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      On the sighted ancestry of blindness – exceptionally preserved eyes of Mesozoic polychelidan lobsters

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          Abstract

          Background

          Modern representatives of Polychelida (Polychelidae) are considered to be entirely blind and have largely reduced eyes, possibly as an adaptation to deep-sea environments. Fossil species of Polychelida, however, appear to have well-developed compound eyes preserved as anterior bulges with distinct sculpturation.

          Methods

          We documented the shapes and sizes of eyes and ommatidia based upon exceptionally preserved fossil polychelidans from Binton (Hettangian, United-Kingdom), Osteno (Sinemurian, Italy), Posidonia Shale (Toarcian, Germany), La Voulte-sur-Rhône (Callovian, France), and Solnhofen-type plattenkalks (Kimmeridgian-Tithonian, Germany). For purposes of comparison, sizes of the eyes of several other polychelidans without preserved ommatidia were documented. Sizes of ommatidia and eyes were statistically compared against carapace length, taxonomic group, and outcrop.

          Results

          Nine species possess eyes with square facets; Rosenfeldia oppeli (Woodward, 1866), however, displays hexagonal facets. The sizes of eyes and ommatidia are a function of carapace length. No significant differences were discerned between polychelidans from different outcrops; Eryonidae, however, have significantly smaller eyes than other groups.

          Discussion

          Fossil eyes bearing square facets are similar to the reflective superposition eyes found in many extant decapods. As such, they are the earliest example of superposition eyes. As reflective superposition is considered plesiomorphic for Reptantia, this optic type was probably retained in Polychelida. The two smallest specimens, a Palaeopentacheles roettenbacheri (Münster, 1839) and a Hellerocaris falloti (Van Straelen, 1923), are interpreted as juveniles. Both possess square-shaped facets, a typical post-larval feature. The eye morphology of these small specimens, which are far smaller than many extant eryoneicus larvae, suggests that Jurassic polychelidans did not develop via giant eryoneicus larvae. In contrast, another species we examined, Rosenfeldia oppeli (Woodward, 1866), did not possess square-shaped facets, but rather hexagonal ones, which suggests that this species did not possess reflective superposition eyes. The hexagonal facets may indicate either another type of superposition eye (refractive or parabolic superposition), or an apposition eye. As decapod larvae possess apposition eyes with hexagonal facets, it is most parsimonious to consider eyes of R. oppeli as apposition eyes evolved through paedomorphic heterochrony.

          Conclusion

          Polychelidan probably originally had reflective superposition. R. oppeli, however, probably gained apposition eyes through paedomorphosis.

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          Most cited references81

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          The Posidonia Shale (Lower Toarcian) of SW-Germany: an oxygen-depleted ecosystem controlled by sea level and palaeoclimate

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            Complex brain and optic lobes in an early Cambrian arthropod.

            The nervous system provides a fundamental source of data for understanding the evolutionary relationships between major arthropod groups. Fossil arthropods rarely preserve neural tissue. As a result, inferring sensory and motor attributes of Cambrian taxa has been limited to interpreting external features, such as compound eyes or sensilla decorating appendages, and early-diverging arthropods have scarcely been analysed in the context of nervous system evolution. Here we report exceptional preservation of the brain and optic lobes of a stem-group arthropod from 520 million years ago (Myr ago), Fuxianhuia protensa, exhibiting the most compelling neuroanatomy known from the Cambrian. The protocerebrum of Fuxianhuia is supplied by optic lobes evidencing traces of three nested optic centres serving forward-viewing eyes. Nerves from uniramous antennae define the deutocerebrum, and a stout pair of more caudal nerves indicates a contiguous tritocerebral component. Fuxianhuia shares a tripartite pre-stomodeal brain and nested optic neuropils with extant Malacostraca and Insecta, demonstrating that these characters were present in some of the earliest derived arthropods. The brain of Fuxianhuia impacts molecular analyses that advocate either a branchiopod-like ancestor of Hexapoda or remipedes and possibly cephalocarids as sister groups of Hexapoda. Resolving arguments about whether the simple brain of a branchiopod approximates an ancestral insect brain or whether it is the result of secondary simplification has until now been hindered by lack of fossil evidence. The complex brain of Fuxianhuia accords with cladistic analyses on the basis of neural characters, suggesting that Branchiopoda derive from a malacostracan-like ancestor but underwent evolutionary reduction and character reversal of brain centres that are common to hexapods and malacostracans. The early origin of sophisticated brains provides a probable driver for versatile visual behaviours, a view that accords with compound eyes from the early Cambrian that were, in size and resolution, equal to those of modern insects and malacostracans.
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              The Burgess Shale anomalocaridid Hurdia and its significance for early euarthropod evolution.

