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      Remnants of ancestral larval eyes in an eyeless mollusk? Molecular characterization of photoreceptors in the scaphopod Antalis entalis

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          Abstract

          Background

          Eyes have evolved and been lost multiple times during animal evolution, however, the process of eye loss has only been reconstructed in a few cases. Mollusks exhibit eyes as varied as the octopod camera eye or the gastropod cup eye and are ideal systems for studying the evolution of eyes, photoreceptors, and opsins.

          Results

          Here, we identify genes related to photoreceptor formation and function in an eyeless conchiferan mollusk, the scaphopod Antalis entalis, and investigate their spatial and temporal expression patterns during development. Our study reveals that the scaphopod early mid-stage trochophore larva has putative photoreceptors in a similar location and with a similar gene expression profile as the trochophore of polyplacophoran mollusks. The apical and post-trochal putative photoreceptors appear to co-express go- opsin, six1/ 2, myoV, and eya, while expression domains in the posterior foot and pavilion (posterior mantle opening) show co-expression of several other candidate genes but not go- opsin. Sequence analysis reveals that the scaphopod Go-opsin amino acid sequence lacks the functionally important lysine (K296; Schiff base) in the retinal-binding domain, but has not accumulated nonsense mutations and still exhibits the canonical G-protein activation domain.

          Conclusions

          The scaphopod Go-opsin sequence reported here is the only known example of a bilaterian opsin that lacks lysine K296 in the retinal-binding domain. Although this may render the Go-opsin unable to detect light, the protein may still perform sensory functions. The location, innervation, development, and gene expression profiles of the scaphopod and polyplacophoran apical and post-trochal photoreceptors suggest that they are homologous, even though the scaphopod post-trochal photoreceptors have degenerated. This indicates that post-trochal eyes are not a polyplacophoran apomorphy but likely a molluscan synapomorphy lost in other mollusks. Scaphopod eye degeneration is probably a result of the transition to an infaunal life history and is reflected in the likely functional degeneration of Go-opsin, the loss of photoreceptor shielding pigments, and the scarce expression of genes involved in phototransduction and eye development. Our results emphasize the importance of studying a phylogenetically broad range of taxa to infer the mechanisms and direction of body plan evolution.

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          Most cited references41

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          Resolving the evolutionary relationships of molluscs with phylogenomic tools.

          Molluscs (snails, octopuses, clams and their relatives) have a great disparity of body plans and, among the animals, only arthropods surpass them in species number. This diversity has made Mollusca one of the best-studied groups of animals, yet their evolutionary relationships remain poorly resolved. Open questions have important implications for the origin of Mollusca and for morphological evolution within the group. These questions include whether the shell-less, vermiform aplacophoran molluscs diverged before the origin of the shelled molluscs (Conchifera) or lost their shells secondarily. Monoplacophorans were not included in molecular studies until recently, when it was proposed that they constitute a clade named Serialia together with Polyplacophora (chitons), reflecting the serial repetition of body organs in both groups. Attempts to understand the early evolution of molluscs become even more complex when considering the large diversity of Cambrian fossils. These can have multiple dorsal shell plates and sclerites or can be shell-less but with a typical molluscan radula and serially repeated gills. To better resolve the relationships among molluscs, we generated transcriptome data for 15 species that, in combination with existing data, represent for the first time all major molluscan groups. We analysed multiple data sets containing up to 216,402 sites and 1,185 gene regions using multiple models and methods. Our results support the clade Aculifera, containing the three molluscan groups with spicules but without true shells, and they support the monophyly of Conchifera. Monoplacophora is not the sister group to other Conchifera but to Cephalopoda. Strong support is found for a clade that comprises Scaphopoda (tusk shells), Gastropoda and Bivalvia, with most analyses placing Scaphopoda and Gastropoda as sister groups. This well-resolved tree will constitute a framework for further studies of mollusc evolution, development and anatomy.
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            Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup.

            Charles Darwin appreciated the conceptual difficulty in accepting that an organ as wonderful as the vertebrate eye could have evolved through natural selection. He reasoned that if appropriate gradations could be found that were useful to the animal and were inherited, then the apparent difficulty would be overcome. Here, we review a wide range of findings that capture glimpses of the gradations that appear to have occurred during eye evolution, and provide a scenario for the unseen steps that have led to the emergence of the vertebrate eye.
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              Phototransduction motifs and variations.

              Seeing begins in the photoreceptors, where light is absorbed and signaled to the nervous system. Throughout the animal kingdom, photoreceptors are diverse in design and purpose. Nonetheless, phototransduction-the mechanism by which absorbed photons are converted into an electrical response-is highly conserved and based almost exclusively on a single class of photoproteins, the opsins. In this Review, we survey the G protein-coupled signaling cascades downstream from opsins in photoreceptors across vertebrate and invertebrate species, noting their similarities as well as differences.
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                Author and article information

                Contributors
                tim.wollesen@embl.de
                c.mcdougall@griffith.edu.au
                arendt@embl.de
                Journal
                EvoDevo
                Evodevo
                EvoDevo
                BioMed Central (London )
                2041-9139
                19 October 2019
                19 October 2019
                2019
                : 10
                : 25
                Affiliations
                [1 ]ISNI 0000 0004 0495 846X, GRID grid.4709.a, EMBL, ; Meyerhofstraße 1, 69117 Heidelberg, Germany
                [2 ]ISNI 0000 0004 0437 5432, GRID grid.1022.1, Australian Rivers Institute, , Griffith University, ; 170 Kessels Road, Nathan, QLD 4111 Australia
                Author information
                http://orcid.org/0000-0003-0464-1254
                http://orcid.org/0000-0002-2116-5651
                http://orcid.org/0000-0001-7833-050X
                Article
                140
                10.1186/s13227-019-0140-7
                6800502
                31641428
                a53f0309-ea3c-4f74-8891-3872f6481548
                © The Author(s) 2019

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 16 July 2019
                : 25 September 2019
                Funding
                Funded by: Association of European Marine Biological Laboratories (ASSEMBLE)
                Award ID: 835 (SBR-1) & 730984
                Award Recipient :
                Funded by: Austrian Science Foundation (FWF)
                Award ID: J4198
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2019

                Developmental biology
                apical organ,evolution and development,gastropod,lophotrochozoan,mollusc,platynereis,polyplacophora,retinal-binding domain,spiralia,vision

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