Oregon-R) females, and mutant females that lacked different components of the female reproductive apparatus.
Results
Many of the gynandromorphs mated but did not expel the mating plug (MP). Some of these — with thousands of sperm in the uterus — failed to take up sperm into the storage organs. There were gynandromorphs that stored plenty of sperm but failed to release them to fertilize eggs. Expelling the MP, sperm uptake into the storage organs, and the release of stored sperm along egg production are separate steps occurring during Drosophila female fertility. Cuticle landmarks of the gynandromorphs revealed that while the nerve foci that control MP expelling and also those that control sperm uptake reside in the abdominal, the sperm release foci derive from the thoracic region of the blastoderm.
Discussion and conclusion
The gynandromorph study is confirmed by analyses of (a) mutations that cause female sterility: Fs(3)Avar (preventing egg deposition), Tm2gs (removing germline cells), and iab-4DB (eliminating gonad formation) and (b) by experimentally manipulated wild-type females: decapitated or cut through ventral nerve cord.
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References
Adams, E. M., Wolfner, M. F. (2007) Seminal proteins but not sperm induce morphological changes in the Drosophila melanogaster female reproductive tract during sperm storage. J. Insect Physiol. 53, 319–331.
Arthur, B. I., Hauschteck-Jungen, E., Nöthiger, R., Ward, P. I. (1998) A female nervous system is necessary for normal sperm storage in Drosophila melanogaster: a masculinized nervous system is as good as none. Proc. R. Soc. Lond. B 265, 1749–1753.
Avila, F. W., Wong, A., Sitnik, J. L., Wolfner, M. F. (2015) Don’t pull the plug! The Drosophila mating plug preserves fertility. Fly 9, 62–67.
Bairati, A., Perotti, M. E. (1970) Occurrence of a complete plug in the genital duct of Drosophila females after mating. Drosophila Information Service 45, 67–68.
Barth, J. M., Szabad, J., Hafen, E., Köhler, K. (2011) Autophagy in Drosophila ovaries is induced by starvation and is required for oogenesis. Cell Death Differ. 18, 915–924.
Bender, W. (2008) MicroRNAs in the Drosophila bithorax complex. Genes Dev. 22, 14–19.
Bertram, M. J., Neubaum, D. M., Wolfner, M. F. (1996) Localization of the Drosophila accessory gland protein Acp36DE in the mated female suggests a role in sperm storage. Insect Biochem. Mol. Biol. 26, 971–980.
Bloch Qazi, M. C., Heifetz, Y., Wolfner, M. F. (2003) The developments between gametogenesis and fertilization: ovulation and female sperm storage in Drosophila melanogaster. Dev. Biol. 256, 195–211.
Bloch Qazi, M. C., Wolfner, M. E. (2003) An early role for the Drosophila melanogaster male seminal protein Acp36DE in female sperm storage. J. Exp. Biol. 206, 3521–528.
Bloch Qazi, M. C., Wolfner, M. F. (2006) Emergence of sperm from female storage sites has egg-influenced and egg-independent phases in Drosophila melanogaster. Biol. Lett. 2, 128–130.
Boyle, M., DiNardo, S. (1995) Specification, migration and assembly of the somatic cells of the Drosophila gonad. Development 121, 1815–1825.
Bussell, J. J., Yapici, N., Zhang, S. X., Dickson, B. J., Vosshall, L. B. (2014) Abdominal-B neurons control Drosophila virgin female receptivity. Curr. Biol. 24, 1584–1595.
Busturia, A., Casanova, J., Sanchez-Herrero, J., Gonzalez, R., Morata, G. (1989) Genetic structure of the abd-A gene of Drosophila. Development 107, 575–583.
Cook, R. (1978) The reproductive behaviour of gynandromorphic Drosophila melanogaster. Z. Naturforsch. 33c, 744–754.
Cumberledge, S., Szabad, J., Sakonju, S. (1992) Gonad formation and development requires the abd-A domain of the bithorax complex in Drosophila melanogaster. Development 115, 395–402.
