Sperm chemotaxis, fluid shear, and the evolution of sexual reproduction.

Chemical communication is fundamental to sexual reproduction, but how sperm search for and find an egg remains enigmatic. For red abalone (Haliotis rufescens), a large marine snail, the relationship between chemical signaling and fluid motion largely determines fertilization success. Egg-derived attractant plumes are dynamic, changing their size and shape in response to unique combinations of physical and chemical environmental features. Attractant plumes that promote sexual reproduction, however, are limited to a precise set of hydrodynamic conditions. Performance-maximizing shears are those that most closely match flows in native spawning habitats. Under conditions in which reproductive success is chronically limited by sperm availability, gametes are under selection for mechanisms that increase sperm-egg encounter. Here, chemoattraction is found to provide a cheap evolutionary alternative for enhancing egg target size without enlarging cytoplasmic and/or cell volume. Because egg signaling and sperm response may be tuned to meet specific fluid-dynamic constraints, shear could act as a critical selective pressure that drives gamete evolution and determines fitness.