Utilization of Mating Behavior as a Parameter to Understand Adaptive Response in Drosophila melanogaster using Ethyl Methanesulfonate and Methyl Methanesulfonate
Authors
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Department of Bioscience, University of Mysore, P.G. Centre, Hemagangothri, Hassan - 573220, Karnataka ,IN
Baladare Udayakumar Divyashree -
Department of Botany, Karnataka State Open University Mukthagangotri, Mysore - 570006, Karnataka ,INKembalu Narayana Ravindra
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Department of Bioscience, University of Mysore, P.G. Centre, Hemagangothri, Hassan - 573220, Karnataka ,INVenkateshaiah Vasudev
DOI:
https://doi.org/10.18311/ti/2023/v30i3/33469Keywords:
Adaptive Response, Challenging Dose, Combined Dose, Conditioning Dose, Courtship Elements, Drosophila melanogaster, EMS, MMS, Mating BehaviourAbstract
Monofunctional alkylating agents, Ethyl Methanesulfonate (EMS) and Methyl Methanesulfonate (MMS) were used to understand adaptive response utilising mating behaviour as a parameter in D. melanogaster. Selected conditioning and challenging doses of EMS (0.5mM and 15mM) or MMS (0.1mM and 3mM) by larval feeding were tested employing different combinations of crosses. The results have revealed that both EMS and MMS affected courtship elements significantly in different combinations of crosses. Nonetheless, significant increases in orientation, tapping, wing vibration and licking were observed when both males and females were treated with a challenging dose of MMS compared to EMS (p<0.05). On par with this, were also the results of female rejection elements in both the tested chemicals. When conditioning and challenging doses were given after 2 hours of time lag between them to 48±4h or 72±4h aged larvae of D. melanogaster, the results showed that male and female courtship elements significantly reduced compared to the additive effect of respective agents. Similarly, the courtship latency and copulation latency were significantly decreased in contrast to copulation duration which was significantly increased (p<0.05). Thus the results demonstrate the presence of adaptive response in D. melanogaster using courtship elements and the authors opine that mating behaviour can be used as a parameter to analyze adaptive response in D. melanogaster within a short period of time compared to other test procedures.
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Accepted 2023-06-30
Published 2023-09-20
References
Sturtevant AH. Experiments on sex recognition and the problem of sexual selection in Drosoophilia. J Anim Behav. 1915; 5(5):351. https://doi.org/10.1037/h0074109 DOI: https://doi.org/10.1037/h0074109
Spieth HT. Mating behaviour with in genus Drosophila (Diptera). Bull Am Mus Natur Hist. 1952; 99:395-474.
Bastock M, Manning A. The courtship of Drosophila melanogaster. Behaviour. 1955; 8(1):85-111. https://doi. org/10.1163/156853955X00184 DOI: https://doi.org/10.1163/156853955X00184
Auerbach C, Robson JM. Production of mutations by allyl isothiocyanate. Nature. 1944; 154:81-81. https://doi. org/10.1038/154081a0 DOI: https://doi.org/10.1038/154081a0
Divyashree BU, Krishna MS, Vasudev V. Analysis of courtship behaviour as a parameter of toxicity of Ethyl Methanesulfonate (EMS) in Drosophila melanogaster. J Adv Zool. 2021; 42(01):34-42. https://doi.org/10.17762/jaz. v42i01.4 DOI: https://doi.org/10.17762/jaz.v42i01.4
Divyashree BU, Vasudev V. Utilization of courtship behavioural elements to understand the toxicity of Methyl methanesulfonate in Drosophila melanogaster. Toxicol Int. 2021; 28(3):245-53. DOI: https://doi.org/10.18311/ti/2021/v28i3/27416
Vasudev V, Gurushankara HP, Mahadimane PV, Khalandar D, Shamprasad BR. Effects of fungicide Dithane M 45 in Drosophila melanogaster on courtship behavior. Dros Inf Serv. 2013; 96:94-98.
