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Behavior and Cytogenetics of Fruitless in Drosophila Melanogaster

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Behavior and Cytogenetics of Fruitless in Drosophila Melanogaster Copyright 0 1989 by the Genetics Society of Amerlcd Behavior and Cytogenetics offruitless in Drosophila melanogaster: Different Courtship Defects Caused by Separate, Closely Linked Lesions Donald A. Gailey and JeffreyC. Hall Department of Biology, Brandeis University, Waltham, Massachusetts02254 Manuscript received September 22, 1988 Accepted for publication December 24, 1988 ABSTRACT Thefruitless (fru)courtship mutant was dissected into three defectsof male reproductive behavior, which were separable as to their genetic etiologies by application of existing and newly induced chromosomal aberrations.fru itself is a small inversion [In(3R)9OC; 9 1B] on genetic andcytological criteria. Uncovering the fru distal breakpoint with deletions usually led to males with two of thefru courtship abnormalities: no copulation attemptswith females (hence, behavioralsterility) and vigorous courtship among males, including the formation of “courtship chains.” However, certain genetic changes involving region 91B resulted in males who formed courtship chains but who mated with females. Uncovering the fru proximal breakpoint led to males that passively elicit inappropriately high levels of courtship. Thiselicitation property was separable genetically from thesterility and chain formation phenotypes and provisionally mapped to the interval 89F-90F, which includes the fru proximal breakpoint. Behavioral sterility and chaining werealso observed in males expressing certain abnormal genotypes, independent of thefru inversion. These included combinations ofdeficiencies, each with a breakpoint in 91B, and a transposon inserted in 91 B. RECOPULATORY behaviors are sex-specific nervous system (CNS). Thus, a search for mutations P components of reproduction. In Drosophila mel- that disrupt the male-specific behavior of attempted anogaster, males respond to females with a stereotypic copulation might not only reveal genes that are rele- set of actions, including following, production of a vant to, for example, male-specific musculature in the courtship song via wing vibration and curling of the abdomen (cf: LAWRENCEand JOHNSTON1984), but abdomen in order to initiate mating(reviews: HALLet that also lead to defects within the CNS. A mutant al. 1980; EWING1983; TOMPKINS1984; HALL1985). that could be in this category is fruitless (fru). A The responses of females to these male behaviors are cytogenetic analysis offru-associated courtship anom- less overt and undoubtedly involve nervous system- alies is the focus of this report. dependent phenomena (e.g., TOMPKINSand HALL fru is a homozygous-viable, male-sterile mutant that 1983). Females perceive male courtship cues that are was induced with X-rays (GILL1963a, b). The effects chemical (reviews: JALLON1984; TOMPKINS1984), of fru seem to be male specific, in that females homo- auditory (e.g., EWINC1977; HALL 1984, 1986), and zygous for fru show no obvious phenotypic or behav- visual (e.g., TOMPKINS1984; MARKOW1987) inna- ioral differences from wild type (HALL1978a). Males ture. Receptive females ultimately respond to the cues homozygous for fru, however, show at least three of conspecific males by slowing their locomotor move- obvious deviations from normal male courtship be- ments, and mating ensues (MARKOWand HANSON havior. (1)They do notcurl their abdomens femalesat 1981; TOMPKINSet al. 1982; GAILEY,LACAILLADE to attempt copulation, and are thereby behaviorally and HAIL 1986). sterile (HALL 1978a); to this extent fru could be an It should be possible in Drosophila to “dissect out” example of a gene controlling male-specific actions in genes pertinent to these behavioral dimorphisms. For courtship. (2) They court otherfru males and normal exanlple, mosaic analysis of precopulatory behavior males (HALL1978a); this could mean that fru is rele- has led to the identification of thoracic tissues which vant to the discrimination by malesof appropriate must be male for copulation attempts tobe performed courtshipobjects, since normal males rarely court by gynandromorphs (HOTTAand BENZER1976; HALL each other. (3) They stimulate normal males to court 1979), implying that this behavior is not generated or them; consequently, courtship-stimulating cues could controlled locally within the male abdomen per se, but emanate from fru males (HALL1978a), a hypothesis probably is subserved by male tissues in the central supported by the results of bioassay experiments in which solvent extracts of fru males stimulated court- Dedicated to R. W. Siege1 and his fruitful career as a ship (TOMPKINS,HALL and HALL1980). geneticist. In the current study we show that the fru pheno- (kwt.ti<< 121: ii:i-78.~(April. 