Placental invasion, preeclampsia risk and adaptive molecular evolution at the origin of the great apes: Evidence from genome-wide analyses
Abstract
Introduction Recent evidence from chimpanzees and gorillas has raised doubts that preeclampsia is a uniquely human disease. The deep extravillous trophoblast (EVT) invasion and spiral artery remodeling that characterizes our placenta (and is abnormal in preeclampsia) is shared within great apes, setting Homininae apart from Hylobatidae and Old World Monkeys, which show much shallower trophoblast invasion and limited spiral artery remodeling. We hypothesize that the evolution of a more invasive placenta in the lineage ancestral to the great apes involved positive selection on genes crucial to EVT invasion and spiral artery remodeling. Furthermore, identification of placentally-expressed genes under selection in this lineage may identify novel genes involved in placental development.Methods We tested for positive selection in approximately 18,000 genes using the ratio of non-synonymous to synonymous amino acid substitution for protein-coding DNA. DAVID Bioinformatics Resources identified biological processes enriched in positively selected genes, including processes related to EVT invasion and spiral artery remodeling.Results Analyses revealed 295 and 264 genes under significant positive selection on the branches ancestral to Hominidae (Human, Chimp, Gorilla, Orangutan) and Homininae (Human, Chimp, Gorilla), respectively. Gene ontology analysis of these gene sets demonstrated significant enrichments for several functional gene clusters relevant to preeclampsia risk, and sets of placentally-expressed genes that have been linked with preeclampsia and/or trophoblast invasion in other studies.Conclusion Our study represents a novel approach to the identification of candidate genes and amino acid residues involved in placental pathologies by implicating them in the evolution of highly-invasive placenta.
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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 [131]
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- Authors
- Crosley, E. J., Elliot, M. G., Christians, J. K., & Crespi, B. J.
- Affiliations
- Simon Fraser University (CA)
- Corresponding author
- Crosley, E.J.
- Venue
- Placenta
- Publisher
- Elsevier BV
- Published
- 2013-02
- Volume
- 34
- Issue
- 2
- Pages
- 127-132
- ISSN
- 0143-4004 (ISSN-L)
- OpenAlex
- W2145203015
- Cited by
- 62
- References
- 63
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 3 · 2023: 3 · 2022: 1 · 2021: 5 · 2020: 4 · 2019: 8 · 2018: 8 · 2017: 4 · 2016: 5 · 2015: 6 · 2014: 6 · 2013: 3
- FWCI
- 5.76
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Placenta (publishedVersion)
- PubMed (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- Funders
- Canadian Institutes of Health Research
- 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
- placental invasion, extravillous trophoblast invasion, spiral artery remodeling, preeclampsia, Hominidae, Homininae, positive selection, adaptive molecular evolution, placental development, comparative genomics
- MeSH terms
- Animals, Pan troglodytes, Female, Gorilla gorilla, Humans, Phylogeny, Placentation, Pre-Eclampsia, Pregnancy, Risk Factors, Selection, Genetic, Trophoblasts, Hominidae, Ape Diseases, Evolution, Molecular, Genome-Wide Association Study, Uterine Artery, Pongo
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