Sega GA. A review of the genetic effects of ethyl methanesulfonate. Mutat Res. 1984; 134(2-3):113-42. https://doi.org/10.1016/0165-1110(84)90007-1 PMid: 6390190 DOI: https://doi.org/10.1016/0165-1110(84)90007-1
Khalandar BB. Studies on adaptive response in the induced diabetic mouse. [PhD thesis]. Mysore: Mysore University; 2016.
Villella A, Hall JC. Neurogenetics of courtship and mating in Drosophila. Adv Genet. 2008; 62:67-184. https://doi. org/10.1016/S0065-2660(08)00603-2 PMid:19010254 DOI: https://doi.org/10.1016/S0065-2660(08)00603-2
Yu J, Wu H, Wen Y, Liu Y, Zhou T, Ni B, Tong C. Identification of seven genes essential for male fertility through a genome-wide association study of nonobstructive azoospermia and RNA interference-mediated large-scale functional screening in Drosophila. Hum Mol Genet. 2015; 24(5):1493-1503. https://doi.org/10.1093/ hmg/ddu557 PMid:25361961 DOI: https://doi.org/10.1093/hmg/ddu557
Samson L, Cairns J. A new pathway for DNA repair in Escherichia coli. Nature. 1977; 267(5608):281-283. https:// doi.org/10.1038/267281a0 PMid:325420 DOI: https://doi.org/10.1038/267281a0
Dimova EG, Bryant PE, Chankova SG. Adaptive response: Some underlying mechanisms and open questions. Genet Mol Biol. 2008; 31:396-408. https://doi.org/10.1590/S1415- 47572008000300002 DOI: https://doi.org/10.1590/S1415-47572008000300002
Vasudev V, Gurushankara HP. Understanding of cytogenetic techniques. New Delhi: Today and Tomorrow Publishers; 2016.
Vasudev V, Krishnamurthy NB. Toxicity of Dithane M-45 on Drosophila melanogaster. Experientia. 1979; 35(4):528- 9. https://doi.org/10.1007/BF01922750 DOI: https://doi.org/10.1007/BF01922750
Delcour J. A rapid and efficient method of egg collecting. Dros Inf Serv. 1969; 44:133-4.
Khalandar BB, Vasudev V. Inducible protective processes in animal systems XIV: Cytogenetic adaptive response induced by EMS or MMS in bone marrow cells of the diabetic mouse. Egypt J Med Hum Genet. 2016; 17(2):201- 8. https://doi.org/10.1016/j.ejmhg.2015.12.007 DOI: https://doi.org/10.1016/j.ejmhg.2015.12.007
Billeter JC, Rideout EJ, Dornan AJ, Goodwin SF. Control of male sexual behavior in Drosophila by the sex determination pathway. Curr Biol. 2006; 16(17):R766-76. https://doi. org/10.1016/j.cub.2006.08.025 PMid:16950103 DOI: https://doi.org/10.1016/j.cub.2006.08.025
Graf U, Würgler FE, Katz AJ, Frei H, Juon H, Hall CB, Kale PG. Somatic mutation and recombination test in Drosophila melanogaster. Environ Mutagen. 1984; 6(2):153-88. https:// doi.org/10.1002/em.2860060206 PMid:6423380 DOI: https://doi.org/10.1002/em.2860060206
Elens AA, Wattiaux JM. Direct observation of sexual isolation. Dros Inf Serv. 1964; 39:118-119.