1989) 774 D. A. Gailey and J. C. Hall TABLE 1 Chromosomal aberrations used in the cytogenetic localizationof thefruitless phenotypes Marker Aberration genotype" Cvtology Origin Referenceb Deficiencies Df(3R)PI4 X-ray LINDSLEYand ZIMM(1985); K. MOSES (personal communication) Df(3R)Cha"' X-ray LINDSLEYand ZIMM(1985); K. MOSES(personal communication) Df(3R)Cha"' 91B;91D X-ray LINDSLEYand ZIMM (1985) Df(3R)Cha"' 90F:91 F' y-ray LINDSLEYand ZIMM (1985); K. MOSES(personal communication) Df(3H)148.5-1 91B3;91D1 y-ray GORCZYCAand HALL(1984); W. M. GELBART (personal communication) Df(3R)DCI 90E1-2;91C3-7 ?-ray This report Df(3R)DG2 89E-F;91B1-2 y-ray This report Df(3R)DG3 89F;90F 7-y This report Df(3R)DG4 90E1-2;90F3-11 ?-ray This report Df(3R)DCS 9OE-F;9lE-F way This report Df(3R)glBXZ 90F8-11;91B1-2 X-ray K. MOSES(personal communication) Df(3R)glBXZO 90C7-8;91B1-2 X-ray K. Mosm (personal communication) Df(3R)gl+BX5 91B1-2;91D1-2 X-ray K. MOSES (personal communication) Df(3R)gl+BX6 90C9-10:90F2-11 X-ray K. MOSES(personal communication) Marked transposon P(w+)ARO-Z w+ inserted at 91B1-2 Transposon LEVIS, HAZELRICCand RUBIN (1985); K. Moses mobilization (personal communication) Duplication Dp(3R)DGd sr+ gl- 81-90A;90F-90A; y-ray This report 90A-100 a Presence (+), or absence (-) of normal marker gene function on aberration-bearing chromosome as inferred from crosses with 6% sr gl or a lethal allele of Cha (choline acetyltransferase). Absence of any marker designation(s) means that particular cross was not performed. Cytology on all chromosomes was provided by K. MOSES,except for Df(3R)ChaM' and Df(3R)148.5-Z.The second through fifth deletions in this table were isolated as Cha- (cf: GORCZYCAand HALL 1984; P. L. MYERS and W. M. GELBART,unpublished data). The last four deletions were derived from a screen for deletions near or including gl (K. MOSES, unpublished data). Indicates cytological information supplied by K. MOSESthat differs slightly from the published breakpoints. Shows no visible aberration in the region ofgl at 91A (K. MOSES,personal communication); Df(jR)P14/Dp(3R)DG is viable and sr+ gl- in phenotype; Df(?R)DG3/Dp(3R)DCis viable and sr+ gl+ (no other crosses were performed). types do not all map to a single genetic locus but are maintained in the laboratory of J. C. HALLby mass transfer associated with a small inversion on the third chro- of unselected adults. Chromosomal aberrations used to map thefruitless phe- mosome. The two mutant behaviors that fru males notypes are listed in Table 1 and schematically presented in themselves display in their courtship co-map with one Figure 1. Markers used in mapping by recombination were breakpoint of this inversion; the mutant behavior that bithorax (b~~~~,3, 58.8), stripe (sr, 3, 62.0) and glass, (gl, 3, fru males elicit from normal males maps provisionally 63.1). to the other breakpoint. Balancer chromosomes (Bal) used were In(3LR)TM3 (=TM3), marked with the dominant mutation Stubble (Sb); In(3LR)TM6 (=TM6),marked with the dominant mutation MATERIALSAND METHODS Ultrabithorax (UbxPl5);and In(3LR)TM6B (=TM6B; CRAY- MER 1984), markedwith the dominant mutationTubby (Tb), The maintenance of fly cultures and procedures of fly which imparts a distinctive body shape in both adults and handling for behavioral assays were as detailed in GAILEY, larvae andfacilitated selection ofhomozygousfru/fru larvae JACKSON and SIEGEL(1 982) and GAILEY, LACAILLADE and for salivary gland squashes. HALL (1986). Flies were grown on a medium containing P(w+)ARO-I is a transposon containing the white+ (w, I, cornmeal, molasses, agar, yeast and the mold-inhibitor Te- 1.5) gene, and was derived from mobilization of the tran- gosept . sposon P[(w,ry)AR]4-3 andreinsertion at the cytogenetic Fly stocks: Several of the genetic variants used in this region91B1-2 (LEVIS, HAZELRIGGand RUBIN 1985; K. analysis appear in LINDSLEYand GRELL (1 968),or LINDSLEY MOSES,personal communication). This transposonis main- and ZIMM (1 985); others arenewly isolated (Table 1). tained in the stock wl'", TM3/ARO-1, which was provided fruitless (fru, 3, 62.0 HALL 1978a)"derived from X-ray to us by K. MOSESand G. M. RUBIN. mutagenesis(GILL 1963a, b). fru/"ru males expressthe Screen for new aberrations in the region of sr and gl: fruitless syndrome of behavioraldefects, frulfru females Wild-type males from a Canton-S strain received 4.5 kR y- appear normal (HALL 1978a).Because of the male sterility, irradiationfrom a 137Cssource, delivered at the rate of fru stocks are kept with balancer chromosomes (see below). approximately 265 R/min. They were immediately crossed The starting stock for the current analysis was TMb/fru, to bx sr gl homozygous females. FI males displaying the sr “I fruitless Courtship I In 4” -”) EFABCDEFABCDEF 90 91 I E3 =a I kc fiu break “g’& 0 0 FIGURE2.-fru courtship chain beh;lvior. To the left are nine Df(3R)g1RX//frumales (see Table 1 and Figure 4 for details on this deletion). Arrows indicate instances of wing vibration. To the right are nine Df(3R)g/RXI/+ males. I. ship stimulation phenotype). One line was selected arbitrar- P (w+) ARO-I ily (a TM6/fru female-derived line) and was the source for FIGURE 1 .-Approximate breakpoint cytology of aberration- fru chromosomes in all further crosses.
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