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Development of pigment-cup eyes in the polychaete Platynereis dumerilii and evolutionary conservation of larval eyes in Bilateria

Detlev Arendt¹, Kristin Tessmar^1,*, Maria-Ines Medeiros de Campos-Baptista¹, Adriaan Dorresteijn² and Joachim Wittbrodt^1,

¹ European Molecular Biology Laboratory, Meyerhofstraße 1, 69117 Heidelberg, Germany
² Institut fuer Allgemeine und Spezielle Zoologie, Justus-Liebig-Universität, Stephanstr. 24, 35390 Giessen, Germany
^* Present address: Department of Biochemistry and Biophysics, University of California San Francisco, 513 Parnassus Avenue, San Francisco, CA 94143, USA

Author for correspondence (e-mail: jochen.wittbrodt{at}embl-heidelberg.de)

Accepted 11 December 2001

The role of Pax6 in eye development in insects and vertebrates supports the view that their eyes evolved from simple pigment-cup ocelli present in their last common ancestors (Urbilateria). The cerebral eyes in errant polychaetes represent prototype invertebrate pigment-cup ocelli and thus resemble the presumed ancestral eyes. We have analysed expression of conserved eye specification genes in the early development of larval and adult pigment-cup eyes in Platynereis dumerilii (Polychaeta, Annelida, Lophotrochozoa). Both larval and adult eyes form in close vicinity of the optic anlagen on both sides of the developing brain ganglia. While pax6 is expressed in the larval, but not in the developing, adult eyes, expression of six1/2 from trochophora stages onwards specifically outlines the optic anlagen and thus covers both the developing larval and adult eyes. Using Platynereis rhabdomeric opsin as differentiation marker, we show that the first pair of adult eye photoreceptor cells is detected within bilateral clusters that transitorily express ath, the Platynereis atonal orthologue, thus resembling proneural sensory clusters. Our data indicate that – similar to insects, but different from the vertebrates – polychaete six1/2 expression outlines the entire visual system from early developmental stages onwards and ath-positive clusters generate the first photoreceptor cells to appear. We propose that pax6-, six1/2- and ath-positive larval eyes, as found in today’s trochophora, were present already in Urbilateria.

Key words: Platynereis, Eye, Evolution, Larval eyes, Adult eyes, six, pax6, Lochotrophozoa, Annelids

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