Adaptive Modifications of the Regulation of Sperm Motility in the Diversification of Reproductive Modes of Amphibians

Abstract

In amphibians, morphologically and physicochemically diversified egg jelly/nest is significant in the evolution of various reproductive modes, while sperm motility and signaling path to regulate it should be adaptively modified to penetrate the egg jelly/nest. Hyposmolality of freshwater and/or a cysteine knot protein called sperm motility-initiating substance (SMIS) initiates and enhances motility, allowing amphibian sperm to penetrate egg jelly/nest. By comparison of the sperm responses to SMIS and hyposmolality in some anuran and urodele species with different reproductive modes, sperm of internally fertilizing Cynops pyrrhogaster and those of arboreally fertilizing Rhacophorus arboreus initiate and enhance motility by SMIS and the combination of SMIS and hyposmolality. In externally fertilizing Buergeria japonica, sperm motility is initiated and enhanced by hyposmolality. A pharmacological study suggests that at least voltage-dependent Ca²⁺ channel and TRP channel mediate the initiation and enhancement of amphibian sperm motility with different combinations. It is suggested that in the diversification of reproductive modes from external fertilization in freshwater to arboreal fertilization and internal fertilization in amphibian evolution, TRP channel and voltage-dependent Ca²⁺ channel are critical in hyposmolality-triggered signaling. The SMIS-triggered one seems to add a specific feature to the regulation of sperm motility, which contributes to the achievement of advanced reproductive modes in amphibians.