The Biology and Evolution of Trematodes

Publisher Summary This chapter discusses ultrastructure of the tegument of Schistosoma mansoni at all stages of the life cycle. The chapter has four main sections dealing respectively with the cercaria, the schistosomulum, the adult trematode, and miracidium and sporocyst. The cercaria section concerns the development of the tegument, the cercarial surface coat, and associated structures of the tegument in developed cercariae. A syncytial tegument connected to subtegmental cells occurs in all adult digenetic trematodes that have been examined and this unusual structure involves unusual cytoplasmic inclusions that are also related to the host-parasite interface. Specialized regions of tegument occur in the oesophagus and the uterus that are regarded as tegumental structures but differ in structure. The oesophagus is primarily concerned with digestion and the function of the intestinal caecum is absorption and egestion. Destruction of the tegument is specially considered in respect of the effects of hypo- and hypertonic media and drugs and host immunity. Finally, the epithelium and associated structures of the miracidium are considered and the contrasting tegument of the daughter sporocyst, which has the syncytial tegument and nucleated subtegumental cells of the typical digenetic trematode. All these and other matters are considered in such intricate detail as is necessary at this time, when ultrastructural detail can improve the understanding of the host-parasite relationship in established schistosomiasis.

Ultrastructure of the Tegument of Schistosoma

Since the work of Dujardin (1845), attempts have been made to decipher acceptable divisions of the trematode groups at higher taxonomic levels, and yet there is still no generally accepted classification of the higher taxa of the Trematoda as there are for other groups of parasitic worms, such as the Monogenea, Cestoda, Nematoda and Acanthocephala. Why is it that workers with a wide knowledge of trematode systematics, such as Dollfus, Stunkard, Manter and especially Yamaguti, have felt unable or unwilling to comment in detail upon the phylogenetic relationships within the group at higher taxonomic levels? One of the main reasons for this state of affairs lies in the fact that, generally speaking, the group is not easily split into major subgroups by obvious, non-homoplasious morphological characters. Early attempts at division, based upon sucker arrangements, i.e. monostome, distome, amphistome and gasterostome, are not satisfactory, as distomes form the vast majority of the Digenea and both monostomes and amphistomes are certainly polyphyletic. In addition, the picture within the Digenea is complicated by the group's complex life-history patterns. Whereas early classifications all tended to be based upon adult (marital) morphology, life-history patterns are given great weight by workers such as Pearson (1972) and Bozhkov (1982). The cercarial morphology is considered the dominant feature in the classification of the group presented by La Rue (1957) and is emphasized in the phylogenetic relationships between the subgroups recognized by Cable (1974). Odening (1961), following an earlier suggestion of Lebour (1912), presented a classification, the major divisions of which were based upon the daughter-parthenita (i.e. the redia or daughter-sporocyst), a stance which he later found untenable (Odening, 1974). Consequently, the wealth of conflicting data from these and other sources has deterred the presentation both of classifications and speculations on evolutionary relationships. The classification of Odening (1974) and the recent cladistic analysis of Brooks, O'Grady & Glen (1985b) utilized data from all of the life-history stages. As the classification of Brooks et al. (1985b) is the most recent, and readily available in English, it must be a serious contender in terms of general acceptance. If it is accepted, then one would hope that this will be on its merits rather than because of its availability or the lack of viable alternatives; but, as discussed below, it is easy to find fault with this classification when it and its premises are examined in detail.

Questions in digenean systematics and evolution.

A census of macroparasites in an intertidal bivalve community, Arcachon Bay, France

Publisher Summary A comparison of helminth life-cycles reveals a number of singular features in the digenean pattern. Thus, in addition to the most singular feature, alternation of generations, there is the ubiquity of the cercaria, a stage designed for escape from the molluscan first host and for swimming, two patterns of behavior that are not called for in many life-cycles. To explain the ubiquity of the cercaria, it is postulated that the present molluscan first intermediate host was the original host of the proto-digenean and that escape of the cercaria from this host is primitive. And to explain the occurrence in many life-cycles of a free-swimming miracidium that penetrates the integument of the molluscan host, it is postulated that in an earlier stage the proto-digenean was an ectoparasite of the mollusc. Assuming that the proto-digenean was a visceral parasite of a mollusc and that it escaped from its host as an adult, presumably tailed, to lay its eggs, then the known life-cycles of contemporary digeneans may be interpreted as suggesting the following order in the acquisition of hosts: (i) vertebrate definitive (two-host life-cycle) and (ii) invertebrate second intermediate (three-host life-cycle). With regard to the succession of generations, it is postulated that the present adult was the original adult, that the mother sporocyst generation was the first of the new generations, that the redia was the second, and that daughter sporocysts have been derived from rediae several times.

A phylogeny of life-cycle patterns of the Digenea.

The germ-cell cycle and method of reproduction in the daughter sporocysts of the bucephalid Cercaria bucephalopsis haimeana (Lacaze-Duthiers, 1854) and the gymnophallid Cercaria dichotoma Lebour, 1911 (non Muller) from the edible cockle, Cardium edule L., have been investigated by the examination of stained sections. A review is given of the principal interpretative theories which attempt to explain the nature of the reproduction and the homology of the germinal sacs of the Digenea. It is suggested that the life-cycle includes a cyclic alternation of homologous generations. Of these, the miracidium/mother-sporocyst and the daughter germinal-sac generations usually reproduce by apomictic parthenogenesis but polyembryony may also occur secondarily in some species.We are very grateful to Dr Gwendolen Rees and Professor E. W. Knight-Jones for considerable help with the manuscript.

Reproduction in the daughter sporocyst of Cercaria bucephalopsis haimeana (Lacaze-Duthiers, 1854) (Bucephalidae) and Cercaria dichotoma Lebour, 1911 (non Müller) (Gymnophallidae)

B. L. James

Papers

Reproduction in the daughter sporocyst of Cercaria bucephalopsis haimeana (Lacaze-Duthiers, 1854) (Bucephalidae) and Cercaria dichotoma Lebour, 1911 (non Müller) (Gymnophallidae)