Ultrastructure of cerebral eyes in Oweniidae and Chaetopteridae (Annelida) – implications for the evolution of eyes in Annelida

Abstract

Background: Recent phylogenomic studies have revealed a robust, new hypothesis of annelid phylogeny. Most surprisingly, a few early branching lineages formed a basal grade, whereas the majority of taxa were categorized as monophyletic Pleistoannelida. Members of these basal groups show a comparatively simple organization lacking certain characters regarded to be annelid specific. Thus, the evolution of organ systems and the characteristics probably present in the last common annelid ancestor require reevaluation. With respect to light-sensitive organs, a pair of simple larval eyes is regarded as being present in their last common ancestor. However, the evolutionary origin and structure of adult eyes remain obscure. Typically, adult eyes are multicellular pigment cups or pinhole eyes with or without a lens comprising rhabdomeric photoreceptor cells (PRCs) and pigmented supportive cells (PSCs) in converse design. However, in the most basal lineages, eyes are only present in a few taxa, and thus far, their ultrastructure is unknown. Results: Ultrastructural investigations of members of Oweniidae and Chaetopteridae reveal a corresponding design of adult cerebral eyes and PRCs. The eyes in species of these groups are simple pigment spot eyes, either forming a flat patch or embedded in a tube-like invagination. They are part of the epidermis and comprise two cell types, PSCs and rhabdomeric PRCs. Both cell types bear microvilli and one more or less reduced cilium. However, the PRCs showed only a moderate increase in the apical membrane surface in the form of irregularly arranged microvilli intermingling with those of the PSCs; a densely arranged brush border of rhabdomeric microvilli was absent. Additionally, both cell types show certain characteristics elsewhere observable in typical epidermal supportive cells. Conclusions: These findings shed new light on the evolutionary history of adult eyes in Annelida. Most likely, the adult eye of the annelid stem species was a pair of simple pigment spot eyes with only slightly specialized PSCs and PRCs being an integrative part of the epidermis. As is the case for the nuchal organs, typical pigment cup adult eyes presumably evolved later in the annelid phylogeny, namely, in the stem lineages of Amphinomida and Pleistoannelida.