Ejima A, Smith BP, Lucas C, Levine JD, Griffith LC. Sequential learning of pheromonal cues modulates memory consolidation in trainer-specific associative courtship conditioning. Curr Biol. 2005; 15(3):194-206. https://doi.org/10.1016/j.cub.2005.01.035 PMid:15694302 PMCid:PMC2805828 DOI: https://doi.org/10.1016/j.cub.2005.01.035
Muller HJ. Artificial transmutation of the gene. Science. 1927; 66(1699):84-7. https://doi.org/10.1126/ science.66.1699.84 PMid:17802387 DOI: https://doi.org/10.1126/science.66.1699.84
Lüning KG. Drosophila-tests in pharmacology. Nature. 1966; 209(5018): 84-6. https://doi.org/10.1038/209084a0 PMid:5925338 DOI: https://doi.org/10.1038/209084a0
Jeggo P, Defais M, Samson L, Schendel P. An adaptive response of E. coli to low levels of alkylating agent: Comparison with previously characterised DNA repair pathways. Mol Gen Genet. 1977; 157(1):1-9. https://doi. org/10.1007/BF00268680 PMid:414071 DOI: https://doi.org/10.1007/BF00268680
Samson L, Schwartz JL. Evidence for an adaptive DNA repair pathway in CHO and human skin fibroblast cell lines. Nature. 1980; 287(5785):861-3. https://doi. org/10.1038/287861a0 PMid:7432501 DOI: https://doi.org/10.1038/287861a0
Karran P, Hjelmgren T, Lindahl T. Induction of a DNA glycosylase for N-methylated purines is part of the adaptive response to alkylating agents. Nature. 1982; 296(5859):770- 3. https://doi.org/10.1038/296770a0 PMid:7040983 DOI: https://doi.org/10.1038/296770a0
Morohoshi F, Munakata N. Adaptive response to simple alkylating agents in Bacillus subtilis cells. Mutat Res. 1983; 110(1):23-37. https://doi.org/10.1016/0027-5107(83) 90015-5 DOI: https://doi.org/10.1016/0027-5107(83)90015-5
Laval F. Repair of methylated bases in mammalian cells during adaptive response to alkylating agents. Biochimie. 1985; 67(3-4):361-4. https://doi.org/10.1016/S0300- 9084(85)80081-X PMid:4041485 DOI: https://doi.org/10.1016/S0300-9084(85)80081-X
Bhattacharya R. An adaptive response of Vibrio cholerae strain OGAWA 154 to furazolidone. Mutat Res. 1989; 225(1- 2):43-7. https://doi.org/10.1016/0165-7992(89)90031-6 PMid: 2913490 DOI: https://doi.org/10.1016/0165-7992(89)90031-6
Basak J. Characterization of the adaptive response to ionizing radiation-induced by low doses of X-rays to Vibrio cholerae cells. Mutat Res. 1996; 372(1):115-118. https://doi. org/10.1016/S0027-5107(96)00177-7 PMid:9003538 DOI: https://doi.org/10.1016/S0027-5107(96)00177-7
Hall JC. Genetics of the nervous system in Drosophila. Q Rev Biophys. 1982; 15(2):223-479. https://doi.org/10.1017/ S0033583500004844 PMid: 6129675 DOI: https://doi.org/10.1017/S0033583500004844
Greenspan RJ, Ferveur JF. Courtship in Drosophila. Annu Rev Genet. 2000; 34(1):205-232. https://doi.org/10.1146/ annurev.genet.34.1.205 PMid:11092827 DOI: https://doi.org/10.1146/annurev.genet.34.1.205
Hall JC. The mating of a fly. Science. 1994; 264(5166):1702- 14. https://doi.org/10.1126/science.8209251 PMid:8209251 DOI: https://doi.org/10.1126/science.8209251
