Comparative ultrastructural investigation of the eu- and paraspermatozoa of 13Protodrilus species (Polychaeta, Annelida) and its taxonomical and phylogenetical implications

Abstract

The morphology of the slender, filiform spermatozoa of 13Protodrilus species of 22 different populations is investigated by light and transmission electron microscopy. All species have two types of spermatoza: fertile euspermatozoa, and paraspermatozoa, which are probably infertile and may comprise up to 20% of the total number of mature gametes. This is the first record of sperm dimorphism in polychaetes. The general construction pattern of the euspermatozoa is very complex. It shows a longish tapering acrosomal vesicle with an internal acrosomal rod, a rod-like conical nucleus, and a midpiece with numerous very complex supporting elements and two thin mitochondrial derivatives. Further, it has a ‘peribasal body’ surrounding the basal body of the axoneme, an anulus region with an ‘anchoring apparatus’ and an anulus cuff. Posteriorly, the tail region proper contains in some species 2 to 9 supporting rods. In several species the euspermatozoon shows very distinct and species-specific alternations of this ‘general pattern’ relating to e.g. size of sperm elements, structure of acrosome and nucleus, presence or absence of axial rod, and number, shape and size of supporting elements in midpiece and tail. In a number of species some sections of the euspermatozoon overlap with each other more or less strongly. The paraspermatozoon has a comparatively simple construction pattern and possesses no supporting structures in midpiece and tail region. The midpiece is very short and, in some species, entirely surrounded by its two thin and elongate mitochondrial derivatives. An axial rod is often missing or reduced; different sperm sections never overlap each other. In contrast to the euspermatozoa, the paraspermatozoa of the different species have a very similar ultrastructure. Their possible function in spermatophore transfer and histolytical opening of the female epidermis is discussed. A comparison of the different forms of euspermatozoa inProtodrilus elucidates possible plesiomorphous and apomorphous sperm traits. Very likely, the hypothetical plesiomorphous type of spermatozoa inProtodrilus has a very similar morphology to that of the paraspermatozoa, which for this reason are considered to be a sort of persisting representatives of the ancientProtodrilus sperm type. InProtodrilus, the different traits of the euspermatozoa represent excellent taxonomic characters for distinguishing species (e.g. ‘sibling species’). They can also be used well for phylogenetics within the genus, whereas the relations ofProtodrilus to other polychaete groups cannot be clarified solely on the basis of sperm characters, since in all groups the sperm structure is primarily an adaptation to a specific mode of reproduction. Generally, the value of sperm characters in phylogenetic considerations at higher taxonomic levels seems to be very limited due to the surprisingly wide range of different sperm structures within a single genus as is demonstrated in the present paper.