Molecular Signatures of Placentation and Secretion Uncovered in Poeciliopsis Maternal Follicles

Abstract

Placentation evolved many times independently in vertebrates. Although the core functions of all placentas are similar, we know less about how this similarity extends to the molecular level. Here, we study Poeciliopsis, a unique genus of live-bearing fish that have independently evolved complex placental structures at least three times. The maternal follicle is a key component of these structures. It envelops yolk-rich eggs and is morphologically simple in lecithotrophic species but has elaborate villous structures in matrotrophic species. Through sequencing, the follicle transcriptome of a matrotrophic, Poeciliopsis retropinna, and lecithotrophic, P. turrubarensis, species we found genes known to be critical for placenta function expressed in both species despite their difference in complexity. Additionally, when we compare the transcriptome of different river populations of P. retropinna, known to vary in maternal provisioning, we find differential expression of secretory genes expressed specifically in the top layer of villi cells in the maternal follicle. This provides some of the first evidence that the placental structures of Poeciliopsis function using a secretory mechanism rather than direct contact with maternal circulation. Finally, when we look at the expression of placenta proteins at the maternal–fetal interface of a larger sampling of Poeciliopsis species, we find expression of key maternal and fetal placenta proteins in their cognate tissue types of all species, but follicle expression of prolactin is restricted to only matrotrophic species. Taken together, we suggest that all Poeciliopsis follicles are poised for placenta function but require expression of key genes to form secretory villi.

Parallel Genomic Changes Drive Repeated Evolution of Placentas in Live-Bearing Fish

“…To gain more insight in the expression of our candidate genes in placental tissue, we used a previously published RNA-seq data set of placental tissue of Poeciliopsis retropinna to see whether our candidate genes are expressed within placental tissue of this species ( Guernsey et al. 2020 ).…”

Embryonic Onset of Sexually Dimorphic Heart Rates in the Viviparous Fish, Gambusia holbrooki

“…Reasons for comparatively closer HRs of G. holbrooki to those of humans are yet unknown. However, it is possible that the shared internal fertilisation with a placenta-like reproductive strategy [ 19 ] may in part explain the evolutionary conservation of the heart function [ 50 ] of G. holbrooki and placental vertebrates. Although the teleost lineage exhibits morphological evolutionary novelty such as bulbus arteriosus, they express genes that are conserved across vertebrates [ 50 ].…”

“…Like in other teleosts, the heart of Poeciliids has two chambers, i.e., single-chambered atrium and ventricle [ 17 ], but both cellular and molecular mechanisms of heart contraction are similar to mammals [ 16 , 18 ]. Part of a complex reproductive adaptation in Poeciliids is a placenta-like specialised tissue suggesting a closer evolutionary link to placentation in mammals [ 19 ]. Therefore, studies on heart and physiology in Poeciliids could answer longstanding questions on sex differentiation, evolution, and developmental mechanisms, as well as assisting in better understanding human cardiac diseases [ 20 ].…”

New insights on folliculogenesis and follicular placentation in marine viviparous fish black rockfish (Sebastes schlegelii)

“…retropinna (Guernsey et al, 2020). Plac8 has been found promoting trophoblast invasion and migration (Mourtada-Maarabouni et al, 2013;Rogulski et al, 2005;Chang et al, 2018).…”

“…The evolution of a novel organ typically involves both functional innovations and a novel structure which is associated with this function. In both Poeciliopsis retropinna and P. turneri (Wourms, 1981;Wourms et al, 1988;Kwan et al, 2015;Guernsey et al, 2020), the inner surface of the maternal follicular epithelium was highly hypertrophied and extensively folded (Grove and Wourms, 1994;Kwan et al, 2015). In Goodeidnae, at mid to late gestation stages, the embryos moved from follicle to the ovarian lumen and developed a trophotaeniae (Knight et al, 1985;Lombardi and Wourms, 1985;Wourms and Callard , 1992;Uribe et al, 2018).…”