The evolution of eyes and their constituent photoreceptor cells in Metazoa in general and in Protostomia in particular remains unresolved with present morphological and developmental genetic data. This is mainly due to the lack of comprehensive ultrastructural data in some lineages, such as in the spiralian taxon Nemertea. The eyes of the derived Neonemertea possess rhabdomeric photoreceptor cells, considered typical of the protostome lineage. In the more basally branching palaeonemertean lineages, ultrastructural data on the eyes are wanting. Ultrastructural investigation of the eyes of the larva of the palaeonemertean Procephalothrix oestrymnicus reveals that, although in a similar position as the eyes of adult neonemertean species, the eyes in palaeonemertean larvae differ fundamentally from the expected protostomian type: They consist of one shading-pigment cell that forms a closed optical cavity embedded in the epidermis. Apart from basally distributed shading-pigment vesicles, the pigment cell apically possesses epidermal cilia and microvilli as well as sub-apical, tubular lens vesicles. Two ciliary photoreceptor cells project flattened ciliary membranes into the optical cavity formed by the pigment cell, whereas their basal portions are situated outside of the optical cavity, next to the shading-pigment cell. Although the structure of the eye in P. oestrymnicus is unparalleled in Nemertea, ciliary photoreceptor cells have been found in larval eyes of several other spiralian lineages. Occurrence of additional ciliary-type eyes in Spiralia deepens the doubts regarding the validity of the hypothesis of an exclusively rhabdomeric line of visual photoreceptor cell evolution in Protostomia.
Sensory organs Eye spot Lophotrochozoa Evolution Development Bilateria Transmission electron microscopy (TEM)
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The staff of the Station de Biologie Marine et Marinarium de Concarneau is gratefully acknowledged for providing facilities while collecting and rearing of Procephalothrix oestrymnicus.
The investigation was financially supported by the German Research Council (DFG, Ba 1520/11-1,2).
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
All applicable international, national and/or institutional guidelines for the care and use of animals were followed. We neither used endangered species nor were the investigated animals collected in protected areas. All animals were collected with the permission of the local marine biological station, the Station de Biologie Marine, Concarneau (France).
Arendt D, Tessmar K, de Campos-Baptista M-IM et al (2002) Development of pigment-cup eyes in the polychaete Platynereis dumerilii and evolutionary conservation of larval eyes in Bilateria. Development 129:1143–1154PubMedGoogle Scholar
Arendt D, Tessmar-Raible K, Snyman H et al (2004) Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain. Science 306:869–871CrossRefPubMedGoogle Scholar
Bartolomaeus T (1992) Ultrastructure of the photoreceptors in the larvae of Lepidochiton cinereus (Mollusca, Polyplacophora) and Lacuna divaricata (Mollusca, Gastropoda). Microfauna Mar 7:215–236Google Scholar
Bartolomaeus T (1993) Different photoreceptors in juvenile Ophelia rathkei (Annelida, Opheliida). Microfauna Mar 8:99–114Google Scholar
Bartolomaeus T, Maslakova SA, von Döhren J (2014) Protonephridia in the larvae of the paleonemertean species Carinoma mutabilis (Carinomidae, Nemertea) and Cephalothrix (Procephalothrix) filiformis (Cephalothricidae Nemertea). Zoomorphology 133:43–57. https://doi.org/10.1007/s00435-013-0206-3CrossRefGoogle Scholar
