Extended embryo retention and viviparity in the first amniotes

Baoyu Jiang; Yiming He; Armin Elsler; Shengyu Wang; Joseph N Keating; Junyi Song; Stuart L Kearns; Michael J Benton

doi:10.1038/s41559-023-02074-0

Extended embryo retention and viviparity in the first amniotes

Baoyu Jiang, Yiming He, Armin Elsler, Shengyu Wang, Joseph N Keating, Junyi Song, Stuart L Kearns, Michael J Benton

Research output: Contribution to journal › Article (Academic Journal) › peer-review

12 Citations (Scopus)

Abstract

The amniotic egg with its complex fetal membranes was a key innovation in vertebrate evolution that enabled the great diversification of reptiles, birds and mammals. It is debated whether these fetal membranes evolved in eggs on land as an adaptation to the terrestrial environment or to control antagonistic fetal-maternal interaction in association with extended embryo retention (EER). Here we report an oviparous choristodere from the Lower Cretaceous period of northeast China. The ossification sequence of the embryo confirms that choristoderes are basal archosauromorphs. The discovery of oviparity in this assumed viviparous extinct clade, together with existing evidence, suggests that EER was the primitive reproductive mode in basal archosauromorphs. Phylogenetic comparative analyses on extant and extinct amniotes suggest that the first amniote displayed EER (including viviparity).

Original language	English
Pages (from-to)	1131-1140
Number of pages	10
Journal	Nature Ecology and Evolution
Volume	7
Issue number	7
Early online date	12 Jun 2023
DOIs	https://doi.org/10.1038/s41559-023-02074-0
Publication status	E-pub ahead of print - 12 Jun 2023

Bibliographical note

Funding Information:
We thank C. O’Donovan, M. Pagel, G. Ruxton and M. Sakamoto for discussions during the course of this study, and M. Laurin and G. Wagner for comments. B.J. was supported by the National Science Foundation of China (award no. 42288201), Strategic Priority Research Program (B) of the Chinese Academy of Sciences (award no. XDB26000000) and Fundamental Research Funds for the Central Universities (award no. 0206-14380137). M.J.B. was funded by a Natural Environment Research Council (NERC) UK (grant no. NE/P013724/1) and European Research Council Advanced Grant (no. 788203). A.E. was funded by NERC UK grant nos. NE/L002434/1 and NE/P013724/1. This work was carried out using the computational facilities of the Advanced Computing Research Centre, University of Bristol ( http://www.bris.ac.uk/acrc/ ).

Funding Information:
We thank C. O’Donovan, M. Pagel, G. Ruxton and M. Sakamoto for discussions during the course of this study, and M. Laurin and G. Wagner for comments. B.J. was supported by the National Science Foundation of China (award no. 42288201), Strategic Priority Research Program (B) of the Chinese Academy of Sciences (award no. XDB26000000) and Fundamental Research Funds for the Central Universities (award no. 0206-14380137). M.J.B. was funded by a Natural Environment Research Council (NERC) UK (grant no. NE/P013724/1) and European Research Council Advanced Grant (no. 788203). A.E. was funded by NERC UK grant nos. NE/L002434/1 and NE/P013724/1. This work was carried out using the computational facilities of the Advanced Computing Research Centre, University of Bristol (http://www.bris.ac.uk/acrc/).

Publisher Copyright:
© 2023, The Author(s).

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title = "Extended embryo retention and viviparity in the first amniotes",

abstract = "The amniotic egg with its complex fetal membranes was a key innovation in vertebrate evolution that enabled the great diversification of reptiles, birds and mammals. It is debated whether these fetal membranes evolved in eggs on land as an adaptation to the terrestrial environment or to control antagonistic fetal-maternal interaction in association with extended embryo retention (EER). Here we report an oviparous choristodere from the Lower Cretaceous period of northeast China. The ossification sequence of the embryo confirms that choristoderes are basal archosauromorphs. The discovery of oviparity in this assumed viviparous extinct clade, together with existing evidence, suggests that EER was the primitive reproductive mode in basal archosauromorphs. Phylogenetic comparative analyses on extant and extinct amniotes suggest that the first amniote displayed EER (including viviparity).",

author = "Baoyu Jiang and Yiming He and Armin Elsler and Shengyu Wang and Keating, {Joseph N} and Junyi Song and Kearns, {Stuart L} and Benton, {Michael J}",

