Components of Segregation Distortion in Drosophila Melanogaster . 111 . Nature of Enhancer of Sd

Analysis of X-ray-induced deletions in the Segregation Distorter (SD) chromosome, SD-5, revealed that this chromosome had a gene proximal to It in the centric heterochromatin of 2L that strongly enhanced the meiotic drive caused by the SD chromosome. This Enhancer of Segregation Distortion [E(SD)] locus had not been characterized in earlier studies of SD chromosomes because it cannot be readily separated by recombination from the Responder (Rsp) locus in the proximal heterochromatin of 2R.-To determine whether E(SD) is a general component of all SD chromosomes and to examine further its effects on distortion, we produced deletions of E(SD) in three additional SD chromosomes. Analysis of these deletions leads to the following conclusions: (1) along with Sd and RsP, E(SD) is common to all SD chromosomes; (2) the E(SD) allele on each SD chromosome enhances distortion by the same amount, which indicates that allelic variation at the E(SD) locus is not responsible for the different drive strengths seen among SD chromosomes; (3) E(SD) causes very little or no distortion by itself in the absence of Sd; (4) E(SD), like Sd, acts in a dosage-dependent manner; ( 5 ) E(SD) exerts its effect in cis or trans to Sd; and (6) if E(SD)+ exists, its function is not related to SD. ALE Drosophila melanogaster heterozygous for a Segregation Distorter M (SD)-bearing second chromosome and a normal homologue produce a vast excess of progeny receiving the SD chromosome, owing to the induced dysfunction of the SD’ gametes (SANDLER, HIRAIZUMI and SANDLER 1959; NICOLETTI, TRIPPA and DEMARCO 1967; HARTL, HIRAIZUMI and CROW 1967; NICOLETTI 1968; TOKUYASU, PEACOCK and HARDY 1977). Dissection of SD chromosomes by recombination and by analysis of deletions indicates that at least two loci are involved in the mechanism of distortion: the Sd locus whose presence is necessary to cause sperm dysfunction and the Rsp locus that behaves as the site at which Sd acts (SANDLER and HIRAIZUMI 1960; HIRAIZUMI and NAKAZIMA 1967; HARTL 1974; HARTL and HIRAIZUMI 1976; GANETZKY 1977; SHARP 1977; BRITTNACHER and GANETZKY 1983). In addition to these two components, other “modifier” loci have been detected on particular SD chromosomes that may also play a role in segregation distortion (SANDLER 1962; KATAOKA 1967; HARTL 1970; MIKLOS 1972; TRIPPA and LOVERRE 1975; HIRAIZUMI, MARTIN and ECKSTRAND 1980). AlGenetics 197: 423-434 July, 1984 424 J. G. BRITTNACHER AND B. GANETZKY though some detailed models of distortion have been proposed in which these other loci are ascribed a central role, in no case has any one of these loci been shown rigorously to be a general component of all SD chromosomes. To obtain a more complete picture of the genetic architecture of SD chromosomes, their origin and evolution in nature and the mechanisms of distortion, the role of these additional loci and their status as general components of SD chromosomes require clarification. One such locus, called Enhancer of Segregation Distortion [E(SD)], was detected in the SD-5 chromosome in the analysis of X-ray-induced SD revertants (GANETZKY 1977; SHARP 1977). Deletion of this element, which was located in or near the proximal heterochromatin of 2L, resulted in a partial loss of distorting ability by the SD-5 chromosome. In the present study, using three additional SD chromosomes structurally distinct from SD-5, we have produced a collection of heterochromatic deletions whose analysis indicates that all of these SD chromosomes carry E(SD). Further examination of these deletions has enabled us to map this component more carefully within the 2L heterochromatin and to analyze further the role of E(SD) in the mechanism of distortion. MATERIALS AND METHODS Chromosomes: For a complete description of the markers used in this study see LINDSLEY and cn bw was used as the standard sensitive tester chromosome. It pk cn bw, a supersensitive tester chromosome, was produced by recombination between It pk cn (obtained from D. HOLM) and cn bw. The It pk cn bw derivative has the Same sensitivity as It pk cn. SD-Roma was collected in Rome, Italy (=SDR-' of NICOLETTI and TRIPPA 1967) and has no inversions. SD-Roma,bw was derived from this chromosome by recombination with cn bw. SD-72 was collected in Madison, Wisconsin (SANDLER, HIRAIZUMI and SANDLER 1959), and carries a pericentric inversion, In(ZLR)39D;42A, and a paracentric inversion, Zn(2R)NS = In(2R)52AZ-B1;56F9-13. SD-5 was collected along with SD-72 in Madison and has two nonoverlapping paracentric inversions, In(2R)45C-F;49A and In(2R)NS. SD-Mad was collected in Madison in 1979 by R. G. TEMIN. It has the same inversions as SD72 but differs from SD-72 by being fully viable and fertile in both sexes when homozygous. Screen for It deletions: SD-Roma,bw/cn bw, SD-72/cn bw and homozygous SD-Mad males were irradiated with 3000-4000 rad of X-rays and mated to b pr It pk cn females. After 3 days, the irradiated males were discarded. The F, males were screened for the appearance of It (light eyes, 2-55.0, salivary chromosome region 40B-F). The putative deletion-bearing flies were mated to recover the treated SD chromosome heterozygous with a balancer chromosome. The treated chromosome was examined in complementation tests with other deletions and lethals at the base of 2L to determine the presence and extent of any newly induced lesion. Test for the ability to distort: T o test the SD chromosomes and their derivatives for the ability to distort, 20 males heterozygous for the chromosome to be tested and a standard chromosome (cn bw, It pk cn bw or SD-5) were singly mated to two cn bw females at 25". Each male and two females were brooded 5 days, transferred to new food vials and brooded another 7 days before being discarded. Offspring from each vial were counted through day 17 after parents were introduced into that vial. The ability of males to cause distortion is expressed in terms of k value, where k is the proportion of offspring that received the chromosome under test among the total progeny. This measurement assumes equal viability of the two chromosomes. However, the X-ray-induced deletions GRELL ( 1 968).