Calcium in the flagellum controls sperm navigation. In sperm of marine invertebrates and mammals, Ca²⁺ signalling has been intensely studied, whereas for fish little is known. In sea urchin sperm, a cyclic nucleotide-gated K⁺ channel (CNGK) mediates a cGMP-induced hyperpolarization that evokes Ca²⁺ influx. Here, we identify in sperm of the freshwater fish Danio rerio a novel CNGK family member featuring non-canonical properties. It is located in the sperm head rather than the flagellum and is controlled by intracellular pH, but not cyclic nucleotides. Alkalization hyperpolarizes sperm and produces Ca²⁺ entry. Ca²⁺ induces spinning-like swimming, different from swimming of sperm from other species. The “spinning” mode probably guides sperm into the micropyle, a narrow entrance on the surface of fish eggs. A picture is emerging of sperm channel orthologues that employ different activation mechanisms and serve different functions. The channel inventories probably reflect adaptations to species-specific challenges during fertilization.

DOI:http://dx.doi.org/10.7554/eLife.07624.001