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Cambrian suspension-feeding lobopodians and the early radiation of panarthropods

BACKGROUND: Arthropoda, Tardigrada and Onychophora evolved from lobopodians, a paraphyletic group of disparate Palaeozoic vermiform animals with soft legs. Although the morphological diversity that this group encompasses likely illustrates the importance of niche diversification in the early radiati...

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Autores principales: Caron, Jean-Bernard, Aria, Cédric
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5282736/
https://www.ncbi.nlm.nih.gov/pubmed/28137244
http://dx.doi.org/10.1186/s12862-016-0858-y
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author Caron, Jean-Bernard
Aria, Cédric
author_facet Caron, Jean-Bernard
Aria, Cédric
author_sort Caron, Jean-Bernard
collection PubMed
description BACKGROUND: Arthropoda, Tardigrada and Onychophora evolved from lobopodians, a paraphyletic group of disparate Palaeozoic vermiform animals with soft legs. Although the morphological diversity that this group encompasses likely illustrates the importance of niche diversification in the early radiation of panarthropods, the ecology of lobopodians remains poorly characterized. RESULTS: Here we describe a new luolishaniid taxon from the middle Cambrian Burgess Shale (Walcott Quarry) in British Columbia, Canada, whose specialized morphology epitomizes the suspension-feeding ecology of this clade, and is convergent with some modern marine animals, such as caprellid crustaceans. This species possesses two long pairs and four shorter pairs of elongate spinose lobopods at the front, each bearing two slender claws, and three pairs of stout lobopods bearing single, strong, hook-like anterior-facing claws at the back. The trunk is remarkably bare, widening rearwards, and, at the front, extends beyond the first pair of lobopods into a small “head” bearing a pair of visual organs and a short proboscis with numerous teeth. Based on a critical reappraisal of character coding in lobopodians and using Bayesian and parsimony-based tree searches, two alternative scenarios for early panarthropod evolution are retrieved. In both cases, hallucigeniids and luolishaniids are found to be extinct radiative stem group panarthropods, in contrast to previous analyses supporting a position of hallucigeniids as part of total-group Onychophora. Our Bayesian topology finds luolishaniids and hallucigeniids to form two successive clades at the base of Panarthropoda. Disparity analyses suggest that luolishaniids, hallucigeniids and total-group Onychophora each occupy a distinct region of morphospace. CONCLUSIONS: Hallucigeniids and luolishaniids were comparably diverse and successful, representing two major lobopodian clades in the early Palaeozoic, and both evolved body plans adapted to different forms of suspension feeding. A Bayesian approach to cladistics supports the view that a semi-sessile, suspension-feeding lifestyle characterized the origin and rise of Panarthropoda from cycloneuralian body plans. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-016-0858-y) contains supplementary material, which is available to authorized users.
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spelling pubmed-52827362017-02-03 Cambrian suspension-feeding lobopodians and the early radiation of panarthropods Caron, Jean-Bernard Aria, Cédric BMC Evol Biol Article BACKGROUND: Arthropoda, Tardigrada and Onychophora evolved from lobopodians, a paraphyletic group of disparate Palaeozoic vermiform animals with soft legs. Although the morphological diversity that this group encompasses likely illustrates the importance of niche diversification in the early radiation of panarthropods, the ecology of lobopodians remains poorly characterized. RESULTS: Here we describe a new luolishaniid taxon from the middle Cambrian Burgess Shale (Walcott Quarry) in British Columbia, Canada, whose specialized morphology epitomizes the suspension-feeding ecology of this clade, and is convergent with some modern marine animals, such as caprellid crustaceans. This species possesses two long pairs and four shorter pairs of elongate spinose lobopods at the front, each bearing two slender claws, and three pairs of stout lobopods bearing single, strong, hook-like anterior-facing claws at the back. The trunk is remarkably bare, widening rearwards, and, at the front, extends beyond the first pair of lobopods into a small “head” bearing a pair of visual organs and a short proboscis with numerous teeth. Based on a critical reappraisal of character coding in lobopodians and using Bayesian and parsimony-based tree searches, two alternative scenarios for early panarthropod evolution are retrieved. In both cases, hallucigeniids and luolishaniids are found to be extinct radiative stem group panarthropods, in contrast to previous analyses supporting a position of hallucigeniids as part of total-group Onychophora. Our Bayesian topology finds luolishaniids and hallucigeniids to form two successive clades at the base of Panarthropoda. Disparity analyses suggest that luolishaniids, hallucigeniids and total-group Onychophora each occupy a distinct region of morphospace. CONCLUSIONS: Hallucigeniids and luolishaniids were comparably diverse and successful, representing two major lobopodian clades in the early Palaeozoic, and both evolved body plans adapted to different forms of suspension feeding. A Bayesian approach to cladistics supports the view that a semi-sessile, suspension-feeding lifestyle characterized the origin and rise of Panarthropoda from cycloneuralian body plans. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-016-0858-y) contains supplementary material, which is available to authorized users. BioMed Central 2017-01-31 /pmc/articles/PMC5282736/ /pubmed/28137244 http://dx.doi.org/10.1186/s12862-016-0858-y Text en © The Author(s). 2017 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.
spellingShingle Article
Caron, Jean-Bernard
Aria, Cédric
Cambrian suspension-feeding lobopodians and the early radiation of panarthropods
title Cambrian suspension-feeding lobopodians and the early radiation of panarthropods
title_full Cambrian suspension-feeding lobopodians and the early radiation of panarthropods
title_fullStr Cambrian suspension-feeding lobopodians and the early radiation of panarthropods
title_full_unstemmed Cambrian suspension-feeding lobopodians and the early radiation of panarthropods
title_short Cambrian suspension-feeding lobopodians and the early radiation of panarthropods
title_sort cambrian suspension-feeding lobopodians and the early radiation of panarthropods
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5282736/
https://www.ncbi.nlm.nih.gov/pubmed/28137244
http://dx.doi.org/10.1186/s12862-016-0858-y
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