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

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.

Convergently evolved placental villi show multiscale structural adaptations to differential placental invasiveness

“…If these structural adaptations in equid villi are a response to reduced nutrient availability through decreased invasiveness into maternal tissue as we propose, our data could provide evidence supporting the 'maternal-fetal conflict hypothesis' in placental evolution. Experimental evidence suggests that placental invasiveness is regulated by the maternal endometrium, such as through the activity of stromal cells, conferring uterine permissiveness [16,[36][37][38][39]. According to the maternal-fetal conflict hypothesis, epitheliochorial placentation evolved as a way for the mother to constrain nutrients from the fetus in species with precocial energy-intensive young, whereas the genes controlling placental development may be selected for optimal nutrient extraction, potentially at the expense of the mother's long-term fitness interests.…”

“…Epitheliochorial placentas are thought to permit less efficient transfer of nutrients from mother to fetus than haemochorial placentas, due to the additional tissue layers between maternal and fetal circulation acting as barriers to transfer [8]. Ancestral trait reconstruction suggests that the ancestral placenta in placental mammals was haemochorial, therefore the epitheliochorial placenta is the derived condition [3,[13][14][15][16]. Evolutionary pressures proposed to favour the origin of a less invasive placenta include protection of the mother from oxidative stress by fetal metabolism [17], protection of the fetus from vertical transmission of parasites from the mother [10], and the increased ability for the mother to withhold nutrients from the fetus in a phenomenon known as 'maternal constraint' [18,19].…”

Post-fertilization transcription initiation in an ancestral LTR retrotransposon drives lineage-specific genomic imprinting ofZDBF2

“…Strand-specific RNA-seq datasets from the human bulk placenta, rhesus macaque trophoblast stem cells, and mouse bulk placenta at E16.5, were downloaded from the accession numbers SRR12363247 and SRR12363248 for humans, SRR1236168 and SRR1236169 for rhesus macaques, and SRR943345 for mice (Necsulea et al 2014; Rosenkrantz et al 2021). Non-directional RNA-seq data from placentas or extra-embryonic tissues of 15 mammalian species, including humans, bonobos, baboons, mice, golden hamsters, rabbits, pigs, cattle, sheep, horses, dogs, bast, elephants, armadillos, and opossums, were downloaded (Armstrong et al 2017; Mika et al 2022). Full-length RNA-seq (based on the smart-seq method) data from human oocytes, zygotes, 2-, 4-, and 8-cell, ICM, and TE were downloaded from previous studies (Kai et al 2022; Zou et al 2022b).…”

The Connection between Immunocompetence and Reproduction in Wildlife

“…For example, in mammals alone, there are numerous differences in the ontogenetic origin and organization of the maternal–fetal interface [ 15 , 16 , 17 ]. These distinct processes are accompanied by different expression profiles of the genes involved [ 18 ]. During gravidity in vertebrates, significant physiological and metabolic alterations occur.…”