Comparative Analysis of Mating Behavior Characteristics of Mutants at the white Locus of Drosophila melanogaster

V.V. Kostenko

Kazan Federal University, Kazan, 420008 Russia

E-mail: vvkostenko1@gmail.com

Received January 18, 2017

Full text PDF

Abstract

Drosophila melanogaster serves as an excellent model system to study the control of innate behaviors. Behavior is the ability of animals to change their actions under the influence of internal and external factors, a characteristic feature of the animal type of organization. Sexual behavior of Drosophila is organized as a complex physiological and biochemical trait and consists of certain successive stages, which, as a rule, are repeated several times until mating occurs. These stages include the exchange of visual, sound, and chemosensory signals between the partners. Drosophila white (w) gene, discovered in 1910 by Thomas Hunt Morgan, encodes a subunit of an ATP-binding cassette (ABC) transporter, which loads up pigment granules and deposits the content to pigment cells in the compound eyes. The white gene has housekeeping functions in the central nervous system in addition to its classical role in eye pigmentation. Previously, we have shown the influence of mutant alleles at the white locus on the locomotor activity in Drosophila adults. Therefore, investigating the effect of different white alleles on behavioral traits, including mating behavior, which is also an important component of adaptation, seems to be of interest.

The influence of mutant alleles at the white locus on mating behavior characteristics in Drosophila melanogaster imagoes has been studied. Mating activity of males, mating receptivity of females, duration and latency of copulation as traits of mating behavior have been examined. The results of the present study and the analysis of published data have demonstrated that different alleles of white locus, in combination with genetic factors, substantially influence the mating behavior of D. melanogaster. It has been shown that mutant alleles at the white locus play a significant role in controlling the mating behavior of females. Furthermore, it has been found that intensively pigmented individuals are characterized by lower latency of copulation and, as a result, longer mating.

Keywords: white locus, pigment mutations, mating behavior, latency of copulation, duration of copulation, Drosophila melanogaster

Figure Captions

Fig. 1. Mating behavior characteristics of females and males of Canton-S and Oregon lines (wild type): mating activity of males (MA), mating receptivity of females (MR), and their temporal characteristics (latency (LC) and duration (DC) of copulation).

Fig. 2. The mating activity of mutants at the white locus of Drosophila melanogaster males.

Fig. 3. The mating receptivity of mutants at the white locus of Drosophila melanogaster females.

Fig. 4. The mean duration of copulation under the conditions of a surplus of females (MA) and males (MR) mutant at the white locus of Drosophila melanogaster imagoes.

Fig. 5. The mean latency of copulation under the conditions of a surplus of females (MA) and males (MR) mutant at the white locus of Drosophila melanogaster imagoes.