Erdélyi, M., Michon, A. M., Guichet, A., Glotzer, J. B., Ephrussi, A. (1995) Requirement for Drosophila cytoplasmic tropomyosin in oskar mRNA localization. Nature 377, 524–527.
Erdélyi, M., Szabad, J. (1989) Isolation and characterization of dominant female sterile mutations of Drosophila melanogaster. I. Mutations on the third chromosome. Genetics 122, 111–127.
Feng, K., Palfreyman, M. T., Hasemeyer, M., Talsma, A., Dickson, B. J. (2014) Ascending SAG neurons control sexual receptivity of Drosophila females. Neuron 83, 135–148.
Garaulet, D. L., Castellanos, M. C., Bejarano, F., Sanfilippo, P., Tyler, D. M., Allan, D. W., Sanchez-Herrero, E., Lai, E. C. (2014) Homeotic function of Drosophila bithorax-complex miRNAs mediates fertility by restricting multiple Hox genes and TALE cofactors in the CNS. Dev. Cell 29, 635–648.
Hall, J. C. (1978) Behavioral analysis in Drosophila mosaics. In: Gehring, W. J. (ed.) Genetic Mosaics and Cell Differentiation. Springer-Verlag, Berlin, pp. 259–305.
Hartenstein, V. (1993) Atlas of Drosophila development. Retrieved from http://www.sdbonline.org/fly/atlas/0607.htm
Hasemeyer, M., Yapici, N., Heberlein, U., Dickson, B. J. (2009) Sensory neurons in the Drosophila genital tract regulate female reproductive behavior. Neuron 61, 511–518.
Heifetz, Y., Lindner, M., Garini, Y., Wolfner, M. F. (2014) Mating regulates neuromodulator ensembles at nerve termini innervating the Drosophila reproductive tract. Curr. Biol. 24, 731–737.
Hildreth, P. E., Lucchesi, J. C. (1963) Fertilization in Drosophila. I. Evidence for regular occurrence of monospermy. Dev. Biol. 6, 262–278.
Hosken, D. J., Martin, O. Y., Wigby, S., Chapman, T., Hodgson, D. J. (2009) Sexual conflict and reproductive isolation in flies. Biol. Lett. 5, 697–699.
Hotta, Y., Benzer, S. (1972) Mapping of behavior in Drosophila mosaics. Nature 240, 527–535.
Hotta, Y., Benzer, S. (1976) Courtship in Drosophila mosaics: sex-specific foci for sequential action patterns. Proc. Natl. Acad. Sci. U. S. A. 73, 4154–4158.
Jallon, J. M., Hotta, Y. (1979) Genetic and behavioral studies of Drosophila female sex appeal. Behav. Genet. 9, 257–275.
Janning, W. (1978) Gynandromoph fate maps in Drosophila. In: Gehring, W. J. (ed.) Genetic Mosaics and Cell Differentiation. Springer-Verlag, Berlin, Heidelberg, New York, pp. 1–28.
Karch, F., Weiffenbach, B., Peifer, M., Bender, W., Duncan, I., Celniker, S., Crosby, M., Lewis, E. B. (1985) The abdominal region of the bithorax complex. Cell 43, 81–96.
Kubli, E., Bopp, D. (2012) Sexual behavior: how sex peptide flips the postmating switch of female flies. Curr. Biol. 22, R520–522.
LaFlamme, B. A., Ram, K. R., Wolfner, M. F. (2012) The Drosophila melanogaster seminal fluid protease “seminase” regulates proteolytic and post-mating reproductive processes. PIoS Genet. 8, e1002435.
Lung, O., Wolfner, M. F. (2001) Identification and characterization of the major Drosophila melanogaster mating plug protein. Insect Biochem. Mol. Biol. 31, 543–551.
Mattei, A. M., Riccio, M. L., Avila, F. W., Wolfner, M. F. (2015) Integrated 3D view of postulating responses by the Drosophila melanogaster female reproductive tract, obtained by micro-computed tomography scanning. Proc. Natl. Acad. Sci. USA 112, 8475–8480.