note = "Funding Information: We thank C. O{\textquoteright}Donovan, M. Pagel, G. Ruxton and M. Sakamoto for discussions during the course of this study, and M. Laurin and G. Wagner for comments. B.J. was supported by the National Science Foundation of China (award no. 42288201), Strategic Priority Research Program (B) of the Chinese Academy of Sciences (award no. XDB26000000) and Fundamental Research Funds for the Central Universities (award no. 0206-14380137). M.J.B. was funded by a Natural Environment Research Council (NERC) UK (grant no. NE/P013724/1) and European Research Council Advanced Grant (no. 788203). A.E. was funded by NERC UK grant nos. NE/L002434/1 and NE/P013724/1. This work was carried out using the computational facilities of the Advanced Computing Research Centre, University of Bristol ( http://www.bris.ac.uk/acrc/ ). Funding Information: We thank C. O{\textquoteright}Donovan, M. Pagel, G. Ruxton and M. Sakamoto for discussions during the course of this study, and M. Laurin and G. Wagner for comments. B.J. was supported by the National Science Foundation of China (award no. 42288201), Strategic Priority Research Program (B) of the Chinese Academy of Sciences (award no. XDB26000000) and Fundamental Research Funds for the Central Universities (award no. 0206-14380137). M.J.B. was funded by a Natural Environment Research Council (NERC) UK (grant no. NE/P013724/1) and European Research Council Advanced Grant (no. 788203). A.E. was funded by NERC UK grant nos. NE/L002434/1 and NE/P013724/1. This work was carried out using the computational facilities of the Advanced Computing Research Centre, University of Bristol (http://www.bris.ac.uk/acrc/). Publisher Copyright: {\textcopyright} 2023, The Author(s).",

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doi = "10.1038/s41559-023-02074-0",

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AU - Jiang, Baoyu

AU - He, Yiming

AU - Elsler, Armin

AU - Wang, Shengyu

AU - Keating, Joseph N

AU - Song, Junyi

AU - Kearns, Stuart L

AU - Benton, Michael J

N1 - Funding Information: We thank C. O’Donovan, M. Pagel, G. Ruxton and M. Sakamoto for discussions during the course of this study, and M. Laurin and G. Wagner for comments. B.J. was supported by the National Science Foundation of China (award no. 42288201), Strategic Priority Research Program (B) of the Chinese Academy of Sciences (award no. XDB26000000) and Fundamental Research Funds for the Central Universities (award no. 0206-14380137). M.J.B. was funded by a Natural Environment Research Council (NERC) UK (grant no. NE/P013724/1) and European Research Council Advanced Grant (no. 788203). A.E. was funded by NERC UK grant nos. NE/L002434/1 and NE/P013724/1. This work was carried out using the computational facilities of the Advanced Computing Research Centre, University of Bristol ( http://www.bris.ac.uk/acrc/ ). Funding Information: We thank C. O’Donovan, M. Pagel, G. Ruxton and M. Sakamoto for discussions during the course of this study, and M. Laurin and G. Wagner for comments. B.J. was supported by the National Science Foundation of China (award no. 42288201), Strategic Priority Research Program (B) of the Chinese Academy of Sciences (award no. XDB26000000) and Fundamental Research Funds for the Central Universities (award no. 0206-14380137). M.J.B. was funded by a Natural Environment Research Council (NERC) UK (grant no. NE/P013724/1) and European Research Council Advanced Grant (no. 788203). A.E. was funded by NERC UK grant nos. NE/L002434/1 and NE/P013724/1. This work was carried out using the computational facilities of the Advanced Computing Research Centre, University of Bristol (http://www.bris.ac.uk/acrc/). Publisher Copyright: © 2023, The Author(s).

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N2 - The amniotic egg with its complex fetal membranes was a key innovation in vertebrate evolution that enabled the great diversification of reptiles, birds and mammals. It is debated whether these fetal membranes evolved in eggs on land as an adaptation to the terrestrial environment or to control antagonistic fetal-maternal interaction in association with extended embryo retention (EER). Here we report an oviparous choristodere from the Lower Cretaceous period of northeast China. The ossification sequence of the embryo confirms that choristoderes are basal archosauromorphs. The discovery of oviparity in this assumed viviparous extinct clade, together with existing evidence, suggests that EER was the primitive reproductive mode in basal archosauromorphs. Phylogenetic comparative analyses on extant and extinct amniotes suggest that the first amniote displayed EER (including viviparity).

AB - The amniotic egg with its complex fetal membranes was a key innovation in vertebrate evolution that enabled the great diversification of reptiles, birds and mammals. It is debated whether these fetal membranes evolved in eggs on land as an adaptation to the terrestrial environment or to control antagonistic fetal-maternal interaction in association with extended embryo retention (EER). Here we report an oviparous choristodere from the Lower Cretaceous period of northeast China. The ossification sequence of the embryo confirms that choristoderes are basal archosauromorphs. The discovery of oviparity in this assumed viviparous extinct clade, together with existing evidence, suggests that EER was the primitive reproductive mode in basal archosauromorphs. Phylogenetic comparative analyses on extant and extinct amniotes suggest that the first amniote displayed EER (including viviparity).

U2 - 10.1038/s41559-023-02074-0

DO - 10.1038/s41559-023-02074-0

M3 - Article (Academic Journal)

C2 - 37308704

SN - 2397-334X

VL - 7

SP - 1131

EP - 1140

JO - Nature Ecology and Evolution

JF - Nature Ecology and Evolution

IS - 7

ER -

Extended embryo retention and viviparity in the first amniotes

Abstract

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