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

胎盘是胎儿的一个器官，在子宫内时将胎儿与母亲联系起来。胎盘的功能是将母体血液中的食物转移给胎儿并清洁胎儿血液。胎盘的结构决定了它的功能效率。在这里，我们将胎盘效率定义为胎盘向胎儿输送营养的速率与胎盘大小的关系。虽然哺乳动物胎盘只进化了一次，但哺乳动物胎盘的形状和大小却有着惊人的变化。胎盘结构的多样性比其他任何器官都要明显得多。大量不同的胎盘类型表明，不同的物种在怀孕时面临不同的要求。然而，我们不理解这些要求是什么，如果我们不知道这些要求是什么，我们就无法满足这些要求。这一点很重要，因为过去塑造胎盘结构的要求也将影响今天的人类和动物健康。胎盘功能不佳不仅会影响胎儿的健康，还会影响母亲和孩子一生的健康。胎盘根据其整体形状、与母亲界面的结构以及母亲和胎儿血液之间的组织层数量进行分类。胎盘结构的多样性表明，不同物种成功繁殖的要求不同。否则，只有一种“最有效”的胎盘类型会进化出来。这个项目将研究含有称为绒毛的指状突起的胎盘。胎盘绒毛独立进化了两次，一次在灵长类动物（如人类）中，一次在有蹄类动物（如牛和羊）中。在人类中，胎盘绒毛与母体血液直接接触。相比之下，在奶牛和绵羊中，胎盘绒毛嵌入母体组织中，不与母体血液接触，这意味着营养物质必须经过更远的距离才能到达婴儿。灵长类动物和有蹄类动物的共同祖先被认为有一个“更有效”的胎盘与母体血液直接接触，所以目前还不清楚为什么有蹄类动物从一个更有效的胎盘进化成一个“效率较低”的胎盘类型。其中一个原因可能是母亲可以保护自己不给胎儿太多的营养，这一过程被称为“母亲约束”，但也可能是有蹄类胎盘的效率不低。我们假设，尽管表面结构相似，牛和羊的绒毛进化得比人类绒毛更有效，以弥补营养素必须旅行的额外距离。此外，我们假设在一个尺度（如绒毛）的效率差异将通过另一个尺度（如胎盘体积）的适应来补偿。该项目将使用新的3D成像方法以以前不可能的方式研究胎盘结构。它将在所有尺寸尺度上对胎盘进行成像，从整个胎盘到最小的微观结构。一旦我们确定了目标物种的胎盘结构，我们将创建计算模型来计算这些胎盘的效率。使用这些计算模型，我们将能够比过去更准确地计算胎盘效率，无论是在胎盘绒毛水平还是评估整个胎盘。我们认为，准确衡量效率必须包括了解整个胎盘。通过将新的3D成像工具与计算建模相结合，该项目将开发新的胎盘效率定量测量方法。如果我们能够解释为什么不同物种具有特定的胎盘类型，那么我们就可以确定这些物种成功繁殖所需的条件。了解生殖成功对于人类和动物的健康，濒危物种的保护以及了解气候变化如何影响人类和动物的生殖成功非常重要。

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.