Regulation of Sperm Activation by SWM-1 Is Required for Reproductive Success of C. elegans Males

Abstract

Sexual reproduction in animals requires the production of highly specialized motile sperm cells that can navigate to and fertilize ova. During sperm differentiation, nonmotile spermatids are remodeled into motile spermatozoa through a process known as spermiogenesis. In nematodes, spermiogenesis, or sperm activation, involves a rapid cellular morphogenesis that converts unpolarized round spermatids into polarized amoeboid spermatozoa capable of both motility and fertilization. Here we demonstrate, by genetic analysis and in vivo and in vitro cell-based assays, that the temporal and spatial localization of spermiogenesis are critical determinants of male fertility in C. elegans, a male/hermaphrodite species. We identify swm-1 as a factor important for male but not hermaphrodite fertility. We show that whereas in wild-type males, activation occurs after spermatids are transferred to the hermaphrodite, swm-1 mutants exhibit ectopic activation of sperm within the male reproductive tract. This ectopic activation leads to infertility by impeding sperm transfer. The SWM-1 protein is composed of a signal sequence and two trypsin inhibitor-like domains and likely functions as a secreted serine protease inhibitor that targets two distinct proteases. These findings support a model in which (1) proteolysis acts as an important in vivo trigger for sperm activation and (2) regulating the timing of proteolysis-triggered activation is crucial for male reproductive success. Furthermore, our data provide insight into how a common program of gamete differentiation can be modulated to allow males to participate in reproduction in the context of a male/hermaphrodite species where the capacity for hermaphrodite self-fertilization has rendered them nonessential for progeny production.