Animal eyes are morphologically diverse. Their assembly, however, always relies on the same basic principle, i.e., photoreceptors located in the vicinity of dark shielding pigment. Cnidaria as the likely sister group to the Bilateria are the earliest branching phylum with a well developed visual system. Here, we show that camera-type eyes of the cubozoan jellyfish, Tripedalia cystophora, use genetic building blocks typical of vertebrate eyes, namely, a ciliary phototransduction cascade and melanogenic pathway. Our findings indicative of parallelism provide an insight into eye evolution. Combined, the available data favor the possibility that vertebrate and cubozoan eyes arose by independent recruitment of orthologous genes during evolution.

Institute of Molecular Genetics Academy of Sciences of the Czech Republic Videnska 1083 142 20 Prague 4 Czech Republic

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Fernald RD. Casting a genetic light on the evolution of eyes. Science. 2006;313:1914–1918. PubMed

Arendt D, Wittbrodt J. Reconstructing the eyes of Urbilateria. Philos Trans R Soc London Ser B. 2001;356:1545–1563. PubMed PMC

Arendt D. Evolution of eyes and photoreceptor cell types. Int J Dev Biol. 2003;47:563–571. PubMed

Viscontini M, Hummel W, Fischer A. Isolation of pterin dimers from the eyes of Platynereis dumerilii (German) Helv Chim Acta. 1970;53:1207–1209.

Shoup JR. The development of pigment granules in the eyes of wild-type and mutant Drosophila melanogaster. J Cell Biol. 1966;29:223–249. PubMed PMC

Hase S, et al. Characterization of the pigment produced by the planarian, Dugesia ryukyuensis. Pigment Cell Res. 2006;19:248–249. PubMed

Conant FS. Notes on the Cubomedusae. Johns Hopkins Univ Circ. 1897;132:8–10.

Pearse JS, Pearse VB. Vision of cubomedusan jellyfishes. Science. 1978;199:458. PubMed

Yamasu T, Yoshida M. Fine structure of complex ocelli of a cubomedusan, Tamoya bursaria. Haeckel Cell Tissue Res. 1976;170:325–339. PubMed

Garm A, O'Connor M, Parkefelt L, Nilsson DE. Visually guided obstacle avoidance in the box jellyfish Tripedalia cystophora and Chiropsella bronzie. J Exp Biol. 2007;210:3616–3623. PubMed

Nilsson DE, Gislen L, Coates MM, Skogh C, Garm A. Advanced optics in a jellyfish eye. Nature. 2005;435:201–205. PubMed

Terakita A. The opsins. Genome Biol. 2005;6:213. PubMed PMC

Arendt D, Tessmar-Raible K, Snyman H, Dorresteijn AW, Wittbrodt J. Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain. Science. 2004;306:869–871. PubMed

Raible F, et al. Opsins and clusters of sensory G protein-coupled receptors in the sea urchin genome. Dev Biol. 2006;300:461–475. PubMed

Marin EP, et al. The amino terminus of the fourth cytoplasmic loop of rhodopsin modulates rhodopsin-transducin interaction. J Biol Chem. 2000;275:1930–1936. PubMed

Coates MM, Garm A, Theobald JC, Thompson SH, Nilsson DE. The spectral sensitivity of the lens eyes of a box jellyfish, Tripedalia cystophora (Conant) J Exp Biol. 2006;209:3758–3765. PubMed

Arnheiter H. Evolutionary biology: Eyes viewed from the skin. Nature. 1998;391:632–633. PubMed

Oetting WS, Garrett SS, Brott M, King RA. P gene mutations associated with oculocutaneous albinism type II (OCA2) Hum Mutat. 2005;25:323. PubMed

Rinchik EM, et al. A gene for the mouse pink-eyed dilution locus and for human type II oculocutaneous albinism. Nature. 1993;361:72–76. PubMed

Fukamachi S, et al. Conserved function of medaka pink-eyed dilution in melanin synthesis and its divergent transcriptional regulation in gonads among vertebrates. Genetics. 2004;168:1519–1527. PubMed PMC

