Musculature of an Early Cambrian cycloneuralian animal

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Abstract

Cycloneuralians are ecdysozoans with a fossil record extending to the Early Cambrian Fortunian Age and represented mostly by cuticular integuments. However, internal anatomies of Fortunian cycloneuralians are virtually unknown, hampering our understanding of their functional morphology and phylogenetic relationships. Here we report the exceptional preservation of cycloneuralian introvert musculature in Fortunian rocks of South China. The musculature consists of an introvert body-wall muscular grid of four circular and 36 radially arranged longitudinal muscle bundles, as well as an introvert circular muscle associated with 19 roughly radially arranged, short retractors. Collectively, these features support at least a scalidophoran affinity, and the absence of muscles associated with a mouth cone and scalids further indicates a priapulan affinity. As in modern scalidophorans, the fossil musculature, and particularly the introvert circular muscle retractors, may have controlled introvert inversion and facilitated locomotion and feeding. This work supports the evolution of scalidophoran-like or priapulan-like introvert musculature in cycloneuralians at the beginning of the Cambrian Period.

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Molecular timetrees reveal a Cambrian colonization of land and a new scenario for ecdysozoan evolution.

Omar Rota-Stabelli, Allison C. Daley, Davide Pisani (2013)

Ecdysozoans have been key components of ecosystems since the early Cambrian, when trilobites and soft-bodied Burgess Shale-type ecdysozoans dominated marine animal communities. Even today, the most abundant animals on Earth are either nematode worms or plankton-forming crustaceans, whereas the most diverse are the insects. Throughout geological time, several ecdysozoan lineages independently colonized land, shaping both marine and terrestrial ecosystems and providing an adequate environment for successive animal terrestrialization. The timing of these events is largely uncertain and has been investigated only partially using molecular data. Here we present a timescale of ecdysozoan evolution based on multiple molecular data sets, the most complete set of fossil calibrations to date, and a thorough series of validation analyses. Results converge on an Ediacaran origin of all major ecdysozoan lineages (∼587-543 million years ago [mya]), followed by a fast Cambrian radiation of the pancrustaceans (∼539-511 mya), a Cambro-Ordovician colonization of land of different arthropod lineages (∼510-471 mya), and a relatively recent radiation of extant nematodes, onychophorans, and tardigrades (∼442 mya). Arthropods colonized land nearly synchronously with land plants. Further diversification within flying insects, nematodes and onychophorans might be related to the evolution of vascular plants and forests. Copyright © 2013 Elsevier Ltd. All rights reserved.

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Independent evolution of striated muscles in cnidarians and bilaterians

Patrick R.H. Steinmetz, Johanna E.M. Kraus, Claire Larroux … (2012)

Striated muscles are present in bilaterian animals (e.g. vertebrates, insects, annelids) and some non-bilaterian eumetazoans (i.e. cnidarians and ctenophores). The striking ultrastructural similarity of striated muscles between these animal groups is thought to reflect a common evolutionary origin 1, 2 . Here we show that a muscle protein core set, including a Myosin type II Heavy Chain motor protein characteristic of striated muscles in vertebrates (MyHC-st), was already present in unicellular organisms before the origin of multicellular animals. Furthermore, myhc-st and myhc-non-muscle (myhc-nm) orthologues are expressed differentially in two sponges, compatible with the functional diversification of myhc paralogues before the origin of true muscles and the subsequent deployment of MyHC-st in fast-contracting smooth and striated muscle. Cnidarians and ctenophores possess myhc-st orthologues but lack crucial components of bilaterian striated muscles, such as troponin complex and titin genes, suggesting the convergent evolution of striated muscles. Consistently, jellyfish orthologues of a shared set of bilaterian z-disc proteins are not associated with striated muscles, but are instead expressed elsewhere or ubiquitously. The independent evolution of eumetazoan striated muscles through the addition of novel proteins to a pre-existing, ancestral contractile apparatus may serve as a paradigm for the evolution of complex animal cell types.

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Complex brain and optic lobes in an early Cambrian arthropod.

Xiaoya Ma, Xianguang Hou, Gregory Edgecombe … (2012)

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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Author and article information

Contributors

Huaqiao Zhang:

ORCID: http://orcid.org/0000-0002-1241-0088

Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing

Shuhai Xiao:

ORCID: http://orcid.org/0000-0003-4655-2663

Role: Formal analysisRole: Funding acquisitionRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – review & editing

Mats E. Eriksson:

ORCID: http://orcid.org/0000-0001-8200-5152

Role: Formal analysisRole: Funding acquisitionRole: ValidationRole: VisualizationRole: Writing – review & editing

Baichuan Duan:

ORCID: http://orcid.org/0000-0003-2188-598X

Role: Formal analysisRole: MethodologyRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – review & editing

Andreas Maas: Role: Formal analysisRole: ValidationRole: VisualizationRole: Writing – review & editing

Journal

Journal ID (nlm-ta): Proc Biol Sci

Journal ID (iso-abbrev): Proc Biol Sci

Journal ID (publisher-id): RSPB

Journal ID (hwp): royprsb

Title: Proceedings of the Royal Society B: Biological Sciences

Publisher: The Royal Society

ISSN (Print): 0962-8452

ISSN (Electronic): 1471-2954

Publication date (Electronic, pub): October 11, 2023

Publication date (Electronic, collection): October 2023

Publication date PMC-release: October 11, 2023

Volume: 290

Issue: 2008

Electronic Location Identifier: 20231803

Affiliations

[ ¹ ] State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, , Nanjing 210008, People's Republic of China

[ ² ] Department of Geosciences, Virginia Tech, , Blacksburg, VA 24061, USA

[ ³ ] Department of Geology, Lund University, , Lund 22362, Sweden

[ ⁴ ] Key Laboratory of Marine Geology and Metallogeny, First Institute of Oceanography, Ministry of Natural Resource, , Qingdao 266061, People's Republic of China

[ ⁵ ] Galgenackerweg 25, Blaustein 89134, Germany,

Author notes

Electronic supplementary material is available online at https://doi.org/10.6084/m9.figshare.c.6858151.

Author information

Huaqiao Zhang http://orcid.org/0000-0002-1241-0088

Shuhai Xiao http://orcid.org/0000-0003-4655-2663

Mats E. Eriksson http://orcid.org/0000-0001-8200-5152

Baichuan Duan http://orcid.org/0000-0003-2188-598X

Article

Publisher ID: rspb20231803

DOI: 10.1098/rspb.2023.1803

PMC ID: 10565385

PubMed ID: 37817588

SO-VID: 4aea9284-7362-4fe3-bc49-f6c38db2aebc

License:

Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

History

Date received : August 10, 2023

Date accepted : September 18, 2023

Funding

Funded by: U.S. National Science Foundation;

Award ID: EAR-2021207

Funded by: Swedish Research Council;

Award ID: 2019-03516

Funded by: Key R&D Program of China;

Award ID: 2022YFF0802700

Funded by: National Natural Science Foundation of China, http://dx.doi.org/10.13039/501100001809;

Award ID: 41921002

Award ID: 42130206

Award ID: 42172020

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