Single-cell transcriptomic atlases of midgestation fetal-maternal interface from opossum, tenrec, guinea pig, and mouse
The origin of this chimeric fetal-maternal tissue poses a unique evolutionary puzzle. We present a multi-species atlas integrating single-cell transcriptomes from opossum (a marsupial), Malagasy common tenrec (an afrotherian), mouse and guinea pig (rodents) with previous macaque and human data (primates). Invasive trophoblasts share a transcriptomic signature across eutherians, likely representing a cell type family that radiated following the evolution of hemochorial placentation. Our data suggest that decidual stromal cells evolved stepwise from an immunomodulatory cell found in Tenrec, followed by acquisition of an endocrine decidual cell in Boreoeutherian mammals. Finally, we identify evolutionary patterns in ligand-receptor signaling among fetal and maternal cells: Consistent with theoretical predictions, fetal and maternal cells show a strong tendency towards disambiguated signaling, however, a predicted escalatory arms race dynamic between them is restricted to few ligands. We reconstruct the uteroplacental cell-cell communication network of the eutherian common ancestor, and infer accelerated signaling loss in Euarchontoglires and accelerated gains in primates. Unexpectedly, fetal trophoblast cell types display strong integration into maternal signaling networks despite their recent evolutionary origin. The tailless tenrec Tenrec ecaudatus is an afrotherian mammal native to Madagascar, related to the elephant and aardvark, and is remarkable for retaining a collection of ancestral eutherian traits. The single known description of the decidual tissue of T. ecaudatus was collected by zoologist and explorer R.H. Goetz in 1936 from a female during mid-gestation. We collected fresh, timed-pregnant uteri from T. ecaudatus at mid-gestation (days 28-30) to address: Which cell types are present in the decidua of a basally branching placental mammal, and how do they, if present, interact with other cells? Furthermore, how does gene expression of the tenrec decidual stromal cell differ from the human? We find that the tenrec possesses a uterine process akin to human predecidualization, involving the upregulation of key decidual transcription factors FOXO1 and KLF7 and effector genes such as IL15, and that this cell type is unique to pregnant animals. Overall design: Cells from midgestation fetal-maternal interface (whole-thickness uterus and placenta) were isolated and subjected to 10x Genomics 3' v3 single-cell RNA-seq.