Comparative ultrastructural study of spermiogenesis in digeneans and monogeneans (Platyhelminthes). Relationships between morphology of spermatozoon, biology of fertilization and phylogeny [Étude ultrastructurale comparée de la spermiogenèse des Digènes et des Monogènes (Plathelminthes). Relations entre la morphologie du spermatozoïde, la biologie de la fécondation et la phylogénie] Dr. Sc. Thesis (1985) in French, with English abstract.
[Comparative ultrastructural study of spermiogenesis in digeneans and monogeneans (Platyhelminthes). Relationships between morphology of spermatozoon, biology of fertilization and phylogeny]
Dr. Sc. Thesis (1985) in French, with English abstract.
Chapter I. Material and methods
A list of the parasites studied (and their hosts) is given: about 40 species of Monogeneans, 10 Digeneans, some Cestodes and Temnocephala.
The methods used for parasite collection, light and transmission electron microscopy are described.
Chapter II. Descriptive study of spermiogenesis and spermatozoa
1. Gross structure of the testis
The testis contains supporting cells, and germinal cells which are grouped in a common cytoplasmic mass at the spermatid stage. The evolution of this mass is described.
A "classical" spermiogenesis is described in the Digeneans: 7 stages are defined. This spermiogenesis is also found in the Polyopisthocotylean Monogeneans. The various processes of spermiogenesis of other species may be compared with the "classical" spermiogenesis; they show modifications which are generally simplifications. A general Table showing the possible homologies between the stages of spermiogenesis found in the different species is proposed. In the case of the schistosome, after analysing the spermiogenesis, we suggest considering its aberrant spermatozoon as "neotenic", because it resembles a precociously matured spermatid. The fate and possible role of two organelles of the spermatid which are absent in the spermatozoon, the centre body and the striated roots, are considered. The process of separation of the nature spermatozoon is discussed. The aberrant case of the Polyopisthocotylean Monogenean Diplozoon is underlined, because it is the single case which cannot be compared with the "classical" spermiogenesis. The spermiogenesis of Monogeneans and Digeneans is compared with that of the other Platyhelminthes: it is close to that of Cestodes, but it shows fundamental differences from that of Turbellarians, in spite of a superficial resemblance of the spermatozoa.
3. Structure of the mature spermatozoa
Spermatozoa of Digeneans and Monogeneans are generally filiform. A Table compares the length of spermatozoa in various species. A "classical" pattern of spermatozoon (or type 1) is described: it comes from the "classical" spermiogenesis. The "classical" spermatozoon contains two axonemes incorporated in the sperm body and cortical longitudinal microtubules. This "classical" pattern is almost universal within Digeneans and Polyopisthocotylean Monogeneans, but is unknown in the Monopisthocotylean Monogeneans. It also exists, in a slightly modified form, in some Cestodes. Spermatozoa of the Monopisthocotylean Monogeneans are classified by means of two simple ultrastructural characteristics, the number of axonemes (1 or 2) and the presence of cortical microtubules, in three patterns (types 2, 3 and 4). The cases of the Digenean Schistosoma (non filiform) and of the Polyopisthocotylean Monogenean Diplozoon (aflagellate) are aberrant and set aside. Comparative diagrams are presented.
4. The organelles of the spermatozoon and their evolution during spermiogenesis
Centrioles of mature spermatozoa are atypical and are generally made up of 9 singlets, instead of the typical structure of triplets found in the spermatids. The axonemes show a special pattern, called 9+ ''1 "; the few variations are presented. The ornamentations associated with the membrane are described. The position of the nucleus is discussed: it is posterior, meaning that spermatozoa of Digeneans and Monogeneans are "inverted" compared with those of other animals. Coils of spermatozoa found in some species are considered to be details added to a fundamentally filiform structure.
5. Motility of spermatozoa
Comparative Tables of spermatozoan motility and ultrastructure (axonemes and microtubules) are given. It is impossible to correlate in a precise manner ultrastructure and motility.
6. Behaviour of the spermatozoa during fertilization
The spermatozoa penetrate the oocyte with the nucleus in a posterior position; available data concern only few species, mainly with "classical" spermatozoa.
7. Partial conclusion after chapter II
Data advanced in this chapter are summarised and discussed.
Chapter III. Morphology of spermatozoa, biology of fertilization and phylogeny
Some classical cases of the literature are considered.
2. Spermatozoa and biology of fertilization
The "classical" spermatozoon (type 1 ) of the Digeneans and Polyopisthocotylean Monogeneans seems to be linked with internal fertilization, through genital ducts (Digeneans) or by hypodermic injection (at least a part of the Polyopisthocotylean Monogeneans). In the monopisthocotylean Monogeneans (with spermatozoa of types 2, 3 and 4), the literature mentions some cases of spermatophores, but it is not possible to establish a strict relationship between these sperm structures and fertilization by spermatophore. The case of the Polyopisthocotylean Monogenean Diplozoon is interesting. In this animal, the biology of fertilization is unique because the two members of the pair are fused, and the spermatozoon is the only aflagellate case known: it displays a remarkable correlation between the biology of fertilization and sperm structure. The case of the schistosomes is discussed. Attempts are made to relate the atypical structure of the spermatozoon to the peculiar characteristics of the schistosomes: gonochorism, progenesis, life in pairs. It seems that life in permanent pairs is a factor of differentiation of atypical sperm structures, in the schistosomes, Diplozoon, and some Didymozoonidae.
3. Spermatozoa and phylogeny
Relationships between phylogeny, taxonomy, biology of fertilization and sperm structure are discussed. In the Trematodes (Digeneans and Aspidogastreans), the sperm structure is very homogenous (type 1) and thus of little use for the understanding of phylogeny within this group. The few variations known (Didymozoata and Strigeata) seem to be linked mainly with the biology of fertilization rather than with phylogeny. In the Monogeneans, comparative spermatology allows us to separate Polyopisthocotyleans and Monopisthocotyleans. Polyopisthocotylean Monogeneans are very homogenous and share type 1 with the Trematodes. The single really different case, Diplozoon, seems to have no phyletic value but is correlated with the biology of fertilization. Monopisthocotylean Monogeneans show three types of spermatozoa. A phyletic scheme built only from sperm ultrastructure shows resemblances with classical phylogenies drawn from the structure of the adults, and a remarkable coincidence with modern phylogenies elaborated from the structure of larvae. The case of the Monogeneans is thus a demonstrative example of the usefulness of comparative spermatology for the understanding of phylogeny.
4. Trends in the evolution of spermatozoa in parasitic Platyhelminthes
Spermatozoa of Platyhelminthes are generally biflagellate. After a comparative study, we consider that the less evolved spermatozoon in the parasitic Platyhelminthes (Monogeneans, Digeneans and Cestodes) is the "classical" type, or type 1. This type 1 is maintained in the Digeneans and Polyopisthocotylean Monogeneans, but is modified in the Cestodes (loss of the mitochondrion, and of one axoneme in some cases), and in the Monopisthocotylean Monogeneans (loss of the microtubules am of one axoneme). The origin of type 1 may possibly be found in the Turbellaria Rhabdocoela Kalyptorhynchia. Comparative and phyletic diagrams of sperm structure in the phylum Platyhelminthes are given.