During meiosis, homologous chromosomes pair, synapse and undergo crossover recombination initiated by SPO-11-dependent DNA double strand breaks (DSBs). Homologous recombination (HR) is the preferred pathway to repair DSBs during meiotic prophase, and RAD-51 assembly and disassembly serves as a readout of ongoing repair by HR. In mammalian cells, the breast cancer 1 gene (BRCA1) is required for HR in somatic cells. In mouse spermatogenesis, BRCA1 is required for successful meiotic sex chromosome inactivation (MSCI), the failure of which leads to pachytene arrest and apoptosis of germ cells. Consequently, the role of BRCA1 in meiotic recombination is unclear. The C. elegans ortholog,
brc-1, has been reported to promote HR at a subset of DSBs in meiotic cells as visualized by altered pattern of RAD-51 foci in
brc-1 hermaphrodite germline nuclei (Adamo et al., 2008). We discovered that in C. elegans males, BRC-1/BRD-1 does not participate in MSCI, which allowed us to investigate the role of BRC-1/BRD-1 in meiotic recombination during spermatogenesis. In contrast to what was observed in hermaphrodites,
brc-1 and
brd-1 mutant males had a reduction in the number of RAD-51 foci, which returned to wild-type levels when non-homologous end joining (NHEJ) was inhibited. Inactivation of NHEJ in
brc-1 or
brd-1 mutant hermaphrodites, in contrast, led to a further increase in the number of RAD-51 foci, suggesting that BRC-1/BRD-1 regulates DSB repair choice differentially in the sexes. We also discovered that BRC-1/ BRD-1 is important for stabilizing the RAD-51 filament when the formation of a crossover-intermediate was disrupted in oogenesis but not spermatogenesis. In pairing center protein (
zim-1,
zim-2,
him-8),
syp-1 or
rad-54 mutants, RAD-51 was precociously removed and reappeared in late pachytene in
brc-1 mutant hermaphrodites. In contrast, in male
brc-1 germ cells RAD-51 foci persisted in the mutants. Furthermore, GFP::COSA-1, which marks designated crossover sites, was also altered differentially in hermaphrodite versus male germ cells. Removal of
brc-1 decreased the average GFP::COSA-1 foci in hermaphrodites, while in
brc-1 males the average number of GFP::COSA-1 increased under conditions where chromosomes can not form a crossover (e.g.,
zim-1 mutant). Our data suggest that there are distinctive mechanisms in which BRC-1/BRD-1 participates in homologous recombination in the two different sexes of C. elegans.