Uncovering molecular signatures of placentation in Tammar wallaby and Poeciliopsis fishes

The placenta is a unique extra-embryonic organ that facilitates pregnancy in many live-bearing animals. Placentas exhibit great morphological diversity both within mammals, but also in many different vertebrate lineages where the placenta evolved independently. Despite this diversity in structure, all placentas must allow for nutrient provisioning, gas exchange, waste removal, endocrine maintenance of pregnancy and protection from pathogens to achieve a successful pregnancy. While these functions are conserved, we know less about how this similarity extends to the molecular level. Here I investigate this using the Tammar wallaby and Poeciliopsis fishes as models. First, I utilize transcriptome sequencing in the tammar wallaby to provide evidence that the classification of therian mammals into eutherian (placental) and marsupial (pouch-bearing) based upon having a 'true' placenta is inaccurate. We show that the tammar yolk sac, often argued to be the cognate of the eutherian yolk sac, is surprisingly similar to the mouse and human placenta. Furthermore, immunofluorescence in tammar placenta demonstrates protein localization of genes known to be essential for eutherian placentation to distinct cell layers of the tammar placenta. This striking molecular conservation suggests that although the marsupial placenta is morphologically simple, it represents a 'true' placenta reminiscent of the most complex eutherian forms. Once we solidify that the tammar wallaby does indeed have a eutherian-like placenta, we examine the evolution of placentation and lactation as strategies for nourishing young. Marsupial biologists have hypothesized that these processes are involved in an evolutionary tradeoff and, as a result, marsupials favored the development of complex lactation while eutherians favored complex placentation to support fetal survival. Interestingly, we find that many of the genetic programs involved in lactation and placentation have been shared, co-opted and exchanged during evolution. These genetic programs have been shifted in both directions: from lactation to placentation and from placentation to lactation. Overall, the recycling of genetic programs to optimize nourishment strategies in each species is a novel finding and surprisingly suggests that placentation and lactation are similar processes. Next, I study Poeciliopsis, a unique genus of live-bearing fish that have evolved placental structures at least three times independently. The maternal follicle is a key component of these structures; it envelops yolk rich eggs and is morphologically simple in non-placental species, but has elaborate villous structures in placental species. Through sequencing the follicle transcriptome of a placental, P. retropinna, and non-placental, 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 exchange between maternal-fetal 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 only placental species show follicle expression of Prolactin. Taken together, we suggest that all Poeciliopsis follicles are poised for placenta function, but require expression of key genes to form villi

Keywords: genetics) degree supervisor.
Developmental Biology.
Advisor: Fraser Hunter B. 
Jarosz Daniel 
Lowe Christopher (Associate professor of biology)