A novel mechanism of sperm motility in a viscous environment: Corkscrew‐shaped spermatozoa cruise by spinning

Abstract

Fertilization of the green tree frog, Rhacophorus arboreus, occurs in the viscous environment of a foam nest, which is laid on vegetation. Their spermatozoa have a characteristic corkscrew-shaped head and a thick tail that extends perpendicularly to its longitudinal axis. However, it is unclear how these corkscrew-shaped spermatozoa move in this highly viscous environment. Here, we found that the spinning of the corkscrew-shaped head, caused by winding and unwinding of the tail, enables the spermatozoa to move through the highly viscous environment of a foam nest, like a corkscrew rotating into a cork. We suggested that dislocations observed in the matrix of satellite microtubules surrounding two axonemes, reflected the planes of sliding of the axonemes, and dyneins on doublets two and six of each axoneme were active during winding and unwinding, respectively. These results provide a novel mechanism for sperm movement that is adapted specifically to a viscous fertilization environment.

A Novel Cysteine Knot Protein for Enhancing Sperm Motility That Might Facilitate the Evolution of Internal Fertilization in Amphibians

“…The foam nest is composed of a highly viscous matrix derived from an oviductal secretion. The sperm of this species exhibit a rotary motion that is specifically adapted to the foam nest matrix[12]. R .…”

“…arboreus sperm done by a screw-shape with doubled axonemes in the tail[30]. As the sperm of both species can move forward only in a viscous matrix[12,29], their unique sperm morphologies are related to the penetration of the egg coat matrix that is optimized for fertilization and embryonic development either inside the female's body or on a tree. These characteristics suggest the possible relationship between the egg coat matrix and sperm morphology during the diversification of reproductive modes: the nature of the matrix is modified adaptively to a specific reproductive mode, whereas sperm morphology is selectively altered to allow forward motility in the modified matrix.…”

Sperm competitiveness in frogs: slow and steady wins the race

“…In vitro studies of externally fertilizing fishes have generally found positive associations between sperm swimming velocity and competitive fertilization success (Gage et al 2004;Casselman et al 2006;Liljedahl et al 2008), and selection from sperm competition does appear to have favoured rapidly swimming and short-lived sperm in these taxa (Cosson et al 2008;Fitzpatrick et al 2009). However, frog sperm are structurally and behaviourally very different from the archetypal sperm of fishes; frog sperm can remain motile for several hours (Hettyey & Roberts 2006;Sherman et al 2008a) and swim very slowly (see also Reyer et al 2003;Edwards et al 2004;Muto & Kubota 2009). In myobatrachids, sperm are propelled by an undulating membrane that is supported by a longitudinal axial fibre that stretches from the base of the head to the tip of the 'tail' (Lee & Jamieson 1992).…”

A comparative ultrastructural analysis of spermatozoa in Pleurodema (Anura, Leptodactylidae, Leiuperinae)

“…A simpler spermatozoon has been associated with aquatic fertilization environments (Jamieson et al, ; Lee and Jamieson, ; Scheltinga et al, ; Scheltinga and Jamieson, ; Garda et al, ). In Rhacophoridae, where the fertilization takes place in foam nests, neither accessory fibers nor an undulating membrane are present, but a packed core of satellite microtubules is observed surrounding the double axoneme (Mainoya, ; Mizuhira et al, ; Muto and Kubota, ). Recently, Muto and Kubota () studied two foam‐nesting Rhacophorids and suggested that the sperm motility is specifically modified for a viscous fertilization environment.…”

“…In Rhacophoridae, where the fertilization takes place in foam nests, neither accessory fibers nor an undulating membrane are present, but a packed core of satellite microtubules is observed surrounding the double axoneme (Mainoya, ; Mizuhira et al, ; Muto and Kubota, ). Recently, Muto and Kubota () studied two foam‐nesting Rhacophorids and suggested that the sperm motility is specifically modified for a viscous fertilization environment. Within Rhacophoridae, members of the genera Chiromantis , Polypedates , and Rhacophorus share common character states, a pair of axonemes surrounded by hundreds of crystallized satellite microtubules in the tail of the spermatozoa.…”