              As the largest predators of the Cambrian seas, the anomalocaridids had an important impact in structuring the first complex marine animal communities, but many aspects of anomalocaridid morphology, diversity, ecology, and affinity remain unclear owing to a paucity of specimens. Here we describe the anomalocaridid Hurdia, based on several hundred specimens from the Burgess Shale in Canada. Hurdia possesses a general body architecture similar to those of Anomalocaris and Laggania, including the presence of exceptionally well-preserved gills, but differs from those anomalocaridids by possessing a prominent anterior carapace structure. These features amplify and clarify the diversity of known anomalocaridid morphology and provide insight into the origins of important arthropod features, such as the head shield and respiratory exites.
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                Author and article information

                Contributors
                denis.audo@univ-rennes1.fr , denis.audo@edu.mnhn.fr
                joachim.haug@palaeo-evo-devo.info
                carolin.haug@palaeo-evo-devo.info
                scharbonnier@mnhn.fr
                guenter.schweigert@smns-bw.de
                carstmue@uni-greifswald.de
                steffen.harzsch@uni-greifswald.de
                Journal
                Zoological Lett
                Zoological Lett
                Zoological Letters
                BioMed Central (London )
                2056-306X
                16 July 2016
                16 July 2016
                2016
                : 2
                : 13
                Affiliations
                [ ]Université de Rennes 1, EA 7316, 263 Avenue du Général Leclerc CS 74205, 35042 Rennes Cedex, France
                [ ]Centre de Recherche sur la Paléobiodiversité et les Paléoenvironnements (CR2P, UMR 7207), Muséum national d’Histoire naturelle, Sorbonne Universités, UPMC, CNRS, 8 rue Buffon, F-75005 Paris, France
                [ ]Department Biologie II und GeoBio-Center, Ludwig-Maximilians-Universität München, Biozentrum der LMU, Großhaderner Str. 2, 82152 Planegg-Martinsried, Germany
                [ ]Staatliches Museum für Naturkunde Stuttgart, Rosenstein 1, 70191 Stuttgart, Germany
                [ ]Zoologisches Institut und Museum, Lehrstuhl Allgemeine und Systematische Zoologie, Ernst-Moritz-Arndt-Universität Greifswald, Anklamer Str. 20, 17487 Greifswald, Germany
                [ ]Zoologisches Institut und Museum, Lehrstuhl Cytologie und Evolutionsbiologie, Ernst-Moritz-Arndt-Universität Greifswald, Soldmannstr. 23, 17489 Greifswald, Germany
                Author information
                http://orcid.org/0000-0003-3486-3552
                Article
                49
                10.1186/s40851-016-0049-0
                4947519
                27429789
                577e6cae-9cc6-49ab-9b60-5e63e04d0074
                © The Author(s). 2016

                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
                : 7 March 2016
                : 7 July 2016
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: Ha 6300/3-1
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2016

                polychelida,solnhofen,la voulte-sur-rhône,osteno,nusplingen,posidonia shale,heterochrony,deep-sea adaptations,superposition eyes

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