Ultrastructure of phaosomous photoreceptors in Stylaria lacustris (Naididae, `Oligochaeta', Clitellata) and their importance for the position of the Clitellata in the phylogenetic system of the Annelida

Abstract

Many species of Naididae possess a pair of pigmented eyes. Within Clitellata, eyes are generally present in Hirudinea, whereas Naididae are the only oligochaete taxon having these sense organs. The eyes of Naididae are epidermal structures and consist of a multicellular pigment cup in which a single row of five to six photoreceptor cells is embedded. The sensory cells are typical phaosomes: the photoreceptive structures (microvilli) project into a cavity formed by the sensory cell itself. In Stylaria lacustris this cavity opens to the exterior, clearly documenting that it represents an invagination of the apical cell membrane. The density of sensory microvilli is comparatively low and a central vitreous body is lacking. Similar phaosomous photoreceptors, not associated with either pigmented or unpigmented supporting cells, occur in the epidermis of the anterior end. These photoreceptors correspond to those found in other Clitellata, confirming that phaosomes are the only known type of photoreceptor cell occurring in this taxon. As a result of their simple structure they have been regarded as plesiomorphic for Annelida. However, an out-group comparison with eyes and photoreceptors occurring in polychaetes and other spiralians reveals that they, in fact, are a rather specialized type of photoreceptor. Despite the simple structure, they most likely represent an autapomorphy of Clitellata. It follows that in all probability, these phaosomes are a secondarily evolved type of photoreceptor, which arose within the oligochaete clade after the primary photoreceptors present in the out-groups had been lost. This loss might have occurred during evolution of a burrowing life style within the sediment and subsequent invasion of the terrestrial environment.