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.2018 Dec 5;285(1892):20182180.
doi: 10.1098/rspb.2018.2180.

Molecular palaeontology illuminates the evolution of ecdysozoan vision

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Molecular palaeontology illuminates the evolution of ecdysozoan vision

James F Fleming et al. Proc Biol Sci..

Abstract

Colour vision is known to have arisen only twice-once in Vertebrata and once within the Ecdysozoa, in Arthropoda. However, the evolutionary history of ecdysozoan vision is unclear. At the molecular level, visual pigments, composed of a chromophore and a protein belonging to the opsin family, have different spectral sensitivities and these mediate colour vision. At the morphological level, ecdysozoan vision is conveyed by eyes of variable levels of complexity; from the simple ocelli observed in the velvet worms (phylum Onychophora) to the marvellously complex eyes of insects, spiders, and crustaceans. Here, we explore the evolution of ecdysozoan vision at both the molecular and morphological level; combining analysis of a large-scale opsin dataset that includes previously unknown ecdysozoan opsins with morphological analyses of key Cambrian fossils with preserved eye structures. We found that while several non-arthropod ecdysozoan lineages have multiple opsins, arthropod multi-opsin vision evolved through a series of gene duplications that were fixed in a period of 35-71 million years (Ma) along the stem arthropod lineage. Our integrative study of the fossil and molecular record of vision indicates that fossils with more complex eyes were likely to have possessed a larger complement of opsin genes.

Keywords: evolution; opsin; phylogeny; vision.

© 2018 The Authors.

PubMed Disclaimer

Conflict of interest statement

We have no competing interests.

Figures

Figure 1.
Figure 1.
Distribution of well-characterized ecdysozoan opsins. Purple: short wave sensitive (SWS), violet: UV and Rh7, light blue: medium wave sensitive (MWS), and green: long wave sensitive (LWS). Black: UV/SWS. In all figures animal silhouettes are fromwww.phylopic.org.
Figure 2.
Figure 2.
The ecdysozoan visual opsin phylogeny, with a focus on the non-arthropod ecdysozoans. New opsins were identified inMeiopriapulus,Paragordius, and three species of Tardigrada, showing independent duplications of visual opsins in these lineages. At key internal nodes (top to bottom): the name of opsin (defined according to the rules in §1b) that is inferred to have existed at that node—based on the results of the ALE analysis. Credibility interval for the age of the duplication is given at key nodes within the tree (in Ma)—see electronic supplementary material, figure S6 for the complete set of results. Only posterior probabilities for nodes with a support value lower than 1 are reported, see electronic supplementary material, figure S5 for the complete set of results.
Figure 3.
Figure 3.
(a) Summary of the evolutionary history of the ecdysozoan visual opsins outside crown Arthropoda. An ecdysozoan timetree displaying both fossil and extant forms. Opsins inferred to have existed in terminal taxa are represented as circles. Squares along the tree indicate gene duplications along the arthropod lineage. The colours of the squares identify duplications between panels (a andb) and do not refer to theλ−max of the duplicating gene. Similarly, the colour of the circles indicating the presence of individual opsins at the tips of the tree do not necessarily indicate theλ−max of that specific opsin, as such values are not known for all the opsins in the tree. Colours are simply used to identify the presence of specific opsins across taxa. (b) Summary scheme concomitantly illustrating the evolution of the molecular and morphological components of the arthropod eye. Top: gene duplication history; gene present at different times and history of gene duplications (average age and 95% credibility intervals). Bottom: age of the nodes representing the separation of stem lineages leading to fossil taxa with specific eye types from the lineage leading to the arthropod last common ancestor. The timescales at the bottom of the figures are in Ma.Colour codes: opsin genes (circles in panela and on top of panelb). White: Rh7/UV/SWS/MWS/LWS; light green: MWS/LWS; fuchsia: Rh7/UV/SWS; dark green: LWS; light blue: MWS; lilac: Rh7; black: UV/SWS; dark purple: UV; dark blue: SWS.Opsin duplications (squares in panela and divergence times credibility bars in panelb). Brown: Rh7/UV/SWS/MSW/LWS to Rh7/UV/SWS and MWS/LWS. Teal: MWS/LWS to MWS and LWS. Light purple: Rh7/UV/SWS to Rh7 and UV/SWS.Age of the stem lineage leading to fossils with specific eye types. Red: age of the stem lineages leading toKerygmachela andPambdelurion (with reflective patches). Yellow: age of the stem lineage leading toOpabinia (with mushroom eyes). Orange: age of the stem lineages leading toAnomalocaris,Fuxianhuia, and Arthropoda (with compound eyes).
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