Ultrastructure of spermatozoa of the amphibia: phylogenetic and taxonomic implications

Scheltinga, David Michael (2002). Ultrastructure of spermatozoa of the amphibia: phylogenetic and taxonomic implications PhD Thesis, School of Biological Sciences, The University of Queensland.

       
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Author Scheltinga, David Michael
Thesis Title Ultrastructure of spermatozoa of the amphibia: phylogenetic and taxonomic implications
School, Centre or Institute School of Biological Sciences
Institution The University of Queensland
Publication date 2002
Thesis type PhD Thesis
Supervisor Barrie Jamieson
Total pages 320
Collection year 2002
Language eng
Subjects 060301 Animal Systematics and Taxonomy
Formatted abstract Spermatozoal morphology of 143 species of amphibians is investigated by light and transmission electron microscopy and described. Relationships between taxa are hypothesised on the basis of shared spermatozoal characters and compared to previous phylogenies based on other character sets.

Of the 28 anuran families currently recognised, description of the spermatozoa of 15 families (Bufonidae, Centrolenidae, Hylidae, Hyperoliidae, Leiopelmatidae, Leptodactylidae, Megophryidae, MicrohyUdae, Myobafrachidae, Pelobatidae, Petropedetidae, Pseudidae, Ranidae, Rhacophoridae, and Rhinodermatidae) are included in the present account.

The Anura can be defined spermatologically on a single autapomorphy, the presence of an axial fibre which is closely associated with doublet 3, being modified into juxta-axonemal and axial portions. An axial fibre being apomorphically lost in some Anura. The spermatozoa of the archaeobatrachians Ascaphidae, Bombinatoridae, Discoglossidae, and Leiopelmatidae appear the most basal, which is in agreement with most phylogenetic analyses. In contrast, the mesobatrachians (Megophryidae, Pelobatidae, Pelodytidae, and Pipidae) do not appear to group together spermatologically and group with differing neobatrachian families. The spermatozoa of Megophryidae and Pelobatidae are similar to those of Hyperoliidae, whereas those of the Pelodytidae are similar to those of the Bufonidae, Centrolenidae, Hylidae, Leptodactylidae, and Rhinodermatidae. Thus the Neobatrachia are also heterogeneous spermatologically. The spermatozoa of the MicrohyUdae and Pseudidae are similar in stmcture, whereas those of the Myobatrachidae are distinctive but all three families appear to share many characters with the pelodytids. However, the MicrohyUdae and Pseudidae are apomorphic in the absence of an axial fibre as are the pipids and ranoids. Several phylogenetic analyses have grouped the MicrohyUdae with the Ranoidea, whereas the pseudids are grouped with the Bufonoidea suggesting that the absence of an axial fibre may be homoplasic between these two groups. The spermatozoa of the Pipidae are similar to those of the Petropedetidae, Ranidae, and Rhacophoridae.

Of the six gymnophionan families currently recognised, description of the spermatozoa of four families (Caeciliidae, Ichthyophiidae, Typhlonectidae, and Uraeotyphlidae) are included in the present account. The spermatozoa of Gymnophiona show four autapomorphies: 1) Penetration of the distal centriole by the axial fibre. 2) Presence of an acrosomal base-plate. 3) Presence of an acrosome seat (flattened apical end of nucleus). 4) Absence of juxta-axonemal fibres. Three plesiomorphic spermatozoal characters are recognised which are not seen in other Amphibia but occur in basal amniotes: 1) presence of mitochondria with a delicate array of concentric cristae; 2) presence of peripheral dense fibres associated with the triplets of the distal centriole; 3) presence of a simple annulus. The presence of an endonuclear canal containing a perforatorium is a plesiomorphic feature of caecilian spermatozoa that is shared with urodeles, some basal anurans, sarcopterygian fish, and some amniotes. Spermatozoal synapomorphies are identified for the Uraeotyphlidae and Ichthyophiidae, and the Caeciliidae and Typhlonectidae, suggesting that the members of each pair of families are more closely related to each other than to other gymnophionans.

Of the ten Urodela families currently recognised, description of the spermatozoon of seven families (Ambystomatidae, Amphiumidae, Dicamptodontidae, Hynobiidae, Plethodontidae (Desmognathinae and Plethodontinae), Rhyacotritonidae, and Salamandridae) are included in the present account. Some additional data on the spermatozoa of the Sirenidae are also presented.

Spermatologically the Sirenidae (suborder Sirenoidea) do not appear to be within the Urodela (suborders Cryptobranchoidea and Salamandroidea). Spermatozoa show two autapomorphic characters for the Urodela: 1) the presence of the nuclear ridge (unknown in cryptobranchids) and; 2) the unilateral modification of the anterior acrosome vesicle. Spermatozoa of the Cryptobranchoidea (Hynobiidae and Cryptobranchidae) appear to possess the most plesiomorphic characters and are linked by only one apomorphy, the loss of mitochondria from the mature spermatozoon, and one character of unknown polarity, the trifoliate acrosome. Spermatologically, the Cryptobranchoidea appears monophyletic and to be the sister taxon to the clade of intemally fertilising salamanders, the Salamandroidea. The spermatozoa of Salamandroidea (ambystomatids, amphiumids, dicamptodontids, plethodontids, proteids, rhyacotritonids, and salamandrids) possess several apomorphic characters for the suborder, including: elongation of the connecting piece; an apically or subapically modified (hooked, knobbed, or barbed) acrosome vesicle; trifoliate axial fibre within the principal piece; elongate annulus; elongate midpiece; and the gentle/gradual merging of the axial fibre/principal piece into the endpiece. The amphiumids appear to form the sister taxon to the rest of the Salamandroidea. The ambystomatids, dicamptodontids, proteids, rhyacotritonids, and salamandrids have two synapomorphic spermatozoal characters: I) presence of a nuclear collar surrounding the connecting piece and; 2) the nuclear ridge in the form of a unilateral ridge. The ambystomatids and dicamptodontids share three synapomorphic characters: 1) centrioles lying at an oblique angle to each other (proximal cenfriole lying parallel to the long axis of the spermatozoon); 2) the juxta-axonemal fibre appearing triangular, or nearly so, in transverse section and; 3) presence of a short tail membrane. However, a tail membrane, though differing slightly, also occurs in amphiumid spermatozoa. Plethodontid spermatozoa show several apomorphic characters, as do its two subfamilies. Plethodontid and amphiumid spermatozoa, plesiomorphically(?), share the extension of the nuclear ridge beyond the nucleus and along the connecting piece (requires confirmation in amphiumids) and a slightly concave nuclear base (in some Plethodontinae).

The spermatozoa of the Lissamphibia possess the autapomorphic character of the presence of a unilateral undulating membrane which connects the axial fibre to the vicinity of doublet 3 of the axoneme. Although the conical perforatorium of urodeles and anurans does not appear to be homologous on present data, if it were proved to be homologous then it would be an apomorphy linking the Anura and Urodela. Gymnophionan spermatozoa possess no apomorphic characters that suggest a closer relationship to either the Urodela or Anura.
Keyword Spermatozoa
Additional Notes Variant title: Spermatozoa of the amphibia

 
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