Protas ME, et al. Genetic analysis of cavefish reveals molecular convergence in the evolution of albinism. Nat Genet. 2006;38:107–111. PubMed

Hodgkinson CA, et al. Mutations at the mouse microphthalmia locus are associated with defects in a gene encoding a novel basic-helix–loop–helix-zipper protein. Cell. 1993;74:395–404. PubMed

Nguyen M, Arnheiter H. Signaling and transcriptional regulation in early mammalian eye development: A link between FGF and MITF. Development. 2000;127:3581–3591. PubMed

Opdecamp K, et al. Melanocyte development in vivo and in neural crest cell cultures: Crucial dependence on the Mitf basic helix–loop–helix zipper transcription factor. Development. 1997;124:2377–2386. PubMed

Goding CR. Mitf from neural crest to melanoma: Signal transduction and transcription in the melanocyte lineage. Genes Dev. 2000;14:1712–1728. PubMed

Piatigorsky J, Horwitz J, Norman BL. J1-crystallins of the cubomedusan jellyfish lens constitute a novel family encoded in at least three intronless genes. J Biol Chem. 1993;268:11894–11901. PubMed

Plachetzki DC, Degnan BM, Oakley TH. The origins of novel protein interactions during animal opsin evolution. PLoS ONE. 2007;2:e1054. PubMed PMC

Gehring WJ, Ikeo K. Pax 6: Mastering eye morphogenesis and eye evolution. Trends Genet. 1999;15:371–377. PubMed

Nilsson DE, Pelger S. A pessimistic estimate of the time required for an eye to evolve. Proc Biol Sci. 1994;256:53–58. PubMed

Kozmik Z, et al. Role of Pax genes in eye evolution: A cnidarian PaxB gene uniting Pax2 and Pax6 functions. Dev Cell. 2003;5:773–785. PubMed

Hill RE, et al. Mouse small eye results from mutations in a paired-like homeobox-containing gene. Nature. 1991;354:522–525. PubMed

Quiring R, Walldorf U, Kloter U, Gehring WJ. Homology of the eyeless gene of Drosophila to the small eye gene in mice and Aniridia in humans. Science. 1994;265:785–789. PubMed

Halder G, Callaerts P, Gehring WJ. Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science. 1995;267:1788–1792. PubMed

Gehring WJ. Historical perspective on the development and evolution of eyes and photoreceptors. Int J Dev Biol. 2004;48:707–717. PubMed

Silver SJ, Rebay I. Signaling circuitries in development: Insights from the retinal determination gene network. Development. 2005;132:3–13. PubMed

Fernald RD. Eyes: Variety, development, and evolution. Brain Behav Evol. 2004;64:141–147. PubMed

Fernald RD. Evolving eyes. Int J Dev Biol. 2004;48:701–705. PubMed

Salvini-Plawen LV, Mayr E. On the evolution of photoreceptors and eyes. Evol Biol. 1977;10:207–263.

Kortschak RD, Samuel G, Saint R, Miller DJ. EST analysis of the cnidarian Acropora millepora reveals extensive gene loss and rapid sequence divergence in the model invertebrates. Curr Biol. 2003;13:2190–2195. PubMed

Putnam NH, et al. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science. 2007;317:86–94. PubMed

Piatigorsky J. Gene Sharing and Evolution: The Diversity of Protein Functions. Cambridge, MA: Harvard Univ Press; 2007.

Cvekl A, Yang Y, Chauhan BK, Cveklova K. Regulation of gene expression by Pax6 in ocular cells: A case of tissue-preferred expression of crystallins in lens. Int J Dev Biol. 2004;48:829–844. PubMed PMC

Kozmik Z, et al. Cubozoan crystallins: Evidence for convergent evolution of Pax regulatory sequences. Evolution Dev. 2008;10:52–61. PubMed

Eakin RM, Westfall JA. Further observation on the fine structure of some invertebrate eyes. Z Zellforsch Mikrosk Anat. 1964;62:310–332. PubMed

Cubozoan genome illuminates functional diversification of opsins and photoreceptor evolution

Eye evolution: common use and independent recruitment of genetic components

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