Acrosome Reaction-Mediated Motility Initiation That Is Critical for the Internal Fertilization of Urodele Amphibians

Abstract

The reproductive modes of extant amphibians are highly diversifi ed in their adaptation to species-specifi c reproductive environments. In the external fertilization of most amphibians, fertilization begins from motility initiation of the sperm by the hyposmolality of freshwater at spawning, whereas in internal fertilization, the sperm initiate motility without any change in osmolality. Acrosome reaction (AR)-mediated motility initiation is an initial event of the internal fertilization of the urodele amphibian Cynops pyrrhogaster , also known as the Japanese fi re belly newt. It initiates motility of female-stored sperm on the surface of the jelly layer in the cloaca. This unique mechanism of motility initiation is based on the fi ne structure of the jelly matrix, in which AR-inducing substance (ARIS) and sperm motilityinitiating substance (SMIS) are localized in the sheet-like structure covering the outer surface and in the granules beneath it. The ARIS and the SMIS repeatedly increase the sperm intracellular Ca 2+ level and result in the sporadic initiation of motility within 4 min. The SMIS activity is also present in the jelly layer of the externally fertilizing anuran amphibian Discoglossus pictus (the Mediterranean painted frog), but a thick layer of matrix simply covers the outer surface of the jelly layer. The AR-mediated mechanism may be established in the reproductive strategies for the internal fertilization of urodeles.

Sperm Proteases that May Be Involved in the Initiation of Sperm Motility in the Newt, Cynops pyrrhogaster

“…At the internal fertilization of C. pyrrhogaster , AR-induced sperm initiate appropriate motility on the egg jelly surface and begin to penetrate into egg jelly [ 27 ]. The gelatinous nature of the jelly matrix provides a mechanical guide for the sperm to the surface of the vitelline envelope [ 28 ], whereas it excludes abnormal sperm in morphology or motility by being trapped in the matrix [ 22 ].…”

NMDA‐type glutamate receptors mediate the acrosome reaction and motility initiation in newt sperm

“…At the onset of internal fertilization in C. pyrrhogaster , sperm in the female reservoir is mechanically inseminated onto the surface of the egg‐jelly (Takayama‐Watanabe et al, ). Subsequently, the acrosome reaction is induced by the ARIS at the surface of the egg‐jelly and the acrosomal enzymes released to digest the surface matrix thereby exposing SMIS to trigger the initiation of sperm motility (Watanabe & Onitake, ; Watanabe et al, ).…”

“…Each signaling path associated with the sperm–egg interaction is adapted to the species‐specific reproductive environment, although how it is established is unknown. The reproductive modes of amphibians have been highly diversified from external fertilization in freshwater to internal fertilization (Duellman & Trueb, ), which makes them a potential research model to understand how the signaling paths in the sperm–egg interaction are modified in response to the reproductive environment (Sato et al, ; Takayama‐Watanabe et al, ; Watanabe & Onitake, ; Yokoe et al, ).…”