The evolutionary significance of placental interdigitation in mammalian reproduction: Contributions from comparative studies
Introduction
The mammalian placenta is central to reproduction, being responsible for supporting fetal growth via transfer of nutrients and oxygen from the mother to the fetus, and for disposing of fetal waste products. It is formed by the contact of extra-embryonic tissues – the chorion and the yolk sac in marsupials, and the chorion and allantois in placental (eutherian) mammals - with maternal uterine tissues [1], [2], [3], [4], [5], [6]. Within this general framework, however, the placenta exhibits great interspecific diversity in gross morphology [1], [2], [3], [4], [5]. In eutherian mammals the placenta can be classified, for example, by its shape (the number and distribution of the areas for nutrient exchange on the placental surface), invasiveness (the number of maternal tissue layers separating maternal blood from fetal tissues), interdigitation (the degree of contact between fetal and maternal tissues at the areas for nutrient exchange), placental weight relative to the neonatal weight, and the relative direction of maternal and fetal blood flows [1], [2], [3], [4], [5]. An open question is whether placental morphology affects the rate of transplacental nutrient transfer and, as a result, fetal development, ultimately leading to the diversity in life history traits that mammals exhibit. Here I focus on the contribution of recent phylogenetic comparative studies to answering this question and investigating the evolutionary history of placental diversity, and argue that the role of placental interdigitation has been mostly overlooked but may provide an important avenue for future studies. I will first briefly present two major hypotheses proposed for the evolution of placental diversity, next discuss studies on the role of interdigitation in fetal growth, and the evolutionary history and plasticity of interdigitation, and lastly propose that future studies could focus on the evolution and implications of other placental traits for maternal investment and fetal development.
Section snippets
Maternal-offspring interactions: mutual advantage and conflict
What are the selective pressures responsible for the evolution of the morphological diversity in placentation? What are the implications of such diversity for fetal growth and maternal reproductive investment? Two non-mutually exclusive hypotheses have been proposed to answer these questions. The mutual advantage hypothesis holds that some placental characteristics enhance the rate of nutrient transfer, ultimately benefitting both the reproductive success of the mother and the development of
Interdigitation is associated with fetal growth rates
Surprisingly, little attention has been paid to diversity in other placental traits, such as interdigitation, that may have a great impact on nutrient transfer rates and fetal growth. Interdigitation refers to the degree of contact between maternal and fetal tissues at the areas of exchange [1], [2], [3], [4]. In the least interdigitated villous placentae, such as those of primates, the areas for nutrient exchange are made of branched villi, while in more interdigitated placentae the villi are
Evolutionary history of interdigitation and its plasticity during development
Several studies investigated the evolutionary history of interdigitation. There is no explicit hypothesis regarding the evolutionary history of this trait as most attention has focussed on invasiveness. However, under a mutual advantage hypothesis, one could predict that if the evolution of placental diversity reflects improved nutrient transfer efficiency, a low interdigitated placenta should be ancestral and a labyrinthine interdigitation derived. Contrary to this suggestion, a highly
Beyond invasiveness and interdigitation
Altogether, comparative studies have revealed that changes in the surface area for exchange, that directly impact fetal growth rates, are achieved evolutionarily by structural modifications leading to interspecific differences in interdigitation, while within species the placenta responds plastically to enhance the surface area for exchange in response to maternal conditions. Maternal body mass and interdigitation together explain approximately 40% of variance in gestation time in mammals [28],
Conclusions
Comparative studies of placental gross morphology can reveal key patterns of associations between placental traits and fetal development, ultimately leading to better understanding of placental evolution and function. Recent analyses have revealed that a higher degree of interdigitation – but not invasiveness – increases fetal growth rates [28], possibly because greater interdigitation enhances the surface area for exchange of nutrients. While these results highlight the importance of
Acknowledgements
I am grateful to Joanna Setchell and Graham Burton for helpful comments on an earlier version of this paper, Derek Wildman, Robert Barton and Anthony Carter for stimulating discussion, and the organizers of the CTR Annual Trophoblast meeting 2011 in Cambridge for the opportunity to present this work.
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