INTRODUCTION In metazoan organisms, cytokinesis is initially driven by the purse-string-like constriction of an actomyosin-based contractile ring and its associated plasma membrane. At the end of cytokinesis, the contractile ring disassembles

In metazoan organisms, cytokinesis is initially driven by the purse-string-like constriction of an actomyosin-based contractile ring and its associated plasma membrane. At the end of cytokinesis, the contractile ring disassembles and the two daughter cells separate (reviewed in Satterwhite and Pollard, 1992; Fishkind and Wang, 1995). Although a large number of protein effectors of cytokinesis have been characterized, crucial mechanistic aspects of the process remain unexplained. For example, it is not clear how filamentous actin (F-actin), myosin II and other cleavage furrow proteins are assembled at the equator of the cell (for review, see Field et al., 1999), how the contractile ring maintains its association with the cell cortex during furrowing, nor how the terminal stage of cytokinesis, which requires proteins distinct from those involved in the previous steps, is regulated (Adachi et al., 1997; Madaule et al., 1998; Powers et al., 1998; Raich et al., 1998; Swan et al., 1998). A remarkable variation of the universal process of cytokinesis occurs during gametogenesis in many organisms: instead of separating, the daughter cells develop as a syncytium, with clonally related cells connected by intercellular bridges called ring canals (Cooley, 1995). During cytoplasmic bridge formation in the Drosophila male germline, structural proteins normally associated with the contractile ring persist to line the ring canal wall. These include the actin-binding protein anillin, and the septins, homologs of yeast bud neck filament proteins (Field and Alberts, 1995; Longtine et al., 1996; Hime et al., 1996). Although F-actin and myosin II are present in constricting contractile rings, they are largely disassembled during intercellular bridge formation in the male germline and do not persist as major components of the resulting ring canals (Hime et al., 1996). Incomplete cytokinesis in the male germline of Drosophila occurs following each of the four mitotic and two meiotic divisions, resulting in syncytial cysts of 64 spermatids connected by 63 ring canals (Lindsley and Tokuyasu, 1980). During meiosis, each primary spermatocyte undergoes two meiotic divisions to generate four early round spermatids, each with a single haploid nucleus. Immediately after meiosis, all of the mitochondria in a spermatid cell aggregate and fuse to form a single mitochondrial derivative (reviewed in Lindsley and Tokuyasu, 1980; Fuller, 1993). Early round spermatids from males defective in meiotic cytokinesis, for example klp3A or tsr, or treated with the anti-microfilament agent cytochalasin B exhibit a ‘four wheel drive’ phenotype, in which four haploid nuclei accompany an abnormally large mitochondrial derivative (Gunsalus et al., 1995; Williams et al., 1995; Giansanti et al., 1998). Here we describe four wheel drive (fwd), a gene required 3855 Development 127, 3855-3864 (2000) Printed in Great Britain © The Company of Biologists Limited 2000 DEV8749