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Single-cell atlases of two lophotrochozoan larvae highlight their complex evolutionary histories

Single-cell atlases of two lophotrochozoan larvae highlight their complex evolutionary histories
Single-cell atlases of two lophotrochozoan larvae highlight their complex evolutionary histories

Pelagic larval stages are widespread across animals, yet it is unclear whether larvae were present in the last common ancestor of animals or whether they evolved multiple times due to common selective pressures. Many marine larvae are at least superficially similar; they are small, swim through the beating of bands of cilia, and sense the environment with an apical organ. To understand these similarities, we have generated single-cell atlases for marine larvae from two animal phyla and have compared their cell types. We found clear similarities among ciliary band cells and between neurons of the apical organ in the two larvae pointing to possible homology of these structures, suggesting a single origin of larvae within Spiralia. We also find several clade-specific innovations in each larva, including distinct myocytes and shell gland cells in the oyster larva. Oyster shell gland cells express many recently evolved genes that have made previous gene age estimates for the origin of trochophore larvae too young.

Animals, Biological Evolution, Larva/physiology, Neurons
2375-2548
Piovani, Laura
812112fa-fc75-45f5-bed6-9d22ae38b0bf
Leite, Daniel J.
bbed475c-565b-4a75-bbeb-d6f1b53ba0f5
Yañez Guerra, Luis Alfonso
cbca947b-bbf0-4b91-96b0-4a126e3b94b6
Simpson, Fraser
614715ab-a068-4d5a-a18f-abb715c87a53
Musser, Jacob M.
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Salvador-Martínez, Irepan
db75cd79-95bf-4b51-a2a2-e36f182926a4
Marlétaz, Ferdinand
d44c06df-bb2e-431f-ab7c-20ff38256475
Jékely, Gáspár
94f0485f-2d93-4df4-b287-1e5b01295578
Telford, Maximilian J.
20523b3d-a698-43ec-92bc-1b28a32bcd4d
Piovani, Laura
812112fa-fc75-45f5-bed6-9d22ae38b0bf
Leite, Daniel J.
bbed475c-565b-4a75-bbeb-d6f1b53ba0f5
Yañez Guerra, Luis Alfonso
cbca947b-bbf0-4b91-96b0-4a126e3b94b6
Simpson, Fraser
614715ab-a068-4d5a-a18f-abb715c87a53
Musser, Jacob M.
d2e0d886-3dac-41a2-a043-b5c55ecd221b
Salvador-Martínez, Irepan
db75cd79-95bf-4b51-a2a2-e36f182926a4
Marlétaz, Ferdinand
d44c06df-bb2e-431f-ab7c-20ff38256475
Jékely, Gáspár
94f0485f-2d93-4df4-b287-1e5b01295578
Telford, Maximilian J.
20523b3d-a698-43ec-92bc-1b28a32bcd4d

Piovani, Laura, Leite, Daniel J., Yañez Guerra, Luis Alfonso, Simpson, Fraser, Musser, Jacob M., Salvador-Martínez, Irepan, Marlétaz, Ferdinand, Jékely, Gáspár and Telford, Maximilian J. (2023) Single-cell atlases of two lophotrochozoan larvae highlight their complex evolutionary histories. Science Advances, 9 (31), [eadg6034]. (doi:10.1126/sciadv.adg6034).

Record type: Article

Abstract

Pelagic larval stages are widespread across animals, yet it is unclear whether larvae were present in the last common ancestor of animals or whether they evolved multiple times due to common selective pressures. Many marine larvae are at least superficially similar; they are small, swim through the beating of bands of cilia, and sense the environment with an apical organ. To understand these similarities, we have generated single-cell atlases for marine larvae from two animal phyla and have compared their cell types. We found clear similarities among ciliary band cells and between neurons of the apical organ in the two larvae pointing to possible homology of these structures, suggesting a single origin of larvae within Spiralia. We also find several clade-specific innovations in each larva, including distinct myocytes and shell gland cells in the oyster larva. Oyster shell gland cells express many recently evolved genes that have made previous gene age estimates for the origin of trochophore larvae too young.

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Accepted/In Press date: 30 June 2023
Published date: 2 August 2023
Additional Information: Funding Information: This work was supported by the European Union’s Horizon 2020 research and innovation program under the Marie Skłodowska-Curie (grant agreement number 766053 EvoCELL: grant to M.J.T. and fellowship to L.P.), Leverhulme Trust Research Project (grant number RPG-2018302 to M.J.T. and fellowship to D.J.L. and grant number RPG-2021-436 to F.M. supporting L.P.), Biotechnology and Biological Sciences Research Council (grant BB/W010305/1 to L.A.Y.G. and grant BB/V01109X/1 to F.M. supporting L.P.), and Royal Society University Research Fellowship (grant number URF\R1\191161 to F.M.).
Keywords: Animals, Biological Evolution, Larva/physiology, Neurons

Identifiers

Local EPrints ID: 483253
URI: http://eprints.soton.ac.uk/id/eprint/483253
ISSN: 2375-2548
PURE UUID: 3087a879-c5f3-4401-8ef3-bca43d9cd03d
ORCID for Luis Alfonso Yañez Guerra: ORCID iD orcid.org/0000-0002-2523-1310

Catalogue record

Date deposited: 26 Oct 2023 17:04
Last modified: 18 Mar 2024 04:15

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Contributors

Author: Laura Piovani
Author: Daniel J. Leite
Author: Luis Alfonso Yañez Guerra ORCID iD
Author: Fraser Simpson
Author: Jacob M. Musser
Author: Irepan Salvador-Martínez
Author: Ferdinand Marlétaz
Author: Gáspár Jékely
Author: Maximilian J. Telford

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