Middleton, C. A., Nongthomba, U., Parry, K., Sweeney, S. T., Sparrow, J. C., Elliott, C. J. H. (2006) Neuromuscular organization and aminergic modulation of contractions in the Drosophila ovary. BMC Biol. 4, 17.
Neubaum, D. M., Wolfner, M. F. (1999) Mated Drosophila melanogaster females require a seminal fluid protein, Acp36DE, to store sperm efficiently. Genetics 153, 845–857.
Polak, M., Starmer, W. T., Barker, J. S. F. (1998) A mating plug and male mate choice in Drosophila hibisci Bock. Animal Behavior 56, 919–926.
Power, M. E. (1948) The thoracico-abdominal nervous system of an adult insect Drosophila melanogaster. J. Comp. Neurol. 88, 347–409.
Rezával, C., Nojima, T., Neville, M. C., Lin, A. C., Goodwin, S. F. (2014) Sexually dimorphic octopaminergic neurons modulate female postmating behaviors in Drosophila. Curr. Biol. 24, 1–6.
Rezával, C., Pavlou, H. J., Dornan, A. J., Chan, Y. B., Kravitz, E. A., Goodwin, S. F. (2012) Neural circuitry underlying Drosophila female postmating behavioral responses. Curr. Biol. 22, 1155–1165.
Santel, A., Winhauer, T., Blümer, N., Renkawitz-Pohl, N. (1997) The Drosophila don juan (dj) gene encodes a novel sperm specific protein component characterized by an unusual domain of a repetitive amino acid motif. Mech. Dev. 64, 19–33.
Szabad, J., Fajszi, C. (1982) Control of female reproduction in Drosophila: genetic dissection using gynandromorphs. Genetics 100, 61–78.
Szabad, J., Máthé, E., Puro, J. (1995) Horka, a dominant mutation of Drosophila, induces nondisjunction and, through paternal effect, chromosome loss and genetic mosaics. Genetics 139, 1585–1599.
Szabad, J., Nöthiger, R. (1992) Gynandromorphs of Drosophila suggest one common primordium for the somatic cells of the female and male gonads in the region of abdominal segments 4 and 5. Development 115, 527–533.
Szalontai, T., Gáspár, I., Belecz, I., Kerekes, I., Erdélyi, M., Boros, I., Szabad, J. (2009) HorkaD, a chromosome instability-causing mutation in Drosophila, is a dominant-negative allele of lodestar. Genetics 181, 367–377.
Takami, Y., Sasabe, M., Nagata, N., Sota, T. (2008) Dual function of seminal substances for mate guarding in a ground beetle. Behav. Ecol. 19, 1173–1178.
Tompkins, L., Hall, J. C. (1983) Identification of brain sites controlling female receptivity in mosaics of Drosophila melanogaster. Genetics 103, 179–195.
Tremml, G., Bienz, M. (1989) Homeotic gene expression in the visceral mesoderm of Drosophila embryos. EMBO J. 8, 2677–2685.
Villella, A., Hall, J. C. (2008) Neurogenetics of courtship and mating in Drosophila. Adv Genet. 62, 67–184.
Yang, C. H., Rumpf, S., Xiang, Y., Gordon, M. D., Song, W., Jan, L. Y., Jan, Y. N. (2009) Control of the postmating behavioral switch in Drosophila females by internal sensory neurons. Neuron 61, 519–526.
Zhou, C., Pan, Y., Robinett, C. C., Meissner, G. W., Baker, B. S. (2014) Central brain neurons expressing doublesex regulate female receptivity in Drosophila. Neuron 83, 149–163.
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Szabad, J., Peng, J. & Kubli, E. Control of mating plug expelling and sperm storage in Drosophila: A gynandromorph- and mutation-based dissection. BIOLOGIA FUTURA 70, 301–311 (2019). https://doi.org/10.1556/019.70.2019.34
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DOI: https://doi.org/10.1556/019.70.2019.34