Abstract
We describe persistent one-way walking of Drosophila melanogaster in a circular arena. Wild-type Canton-S adult flies walked in one direction, counter-clockwise or clockwise, for minutes, whereas white-eyed mutant \(w^{1118}\) changed directions frequently. Locomotion in the circular arena could be classified into four components: counter-clockwise walking, clockwise walking, nondirectional walking and pausing. Genetic analysis revealed that while wild-type genetic background was associated with reduced directional change and reduced numbers of one-way (including counter-clockwise and clockwise) and nondirectional walks, the white (\(w^+\)) locus promoted persistent one-way walking by increasing the maximal duration of one-way episodes. The promoting effect of \(w^+\) was further supported by the observations that (1) \(w^+\) duplicated to the Y chromosome, (2) four genomic copies of mini-white inserted on the autosomes, and (3) pan-neuronal overexpression of the White protein increased the maximal duration of one-way episodes, and that RNAi knockdown of \(w^+\) in the neurons decreased the maximal duration of one-way episodes. These results suggested a pleiotropic function of \(w^+\) in promoting persistent one-way walking in the circular arena.
Similar content being viewed by others
References
Anaka M, MacDonald CD, Barkova E, Simon K, Rostom R, Godoy RA, Haigh AJ, Meinertzhagen IA, Lloyd V (2008) The white gene of Drosophila melanogaster encodes a protein with a role in courtship behavior. J Neurogenet 22:243–76
Arkhipova I, Li J, Meselson M (1997) On the mode of gene-dosage compensation in Drosophila. Genetics 145:729–736
Awasaki T, Lai SL, Ito K, Lee T (2008) Organization and postembryonic development of glial cells in the adult central brain of Drosophila. J Neurosci 28:13742–13753
Bidaye SS, Machacek C, Wu Y, Dickson BJ (2014) Neuronal control of Drosophila walking direction. Science 344:97–101
Borycz J, Borycz JA, Kubów A, Lloyd V, Meinertzhagen IA (2008) Drosophila ABC transporter mutants white, brown and scarlet have altered contents and distribution of biogenic amines in the brain. J Exp Biol 211:3454–66
Bouhuys A (1964) Respiratory dead space. Section 3: respiration. Handb Physiol 1:699
Calenge C (2006) The package “adehabitat” for the r software: a tool for the analysis of space and habitat use by animals. Ecol Model 197:516–519
Campbell JL, Nash HA (2001) Volatile general anesthetics reveal a neurobiological role for the white and brown genes of Drosophila melanogaster. J Neurobiol 49:339–49
Carpenter FW (1905) The reactions of the pomace fly (Drosophila ampelophila Loew) to light, gravity, and mechanical stimulation. Am Nat 39:157–71
Cole BJ (1995) Fractal time in animal behaviour: the movement activity of Drosophila. Anim Behav 50:1317–1324
Cole WH (1922) Note on the relation between the photic stimulus and the rate of locomotion in Drosophila. Science 55:678–9
Colomb J, Reiter L, Blaszkiewicz J, Wessnitzer J, Brembs B (2012) Open source tracking and analysis of adult Drosophila locomotion in buridan’s paradigm with and without visual targets. PLoS ONE 7:e42247
Dreesen T, Johnson D, Henikoff S (1988) The brown protein of Drosophila melanogaster is similar to the white protein and to components of active transport complexes. Mol Cell Biol 8:5206–5215
Evans JM, Day JP, Cabrero P, Dow JA, Davies SA (2008) A new role for a classical gene: white transports cyclic GMP. J Exp Biol 211:890–9
Ewing AW (1963) Attempts to select for spontaneous activity in Drosophila melanogaster. Anim Behav 11:369–78
Gomez-Marin A, Oron E, Gakamsky A, Valente D, Benjamini Y, Golani I (2016) Generative rules of Drosophila locomotor behavior as a candidate homology across phyla. Sci Rep 6:27555
Grima B, Chélot E, Xia R, Rouyer F (2004) Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature 431:869–873