Greenspan RJ. Understanding the genetic construction of behavior. Sci Am. 1995; 272(4):72-78. https://doi. org/10.1038/scientificamerican0495-72 PMid: 7716488 DOI: https://doi.org/10.1038/scientificamerican0495-72
Ryner LC, Goodwin SF, Castrillon DH, Anand A, Villella A, Baker BS, ... Wasserman SA. Control of male sexual behaviour and sexual orientation in Drosophila by the fruitless gene. Cell. 1996; 87(6):1079-89. https://doi. org/10.1016/S0092-8674(00)81802-4 PMid:8978612 DOI: https://doi.org/10.1016/S0092-8674(00)81802-4
Finley KD, Taylor BJ, Milstein M, McKeown M. Dissatisfaction, a gene involved in sex-specific behaviour and neural development of Drosophila melanogaster. Proc Natl Acad Sci USA. 1997; 94(3):913-918. https:// doi.org/10.1073/pnas.94.3.913 PMid:9023356 PMCid: PMC19613 DOI: https://doi.org/10.1073/pnas.94.3.913
Hall JC, Alahiotis SN, Strumpf DA, White K. Behavioral and biochemical defects in temperature-sensitive acetylcholinesterase mutants of Drosophila melanogaster. Genetics.1980; 96(4):939-965. https://doi.org/10.1093/ genetics/96.4.939 PMid:6790339 PMCid:PMC1219310 DOI: https://doi.org/10.1093/genetics/96.4.939
Yamamoto D, Nakano Y. Genes for sexual behaviour. Biochem Biophys Res Commun. 1998; 246(1):1-6. https:// doi.org/10.1006/bbrc.1998.8259 PMid: 9600058 DOI: https://doi.org/10.1006/bbrc.1998.8259
van der Voet M, Nijhof B, Oortveld MA, Schenck A. Drosophila models of early onset cognitive disorders and their clinical applications. Neurosci Biobehav Rev. 2014; 46:326-42. https://doi.org/10.1016/j.neubiorev.2014.01.013 PMid:24661984 DOI: https://doi.org/10.1016/j.neubiorev.2014.01.013
Rubin GM, Hong L, Brokstein P, Evans-Holm M, Frise E, Stapleton M, Harvey DA. A Drosophila complementary DNA resource. Science. 2000; 287(5461):2222-2224. https:// doi.org/10.1126/science.287.5461.2222 PMid:10731138 DOI: https://doi.org/10.1126/science.287.5461.2222
Spieth HT. Courtship behavior in Drosophila. Annu Rev Entomol. 1974; 19(1):385-405. https://doi.org/10.1146/ annurev.en.19.010174.002125 PMid:4205689 DOI: https://doi.org/10.1146/annurev.en.19.010174.002125
Manning A. Drosophila and the evolution of behaviour. Viewpoints in Biology. 1965; 4:125-169.
Paterson HE. A comment on “mate recognition systems”. Evolution. 1980; 34(2):330-331. https://doi. org/10.1111/j.1558-5646.1980.tb04821.x PMid: 28563439 DOI: https://doi.org/10.1111/j.1558-5646.1980.tb04821.x
Manoli DS, Foss M, Villella A, Taylor BJ, Hall JC, Baker BS. Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature. 2005; 436(7049):395-400. https://doi.org/10.1038/nature03859 PMid:15959468 DOI: https://doi.org/10.1038/nature03859
Stockinger P, Kvitsiani D, Rotkopf S, Tirián L, Dickson BJ. Neural circuitry that governs Drosophila male courtship behavior. Cell. 2005; 121(5):795-807. https://doi. org/10.1016/j.cell.2005.04.026 PMid:15935765 DOI: https://doi.org/10.1016/j.cell.2005.04.026
Pavlou HJ, Goodwin SF. Courtship behavior in Drosophila melanogaster: Towards a ‘courtship connectome’. Curr Opin Neurobiol. 2013; 23(1):76-83. https://doi.org/10.1016/j. conb.2012.09.002 PMid:23021897 PMCid:PMC3563961 DOI: https://doi.org/10.1016/j.conb.2012.09.002
