Evolution of Factors Affecting Placental Oxygen Transfer
Introduction
It is self evident that each of type of placenta is designed to meet the oxygen requirements of the fetus that it serves. There is nonetheless reason to think that optimisation of placental gas exchange has followed a different course in different orders or families of placental mammals. This review will explore the factors that determine placental oxygen transfer and discuss how some of them have evolved. It will become apparent that for continuous variables, such as the rate of placental blood flow, we are as yet unable to trace evolutionary trends. Discontinuous variables, for which we can define character states, are more amenable to analysis. This will be exemplified with blood oxygen affinity, which revolves around evolution of the beta-globin gene, and placental diffusing capacity, which depends in part on the structure of the interhaemal barrier.
The focus will be on oxygen supply to the fetus near term of pregnancy. The placenta plays a different role during embryonic development up to and including organogenesis. The events of this period need to take place in a low oxygen environment [1]. Molecules such as embryonic haemoglobins are designed as much to protect cells from high PO2 levels as for oxygen delivery to tissues [2], [3]. Embryonic development occupies a greater part of gestation in a mouse than in a guinea pig. Murine rodents have adopted a reproductive strategy that leads to delivery of poorly developed or altricial young. This pattern is found in most small mammals; it implies a short gestation and usually is associated with a large litter size [4]. The alternative strategy, found in all large mammals, leads to delivery of well developed or precocial young. This requires a much longer gestation period and a smaller litter size. The human newborn is sometimes characterised as secondarily altricial because a baby is rather well developed at birth yet still entirely dependent on parental care [5].
Short gestations leading to delivery of altricial young typically have a growth spurt in the last few days of gestation. Evolution of the alternative strategy with a longer gestation and larger, precocial neonates may well require more complex adaptations to ensure an adequate oxygen supply. In a concluding section it will be discussed if there is evidence to support this prediction.
Section snippets
Oxygen delivery and oxygen consumption
The placenta facilitates gaseous exchange between the maternal and fetal circulations. The principal factors affecting placental exchange of oxygen have been reviewed extensively [6], [7], [8], [9], [10] and are summarised in Table 1. Oxygen delivery to the gravid uterus depends on the rate of uterine blood flow and the oxygen content ([O2]) of maternal arterial blood:Since arterial blood is almost fully saturated, its
Blood oxygen affinity
In most species examined, the oxygen affinity of fetal blood exceeds that of maternal blood and this facilitates placental oxygen transfer. In human pregnancy, if maternal and fetal bloods equilibrate at a PO2 of 30 mm Hg, maternal haemoglobin will be about 50% saturated, whilst fetal haemoglobin will have achieved an oxygen saturation of about 80% [6]. This explains why fetal blood is quite highly saturated even at the low PO2 levels found in the umbilical vein. A common measure of oxygen
Vascular architecture
Efficiency of gas exchange is to some extent dependent on the vascular architecture of the placenta. In the labyrinth of hystricognath rodents, such as the guinea pig or capybara (Hydrochoeris hydrochaeris), maternal blood flows in trophoblastic channels that run parallel to fetal capillaries [40]. This arrangement enables the placenta to act as a countercurrent exchanger. There are no known instances of placentas with mainly concurrent flow. Cross current flow does occur, however, as in the
Placental diffusing capacity
Placental factors of importance for fetal oxygen supply include oxygen consumption by the placenta itself. This has been reliably measured only in ruminants [13], [16] and recently in human pregnancy [15]. Thus there are not enough data for phylogenetic analysis. The other placental factor of importance to oxygen transfer is the diffusing capacity. This can be determined experimentally by measuring diffusing capacity for carbon monoxide [48]. Data is available for several species [7], but still
Reproductive strategies and placental evolution
Although we are far from understanding what drives placental evolution, several of the trends discussed in this review can be linked to a change in reproductive strategy involving lengthier gestation and more highly developed young. It is far from obvious what advantage accrues to horses, antelopes or pangolins from having epitheliochorial placentation. One recent suggestion is that it allows a much different immunological relationship between mother and fetus somewhat akin to that of a
Conclusion
Many of the factors regulating fetal oxygen supply, including the oxygen capacity (haemoglobin concentration) of fetal and maternal blood and rates of blood flow in the two circulations, are continuous variables difficult to analyse in a phylogenetic framework. Others require complex physiological measurements that have been made in few species; an example is the oxygen consumption of the placenta itself. There are also adaptations too widespread to carry a phylogenetic signal. For instance, in
Conflict of interest
The author does not have any potential or actual personal, political, or financial interest in the material, information, or techniques described in the paper.
Acknowledgements
The views here expressed are those of the author but it is a pleasure to mention stimulating discussions with Kevin L. Campbell, Allen C. Enders, Robert D. Martin, Andrea Mess and Peter Vogel.
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