Elsevier

Placenta

Volume 30, Supplement, March 2009, Pages 19-25
Placenta

Evolution of Factors Affecting Placental Oxygen Transfer

https://doi.org/10.1016/j.placenta.2008.11.006Get rights and content

Abstract

A review is given of the factors determining placental oxygen transfer and the oxygen supply to the fetus. In the case of continuous variables, such as the rate of placental blood flow, it is not possible to trace evolutionary trends. Discontinuous variables, for which we can define character states, are more amenable to analysis. This is exemplified by factors contributing, respectively, to blood oxygen affinity and placental diffusing capacity. Comparative genomics has given fresh insight into the evolution of the beta-globin gene complex. In higher primates, duplication of an embryonic gene yielded HBG-T2, a gene that is expressed in the fetus and confers high oxygen affinity on its haemoglobin. A separate event in ruminants involved duplication of an adult gene, again resulting in a fetally expressed variant (HBB-T3) that conveys high oxygen affinity. In rodents and lagomorphs, where fetal and adult haemoglobin are not different, developmental regulation of 2, 3-diphosphoglycerate ensures the high oxygen affinity of fetal blood. Oxygen diffusing capacity is dependent on diffusion distance, which may vary with the type of interhaemal barrier. It has been shown that epitheliochorial placentation is a derived state and that the common ancestor of placental mammals probably had a placenta of the endotheliochorial type. Where evolutionary trends are implied for mammals as a whole or within orders such as primates they often accompany a switch in reproductive strategy that is manifested in a change of newborn state from poorly developed (altricial) to well developed (precocial).

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:Oxygen delivery to uterus and placenta=Uterine blood flow×[O2]uterine arterySince 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.

References (71)

  • M.A. Miglino et al.

    Vascular organization of the hystricomorph placenta: a comparative study in the agouti, capybara, guinea pig, paca and rock cavy

    Placenta

    (2004)
  • H.J. Schröder

    Comparative aspects of placental exchange functions

    Eur J Obstet Gynecol Reprod Biol

    (1995)
  • A.M. Carter et al.

    Structure of the definitive placenta of the tenrec, Echinops telfairi

    Placenta

    (2004)
  • K. Klisch et al.

    Evolutionary differentiation of Cetartiodactyl placentae in the light of the viviparity-driven conflict hypothesis

    Placenta

    (2007)
  • M.S. Springer et al.

    Molecules consolidate the placental mammal tree

    Trends Ecol Evol

    (2004)
  • P. Vogel

    The current molecular phylogeny of Eutherian mammals challenges previous interpretations of placental evolution

    Placenta

    (2005)
  • R.D. Martin

    Human reproduction: a comparative background for medical hypotheses

    J Reprod Immunol

    (2003)
  • A. Mess et al.

    Evolution of the placenta during the early radiation of placental mammals

    Comp Biochem Physiol A Mol Integr Physiol

    (2007)
  • R. Pijnenborg et al.

    The uterine spiral arteries in human pregnancy: facts and controversies

    Placenta

    (2006)
  • C.J. Douady et al.

    Molecular phylogenetic evidence confirming the Eulipotyphla concept and in support of hedgehogs as the sister group to shrews

    Mol Phylogenet Evol

    (2002)
  • R.M. Wells

    Evolution of haemoglobin function: molecular adaptations to environment

    Clin Exp Pharmacol Physiol

    (1999)
  • R.D. Martin et al.

    Gestation period, neonatal size and maternal investment in placental mammals

    Nature

    (1985)
  • A. Portmann

    Die Tragzeiten der Primaten und die Dauer der Schwangerschaft beim Menschen: Ein Problem der Vergleichende Biologie

    Rev Zool

    (1941)
  • J. Metcalfe et al.

    Gas exchange in the pregnant uterus

    Physiol Rev

    (1967)
  • L.D. Longo

    Respiratory gas exchange in the placenta

  • A.M. Carter

    Factors affecting gas transfer across the placenta and the oxygen supply to the fetus

    J Dev Physiol

    (1989)
  • A.M. Carter

    Placental oxygen transfer and the oxygen supply to the fetus

    Fetal Matern Med Rev

    (1999)
  • G. Chamberlain et al.

    Clinical physiology in obstetrics

    (1998)
  • R.B. Wilkening et al.

    Fetal oxygen uptake, oxygenation and acid-base balance as a function of uterine blood flow

    Am J Physiol

    (1983)
  • D.R. Bonds et al.

    Estimation of human fetal-placental unit metabolic rate by application of the Bohr principle

    J Dev Physiol

    (1986)
  • Acharya G, Sitras V. Oxygen uptake of the human fetus at term. Acta Obstet Gynec Scand 2008 Nov 8:1–6 [Epub ahead of...
  • A.W. Bell et al.

    Metabolic and circulatory studies of fetal lamb at midgestation

    Am J Physiol

    (1986)
  • H. Bartels

    Prenatal respiration

    (1970)
  • H. Dickinson et al.

    Maternal dexamethasone treatment at midgestation reduces nephron number and alters renal gene expression in the fetal spiny mouse

    Am J Physiol Regul Integr Comp Physiol

    (2007)
  • R.E. Behrman et al.

    A comparison of the oxygen affinity of maternal and fetal blood of the Macaca mulatta

    Q J Exp Physiol Cogn Med Sci

    (1963)
  • Cited by (0)

    View full text