Jallon JM. A few chemical words exchanged by Drosophila during courtship and mating. Behav Genet. 1984; 14(5):441- 78. https://doi.org/10.1007/BF01065444 PMid:6441563 DOI: https://doi.org/10.1007/BF01065444
Ferveur JF. Cuticular hydrocarbons: their evolution and roles in Drosophila pheromonal communication. Behav Genet. 2005; 35(3):279-95. https://doi.org/10.1007/s10519- 005-3220-5 PMid:15864443 DOI: https://doi.org/10.1007/s10519-005-3220-5
Antony C, Jallon JM. The chemical basis for sex recognition in Drosophila melanogaster. J Insect Physiol. 1982; 28(10):873- 880. https://doi.org/10.1016/0022-1910(82)90101-9 DOI: https://doi.org/10.1016/0022-1910(82)90101-9
Foley B, Chenoweth SF, Nuzhdin SV, Blows MW. Natural genetic variation in cuticular hydrocarbon expression in male and female Drosophila melanogaster. Genetics. 2007; 175(3):1465-77. https://doi.org/10.1534/ genetics.106.065771 PMid:17194783 PMCid:PMC1840094 DOI: https://doi.org/10.1534/genetics.106.065771
Kurtovic A, Widmer A, Dickson BJ. A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature. 2007; 446(7135):542-6. https://doi.org/10.1038/nature05672 PMid:17392786 DOI: https://doi.org/10.1038/nature05672
Ejima A, Smith BP, Lucas C, Van Naters WVDG, Miller CJ, Carlson JR, Griffith LC. Generalization of courtship learning in Drosophila is mediated by cis-vaccenyl acetate. Curr Biol. 2007; 17(7):599-605. https://doi.org/10.1016/j. cub.2007.01.053 PMid:17363250 PMCid:PMC1913718 DOI: https://doi.org/10.1016/j.cub.2007.01.053
Siwicki KK, Riccio P, Ladewski L, Marcillac F, Dartevelle L, Cross SA, Ferveur JF. The role of cuticular pheromones in courtship conditioning of Drosophila males. Learn Mem. 2005; 12(6):636-45. https://doi.org/10.1101/lm.85605 PMid:16287720 PMCid:PMC1356183 DOI: https://doi.org/10.1101/lm.85605
Vosshall LB. Olfaction in Drosophila. Curr Opin Neurobiol. 2000; 10(4):498-503. https://doi.org/10.1016/S0959- 4388(00)00111-2 PMid:10981620 DOI: https://doi.org/10.1016/S0959-4388(00)00111-2
Dahanukar A, Hallem EA, Carlson JR. Insect chemoreception. Curr Opin Neurobiol. 2005; 15(4):423- 430. https://doi.org/10.1016/j.conb.2005.06.001 PMid: 16006118 DOI: https://doi.org/10.1016/j.conb.2005.06.001
Nazari M, Hegde SN. Effect of fluoxetine on the courtship latency, mating latency and copulation duration of Drosophila melanogaster. J Postgrad Med Inst. 2006; 20(1):58-63.
Nazari M. Effect of fluoxetine on the sexual behaviour of Drosophila melanogaster. J Postgrad Med Inst. 2011; 25(4):298-303.
Roy SS, Ghosh S. Effects of Fruit Ripening Retardant Alar (Daminozide) on Behaviour of Drosophila melanogaster. Pro Zool Soci. 2019; 73(3):296-301. https://doi.org/10.1007/ s12595-019-00316-3 DOI: https://doi.org/10.1007/s12595-019-00316-3
Ehrman L, Parsons PA. Behavior genetics and evolution. New York: McGraw-Hill; 1981. p. 450.
Spieth HT, Ringo JM. Mating behaviour and sexual isolation in Drosophila. In: The Genetics and Biology of Drosophila. Academic press, London; 1983. p. 223-24.
