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Placental evolution from a three-dimensional and multiscale structural perspective

Placental evolution from a three-dimensional and multiscale structural perspective
Placental evolution from a three-dimensional and multiscale structural perspective

The placenta mediates physiological exchange between the mother and the fetus. In placental mammals, all placentas are descended from a single common ancestor and functions are conserved across species; however, the placenta exhibits radical structural diversity. The selective pressures behind this structural diversity are poorly understood. Traditionally, placental structures have largely been investigated by grouping them into qualitative categories. Assessing the placenta on this basis could be problematic when inferring the relative "efficiency"of a placental configuration to transfer nutrients from mother to fetus. We argue that only by considering placentas as three-dimensional (3D) biological structures, integrated across scales, can the evolutionary questions behind their enormous structural diversity be quantitatively determined. We review the current state of placental evolution from a structural perspective, detail where 3D imaging and computational modeling have been used to gain insight into placental function, and outline an experimental roadmap to answer evolutionary questions from a multiscale 3D structural perspective. Our approach aims to shed light on placental evolution, and can be transferred to evolutionary investigations in any organ system.

evolution, mammal, microscopy, placenta, three-dimensional
0014-3820
13-25
Laundon, Davis
b2ba5687-d949-47dd-b84f-fb3c0c032550
Gostling, Neil J.
4840aa40-cb6c-4112-a0b9-694a869523fc
Sengers, Bram G.
d6b771b1-4ede-48c5-9644-fa86503941aa
Chavatte-Palmer, Pascale
3b1ff263-828e-4f55-ab66-13168e3ed45f
Lewis, Rohan M.
caaeb97d-ea69-4f7b-8adb-5fa25e2d3502
Laundon, Davis
b2ba5687-d949-47dd-b84f-fb3c0c032550
Gostling, Neil J.
4840aa40-cb6c-4112-a0b9-694a869523fc
Sengers, Bram G.
d6b771b1-4ede-48c5-9644-fa86503941aa
Chavatte-Palmer, Pascale
3b1ff263-828e-4f55-ab66-13168e3ed45f
Lewis, Rohan M.
caaeb97d-ea69-4f7b-8adb-5fa25e2d3502

Laundon, Davis, Gostling, Neil J., Sengers, Bram G., Chavatte-Palmer, Pascale and Lewis, Rohan M. (2024) Placental evolution from a three-dimensional and multiscale structural perspective. Evolution, 78 (1), 13-25, [qpad209]. (doi:10.1093/evolut/qpad209).

Record type: Article

Abstract

The placenta mediates physiological exchange between the mother and the fetus. In placental mammals, all placentas are descended from a single common ancestor and functions are conserved across species; however, the placenta exhibits radical structural diversity. The selective pressures behind this structural diversity are poorly understood. Traditionally, placental structures have largely been investigated by grouping them into qualitative categories. Assessing the placenta on this basis could be problematic when inferring the relative "efficiency"of a placental configuration to transfer nutrients from mother to fetus. We argue that only by considering placentas as three-dimensional (3D) biological structures, integrated across scales, can the evolutionary questions behind their enormous structural diversity be quantitatively determined. We review the current state of placental evolution from a structural perspective, detail where 3D imaging and computational modeling have been used to gain insight into placental function, and outline an experimental roadmap to answer evolutionary questions from a multiscale 3D structural perspective. Our approach aims to shed light on placental evolution, and can be transferred to evolutionary investigations in any organ system.

Text
qpad209 - Accepted Manuscript
Available under License Creative Commons Attribution.
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More information

e-pub ahead of print date: 17 November 2023
Published date: January 2024
Additional Information: Funding Information: This work was supported by the Leverhulme Trust grant number RPG-2019-208. Publisher Copyright: © 2023 The Author(s). Published by Oxford University Press on behalf of The Society for the Study of Evolution (SSE).
Keywords: evolution, mammal, microscopy, placenta, three-dimensional

Identifiers

Local EPrints ID: 484959
URI: http://eprints.soton.ac.uk/id/eprint/484959
ISSN: 0014-3820
PURE UUID: 31bff6aa-4d54-4de6-b859-da0cefa05ed8
ORCID for Davis Laundon: ORCID iD orcid.org/0000-0002-1508-664X
ORCID for Neil J. Gostling: ORCID iD orcid.org/0000-0002-5960-7769
ORCID for Bram G. Sengers: ORCID iD orcid.org/0000-0001-5859-6984
ORCID for Rohan M. Lewis: ORCID iD orcid.org/0000-0003-4044-9104

Catalogue record

Date deposited: 27 Nov 2023 17:32
Last modified: 20 Feb 2024 03:13

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Contributors

Author: Davis Laundon ORCID iD
Author: Bram G. Sengers ORCID iD
Author: Pascale Chavatte-Palmer
Author: Rohan M. Lewis ORCID iD

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