Episodic rolling and transient attachments create diversity in sperm swimming behavior

BACKGROUND: Frequency and asymmetry of the flagellar waveform of sperm are controlled by cAMP-mediated and Ca(2+)-dependent signaling pathways, but additional mechanisms modulate sperm swimming behavior. Here, high-speed imaging of free-swimming mouse sperm simultaneously reports flagellar waveform, orientation of sperm head, and swimming paths. RESULTS: We found many sperm roll (rotate around their long axis) at intervals closely tied to flagellar beat frequency, allowing an asymmetrical flagellar beat to form linear averaged swimming trajectories. For non-rolling sperm, flagellar waveform asymmetry dictated circular path trajectories. Sparse rolling produced abrupt changes in swimming trajectories that occurred spontaneously, unaffected by blockade or engagement of cAMP- or Ca(2+)-mediated flagellar responses. Still other sperm loosely attached (tethered) to surfaces or other cells. Sperm tethered to each other in duos or trios could have narrowed swimming paths, allowing enhanced progression. CONCLUSIONS: We propose that transient episodes of rolling and reversible attachments are organizing principles that determine diverse swimming behaviors, which may have roles in selection of the fertilizing sperm. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12915-014-0067-3) contains supplementary material, which is available to authorized users.