Hing AL, Carlson JR (1996) Male-male courtship behavior induced by ectopic expression of the Drosophila white gene: role of sensory function and age. J Neurobiol 30:454–64
Kain JS, Stokes C, de Bivort BL (2012) Phototactic personality in fruit flies and its suppression by serotonin and white. Proc Natl Acad Sci USA 109:19834–9
Liu L, Davis RL, Roman G (2007) Exploratory activity in Drosophila requires the kurtz nonvisual arrestin. Genetics 175:1197–212
McEwen RS (1918) The reactions to light and to gravity in Drosophila and its mutants. J Exp Zool 25:49–106
Morgan TH (1910) Sex limited inheritance in Drosophila. Science 32:120–2
O’Hare K, Murphy C, Levis R, Rubin GM (1984) DNA sequence of the white locus of Drosophila melanogaster. J Mol Biol 180:437–55
Qian S, Pirrotta V (1995) Dosage compensation of the Drosophila white gene requires both the X chromosome environment and multiple intragenic elements. Genetics 139:733–44
Qiu S, Xiao C, Robertson RM (2016) Pulsed light stimulation increases boundary preference and periodicity of episodic motor activity in Drosophila melanogaster. PLoS ONE 11:e0163976
Qiu S, Xiao C, Robertson RM (2017) Different age-dependent performance in Drosophila wild-type Canton-S and the white mutant w1118 flies. Comp Biochem Physiol A 206:17–23
Core Team R (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Sarkar D (2008) Lattice: multivariate data visualization with R. Springer, New York
Sitaraman D, Zars M, Laferriere H, Chen YC, Sable-Smith A, Kitamoto T, Rottinghaus GE, Zars T (2008) Serotonin is necessary for place memory in Drosophila. Proc Natl Acad Sci USA 105:5579–84
Soibam B, Goldfeder RL, Manson-Bishop C, Gamblin R, Pletcher SD, Shah S, Gunaratne GH, Roman GW (2012) Modeling Drosophila positional preferences in open field arenas with directional persistence and wall attraction. PLoS ONE 7:e46570
Sullivan DT, Sullivan MC (1975) Transport defects as the physiological basis for eye color mutants of Drosophila melanogaster. Biochem Genet 13:603–13
Tearle R, Belote J, McKeown M, Baker B, Howells A (1989) Cloning and characterization of the scarlet gene of Drosophila melanogaster. Genetics 122:595–606
Vermehren-Schmaedick A, Ainsley JA, Johnson WA, Davies SA, Morton DB (2010) Behavioral responses to hypoxia in Drosophila larvae are mediated by atypical soluble guanylyl cyclases. Genetics 186:183–96
Xiao C, Qiu S, Robertson RM (2017) The white gene controls copulation success in Drosophila melanogaster. Sci Rep 7:7712
Xiao C, Robertson RM (2015) Locomotion induced by spatial restriction in adult Drosophila. PLoS ONE 10:e0135825
Xiao C, Robertson RM (2016) Timing of locomotor recovery from anoxia modulated by the white gene in Drosophila. Genetics 203:787–797
Xiao C, Robertson RM (2017) White-cGMP interaction promotes fast locomotor recovery from anoxia in adult Drosophila. PLoS ONE 12:e0168361
Zhang S, Binari R, Zhou R, Perrimon N (2010) A genomewide rna interference screen for modifiers of aggregates formation by mutant huntingtin in Drosophila. Genetics 184:1165–79
Zhang SD, Odenwald WF (1995) Misexpression of the white (w) gene triggers male-male courtship in Drosophila. Proc Natl Acad Sci USA 92:5525–9
Funding
This study was funded by Natural Sciences and Engineering Research Council of Canada (NSERC) Grant (RGPIN 40930-09) to R.M.R.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Statement of human and animal rights
This article does not contain any studies with human participants performed by any of the authors.
Additional information
Edited by Yong-Kyu Kim.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Xiao, C., Qiu, S. & Robertson, R.M. Persistent One-Way Walking in a Circular Arena in Drosophila melanogaster Canton-S Strain. Behav Genet 48, 80–93 (2018). https://doi.org/10.1007/s10519-017-9881-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10519-017-9881-z