New data on spermiogenesis and the ultrastructure of spermatozoa of 'true' tapeworms (Eucestoda) are summarized. Since 2001, more than 50 species belonging to most orders of the Eucestoda have been studied or reinvestigated, particularly members of the Caryophyllidea, Spathebothriidea, Diphyllobothriidea, Bothriocephalidea, Trypanorhyncha, Tetraphyllidea, Proteocephalidea, and Cyclophyllidea. A new classification of spermatozoa of eucestodes into seven basic types is proposed and a key to their identification is given. For the first time, a phylogenetic tree inferred from spermatological characters is provided. New information obtained in the last decade has made it possible to fill numerous gaps in the character data matrix, enabling us to carry out a more reliable analysis of the evolution of ultrastructural characters of sperm and spermiogenesis in eucestodes. The tree is broadly congruent with those based on morphological and molecular data, indicating that convergent evolution of sperm characters in cestodes may not be as common as in other invertebrate taxa. The main gaps in the current knowledge of spermatological characters are mapped and topics for future research are outlined, with special emphasis on those characters that might provide additional information about the evolution of tapeworms and their spermatozoa. Future studies should be focused on representatives of those major groups (families and orders) in which molecular data indicate paraphyly or polyphyly (e.g. 'Tetraphyllidea' and Trypanorhyncha) and on those that have a key phylogenetic position among eucestodes (e.g. Diphyllidea, 'Tetraphyllidea', Lecanicephalidea, Nippotaeniidea).
The present paper describes the characteristic ultrastructural features of spermiogenesis and the spermatozoon of Monorchis parvus (Trematoda, Digenea, Monorchiidae). This spermiogenesis is characterized by a flagellar rotation of about 120 degrees and the formation of a novel ultrastructural element: a centriolar extension. It nevertheless follows the general pattern of digeneans. It begins with the formation of a differentiation zone, comprising striated rootlets associated with two centrioles and an intercentriolar body. The mature spermatozoon presents features allowing the distinction between M. parvus and other digenetic trematodes. It possesses an original anterior extremity. The two central elements of the axonemes appear prior to the peripheral doublets. The external ornamentations of the cell membrane are formed parallel to the central elements. Another peculiarity of the male gamete is the presence of two mitochondria. M. parvus, therefore, differs distinctly from other digenetic trematodes.
This paper constitutes the first ultrastructural study of spermiogenesis and the spermatozoon of a Digenea belonging to the family Zoogonidae, Diphterostomum brusinae. Spermiogenesis follows the general pattern found in the digeneans. It begins with the formation of a differentiation zone in the spermatid. The two centrioles give rise to flagella. These two flagella undergo a rotation of 90 degrees and fuse with the median cytoplasmic process. The proximo-distal fusion occurs at the level of attachment zones. The mature spermatozoon of D. brusinae presents all the features found in the digeneans gametes: two axonemes, mitochondrion, nucleus and two bundles of parallel cortical microtubules. Nevertheless, several characteristics distinguish the spermatozoon of D. brusinae from other digeneans, in particular the external ornamentations of the plasma membrane and the anterior and posterior extremities. The description of the ultrastructural features of reproduction in this species would contribute to the understanding of the phylogenetic relationships in the Zoogonidae family.
Spermiogenesis and ultrastructure of the spermatozoon of the pseudophyllidean cestode Triaenophorus nodulosus (Pallas, 1781), a parasite of pike Esox lucius, has been studied by transmission electron microscopy. Spermiogenesis involves firstly the formation of a zone of differentiation with two centrioles associated with striated roots, and an intercentriolar body between them, subsequent growth of the two flagella of unequal length, and a formation of a median cytoplasmic process exhibiting patches of dense material. The nucleus penetrates into spermatid body after flagellar rotation and proximo-distal fusion has started. The mature spermatozoon of T. nodulosus is filiform and contains two axonemes of 9+"1" pattern of the Trepaxonemata, nucleus, cortical microtubules parallel to the spermatozoon axis, and electron-dense granules. The anterior extremity of the gamete contains a single centriole surrounded by numerous electron-dense tubular structures exhibiting spiral arrangement and giving rise to lateral projections, which correspond to the crested body. When the crested body disappears, the spiral pattern of electron-dense tubular structures is changed into a ring, persisting until the centriole of the second axonemes appears. This structure of the crested body of T. nodulosus is unique among the Eucestoda.
