Metazoan opsin evolution reveals a simple route to animal vision

All known visual pigments in Neuralia (Cnidaria, Ctenophora, and Bilateria) are composed of an opsin (a seven-transmembrane G protein-coupled receptor), and a light-sensitive chromophore, generally retinal. Accordingly, opsins play a key role in vision. There is no agreement on the relationships of the neuralian opsin subfamilies, and clarifying their phylogeny is key to elucidating the origin of this protein family and of vision. We used improved methods and data to resolve the opsin phylogeny and explain the evolution of animal vision. We found that the Placozoa have opsins, and that the opsins share a common ancestor with the melatonin receptors. Further to this, we found that all known neuralian opsins can be classified into the same three subfamilies into which the bilaterian opsins are classified: the ciliary (C), rhabdomeric (R), and go-coupled plus retinochrome, retinal G protein-coupled receptor (Go/RGR) opsins. Our results entail a simple scenario of opsin evolution. The first opsin originated from the duplication of the common ancestor of the melatonin and opsin genes in a eumetazoan (Placozoa plus Neuralia) ancestor, and an inference of its amino acid sequence suggests that this protein might not have been light-sensitive. Two more gene duplications in the ancestral neuralian lineage resulted in the origin of the R, C, and Go/RGR opsins. Accordingly, the first animal with at least a C, an R, and a Go/RGR opsin was a neuralian progenitor.

[1]  Karin Nordström,et al.  A simple visual system without neurons in jellyfish larvae , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[2]  D. Richter,et al.  Origin of metazoan cadherin diversity and the antiquity of the classical cadherin/β-catenin complex , 2012, Proceedings of the National Academy of Sciences.

[3]  W. Gehring Chance and Necessity in Eye Evolution , 2011, Genome biology and evolution.

[4]  Thérèse A. Holton,et al.  Deep Genomic-Scale Analyses of the Metazoa Reject Coelomata: Evidence from Single- and Multigene Families Analyzed Under a Supertree and Supermatrix Paradigm , 2010, Genome biology and evolution.

[5]  Nicholas H. Putnam,et al.  The Trichoplax genome and the nature of placozoans , 2008, Nature.

[6]  Thomas W Cronin,et al.  Shedding new light on opsin evolution , 2012, Proceedings of the Royal Society B: Biological Sciences.

[7]  Davide Pisani,et al.  Phylogenetic-signal dissection of nuclear housekeeping genes supports the paraphyly of sponges and the monophyly of Eumetazoa. , 2009, Molecular biology and evolution.

[8]  B. Morgenstern,et al.  Improved Phylogenomic Taxon Sampling Noticeably Affects Nonbilaterian Relationships , 2010, Molecular biology and evolution.

[9]  H. Philippe,et al.  Resolving Difficult Phylogenetic Questions: Why More Sequences Are Not Enough , 2011, PLoS biology.

[10]  Mark Wilkinson,et al.  Of clades and clans: terms for phylogenetic relationships in unrooted trees. , 2007, Trends in ecology & evolution.

[11]  D. Erwin Early origin of the bilaterian developmental toolkit , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[12]  A. Löytynoja,et al.  Phylogeny-Aware Gap Placement Prevents Errors in Sequence Alignment and Evolutionary Analysis , 2008, Science.

[13]  Corinne Da Silva,et al.  Phylogenomics Revives Traditional Views on Deep Animal Relationships , 2009, Current Biology.

[14]  B. Schierwater,et al.  Concatenated Analysis Sheds Light on Early Metazoan Evolution and Fuels a Modern “Urmetazoon” Hypothesis , 2009, PLoS biology.

[15]  Cestmir Vlcek,et al.  Assembly of the cnidarian camera-type eye from vertebrate-like components , 2008, Proceedings of the National Academy of Sciences.

[16]  Todd H. Oakley,et al.  The Amphimedon queenslandica genome and the evolution of animal complexity , 2010, Nature.

[17]  D. Erwin,et al.  The Cambrian Conundrum: Early Divergence and Later Ecological Success in the Early History of Animals , 2011, Science.

[18]  Benjamin M. Wheeler,et al.  The dynamic genome of Hydra , 2010, Nature.

[19]  David Q. Matus,et al.  Broad phylogenomic sampling improves resolution of the animal tree of life , 2008, Nature.

[20]  W. Gehring,et al.  Evolution and Functional Diversity of Jellyfish Opsins , 2008, Current Biology.

[21]  Kosuke Takano,et al.  Jellyfish vision starts with cAMP signaling mediated by opsin-Gs cascade , 2008, Proceedings of the National Academy of Sciences.

[22]  E. Davidson,et al.  Gene Regulatory Networks and the Evolution of Animal Body Plans , 2006, Science.

[23]  Akihisa Terakita,et al.  The opsins , 2005, Genome Biology.

[24]  M. Wiener,et al.  Animal eyes. , 1957, The American orthoptic journal.

[25]  Peter G Foster,et al.  Modeling compositional heterogeneity. , 2004, Systematic biology.

[26]  J. Nathans,et al.  Isolation, sequence analysis, and intron-exon arrangement of the gene encoding bovine rhodopsin , 1983, Cell.

[27]  Gordon L. Fain,et al.  Phototransduction and the Evolution of Photoreceptors , 2010, Current Biology.

[28]  Nicholas H. Putnam,et al.  Sea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization , 2007, Science.

[29]  Hidetoshi Shimodaira An approximately unbiased test of phylogenetic tree selection. , 2002, Systematic biology.

[30]  Lars Gislén,et al.  Advanced optics in a jellyfish eye , 2005, Nature.

[31]  Todd H. Oakley,et al.  The Origins of Novel Protein Interactions during Animal Opsin Evolution , 2007, PloS one.

[32]  A. H. Clark,et al.  Animal evolution , 1981 .

[33]  Todd H. Oakley,et al.  The evolution of phototransduction from an ancestral cyclic nucleotide gated pathway , 2010, Proceedings of the Royal Society B: Biological Sciences.

[34]  H. Schiöth,et al.  The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. , 2003, Molecular pharmacology.

[35]  Todd H. Oakley,et al.  Blue-light-receptive cryptochrome is expressed in a sponge eye lacking neurons and opsin , 2012, Journal of Experimental Biology.