, Volume 137, Issue 2, pp 241–248 | Cite as

Unexpected ultrastructure of an eye in Spiralia: the larval ocelli of Procephalothrix oestrymnicus (Nemertea)

  • Jörn von Döhren
  • Thomas Bartolomaeus
Original paper


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) 



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.

Ethical approval

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).


  1. Andrade SCS, Strand M, Schwartz M et al (2012) Disentangling ribbon worm relationships: multi-locus analysis supports traditional classification of the phylum Nemertea. Cladistics 28:141–159. CrossRefGoogle Scholar
  2. Andrade SCS, Montenegro H, Strand M et al (2014) A transcriptomic approach to ribbon worm systematics (Nemertea): resolving the pilidiophora problem. Mol Biol Evol 31:3206–3215. CrossRefPubMedGoogle Scholar
  3. Arendt D (2003) Evolution of eyes and photoreceptor cell types. Int J Dev Biol 47:563–571PubMedGoogle Scholar
  4. Arendt D, Wittbrodt J (2001) Reconstructing the eyes of Urbilateria. Philos Trans R Soc London B Biol Sci 356:1545–1563CrossRefPubMedPubMedCentralGoogle Scholar
  5. 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
  6. 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
  7. 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
  8. Bartolomaeus T (1993) Different photoreceptors in juvenile Ophelia rathkei (Annelida, Opheliida). Microfauna Mar 8:99–114Google Scholar
  9. 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. CrossRefGoogle Scholar
  10. 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
  11. 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
  12. Blumer MJF (1995) The ciliary photoreceptor in the teleplanic veliger larvae of Smaragdia sp. and Strombus sp. (Mollusca, Gastropoda). Zoomorphology 115:73–81CrossRefGoogle Scholar
  13. Blumer MJF (1996) Alterations of the eyes during ontogenesis in Aporrhais pespelecani (Mollusca, Caenogastropoda). Zoomorphology 116:123–131CrossRefGoogle Scholar
  14. Blumer MJF (1998) Alterations of the eyes of Carinaria lamarcki (Gastropoda, Heteropoda) during the long pelagic cycle. Zoomorphology 118:183–194CrossRefGoogle Scholar
  15. Blumer MJF (1999) Development of a unique eye: photoreceptors of the pelagic predator Atlanta peroni (Gastropoda, Heteropoda). Zoomorphology 119:81–91CrossRefGoogle Scholar
  16. 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
  17. 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
  18. Eakin RM (1979) Evolutionary significance of photoreceptors: in retrospect. Am Zool 19:647–653CrossRefGoogle Scholar
  19. Eakin RM, Brandenburger JL (1981) Fine structure of the eyes of Pseudoceros canadensis (Turbellaria, Polycladida). Zoomorphology 98:1–16CrossRefGoogle Scholar
  20. Eakin RM, Westfall JA (1964) Further observations on the fine structure of some invertebrate eyes. Zeitschrift für Zellforsch mikroskopische Anat 62:310–332CrossRefGoogle Scholar
  21. Eakin RM, Westfall JA (1968) Fine structure of nemertean ocelli. Am Zool 8:803Google Scholar
  22. 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
  23. 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
  24. Hubrecht AAW (1879) The genera of European nemerteans critically revised, with description of several new species. Notes from Leyden Museum 1:193–232Google Scholar
  25. Hughes RL, Woollacott RM (1978) Ultrastructure of potential photoreceptor organs in the larva of Scrupocellaria bertholetti (Bryozoa). Zoomorphologie 91:225–234CrossRefGoogle Scholar
  26. 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
  27. 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
  28. 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
  29. Kremer JR, Mastronarde DN, McIntosh JR (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116:71–76CrossRefPubMedGoogle Scholar
  30. Kvist S, Laumer CE, Junoy J, Giribet G (2014) New insights into the phylogeny, systematics and DNA barcoding of Nemertea. Invertebr Syst 28:287–308. CrossRefGoogle Scholar
  31. 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
  32. Lanfranchi A, Bedini C, Ferrero E (1981) The ultrastructure of the eyes in larval and adult polyclads (Turbellaria). Hydrobiologia 84:267–275CrossRefGoogle Scholar
