A comparison of spermiogenesis and spermatozoal ultrastructure in Megascolecid and Lumbricid earthworms (Oligochaeta : Annelida)

Abstract

Spermiogenesis of six species of megascolecid earthworms has been investigated by electron microscopy. Numerous spermatids are joined to a central anucleate mass, forming a morula. Connection is made by a filament-clothed bridge, the zonula collaris. At least nine mitochondria are observed in a young spermatid but in all cases only six persist, with their juxtaposed surfaces radiating from a central axis, in the middle piece. A stack of golgi cisternae is present distally and is associated with the immature acrosome, which is subsequently transported proximally and interposed between nucleus and zonula collaris. Microtubules of the manchette ensheath the acrosome nucleus and incipient middle piece and, subsequently, all cytoplasm peripheral to the manchette with the exception of the plasma membrane is eliminated. Cytomorphogenetic changes, including great elongation and condensation of the nucleus, result in a free filamentous spermatozoon with a tapering tubular acrosome, an extremely elongate nucleus (total length 10 ¼m, cf. 20-30 ¼m in Lumbricus) a small but elongate middle piece (0.5 - 1.4 ¼m long) and long flagellum. Close agreement thus exists with spermiogenesis in the Lumbricidae, and the acrosome, which is among the most complex in the animal kingdom, shows general homology with that of Lumbricus. Significant differences from Lumbricus include the domed proximal end of the nucleus, the less discrete basal compartment, the conspicuous limen and greater separation of the outer wall of the acrosomal vesicle from the acrosome wall. A centriole with nine satellites peripheral to nine microtubules is demonstrable. A tetragon configuration in which two central fibres are added to the usual nine doublet+two central singlet microtubules is demonstrated in the proximal flagellum after a short region with a single central filament, but further distally the two fibres cease, giving the normal 9+2. Terminally the doublets are replaced by singlets and the number of microtubules is reduced. Glycogen granules are conspicuous, peripheral to the microtubules through much of the proximal axoneme as in lumbricids. A species of Cryptodrilus shows an asymmetrical 3+2 arrangement of satellites in a peripheral circlet, which exemplifies the taxonomic value of spermatozoal ultrastructure. It is confirmed that oligochaete spermatozoa are fundamentally different from those of polychaetes and archiannelids.