Hardly Venus’s servant—morphological adaptations of Veneriserva to an endoparasitic lifestyle and its phylogenetic position within Dorvilleidae (Annelida)

Abstract

Endoparasitic annelids living inside another annelid host are known, particularly with regard to Oenonidae, but in general are poorly studied. The dorvilleid Veneriserva pygoclava is known from southern California, and its genus name (Latin = Venus’s servant) alludes to the close association with the host aphroditid scaleworm Aphrodita longipalpa. Little is known on fundamental questions on the biology of Veneriserva pygoclava. What is its mode of reproduction? How do they feed? How do they penetrate the host? We have studied multiple parasitized hosts and V. pygoclava specimens, using an integrative approach, combining µCT, histology, and electron microscopy. 3D reconstructions from µCT data of a parasitized Aphrodita show the exact position of the parasites in their natural condition within the host’s coelomic cavity. Ultrastructural investigations of the parasites revealed interesting adaptations to their lifestyle such as the complete reduction of their gut, despite the presence of a functional jaw apparatus and a modified epidermis enabling nutrient uptake from the host’s coelomic fluid. In addition to these, we also investigated spermatogenesis and oogenesis in V. pygoclava. Sperm morphology indicates an external fertilization of eggs within the coelomic cavity of the host. Mature male and female parasites living inside the same mature host and the presence of juvenile V. pygoclava within juveniles of Aphrodita suggest an obligate form of parasitism with a very early penetration of the hosts. In addition to our detailed morphological investigation, we conducted a phylogenetic analysis showing the position of Veneriserva within Dorvilleidae and its position was recovered nested among taxa of the Iphitime. Our phylogenetic analyses also show that the taxation Ophryotrocha puerilis siberti should be given full species rank and referred to as Ophryotrocha siberti. Finally, we publish here the full mitochondrial genome of V. pygoclava and discuss its novel gene order with reference to other annelids.