Novel tissue interactions support the evolution of placentation

Abstract

Organ development occurs through the coordinated interaction of distinct tissue types. So, a question at the core of understanding the evolution of new organs is, how do new tissue-tissue signalling networks arise? The placenta is a great model for understanding the evolution of new organs, because placentas have evolved repeatedly, evolved relatively recently in some lineages, and exhibit intermediate forms in extant clades. Placentas, like other organs, form from the interaction of two distinct tissues, one maternal and one fetal. If each of these tissues produces signals that can be received by the other, then the apposition of these tissues is likely to result in new signalling dynamics that can be used as a scaffold to support placenta development. Using published data and examples, in this review I demonstrate that placentas are derived from hormonally active organs, that considerable signalling potential exists between maternal and fetal tissues in egg-laying vertebrates, that this signalling potential is conserved through the oviparity-viviparity transition, and that consequences of these interactions form the basis of derived aspects of placentation including embryo implantation. I argue that the interaction of placental tissues, is not merely a consequence of placenta formation, but that novel interactions form the basis of new placental regulatory networks, functions, and patterning mechanisms.

Embryonic specializations for vertebrate placentation

“…In some squamates, the chorioallantois directly influences maternal tissues, probably causing uterine epithelium hypertrophy and growth of maternal blood vessels [94]. The chorioallantois is ancestrally an endocrine organ [95], and its retention in viviparous species results in substantial potential for maternal-fetal signalling [96].…”

Comparing the potential for maternal–fetal signalling in oviparous and viviparous lizards

“…While maternal and fetal tissues were spatially separated in oviparous taxa, these data show that egg retention and loss of the eggshell are likely sufficient to establish routes of maternal–fetal communication in skinks.

Figure 3Signalling interaction map showing the potential for signalling between uterus (red) and chorioallantoic membrane (CAM, blue) in egg-laying and live-bearing skinks (modified from Griffith [9]). The majority of the potential signalling pathways are conserved between both species (blue/red arrows), however novel signalling pathways (yellow arrows) exist in each species.

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“…Signalling interaction map showing the potential for signalling between uterus (red) and chorioallantoic membrane (CAM, blue) in egg-laying and live-bearing skinks (modified from Griffith [9]). The majority of the potential signalling pathways are conserved between both species (blue/red arrows), however novel signalling pathways (yellow arrows) exist in each species.…”

“…The uterus is also a hormone-producing organ and can likely transport hormone signals to embryos during pregnancy [13]. Owing to the hormones produced by these tissues in live-bearing species and their egg-laying relatives, researchers have proposed that maternal–fetal signalling may be a consequence of egg retention and eggshell loss, rather than a derived feature of placentation (figure 1) [2,9]. In this article, we investigate the potential for signalling based on ligand and receptor gene expression, to examine how the novel apposition of maternal and fetal tissues may facilitate maternal–fetal signalling.…”

“…As viviparous species can provide nutrition via the placenta, this offers a novel opportunity for the fetus to influence maternal provisioning. While there is evidence for fetal control of maternal placenta development [8], how maternal-fetal signalling evolved is poorly understood [9].…”