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Comparative genomics of hormonal signaling in the chorioallantoic membrane of oviparous and viviparous amniotes.
Abstract: In oviparous amniotes (reptiles, birds, and mammals) the chorioallantoic membrane (CAM) lines the inside of the egg and acts as the living point of contact between the embryo and the outside world. In livebearing (viviparous) amniotes, communication during embryonic development occurs across placental tissues, which form between the uterine tissue of the mother and the CAM of the embryo. In both oviparous and viviparous taxa, the CAM is at the interface of the embryo and the external environment and can transfer signals from there to the embryo proper. To understand the evolution of placental hormone production in amniotes, we examined the expression of genes involved in hormone synthesis, metabolism, and hormone receptivity in the CAM of species across the amniote phylogeny. We collected transcriptome data for the chorioallantoic membranes of the chicken (oviparous), the lizards Lerista bougainvillii (both oviparous and viviparous populations) and Pseudemoia entrecasteauxii (viviparous), and the horse Equus caballus (viviparous). The viviparous taxa differ in their mechanisms of nutrient provisioning: L. bougainvillii is lecithotrophic (embryonic nourishment is provided via the yolk only), but P. entrecasteauxii and the horse are placentotrophic (embryos are nourished via placental transport). Of the 423 hormone-related genes that we examined, 91 genes are expressed in all studied species, suggesting that the chorioallantoic membrane ancestrally had an endocrine function. Therefore, the chorioallantoic membrane appears to be a highly hormonally active organ in all amniotes. No genes are expressed only in viviparous species, suggesting that the evolution of viviparity has not required the recruitment of any specific hormone-related genes. Our data suggest that the endocrine function of the CAM as a placental tissue evolved in part through co-option of ancestral gene expression patterns.
Copyright © 2016 Elsevier Inc. All rights reserved.
Publication Date: 2016-04-19 PubMed ID: 27102939DOI: 10.1016/j.ygcen.2016.04.017Google Scholar: Lookup The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
Summary
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The research focuses on understanding the evolution of placental hormone production in amniotes. It provides a comparative genomic analysis of hormonal signaling in the chorioallantoic membrane (CAM) of egg-laying and live-bearing species. The researchers studied the gene expression related to hormone synthesis and metabolism in various species and concluded that the CAM likely had an ancestral endocrine function, and no new hormones were required for the evolution of live-birth.
Hormonal Signaling in Chorioallantoic Membrane
- The study is centered around the chorioallantoic membrane (CAM), a crucial organ lining the inside of the egg in oviparous, or egg-laying species (like reptiles, birds, and certain mammals), and acting as a connection point between the fetus and the mother in viviparous, or live-bearing species (like humans and horses).
- The CAM acts as a medium for communication during embryonic development, transferring signals from the external environment to the embryo.
Exploring Evolution of Hormonal Production
- The objective of this study was to understand how placental hormone production, a critical aspect of embryonic nourishment and development, evolved in amniotes, a group including most mammals, birds, and reptiles.
- The researchers looked into the expression of genes that are involved with hormone synthesis, processing, and receptivity. They did this by collecting transcriptome data from the CAMs of a chicken, two types of lizards (one species has both egg-laying and live-bearing populations, while the other is purely live-bearing), and a horse.
- Through this data, they studied the similarities and differences in gene expression across these species to draw conclusions about the evolutionary process.
Insights from the Research
- The primary finding was that out of 423 hormone-related genes, 91 were expressed in all studied species. This suggests that the CAM ancestrally had an endocrine function and was a highly hormonal active organ in everyone.
- Moreover, no genes were found to be expressed solely in live-bearing species. This implies that the evolution from egg-laying to live-birth did not require the involvement of any new hormone-related genes.
- This research indicates that the hormonal function of the CAM as a part of the placental tissue possibly evolved through the co-option of existing gene expression patterns, instead of the development of entirely new ones.
Cite This Article
APA
Griffith OW, Brandley MC, Whittington CM, Belov K, Thompson MB.
(2016).
Comparative genomics of hormonal signaling in the chorioallantoic membrane of oviparous and viviparous amniotes.
Gen Comp Endocrinol, 244, 19-29.
https://doi.org/10.1016/j.ygcen.2016.04.017 Publication
Researcher Affiliations
- School of Life and Environmental Sciences, Heydon-Laurence Building, University of Sydney, Sydney, NSW 2006, Australia; Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT, United States. Electronic address: oliver.griffith@yale.edu.
