Gene expression phylogenies and ancestral transcriptome reconstruction resolves major transitions in the origins of pregnancy

  1. Katelyn Mika
  2. Camilla M Whittington
  3. Bronwyn M McAllan
  4. Vincent J Lynch  Is a corresponding author
  1. University of Chicago, United States
  2. University of Sydney, Australia
  3. University at Buffalo, State University of New York, United States

Abstract

Structural and physiological changes in the female reproductive system underlie the origins of pregnancy in multiple vertebrate lineages. In mammals, the glandular portion of the lower reproductive tract has transformed into a structure specialized for supporting fetal development. These specializations range from relatively simple maternal nutrient provisioning in egg-laying monotremes to an elaborate suite of traits that support intimate maternal-fetal interactions in Eutherians. Among these traits are the maternal decidua and fetal component of the placenta, but there is considerable uncertainty about how these structures evolved. Previously we showed that changes in uterine gene expression contributes to several evolutionary innovations during the origins of pregnancy (Marinic, Mika, and Lynch 2021). Here we reconstruct the evolution of entire transcriptomes ('ancestral transcriptome reconstruction') and show that maternal gene expression profiles are correlated with degree of placental invasion. These results indicate that an epitheliochorial-like placenta evolved early in the mammalian stem-lineage and that the ancestor of Eutherians had a hemochorial placenta, and suggest maternal control of placental invasiveness. These data resolve major transitions in the evolution of pregnancy and indicate that ancestral transcriptome reconstruction can be used to study the function of ancestral cell, tissue, and organ systems.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting file; Source Data files have been provided for Figures 2, 3 and 5.

Article and author information

Author details

  1. Katelyn Mika

    Department of Human Genetics, University of Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2170-9364
  2. Camilla M Whittington

    School of Life and Environmental Sciences, University of Sydney, Sydney, Australia
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5765-9699
  3. Bronwyn M McAllan

    School of Life and Environmental Sciences, University of Sydney, Sydney, Australia
    Competing interests
    The authors declare that no competing interests exist.
  4. Vincent J Lynch

    Department of Biological Sciences, University at Buffalo, State University of New York, Buffalo, United States
    For correspondence
    vjlynch@buffalo.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5311-3824

Funding

March of Dimes Foundation

  • Vincent J Lynch

Burroughs Wellcome Fund (1013760)

  • Vincent J Lynch

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Antonis Rokas, Vanderbilt University, United States

Version history

  1. Preprint posted: September 27, 2021 (view preprint)
  2. Received: September 30, 2021
  3. Accepted: June 29, 2022
  4. Accepted Manuscript published: June 30, 2022 (version 1)
  5. Version of Record published: July 12, 2022 (version 2)

Copyright

© 2022, Mika et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Katelyn Mika
  2. Camilla M Whittington
  3. Bronwyn M McAllan
  4. Vincent J Lynch
(2022)
Gene expression phylogenies and ancestral transcriptome reconstruction resolves major transitions in the origins of pregnancy
eLife 11:e74297.
https://doi.org/10.7554/eLife.74297

Share this article

https://doi.org/10.7554/eLife.74297

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