Spermiogenesis and the ultrastructural features of the spermatozoon of Diphyllobothrium latum (Cestoda, Pseudophyllidea) are described using transmission electron microscopy. Spermiogenesis is characterized by the development of two flagella of unequal length that grow asynchronously. When the first growing flagellum starts to rotate, the second one develops. Flagellar rotation is thus asymmetric and asynchronic. It is followed by proximodistal fusion with the median cytoplasmic process. Electron-dense material is present in the apical region of the zone of differentiation in the early stages of spermiogenesis. The intercentriolar body consists of seven plates: three are electron-dense. Four attachment zones occur in the median cytoplasmic process. An atypical arrangement of striated roots was occasionally observed. The mature spermatozoon possesses two axonemes of 9 + "1" trepaxonematan pattern, nucleus, cortical microtubules, electron-dense granules, and lacks mitochondria. The ultrastructure of the anterior extremity of the spermatozoon in D. latum clearly differs from that in the bothriocephalid pseudophyllideans, mainly in the absence of a crested body and a ring of electron-dense tubular structures. The spermatological data support the assumption that the order Pseudophyllidea is formed by two unrelated clades, "Bothriocephalidea" and "Diphyllobothriidea."
Using transmission electron microscopy, spermiogenesis and the spermatozoon ultrastructural organization are described in Ligula intestinalis (Linnaeus, 1758) (Diphyllobothriidea), a parasite of the great crested grebe Podiceps cristatus (Linnaeus, 1758). Spermiogenesis starts with the differentiation zone of 2 striated rootlets, 2 centrioles giving rise to 2 flagella, and an intercentriolar body. The latter is composed of 5 electron-dense layers separating 4 electron-lucent layers. In the early stages of spermiogenesis, an electron-dense material is present in the apical region of the differentiation zone. Later, the flagella undergo a rotation and fuse with the cytoplasmic extension in a proximo-distal process. The spermatozoon contains 2 axonemes with a 9 + "1" trepaxonematan pattern, the nucleus, the cortical microtubules, and an electron-dense zone. The spermatozoon anterior extremity in L. intestinalis is characterized by the absence of crested bodies and a ring of electron-dense cortical microtubules. Some characters of spermiogenesis and spermatozoon in L. intestinalis confirm the recent splitting of "Pseudophyllidea" into 2 new orders, i.e., Bothriocephalidea and Diphyllobothriidea. The process of spermiogenesis is similar in both orders for the "type I" of spermiogenesis and the presence of electron-dense material. However, the intercentriolar body is clearly more developed in the Diphyllobothriidea than in the Bothriocephalidea. Moreover, these 2 orders seem to differ in the presence or absence of a ring of electron-dense cortical microtubules in the anterior extremity of the spermatozoon.
The spatial distribution of parasite communities from teleost fishes (Diplodus vulgaris, Mullus surmuletus, Pagellus erythrinus, Phycis phycis, Scorpaena scrofa and Symphodus tinca) was studied in the Bonifacio Strait Marine Reserve (Corsica Island) with different protection levels. Canonical correspondence analysis was used to study spatial patterns and to quantify the importance of site influence on parasite communities. To supplement these results, we used the indicator species analysis (Indval) to identify parasite species as bioindicators of a given ecosystem. Moreover, fish spatial distribution in the marine reserve was evaluated in order to link parasite species occurrence and fish abundance. Several parasite species were associated with a specific site, and some of them were considered as site bioindicators, especially in the western part of the protected area (Bruzzi and Moines Islands). However, the relative abundance of fish followed a different spatial pattern. Stronger fish abundance was observed in the eastern part of the reserve (Lavezzi Islands). The parasite species were correlated to sites inside as well outside the reserve. The parasite distribution seemed not to be influenced by the protection status of the site. Furthermore, in our study, most of the parasite species were not linked to a site. The most important factor influencing their distribution was host specificity. This suggested that the parasite life traits history remained a fundamental determinant in the community composition.
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