Sperm Activation: Time and Tide Wait for No Sperm

Studies of the reproductive biology of the nematode Caenorhabditis elegans are providing valuable insights into the evolution and diversity of reproductive strategies [1,2]. The successful production of progeny in any species also highlights many fundamental problems in cell biology. Research on the amoeboid sperm of nematodes addresses a number of issues of broad biological significance, including cellular differentiation, cell polarity, signaling mechanisms and directed migratory behavior. C. elegans comes in two sexes: males and hermaphrodites. Adult males produce sperm throughout their reproductive life. Hermaphrodites produce several hundred sperm during their final larval stage and then switch to oocyte production as adults; they then self-fertilize until their sperm supply is exhausted. Hermaphrodites that have mated, however, produce outcrossed progeny as a result of sperm competition — in C. elegans, male-derived sperm are competitively superior to hermaphrodite-derived sperm for oocyte fertilization [3–5]. Mature oocytes are ovulated into the spermatheca (Figure 1A), which is the normal site of sperm storage and fertilization in C. elegans. Fertilization is very efficient; in the unmated hermaphrodite, sperm are a limited resource and virtually every functional sperm will fertilize an egg [5,6]. This is a result of the tight coordination of fertilization with oocyte maturation, ovulation, sperm signaling and sperm migratory behavior [7–9]. The crowded 'cannot miss' nature of the worm reproductive tract may also contribute to this efficiency. Haploid spermatids produced by males or hermaphrodites must undergo spermiogenesis — also known as sperm activation — to become fertilization competent. In C. elegans, this refers to the process of post-meiotic cellular differentiation which converts round, non-motile spermatids to polar, motile spermatozoa (Figure 1B). Spermiogenesis and its underlying signaling mechanisms are particularly interesting, as the dramatic and rapid cellular changes that occur must be driven without any new transcription or translation as sperm lack the cellular machinery required for these processes. Spermatids undergo activation in different contexts and locations depending on their origin (Figure 1A). Hermaphrodite-derived spermatids activate when they are pushed from the proximal gonad into the spermatheca during the first few rounds of ovulation in young adult worms. Male-derived spermatids activate immediately after they are transferred to the hermaphrodite uterus. Genetic studies have identified sterile mutants with defects in spermiogenesis (reviewed in [10]). Some mutations affect spermiogenesis in both sexes (spe-6 and fer-15) while other mutations (spe-8, spe-12, spe-19, spe-27 and spe-29, collectively known as the 'spe-8 group') are required for hermaphrodite-derived sperm activation but not …