Convergent evolution of placental villi in primates and ungulates: Are some placentas more efficient than others?

The placenta is a fetal organ which connects the fetus to its mother while in the womb. The functions of the placenta are to transfer food from maternal blood to the fetus and clean the fetal blood. The structure of the placenta determines how efficiently it can function. Here, we define placental efficiency as the rate at which the placenta transfers nutrients to the fetus in relation to placental size. While the mammalian placenta only evolved once, mammalian placentas come in a remarkable array of shapes and sizes. The variety of placental structures is much more pronounced than for any other organ. The large number of different placental types suggests that different species face different requirements in pregnancy. However, we do not understand what these requirements are, and if we do not know what they are we cannot address them. This is important because the requirements which shaped placental structure in the past will also affect human and animal health today. Poor placental function does not just affect the health of the fetus, it affects the health of the mother and of the child throughout its life. Placentas are categorised based on their overall shape, the structure of the interface with the mother, and the number of tissue layers between the maternal and fetal blood. The diversity of placental structures suggests that the requirements for successful reproduction differ for different species. Otherwise, only one 'most efficient' type of placenta would have evolved. This project will study placentas that contain finger-like projections called villi. Placental villi evolved independently twice, once in primates (e.g. humans) and once in ungulates (e.g. cows and sheep). In humans, placental villi are in direct contact with maternal blood. By contrast, in cows and sheep, the placental villi are embedded in maternal tissue and have no contact with maternal blood, which means nutrients have to travel further to reach the baby. The common ancestor of primates and ungulates is believed to have had a 'more efficient' placenta in direct contact with maternal blood, so it is unclear why the ungulates have evolved a 'less efficient' placental type from a more efficient one. One reason for this may be so that the mother can protect herself from giving too many nutrients to the fetus, a process called 'maternal constraint' when times are hard. However, it may be that the ungulate placentas are not less efficient. We hypothesise that, despite superficial structural similarity, cow and sheep villi have evolved to be more efficient than human villi to make up for the extra distance nutrients must travel. Furthermore, we hypothesise that differences in efficiency at one scale (e.g. villi) will be compensated for by adaptations at another scale (e.g. placental volume). This project will use new 3D imaging approaches to study placental structure in ways that were not previously possible. It will image the placenta across all size scales, from the whole placenta down to the smallest microscopic structures. Once we have determined placental structures in the target species, we will create computational models of how efficient these placentas are. Using these computational models, we will be able to calculate placental efficiency much more accurately than in the past, both at the level of placental villi and to assess the placenta as a whole. We think an accurate measure of efficiency must include understanding the whole placenta. By combining new 3D imaging tools across scales with computational modelling, this project will develop new quantitative measures of placental efficiency. If we can explain why different species have certain placental types, we can then establish what those species need to reproduce successfully. Understanding reproductive success is important for human and animal health, the conservation of endangered species, and understanding how climate change may affect reproductive success in humans and animals.