References

1. Dukas R., Mooers A.Ø. Environmental enrichment improves mating success in fruit flies. Anim. Behav., 2003, vol. 66, no. 4, pp. 741–749. doi: 10.1006/anbe.2002.2261.
2. Yurkovic A., Wang O., Basu A.C., Kravitz E.A. Learning and memory associated with aggression in Drosophila melanogaster. Proc. Natl. Acad. Sci. U. S. A., 2006, vol. 103, no. 46, pp. 17519–17524. doi: 10.1073/pnas.0608211103.
3. Hall J.C. Courtship lite: A personal history of reproductive behavioral neurogenetics in Drosophila. J. Neurogenet., 2002, vol. 16, pp. 135–163. doi: 10.1080/01677060290024628.
4. Krstic D., Boll W., Noll M. Sensory integration regulating male courtship behavior in Drosophila. PLoS One, 2009, vol. 4, no. 2, art. e4457, pp. 1–13. doi: 10.1371/journal.pone.0004457.
5. Anaka M., MacDonald C.D., Barkova E., Simon K., Rostom R., Godoy R. A., Haigh A.J., Meinertzhagen I.A., Lloyd V. The white gene of Drosophila melanogaster encodes a protein with a role in courtship behavior. J. Neurogenet., 2008, vol. 22, no. 4, pp. 243–276. doi: 10.1080/01677060802309629.
6. Krstic D., Boll W., Noll M. Influence of the white locus on the courtship behavior of Drosophila males. PLoS One, 2013, vol. 8, no. 10, art. e77904, pp. 1–8. doi: 10.1371/journal.pone.0077904.
7. Xiao C., Qiu S., Robertson R.M. Mating success associated with white gene in Drosophila melanogaster. bioRxiv. Available at: http://biorxiv.org/content/biorxiv/early/2016/08/31/072710.full.pdf.
8. Mackay T.F.C., Heinsohn S.L., Lyman R.F., Moehring A.J., Morgan T.J., Rollmann S.M. Genetics and genomics of Drosophila mating behavior. Proc. Natl. Acad. Sci. U. S. A., 2005, vol. 102, suppl. 1, pp. 6622–6629. doi: 10.1073/pnas.0501986102.
9. Moehring A.J., Mackay T.F.C. The quantitative genetic basis of male mating behavior in Drosophila melanogaster. Genetics, 2004, vol. 167, no. 3, pp. 1249–1263. doi: 10.1534/genetics.103.024372.
10. Green M.M. The “genesis of the White-Eyed Mutant” in Drosophila melanogaster: A reappraisal. Genetics, 1996, vol. 142, no. 2, pp. 329–331.
11. Sullivan D.T., Grillo S.L., Kitos R.J. Subcellular localization of the first three enzymes of the ommochrome synthetic pathway in Drosophila melanogaster. J. Exp. Zool., 1974, vol. 188, no. 2, pp. 225–233. doi: 10.1002/jez.1401880210.
12. Summers K.M., Howells A.J., Pyliotis N.A. Biology of eye pigmentation in insects. Adv. Insect Physiol., 1982, vol. 16, pp. 119–166. doi: 10.1016/S0065-2806(08)60153-8.
13. Ewart G.D., Howells A.J. ABC transporters involved in transport of eye pigment precursors in Drosophila melanogaster. Methods Enzymol., 1998, vol. 292, pp. 213–224. doi: 10.1016/S0076-6879(98)92017-1.
14. Borycz J., Borycz J.A., Kubów A., Lloyd V., Meinertzhagen I.A. Drosophila ABC transporter  mutants white, brown and scarlet have altered contents and distribution of biogenic amines in the brain. J. Exp. Biol., 2008, vol. 211, pp. 3454–3466. doi: 10.1242/jeb.021162.
15. Campbell J.L., Nash H.A. Volatile general anesthetics reveal a neurobiological role for the white and brown genes of Drosophila melanogaster. J. Neurobiol., 2001, vol. 49, no. 4, pp. 339–349.
16. Hoyer S.C., Eckart A., Herrel A., Zars T., Fischer S.A. Octopamine in male aggression of Drosophila. Curr. Biol., 2008, vol. 18, no. 3, pp. 159–167. doi: 10.1016/j.cub.2007.12.052.
17. Sitaraman D., Zars M., LaFerriere H., Chen Y.C., Sable-Smith A. Serotonin is necessary for place memory in Drosophila. Proc. Natl. Acad. Sci. U. S. A., 2008, vol. 105, no. 14, pp. 5579–5584. doi: 10.1073/pnas.0710168105.
18. Kostenko V.V., Vorob'eva L.I. The influence of white allels and genetic background on locomotor activity of adult Drosophila melanogaster. Vestn. Khar'k. Nats. Univ. im. V. N. Karazina, Ser. Biol., 2012, vol. 16, no. 1035. pp. 90–96. (In Russian)
19. Pole I.R. The analysis of genetic determination of male mating activity in Drosophila melanogaster. Extended Abstract of Cand. Biol. Sci. Diss. Leningrad, 1979. 20 p. (In Russian)
20. Subotcheva E.A., Romanova N.I., Karpova N.N., Yuneva A.O., Kim A.I. Male reproductive behavior in Drosophila melanogaster strains with different allels of the flamenco gene. Genetics, 2003, vol. 39, no. 5, pp. 553–558. doi: 10.1023/A:1023735717768.
21. da Silva L.B., Valente V.L.S. A temporal analysis of sexual activity in a natural population of Drosophila willistoni. Hereditas, 2000, vol. 133, no. 3, pp. 211–216. doi: 10.1111/j.1601-5223.2000.00211.x.
22. Lakin G.F. Biometrics. Moscow, Vyssh. Shk., 1990. 351 p. (In Russian)
23. Yamamoto D., Jallon J.M., Komatsu A. Genetic dissection of sexual behavior in Drosophila melanogaster. Annu. Rev. Entomol., 1997, vol. 42, pp. 551–585. doi: 10.1146/annurev.ento.42.1.551.
24. Kalmus H. The optomotor responses of some eye mutants of Drosophila. J. Genet., 1943, vol. 45, p. 206–213.
25. Wu C.F., Wong F. Frequency characteristics in the visual system of Drosophila. Genetic dissection of electroretinogram components. J. Gen. Physiol., 1977, vol. 69, no. 6, pp. 705–724. doi: 10.1085/jgp.69.6.705.
26. Van Swinderen B., Andretic R. Dopamine in Drosophila: Setting arousal thresholds in a miniature brain. Proc. R. Soc. B., 2011, vol. 278, pp. 906–913. doi:10.1098/rspb.2010.2564.
27. Andretic R., van Swinderen B., Greenspan R.J. Dopaminergic modulation of arousal in Drosophila. Curr. Biol., 2005, vol. 15, no. 13, pp. 1165–1175. doi: 10.1016/j.cub.2005.05.025.
28. Erhardt S., Schwieler L., Nilsson L., Linderholm K., Engberg G. The kynurenic acid hypothesis of schizophrenia. Physiol. Behav., 2007, vol. 92, nos. 1–2, pp. 203–209. doi: 10.1016/j.physbeh.2007.05.025.
29. Saleem, S., Ruggles P.H., Abbott W.K., Carney G.E. Sexual experience enhances Drosophila melanogaster male mating behavior and success. PLoS One, 2014, vol. 9, no. 5, art. e96639, pp. 1–8. doi: 10.1371/journal.pone.0096639.

For citation: Kostenko V.V. Comparative analysis of mating behavior characteristics of mutants at the white locus of Drosophila melanogaster. Uchenye Zapiski Kazanskogo Universiteta. Seriya Estestvennye Nauki, 2017, vol. 159, no. 2, pp. 293–305. (In Russian)

The content is available under the license Creative Commons Attribution 4.0 License.