Ultrastructure of pigmented adult eyes in errant polychaetes (Annelida): implications for annelid evolution

Abstract

The evolution of photoreceptor cells and eyes in Metazoa is far from being resolved, although recent developmental and structural studies have provided strong evidence for a common origin of photoreceptor cells and existence of sister cell types already in early metazoans. These sister cell types are ciliary and rhabdomeric photoreceptor cells, depending on which part of each cell is involved in photoreception proper. However, a crucial point in eye evolution is how the enormous structural diversity of photoreceptor cells and visual systems developed, given the general molecular conservation of the photoreceptor cells. One example of this diversity can be observed in Annelida. Within the polychaetes the errant forms, taxon Aciculata, constitute the only group possessing true multicellular eyes in the adult stage. Thus far these organs have been investigated only in taxa of Phyllodocida, a subgroup of Aciculata. Data on Eunicida and Amphinomida as well as certain phyllodocidan taxa had been lacking. The ultrastructure of these adult eyes was investigated in various species of errant polychaetes, belonging to Amphinomidae, Eunicidae and Hesionidae, to elucidate whether they provide any phylogenetic clues regarding either the evolution of visual systems in Annelida or lophotrochozoan phylogeny in general. These eyes are composed of numerous supportive pigment cells and rhabdomeric photoreceptor cells and sometimes additional cell types. As a rule the pigment and rhabdomeric cell types form a continuous epithelium in which the two types intermingle. Presence of granules with shading pigment in sensory cells is a common feature but is apparently restricted to a taxon comprising Phyllodocida and Eunicida s. str. Very likely a lens-like structure does not belong to the ground pattern of annelid eyes, despite its presence in Phyllodocida. These lens-like structures are formed by secretions or cellular processes of the pigment cells. In many species the eye cup communicates with the exterior via a small cuticularized canal. This canal is interpreted as a rudiment due to the mode of formation in the epidermis. With respect to current phylogenetic hypotheses, these multicellular eyes have either been developed in the stem species of a taxon Aciculata nested within the polychaetes or have been evolved in the stem lineage of Annelida. Similarities to gastropod eyes are interpreted as convergent and not as indication of common origin. Except for the photoreceptor cells proper, the structure of the adult eyes in polychaetes most likely does not help to resolve lophotrochozoan phylogeny.

The ‘division of labour’ model of eye evolution

“…For example, pigment vesicles have been found in cephalopod (Yamamoto et al 1965;Budelmann et al 1997) and gastropod eyes (Blumer 1999;Zhukov et al 2006) and appear to be a common feature of annelids with multicellular adult eyes, as observed in the Platynereis adult eye PRCs (Rhode 1992); at least in Phyllodocida and Eunicida, this very likely belongs to the ground pattern of eyes, and in these taxa, the absence of pigment vesicles may be interpreted as a secondary character state (Suschenko & Purschke 2009). In line with a general affinity of PRC and SPC, the retina of the Patella eye is exclusively composed of pigmented PRCs ( figure 4b).…”

“…Polygordius sp. (Brandenburger & Eakin 1981) as well as in multicellular adult eyes Suschenko & Purschke 2009). However, there are a few known examples of rhabdomeric PRCs in annelids possessing more than one cilium (e.g.…”

Systematics, evolution and phylogeny of Annelida – a morphological perspective

“…bicellular only, comprising one photoreceptor and one pigment cell. These polychaetes often have fewer segments than errant polychaetes and the body may be divided into different regions (Hartmann-Schröder, 1971;Fauchald, 1977;Suschenko and Purschke, 2009). With respect to the characters mentioned above Clitellata show simple chaetae and lack parapodia as well as any appendage on the prostomium, peristomium and pygidium ( fig.…”

Morphology and deep metazoan phylogeny

“…We start this Special Volume with a review on the need for a standardized language for morphological descriptions (Vogt 2009), because besides the search for new characters it is equally important to develop appropriate methods to deal with such data. Contributions of Harzsch et al (2009), Rothe andSchmidtRhaesa (2009), Heuer andLoesel (2009) and Suschenko and Purschke (2009) present new data on the structure of the nervous system and photoreceptors. Scholtz and Ungerer investigate the cleavage and gastrulation in pycnogonids.…”

“…The program unites molecular and morphological approaches; this Special Volume will present process of the morphological projects. Please note that the three articles by Harzsch et al (2009), Stach (2009 and Suschenko and Purschke (2009) also belong into this Special Volume, but were printed earlier due to restricted space.…”