The male germ line produces only male gametes, spermatids. As in the hermaphrodite, the male germ line exhibits distal-proximal polarity with a mitotic cell population located at the most distal end of the gonad (DG) and meiotic cells extending proximally. Gametogenesis occurs in the proximal germ line and the resulting spermatids are stored in the seminal vesicle until ejaculation (MaleReproFIG 17A; Hirsh et al., 1976; Klass et al., 1976; Kimble and Hirsh, 1979).

Much of the male germ line is a syncytium. Germ cells have incomplete borders and are connected to one another via a central canal, the rachis (MaleReproFIG 17B and 17C). The germ line is ensheathed only by the gonadal basal lamina (gbl) which also covers the somatic portion of the gonad.

2 Mitosis in the Germ Line

As in the hermaphrodite, the distal end of the male germ line (MaleReproFIG 18A) contains a stem cell population and is referred to as the mitotic zone. As germ cells move away from the influence of the distal tip cell (DTC, described in Male Reproductive System - Somatic Gonad), they enter meiosis I, proceeding through prophase I to pachytene (Hirsh et al., 1976). Nuclear morphology at various stages of mitosis and meiosis I can visualized with DAPI staining (examples from the hermaphrodite germ line, highlighting stage-specific characteristics, are shown in MaleReproFIG 18B-D).

3 Spermatogenesis and Spermiogenesis

See Sperm Gallery for detailed pictures and videos

After pachytene, the precursor of spermatids, the spermatocytes, detach from the rachis and complete meiosis generating haploid spermatids (MaleReproFIG 19 and 20). This process of spermatid formation is called spermatogenesis. Spermatids are stored in the seminal vesicle until ejaculation. Spermiogenesis, activation of sessile spermatids into crawling spermatozoa, occurs after mating, in the hermaphrodite uterus (see Spermiogenesis Figure and Video). Some spermatids that remain in the male after mating, however, may mature into spermatozoa and can be seen swimming around the vas deferens and seminal vesicle (Ward and Carrel, 1979). Recent studies suggest that the male gonad contains substances that prevent premature activation of spermatids prior to sperm transfer (Stanfield and Villeneuve, 2004).

Developing spermatocytes contain a large number of specialized vesicles called FB-MOs (Fibrous Body-Membranous Organelle) (MaleReproFIG 21, 22 and 23). These organelles contain proteins required in the future spermatid and spermatozoon, including MSP (Major Sperm Protein; Wolf et al., 1978; Ward and Klass,1982). During development, the FB-MOs partition with the portion of the spermatocyte destined to become the future spermatid (Ward, 1986). The residual body (MaleReproFIG 22; Dividing Spermatocytes Figure) acts as a depot for proteins and organelles no longer required by the developing spermatid (L'Hernault, 1997; Arduengo et al., 1998; Kelleher et al., 2000).

Maturing spermatids and spermatozoa have highly condensed nuclei (N) and tightly packed mitochondria (M) (MaleReproFIG 23; Spermatozoon TEM Figure). In spermatids, MOs (now lacking FB) locate near the cell periphery. During spermatid activation, MOs fuse with the plasma membrane releasing their contents (primarily glycoproteins) onto the cell surface. A fusion pore is generated on the cell surface by the MO collar (MaleReproFIG 24). Mutants affected in MO fusion produce sperm with defective motility suggesting that MO content enhances sperm mobility (Ward et al., 1981; Roberts et al, 1986; Achanzar and Ward, 1997). Spermatid activation also involves the formation of a foot or pseudopodium (MaleReproFIG 24; Spermatozoon SEM Figure). In contrast to sperm in other phyla, C. elegans sperm lack flagella. Pseudopodia allow spermatozoa to attach to the walls of the spermathecal or seminal vesicle lumen and to crawl (see Crawling Sperm Video). This motility is driven by dynamic polymerization of MSP (Major Sperm Protein). In addition to an intracellular cytoskeletal function, MSP contains sequences that mediate extracellular signaling (see Oocyte maturation section of Hermaphrodite Reproductive System - Germ Line; Miller et al, 2001; Italiano et al., 1996; Roberts and Stewart, 2000).

Male germ line development spans L1 to early adulthood. All germ cells are descended from either Z2 or Z3 (Kimble and Hirsh, 1979). Key events in germ line development are summarized in MaleReproFIG 25. In contrast to somatic lineage development in C. elegans, germ line cell divisions appear to be variable with respect to their timing and planes of division (Kimble and Hirsh, 1979) and hence the precise lineal relationships between these cells are not known.

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