Ferveur JF, Cobb M. Behavioral and evolutionary roles of cuticular hydrocarbons in Diptera. In: Insect hydrocarbons: biology, biochemistry and chemical ecology. Cambridge university Press, Cambridge. 2010. p. 325-43. https://doi. org/10.1017/CBO9780511711909.016 DOI: https://doi.org/10.1017/CBO9780511711909.016
Watanabe K, Toba G, Koganezawa M, Yamamoto D. Gr39a, a highly diversified gustatory receptor in Drosophila, has a role in sexual behavior. Behav Genet. 2011; 41(5):746-53. https://doi.org/10.1007/s10519-011-9461-6 PMid:21416142 DOI: https://doi.org/10.1007/s10519-011-9461-6
Moon SJ, Lee Y, Jiao Y, Montell C. A Drosophila gustatory receptor essential for aversive taste and inhibiting male-to-male courtship. Curr Biol. 2009; 19(19):1623-7. https://doi.org/10.1016/j.cub.2009.07.061 PMid:19765987 PMCid:PMC2762023 DOI: https://doi.org/10.1016/j.cub.2009.07.061
Toda H, Zhao X, Dickson BJ. The Drosophila female aphrodisiac pheromone activates ppk23 (+) sensory neurons to elicit male courtship behavior. Cell rep. 2012; 1(6):599-607. https://doi.org/10.1016/j.celrep.2012.05.007 PMid:22813735 DOI: https://doi.org/10.1016/j.celrep.2012.05.007
Nayak SV, Singh RN. Sensilla on the tarsal segments and mouthparts of adult Drosophila melanogaster Meigen (Diptera: Drosophilidae). Int J Insect Morphol Embryol. 1983; 12(5-6):273-291. https://doi.org/10.1016/0020- 7322(83)90023-5 DOI: https://doi.org/10.1016/0020-7322(83)90023-5
Stocker RF. The organization of the chemosensory system in Drosophila melanogaster: A rewiew. Cell Tissue Research. 1994; 275(1):3-26. https://doi.org/10.1007/BF00305372 PMid:8118845 DOI: https://doi.org/10.1007/BF00305372
Kohatsu S, Koganezawa M, Yamamoto D. Female contact activates male-specific interneurons that trigger stereotypic courtship behavior in Drosophila. Neuron. 2011; 69(3):498- 508. https://doi.org/10.1016/j.neuron.2010.12.017 PMid: 21315260 DOI: https://doi.org/10.1016/j.neuron.2010.12.017
Ewing AW. The influence of wing area on the courtship behaviour of Drosophila melanogaster. Anim Behav. 1964; 12(2-3):316-20. https://doi.org/10.1016/0003- 3472(64)90018-1 DOI: https://doi.org/10.1016/0003-3472(64)90018-1
Antony C, Davis TL, Carlson DA, Pechine JM, Jallon JM. Compared behavioral responses of male Drosophila melanogaster (Canton S) to natural and synthetic aphrodisiacs. J Chem Ecol. 1985; 11(12):1617-29. https:// doi.org/10.1007/BF01012116 PMid:24311330 DOI: https://doi.org/10.1007/BF01012116
Ferveur JF, Sureau G. Simultaneous influence on male courtship of stimulatory and inhibitory pheromones produced by live sex-mosaic Drosophila melanogaster. Proc Biol Sci. 1996; 263(1373):967-73. https://doi.org/10.1098/ rspb.1996.0143 PMid:8805834 DOI: https://doi.org/10.1098/rspb.1996.0143
Bennet-Clark HC, Ewing AW. The love song of the fruit fly. Sci Am. 1970; 223(1):85-90. https://doi.org/10.1038/ scientificamerican0770-84 DOI: https://doi.org/10.1038/scientificamerican0770-84
von Schilcher F. The function of pulse song and sine song in the courtship of Drosophila melanogaster. Anim Behav. 1976; 24(3):622-5. https://doi.org/10.1016/S0003- 3472(76)80076-0 DOI: https://doi.org/10.1016/S0003-3472(76)80076-0