Beckers P, von Döhren J (2015) Nemertea (Nemertini). In: Schmidt-Rhaesa A, Harzsch S, Purschke G (eds) Structure and evolution of invertebrate nervous systems. Oxford University Press, Oxford, pp 148–165CrossRefGoogle Scholar
Blumer M (1994) The ultrastructure of the eyes in the veliger-larvae of Aporrhais sp. and Bittium reticulatum (Mollusca, Caenogastropoda). Zoomorphology 114:149–159CrossRefGoogle Scholar
Blumer MJF (1995) The ciliary photoreceptor in the teleplanic veliger larvae of Smaragdia sp. and Strombus sp. (Mollusca, Gastropoda). Zoomorphology 115:73–81CrossRefGoogle Scholar
Blumer MJF (1996) Alterations of the eyes during ontogenesis in Aporrhais pespelecani (Mollusca, Caenogastropoda). Zoomorphology 116:123–131CrossRefGoogle Scholar
Blumer MJF (1998) Alterations of the eyes of Carinaria lamarcki (Gastropoda, Heteropoda) during the long pelagic cycle. Zoomorphology 118:183–194CrossRefGoogle Scholar
Blumer MJF (1999) Development of a unique eye: photoreceptors of the pelagic predator Atlanta peroni (Gastropoda, Heteropoda). Zoomorphology 119:81–91CrossRefGoogle Scholar
Charpignon V (2006) Homeobox-containing genes in the nemertean Lineus: key players in the antero-posterior body patterning and in the specification of the visual structures. Dissertation, Universität Basel, Université de ReimsGoogle Scholar
Darwin C (1859) The origin of species by means of natural selection, or the preservation of favored races in the struggle for life, 1st edn. John Murray, LondonGoogle Scholar
Eakin RM (1979) Evolutionary significance of photoreceptors: in retrospect. Am Zool 19:647–653CrossRefGoogle Scholar
Eakin RM, Brandenburger JL (1981) Fine structure of the eyes of Pseudoceros canadensis (Turbellaria, Polycladida). Zoomorphology 98:1–16CrossRefGoogle Scholar
Eakin RM, Westfall JA (1964) Further observations on the fine structure of some invertebrate eyes. Zeitschrift für Zellforsch mikroskopische Anat 62:310–332CrossRefGoogle Scholar
Eakin RM, Westfall JA (1968) Fine structure of nemertean ocelli. Am Zool 8:803Google Scholar
Gibson R (1990) The macrobenthic nemertean fauna of Hong Kong. In: Morton B (ed) The marine flora and fauna of Hong Kong and southern China. University Press, Hong Kong, pp 33–212Google Scholar
Gibson R, Sundberg P (1992) Three new nemerteans from Hong Kong. In: Morton B (ed) The marine flora and fauna of Hong Kong and southern China. University Press., Hong Kong, pp 97–129Google Scholar
Hubrecht AAW (1879) The genera of European nemerteans critically revised, with description of several new species. Notes from Leyden Museum 1:193–232Google Scholar
Hughes RL, Woollacott RM (1978) Ultrastructure of potential photoreceptor organs in the larva of Scrupocellaria bertholetti (Bryozoa). Zoomorphologie 91:225–234CrossRefGoogle Scholar
Iwata F (1960) Studies on the comparative embryology of nemerteans with special reference to their interrelationships. Publs Akkeshi mar biol Stn 10:1–55Google Scholar
Jespersen Å, Lützen J (1988) Fine structure of the eyes of three species of hoplonemerteans (Rhynchocoela: Enopla). New Zeal J Zool Zool 15:203–210CrossRefGoogle Scholar
Kajihara H, Kakui K, Yamasaki H, Hiruta SF (2015) Tubulanus tamias sp. nov. (Nemertea: Palaeonemertea) with two different types of epidermal eyes. Zool Sci 32:596–604CrossRefPubMedGoogle Scholar
Kremer JR, Mastronarde DN, McIntosh JR (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116:71–76CrossRefPubMedGoogle Scholar
Kvist S, Chernyshev AV, Giribet G (2015) Phylogeny of Nemertea with special interest in the placement of diversity from Far East Russia and northeast Asia. Hydrobiologia 760:105–119CrossRefGoogle Scholar
Lanfranchi A, Bedini C, Ferrero E (1981) The ultrastructure of the eyes in larval and adult polyclads (Turbellaria). Hydrobiologia 84:267–275CrossRefGoogle Scholar