- School of Life and Environmental Sciences, Heydon-Laurence Building, University of Sydney, Sydney, NSW 2006, Australia; New York University - Sydney, The Rocks, NSW 2000, Australia.
- School of Life and Environmental Sciences, Heydon-Laurence Building, University of Sydney, Sydney, NSW 2006, Australia; Faculty of Veterinary Science, University of Sydney, Sydney, NSW 2006, Australia.
- Faculty of Veterinary Science, University of Sydney, Sydney, NSW 2006, Australia.
- School of Life and Environmental Sciences, Heydon-Laurence Building, University of Sydney, Sydney, NSW 2006, Australia.
MeSH Terms
- Animals
- Chickens
- Chorioallantoic Membrane / metabolism
- Female
- Genomics
- Horses
- Lizards
- Mammals
- Oviparity / physiology
- Pregnancy
- Signal Transduction
Citations
This article has been cited 13 times.- Whittington CM, Buddle AL, Griffith OW, Carter AM. Embryonic specializations for vertebrate placentation. Philos Trans R Soc Lond B Biol Sci 2022 Dec 5;377(1865):20210261.
- Wen J, Ishihara T, Renfree MB, Griffith OW. Comparing the potential for maternal-fetal signalling in oviparous and viviparous lizards. Philos Trans R Soc Lond B Biol Sci 2022 Dec 5;377(1865):20210262.
- Whittington CM, Van Dyke JU, Liang SQT, Edwards SV, Shine R, Thompson MB, Grueber CE. Understanding the evolution of viviparity using intraspecific variation in reproductive mode and transitional forms of pregnancy. Biol Rev Camb Philos Soc 2022 Jun;97(3):1179-1192.
- Kumar N, Lohrentz A, Gahr M, Groothuis TGG. Steroid receptors and their regulation in avian extraembryonic membranes provide a novel substrate for hormone mediated maternal effects. Sci Rep 2019 Aug 8;9(1):11501.
- Griffith OW, Chavan AR, Pavlicev M, Protopapas S, Callahan R, Maziarz J, Wagner GP. Endometrial recognition of pregnancy occurs in the grey short-tailed opossum ( Monodelphis domestica). Proc Biol Sci 2019 Jun 26;286(1905):20190691.
- Groothuis TGG, Hsu BY, Kumar N, Tschirren B. Revisiting mechanisms and functions of prenatal hormone-mediated maternal effects using avian species as a model. Philos Trans R Soc Lond B Biol Sci 2019 Apr 15;374(1770):20180115.
- Carter AM. Recent advances in understanding evolution of the placenta: insights from transcriptomics. F1000Res 2018;7:89.
- Griffith OW, Chavan AR, Protopapas S, Maziarz J, Romero R, Wagner GP. Embryo implantation evolved from an ancestral inflammatory attachment reaction. Proc Natl Acad Sci U S A 2017 Aug 8;114(32):E6566-E6575.
- Whittington CM, Danastas K, Grau GE, Murphy CR, Thompson MB. Expression of VEGF (111) and other VEGF-A variants in the rat uterus is correlated with stage of pregnancy. J Comp Physiol B 2017 Feb;187(2):353-360.
- Griffith OW, Brandley MC, Belov K, Thompson MB. Reptile Pregnancy Is Underpinned by Complex Changes in Uterine Gene Expression: A Comparative Analysis of the Uterine Transcriptome in Viviparous and Oviparous Lizards. Genome Biol Evol 2016 Oct 30;8(10):3226-3239.
- Conceição JDS, Khatlab AS, Gasparino E, Santana TP, Carvalho AS, Batista MVA, Filho MS, Guimaraes SEF, Vieira JS, Vesco APD. Combined effects of incubation temperature and lipopolysaccharide exposure on immune response modulation in the quail gut. Poult Sci 2026 Jan 13;105(4):106418.
- Schäffers OJM, Gribnau J, van Rijn BB, Bunnik EM. Ethical considerations for advancing research using organoid models derived from the placenta. Hum Reprod Update 2025 Jul 1;31(4):392-401.
- Plianchaisuk A, Kusama K, Kato K, Sriswasdi S, Tamura K, Iwasaki W. Origination of LTR Retroelement-Derived NYNRIN Coincides with Therian Placental Emergence. Mol Biol Evol 2022 Sep 1;39(9).
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