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Research Article

Metazoan opsin evolution reveals a simple route to animal vision

Roberto Feuda, Sinead C. Hamilton, James O. McInerney, and Davide Pisani
  1. aDepartment of Biology, National University of Ireland Maynooth, Kildare, Ireland; and
  2. bSchool of Biological Sciences and School of Earth Sciences, University of Bristol, Bristol BS8 1UG, United Kingdom

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PNAS first published October 29, 2012; https://doi.org/10.1073/pnas.1204609109
Roberto Feuda
aDepartment of Biology, National University of Ireland Maynooth, Kildare, Ireland; and
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Sinead C. Hamilton
aDepartment of Biology, National University of Ireland Maynooth, Kildare, Ireland; and
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James O. McInerney
aDepartment of Biology, National University of Ireland Maynooth, Kildare, Ireland; and
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Davide Pisani
aDepartment of Biology, National University of Ireland Maynooth, Kildare, Ireland; and
bSchool of Biological Sciences and School of Earth Sciences, University of Bristol, Bristol BS8 1UG, United Kingdom
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  • For correspondence: davide.pisani@nuim.ie
  1. Edited by David M. Hillis, University of Texas at Austin, Austin, TX, and approved September 13, 2012 (received for review March 21, 2012)

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Abstract

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.

  • ancestral character state reconstruction
  • Metazoa
  • protein evolution

Footnotes

  • ↵1To whom correspondence should be addressed. E-mail: davide.pisani{at}nuim.ie.
  • Author contributions: J.O.M. and D.P. designed research; R.F. performed research; S.C.H. contributed new reagents/analytic tools; R.F. and D.P. analyzed data; and R.F., S.C.H., J.O.M., and D.P. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1204609109/-/DCSupplemental.

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Early evolution of vision
Roberto Feuda, Sinead C. Hamilton, James O. McInerney, Davide Pisani
Proceedings of the National Academy of Sciences Oct 2012, 201204609; DOI: 10.1073/pnas.1204609109

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Early evolution of vision
Roberto Feuda, Sinead C. Hamilton, James O. McInerney, Davide Pisani
Proceedings of the National Academy of Sciences Oct 2012, 201204609; DOI: 10.1073/pnas.1204609109
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