  33. Loosli F, Kmita-Cunisse M, Gehring WJ (1996) Isolation of a Pax-6 homolog from the ribbonworm Lineus sanguineus. Proc Natl Acad Sci 93:2658–2663CrossRefPubMedPubMedCentralGoogle Scholar
  34. Maslakova SA, Martindale MQ, Norenburg JL (2004) Fundamental properties of the spiralian developmental program are displayed by the basal nemertean Carinoma tremaphoros (Palaeonemertea, Nemertea). Dev Biol 267:342–360. CrossRefPubMedGoogle Scholar
  35. Nilsson D-E (2009) The evolution of eyes and visually guided behaviour. Philos Trans R Soc London B Biol Sci 364:2833–2847CrossRefPubMedPubMedCentralGoogle Scholar
  36. Nilsson D-E (2013) Eye evolution and its functional basis. Vis Neurosci 30:5–20CrossRefPubMedPubMedCentralGoogle Scholar
  37. Norenburg JL, Stricker SA (2002) Phylum Nemertea. In: Young CM (ed) Atlas of marine invertebrate larvae. Academic Press, San Diego, pp 163–177Google Scholar
  38. Passamaneck YJ, Furchheim N, Hejnol A et al (2011) Ciliary photoreceptors in the cerebral eyes of a protostome larva. Evodevo 2:6CrossRefPubMedPubMedCentralGoogle Scholar
  39. Porter ML, Blasic JR, Bok MJ et al (2011) Shedding new light on opsin evolution. Proc R Soc London Ser B Biol Sci 279:3–14CrossRefGoogle Scholar
  40. Purschke G, Arendt D, Hausen H, Müller MCM (2006) Photoreceptor cells and eyes in Annelida. Arthropod Struct Dev 35:211–230CrossRefPubMedGoogle Scholar
  41. Randel N, Jékely G (2016) Phototaxis and the origin of visual eyes. Proc R Soc London Ser B Biol Sci 371:20150042Google Scholar
  42. Ritger RK, Norenburg JL (2006) Tubulanus riceae new species (Nemertea: Anopla: Palaeonemertea: Tubulanidae), from South Florida, Belize and Panama. J Nat Hist 40:931–942CrossRefGoogle Scholar
  43. Ruppert EE (1978) A review of metamorphosis of turbellarian larvae. In: Chia F-S, Rice ME (eds) Settlement and metamorphosis of marine invertebrate larvae. Elsevier, New York, pp 65–82Google Scholar
  44. Schindelin J, Arganda-Carreras I, Frise E et al (2012) Fiji: an open-source platform for biological-image analysis. Nat Meth 9:676–682CrossRefGoogle Scholar
  45. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. CrossRefPubMedPubMedCentralGoogle Scholar
  46. Smith JE (1935) Memoirs: the early development of the nemertean Cephalothrix rufifrons. Q J Microsc Sci 2:335–381Google Scholar
  47. Storch V, Moritz K (1971) Zur Feinstruktur der Sinnesorgane von Lineus ruber OF Müller (Nemertini, Heteronemertini). Cell Tissue Res 117:212–225Google Scholar
  48. Thollesson M, Norenburg JL (2003) Ribbon worm relationships: a phylogeny of the phylum Nemertea. Proc Biol Sci 270:407–415. CrossRefPubMedPubMedCentralGoogle Scholar
  49. Vernet G (1970) Ultrastructure des photorécepteurs de Lineus ruber (O.F. Müller)(Hétéronémertes Lineïdae). Cell Tissue Res 104:494–506Google Scholar
  50. Vernet G (1974) Étude ultrastructurale de cellules présumées photoréceptrices dans les ganglions cérébroïdes des Lineidae (Hétéronemertes). Ann des Sci Nat Biol Anim 16:27–36Google Scholar
  51. von Döhren J (2008) Zur Phylogenie der Nemertea: Vergleichende Untersuchungen der Reproduktion und Entwicklung. Dissertation, Freie Universität BerlinGoogle Scholar
  52. von Döhren J (2015) Nemertea. In: Wanninger A (ed) Evolutionary Developmental Biology of Invertebrates: vol 2 Lophotrochozoa (Spiralia). Springer, Wien, pp 155–192CrossRefGoogle Scholar
  53. von Döhren J (2016) Development of the nervous system of Carinina ochracea (Palaeonemertea, Nemertea). PLoS One 11:23Google Scholar
  54. von Döhren J, Bartolomaeus T ((2007) Ultrastructure and development of the rhabdomeric eyes in Lineus viridis (Heteronemertea, Nemertea). Zoology 110:430–438. CrossRefGoogle Scholar
  55. Woollacott RM, Eakin RM (1973) Ultrastructure of a potential photoreceptoral organ in the larva of an entoproct. J Ultrastruct Res 43:412–425CrossRefPubMedGoogle Scholar
  56. Woollacott RM, Zimmer RL (1972) Fine structure of a potential photoreceptor organ in the larva of Bugula neritina (Bryozoa). Cell Tissue Res 123:458–469Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute of Evolutionary Biology and EcologyUniversity of BonnBonnGermany

Personalised recommendations