Rideout EJ, Billeter JC, Goodwin SF. The sex-determination genes fruitless and doublesex specify a neural substrate required for courtship song. Curr Biol. 2007; 17(17):1473-8. https://doi.org/10.1016/j.cub.2007.07.047 PMid:17716899 PMCid:PMC2583281 DOI: https://doi.org/10.1016/j.cub.2007.07.047
Clyne JD, Miesenböck G. Sex-specific control and tuning of the pattern generator for courtship song in Drosophila. Cell. 2008; 133(2):354-63. https://doi.org/10.1016/j. cell.2008.01.050 PMid:18423205 DOI: https://doi.org/10.1016/j.cell.2008.01.050
Villella A, Gailey DA, Berwald B, Ohshima S, Barnes PT, Hall JC. Extended reproductive roles of the fruitless gene in Drosophila melanogaster revealed by behavioral analysis of new fru mutants. Genetics. 1997; 147(3):1107-30. https://doi.org/10.1093/genetics/147.3.1107 PMid:9383056 PMCid:PMC1208237 DOI: https://doi.org/10.1093/genetics/147.3.1107
Marcillac F, Grosjean Y, Ferveur JF. A single mutation alters production and discrimination of Drosophila sex pheromones. Proc Biol Sci. 2005; 272(1560):303-9. https://doi.org/10.1098/rspb.2004.2971 PMid:15705556 PMCid:PMC1634977 DOI: https://doi.org/10.1098/rspb.2004.2971
Ueyama M, Chertemps T, Labeur C, Wicker-Thomas C. Mutations in the desat1 gene reduces the production of courtship stimulatory pheromones through a marked effect on fatty acids in Drosophila melanogaster. Insect Biochem Mol Biol. 2005; 35(8):911-20. https://doi.org/10.1016/j. ibmb.2005.03.007 PMid:15944086 DOI: https://doi.org/10.1016/j.ibmb.2005.03.007
Labeur C, Dallerac R, Wicker-Thomas C. Involvement of desat1 gene in the control of Drosophila melanogaster pheromone biosynthesis. Genetica. 2002; 114(3):269- 74. https://doi.org/10.1023/A:1016223000650 PMid:12206365 DOI: https://doi.org/10.1023/A:1016223000650
Chertemps T, Duportets L, Labeur C, Ueyama M, Wicker‐ Thomas C. A female‐specific desaturase gene responsible for diene hydrocarbon biosynthesis and courtship behaviour in Drosophila melanogaster. Insect Mol Biol. 2006; 15(4):465- 73. https://doi.org/10.1111/j.1365-2583.2006.00658.x PMid:16907833 DOI: https://doi.org/10.1111/j.1365-2583.2006.00658.x
Wicker-Thomas C, Guenachi I, Keita YF. Contribution of oenocytes and pheromones to courtship behaviour in Drosophila. BMC Biochem. 2009; 10(1):1-8. https://doi. org/10.1186/1471-2091-10-21 PMid:19671131 PMCid: PMC2734525 DOI: https://doi.org/10.1186/1471-2091-10-21
Hegde SN, Krishnamurthy NB. Studies on mating behaviour in the Drosophila bipectinata complex. Aust J Zool. 1979; 27(3):421-31. https://doi.org/10.1071/ZO9790421 DOI: https://doi.org/10.1071/ZO9790421
Marcillac F, Ferveur JF. A set of female pheromones affects reproduction before, during and after mating in Drosophila. J. Exp Biol. 2004; 207(22): 3927-33. https://doi.org/10.1242/ jeb.01236 PMid:15472023 DOI: https://doi.org/10.1242/jeb.01236
Manning A. The control of sexual receptivity in female Drosophila. Anim Behav. 1967; 15(2-3):239-50. https://doi. org/10.1016/0003-3472(67)90006-1 PMid:6030948 DOI: https://doi.org/10.1016/0003-3472(67)90006-1
