Cited by 26Pregnancy and preeclampsia studiesEvolution and Genetic DynamicsReproductive System and Pregnancy

Genetic recapitulation of human pre-eclampsia risk during convergent evolution of reduced placental invasiveness in eutherian mammals

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Elliot, Michael G., Crespi, Bernard J.·2015·Philosophical Transactions of the Royal Society B: Biological Sciences

Abstract

The relationship between phenotypic variation arising through individual development and phenotypic variation arising through diversification of species has long been a central question in evolutionary biology. Among humans, reduced placental invasion into endometrial tissues is associated with diseases of pregnancy, especially pre-eclampsia, and reduced placental invasiveness has also evolved, convergently, in at least 10 lineages of eutherian mammals. We tested the hypothesis that a common genetic basis underlies both reduced placental invasion arising through a developmental process in human placental disease and reduced placental invasion found as a derived trait in the diversification of Euarchontoglires (rodents, lagomorphs, tree shrews, colugos and primates). Based on whole-genome analyses across 18 taxa, we identified 1254 genes as having evolved adaptively across all three lineages exhibiting independent evolutionary transitions towards reduced placental invasion. These genes showed strong evidence of enrichment for associations with pre-eclampsia, based on genetic-association studies, gene-expression analyses and gene ontology. We further used in silico prediction to identify a subset of 199 genes that are likely targets of natural selection during transitions in placental invasiveness and which are predicted to also underlie human placental disorders. Our results indicate that abnormal ontogenies can recapitulate major phylogenetic shifts in mammalian evolution, identify new candidate genes for involvement in pre-eclampsia, imply that study of species with less-invasive placentation will provide useful insights into the regulation of placental invasion and pre-eclampsia, and recommend a novel comparative functional-evolutionary approach to the study of genetically based human disease and mammalian diversification.

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Crossref · 10.1098/rstb.2014.0069

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  • Epitheliochorial placentation avoids many of the immunological and hemodynamic problems associated with invasive forms of placentation that underlie complications of human pregnancy such as pre-eclampsia.

    “Epitheliochorial placentation avoids many of the immunological and hemodynamic problems associated with the invasive forms that underlie complications of human pregnancy, such as pre-eclampsia, and these may have operated as selective pressures over the millennia (131, 170, 231).”

    From Placental Origins of Chronic Disease (2016) · cites this paper as [170]

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Authors
Elliot, M. G., & Crespi, B. J.
Affiliations
  • University of Cambridge (GB)
  • Simon Fraser University (CA)
Corresponding author
Elliot, Michael G.
Venue
Philosophical Transactions of the Royal Society B: Biological Sciences
Published
2015-03-05
Volume
370
Issue
1663
Pages
20140069
ISSN
  • 0962-8436 (ISSN-L)
  • 1471-2970
OpenAlex
W2017921408
Cited by
26
References
111
Citations by year
2025: 3 · 2024: 1 · 2023: 1 · 2022: 2 · 2021: 3 · 2020: 4 · 2019: 1 · 2017: 2 · 2016: 5 · 2015: 4
FWCI
4.16
Type
journal article
Language
en
Open access
Locations
  • Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
Topics
  • Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
  • Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
Keywords
preeclampsia, placental invasion, convergent evolution, placental mammals, Euarchontoglires, placental development, natural selection, candidate genes, placental disease, primates, colugos, tree shrew, lagomorphs
MeSH terms
Adaptation, Biological, Animals, Biological Evolution, Female, Genes, Humans, Mammals, Placenta Diseases, Pre-Eclampsia, Pregnancy, Selection, Genetic, Species Specificity, Genomics

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