Decision letter: COMP-1 promotes competitive advantage of nematode sperm

Abstract

The ornate feathers of a peacock and the antlers of a stag are both traits that have evolved because they help a male to outcompete his rivals and mate with more females. Similarly, in species where each female mates with multiple males, a male can improve his reproductive success if his sperm outcompetes the other males' sperm and fertilizes the female's eggs. One way that males try to gain a competitive edge is by producing large quantities of sperm. However, it is also possible that males could compete by generating higher-quality sperm, for example, cells that are better at migrating through the reproductive tract. A microscopic worm called Caenorhabditis elegans is often used to investigate sperm competition. Each worm is either a hermaphrodite or a male; and hermaphrodites store their sperm within a storage structure and use it later to fertilize their own eggs. However, if a hermaphrodite mates with a male, the male's sperm displaces the hermaphrodite's stored sperm and fertilizes the eggs instead. The male's sperm cells were thought to be more competitive because they are larger and faster than the hermaphrodite's sperm, but recent findings suggest a more complex scenario. Hansen et al. identified a genetic mutation that causes male C. elegans sperm cells to lose their competitive advantage. Male worms with a mutation in a gene called comp-1 produce sperm cells that are normal in size, but that cannot outcompete sperm from a non-mutant hermaphrodite. Although sperm cells from a comp-1 mutant male can migrate through the reproductive tract and fertilize eggs when other sperm are not present, in competitive situations the mutant sperm cells have difficulties migrating and are often absent from the hermaphrodite's sperm storage structure. Thus, they no longer come into contact with the eggs that they seek to fertilize. Sperm cells from hermaphrodite comp-1 mutants have similar defects; but when a comp-1 mutant male mates with a comp-1 mutant hermaphrodite, the mutant male sperm regains its fertilization advantage. The identification of the comp-1 gene provides a preview into a complex network of environmental cues and genetically encoded traits that influence which sperm cells are most likely to fertilize an egg cell, and thus live on in the next generation.