Ultrastructural analysis of spermiogenesis in Rhacophorus arboreus (Amphibia, Anura, Rhacophoridae)

Abstract

The spermatozoa of the Japanese green tree frog, Rhacophorus arboreus (Amphibia, Anura, Rhacophoridae), have a characteristic corkscrew-shaped head and a thick tail that extends perpendicular to the longitudinal axis of the head. We examined the process of spermatogenesis in Rh. arboreus, particularly spermiogenesis, using light and transmission electron microscopy. Spermiogenesis was categorized into the early, mid, and late stages based on the spermatid morphology and their location within the cyst. Early spermatids had a round nucleus and two independent flagella that elongated from a pair of parallel centrioles. The centrioles became embedded in centriolar adjunct material and attached to the nucleus. Then, the flagella were covered with a mantle-like cytoplasm that contained many microtubules. An acrosome appeared on the pointed side of the slightly elongated nucleus. Mid spermatids had an elongated rod-like head. As the nucleus elongated, the chromatin fibers became thicker and were arranged parallel to the elongation axis. An elongated acrosome was attached helically along the lateral side of the elongated nucleus. The biflagellate spermatids transformed into monoflagellate spermatids with two axonemes through a process in which the plasma membrane of each flagellum expanded. Late spermatids had a coiled or corkscrew-shaped head. An acrosome was located on the inside of the coiled cone composed of a nucleus. Parallel microtubules were connected in rows, and then became crystallized in the tail. The present report contains the first morphological description of spermatogenesis in Rhacophorus and suggests that spermiogenesis evolved to adapt to the fertilization environment.

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

“…pyrrhogaster sperm being characterized by a stiff axial rod attaching the undulating membrane to one side of the tail[29], and 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.…”

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

“…Furthermore, it has been reported in urodeles (Picheral, ; Jamieson, ; Scheltinga, ), and basal amniotes (Healy and Jamieson, ; Jamieson and Healy, ). Conversely, the subacrosomal cone is absent in some basal anuran families such as Alytidae (Furieri, ), Bombinatoridae (Furieri, ; Pugin‐Ríos, ), Pipidae (Reed and Stanley, ; Bernardini et al, ) and Scaphiopodidae ( Scaphiopus , James, ; Morrisett, ), and the studied victoranuran ranoid families ( sensu Frost et al, ), as Dicroglossidae, Mantellidae, Phrynobatrachidae, Ptychadenidae (Scheltinga, ), Ranidae (Poirier and Spink, ; Pugin‐Ríos, ; Scheltinga, ), and Rhacophoridae (Mainoya, ; Mizuhira et al, ; Muto and Kubota, ). As we pointed out in the description of character 0, both the definition and homology of the subacrosomal cone and conical perforatorium have been largely discussed (e.g., Lee and Jamieson, , Jamieson et al, ; Scheltinga et al, ; Garda et al ; Scheltinga, ).…”

“…A mitochondrial collar present at the anterior portion of the tail (character 2: 1) is shared by Batrachylidae, Bufonidae, Centrolenidae, Dendrobatidae, Hylidae, Leptodactylidae, Microhylidae, and Rhinodermatidae (Pugin‐Ríos, ; Pugin and Garrido, ; Jamieson et al, ; Lee and Jamieson, ; Meyer et al, ; Garda et al, ; Scheltinga et al, ; Aguiar‐Jr et al, 2003, 2004; Veiga‐Menoncello et al, ; Santos et al, ), with the exception of a few species. The mitochondrial collar is absent in urodeles, gymnophionans, most of the basal anuran clades, the anomocoelan families, Ptychadenidae and the victoranuran families examined, including Ranidae, and Dicroglossidae, Mantellidae, Phrynobatrachidae, and Rhacophoridae (Poirier and Spink, ; Pugin‐Ríos, ; Mainoya, ; Mizuhira et al, ; Scheltinga ; Muto and Kubota, ). Formerly, a well‐developed mitochondrial collar, but often transient, was considered a synapomorphic condition of “Bufonoidea” (myobatrachids, leptodactylids, hylids, and bufonids; Lee and Jamieson, ).…”