Sex and flow: the consequences of fluid shear for sperm-egg interactions

Fertilization is a complex interaction among biological traits of gametes and physical properties of the fluid environment. At the scale of fertilization (0.01-1 mm), sperm encounter eggs while being transported within a laminar (or viscous) shear flow. Varying laminar-shear in a Taylor-Couette flow tank, our experiments simulated important aspects of small-scale turbulence within the natural habitats of red abalone (Haliotis rufescens), a large marine mollusk and external fertilizer. Behavioral interactions between individual cells, sperm-egg encounter rates, and fertilization success were quantified, simultaneously, using a custom-built infrared laser and computer-assisted video imaging system. Relative to still water, sperm swam faster and moved towards an egg surface, but only in comparatively slow flows. Encounter rate, swim speed and orientation, and fertilization success each peaked at the lowest shear tested (0.1 s(-1)), and then decayed as shear increased beyond 1.0 s(-1). The decay did not result, however, from damage to either sperm or eggs. Analytical and numerical models were used to estimate the propulsive force generated by sperm swimming (F-swim) and the shear force produced by fluid motion within the vicinity of a rotating egg (F-shear). To first order, male gametes were modeled as prolate spheroids. The ratio F-swim/F-shear was useful in explaining sperm-egg interactions. At low shears where F-swim/F-shear> 1, sperm swam towards eggs, encounter rates were pronounced, and fertilization success was very high; behavior overpowered fluid motion. In contrast, sperm swimming, encounter rate and fertilization success all decayed rapidly when F-swim/F-shear< 1; fluid motion dominated behavior. The shears maximizing fertilization success in the lab typically characterized natural flow microenvironments of spawning red abalone. Gamete behavior thus emerges as a critical determinant of sexual reproduction in the turbulent sea.