Cook R, Connolly K. Rejection responses by female Drosophila melanogaster: their ontogeny, causality and effects upon the behaviour of the courting male. Behaviour. 1973; 44(1-2):142-65. https://doi.org/10.1163/156853973X00364 DOI: https://doi.org/10.1163/156853973X00364
Nakano Y, Fujitani K, Kurihara J, Ragan J, Usui-Aoki K, Shimoda L, Yamamoto D. Mutations in the novel membrane protein spinster interfere with programmed cell death and cause neural degeneration in Drosophila melanogaster. Mol Cell Biol. 2001; 21(11):3775-88. https://doi. org/10.1128/MCB.21.11.3775-3788.2001 PMid:11340170 PMCid:PMC87027 DOI: https://doi.org/10.1128/MCB.21.11.3775-3788.2001
Brown RGB. Courtship behaviour in the Drosophila obscura group. I: D. pseudoobscura. Behaviour. 1964; 23(1-2):61- 105. https://doi.org/10.1163/156853964X00094 DOI: https://doi.org/10.1163/156853964X00094
Scott D, Richmond RC, Carlson DA. Pheromones exchanged during mating: a mechanism for mate assessment in Drosophila. Anim Behav. 1988; 36(4):1164-73. https://doi. org/10.1016/S0003-3472(88)80075-7 DOI: https://doi.org/10.1016/S0003-3472(88)80075-7
Tompkins L, Gross AC, Hall JC, Gailey DA, Siegel RW. The role of female movement in the sexual behavior of Drosophila melanogaster. Behav Genet. 1982; 12(3):295- 307. https://doi.org/10.1007/BF01067849 PMid:6812562 DOI: https://doi.org/10.1007/BF01067849
Lindahl T, Sedgwick B, Sekiguchi M, Nakabeppu Y. Regulation and expression of the adaptive response to alkylating agents. Annu Rev Biochem. 1988; 57(1):133- 157. https://doi.org/10.1146/annurev.bi.57.070188.001025 PMid:3052269 DOI: https://doi.org/10.1146/annurev.bi.57.070188.001025
Ferveur JF, Jallon JM. Nerd, a locus on chromosome III, affects male reproductive behavior in Drosophila melanogaster. Naturwissenschaften. 1993; 80(10):474-5. https://doi.org/10.1007/BF01136042 PMid:8264803 DOI: https://doi.org/10.1007/BF01136042
Kaya B, Creus A, Velázquez A, Yanikoğlu A, Marcos R. Induction of an adaptive response in Drosophila imaginal disc cells exposed in vivo to low doses of alkylating agents. Mutagenesis. 2000; 15(4):337-40. https://doi.org/10.1093/ mutage/15.4.337 PMid:10887213 DOI: https://doi.org/10.1093/mutage/15.4.337
Savina N, Dalivelya O, Kuzhir T. Adaptive response to alkylating agents in the Drosophila sex-linked recessive lethal assay. Mutat Res. 2003; 535(2):195-204. doi: 10.1016/ s1383-5718(02)00323-6. PMID: 12581538. https://doi. org/10.1016/S1383-5718(02)00323-6 PMid:12581538 DOI: https://doi.org/10.1016/S1383-5718(02)00323-6
Dhananjaya SG. Studies on the adaptive response of Drosophila melanogaster to a few alkylating agents. [PhD thesis]. Shankaraghatta, India; Kuvempu University; 2005.
Kumar MVT. Contribution to the knowledge of induction of adaptive response in Drosophila melanogaster exposed to Ethyl Nitrosourea and Methyl Nitrosourea. [PhD thesis]. Shankaraghatta, India; Kuvempu University; 2012.
Mahadimane PV, Vasudev V. Inducible protective processes in animal systems XIII: Comparative analysis of induction of adaptive response by EMS and MMS in Ehrlich Ascites Carcinoma cells. Scientifica. 2014; (5608):703136. https:// doi.org/10.1155/2014/703136 PMid:24999435 PMCid: PMC4066937 DOI: https://doi.org/10.1155/2014/703136
