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The visual pathway in sea spiders (Pycnogonida) displays a simple serial layout with similarities to the median eye pathway in horseshoe crabs

BACKGROUND: Phylogenomic studies over the past two decades have consolidated the major branches of the arthropod tree of life. However, especially within the Chelicerata (spiders, scorpions, and kin), interrelationships of the constituent taxa remain controversial. While sea spiders (Pycnogonida) ar...

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Autor principal: Brenneis, Georg
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8796508/
https://www.ncbi.nlm.nih.gov/pubmed/35086529
http://dx.doi.org/10.1186/s12915-021-01212-z
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author Brenneis, Georg
author_facet Brenneis, Georg
author_sort Brenneis, Georg
collection PubMed
description BACKGROUND: Phylogenomic studies over the past two decades have consolidated the major branches of the arthropod tree of life. However, especially within the Chelicerata (spiders, scorpions, and kin), interrelationships of the constituent taxa remain controversial. While sea spiders (Pycnogonida) are firmly established as sister group of all other extant representatives (Euchelicerata), euchelicerate phylogeny itself is still contested. One key issue concerns the marine horseshoe crabs (Xiphosura), which recent studies recover either as sister group of terrestrial Arachnida or nested within the latter, with significant impact on postulated terrestrialization scenarios and long-standing paradigms of ancestral chelicerate traits. In potential support of a nested placement, previous neuroanatomical studies highlighted similarities in the visual pathway of xiphosurans and some arachnopulmonates (scorpions, whip scorpions, whip spiders). However, contradictory descriptions of the pycnogonid visual system hamper outgroup comparison and thus character polarization. RESULTS: To advance the understanding of the pycnogonid brain and its sense organs with the aim of elucidating chelicerate visual system evolution, a wide range of families were studied using a combination of micro-computed X-ray tomography, histology, dye tracing, and immunolabeling of tubulin, the neuropil marker synapsin, and several neuroactive substances (including histamine, serotonin, tyrosine hydroxylase, and orcokinin). Contrary to previous descriptions, the visual system displays a serial layout with only one first-order visual neuropil connected to a bilayered arcuate body by catecholaminergic interneurons. Fluorescent dye tracing reveals a previously reported second visual neuropil as the target of axons from the lateral sense organ instead of the eyes. CONCLUSIONS: Ground pattern reconstruction reveals remarkable neuroanatomical stasis in the pycnogonid visual system since the Ordovician or even earlier. Its conserved layout exhibits similarities to the median eye pathway in euchelicerates, especially in xiphosurans, with which pycnogonids share two median eye pairs that differentiate consecutively during development and target one visual neuropil upstream of the arcuate body. Given multiple losses of median and/or lateral eyes in chelicerates, and the tightly linked reduction of visual processing centers, interconnections between median and lateral visual neuropils in xiphosurans and arachnopulmonates are critically discussed, representing a plausible ancestral condition of taxa that have retained both eye types. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-021-01212-z.
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spelling pubmed-87965082022-02-03 The visual pathway in sea spiders (Pycnogonida) displays a simple serial layout with similarities to the median eye pathway in horseshoe crabs Brenneis, Georg BMC Biol Research Article BACKGROUND: Phylogenomic studies over the past two decades have consolidated the major branches of the arthropod tree of life. However, especially within the Chelicerata (spiders, scorpions, and kin), interrelationships of the constituent taxa remain controversial. While sea spiders (Pycnogonida) are firmly established as sister group of all other extant representatives (Euchelicerata), euchelicerate phylogeny itself is still contested. One key issue concerns the marine horseshoe crabs (Xiphosura), which recent studies recover either as sister group of terrestrial Arachnida or nested within the latter, with significant impact on postulated terrestrialization scenarios and long-standing paradigms of ancestral chelicerate traits. In potential support of a nested placement, previous neuroanatomical studies highlighted similarities in the visual pathway of xiphosurans and some arachnopulmonates (scorpions, whip scorpions, whip spiders). However, contradictory descriptions of the pycnogonid visual system hamper outgroup comparison and thus character polarization. RESULTS: To advance the understanding of the pycnogonid brain and its sense organs with the aim of elucidating chelicerate visual system evolution, a wide range of families were studied using a combination of micro-computed X-ray tomography, histology, dye tracing, and immunolabeling of tubulin, the neuropil marker synapsin, and several neuroactive substances (including histamine, serotonin, tyrosine hydroxylase, and orcokinin). Contrary to previous descriptions, the visual system displays a serial layout with only one first-order visual neuropil connected to a bilayered arcuate body by catecholaminergic interneurons. Fluorescent dye tracing reveals a previously reported second visual neuropil as the target of axons from the lateral sense organ instead of the eyes. CONCLUSIONS: Ground pattern reconstruction reveals remarkable neuroanatomical stasis in the pycnogonid visual system since the Ordovician or even earlier. Its conserved layout exhibits similarities to the median eye pathway in euchelicerates, especially in xiphosurans, with which pycnogonids share two median eye pairs that differentiate consecutively during development and target one visual neuropil upstream of the arcuate body. Given multiple losses of median and/or lateral eyes in chelicerates, and the tightly linked reduction of visual processing centers, interconnections between median and lateral visual neuropils in xiphosurans and arachnopulmonates are critically discussed, representing a plausible ancestral condition of taxa that have retained both eye types. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-021-01212-z. BioMed Central 2022-01-28 /pmc/articles/PMC8796508/ /pubmed/35086529 http://dx.doi.org/10.1186/s12915-021-01212-z Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Brenneis, Georg
The visual pathway in sea spiders (Pycnogonida) displays a simple serial layout with similarities to the median eye pathway in horseshoe crabs
title The visual pathway in sea spiders (Pycnogonida) displays a simple serial layout with similarities to the median eye pathway in horseshoe crabs
title_full The visual pathway in sea spiders (Pycnogonida) displays a simple serial layout with similarities to the median eye pathway in horseshoe crabs
title_fullStr The visual pathway in sea spiders (Pycnogonida) displays a simple serial layout with similarities to the median eye pathway in horseshoe crabs
title_full_unstemmed The visual pathway in sea spiders (Pycnogonida) displays a simple serial layout with similarities to the median eye pathway in horseshoe crabs
title_short The visual pathway in sea spiders (Pycnogonida) displays a simple serial layout with similarities to the median eye pathway in horseshoe crabs
title_sort visual pathway in sea spiders (pycnogonida) displays a simple serial layout with similarities to the median eye pathway in horseshoe crabs
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8796508/
https://www.ncbi.nlm.nih.gov/pubmed/35086529
http://dx.doi.org/10.1186/s12915-021-01212-z
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