The marsupial placenta: A phylogenetic analysis

Abstract

The structure, physiology, and endocrinology of the yolk sac placenta of different marsupial groups is compared and phylogenetically analyzed to provide information on placental characters in the marsupial stem species. We conclude that the marsupial stem species possessed a functional yolk sac placenta. Histotrophic nutrition by uterine secretion decreased during late pregnancy and at least half of the yolk sac was vascularized at the time of shell coat rupture. Due to yolk sac fusion, the larger part of the avascular, bilaminar yolk sac could not serve as a placenta at late gestation in the polyovular marsupial stem species. The bilaminar yolk sac gained a relatively greater importance for nutrition in monovular australidelphians. In macropodids a greater proportion of the yolk sac remained bilaminar at the time of shell coat rupture than in the stem species. Another derived feature of macropodids is the sustained plasma progesterone synthesis that is in turn responsible for an extended secretory phase of the uterus and a lengthened gestation. The placenta of the marsupial stem species was probably capable of metabolising histo- and hemotrophes. Recognition of pregnancy during early stages of development is a derived character of macropodids that we suggest did not occur in the marsupial stem species. However, birth and birth behaviour were apparently induced by prostaglandins in the marsupial stem species. Although the yolk sac formed the definitive placenta, it is likely that the allantois provided a supplementary placental function in the marsupial stem species, but that the role of the allantois became progressively less important during the evolution of marsupial placentation.

Evolutionary transformations of fetal membrane characters in Eutheria with special reference to Afrotheria

“…MacClade is a widely accepted tool for analyzing phylogenetic hypotheses and reconstructing and displaying character evolution on a phylogenetic tree. Character optimization is an approach previously used to trace character evolution in fetal membranes (Freyer et al, 2003;Mess, 2003;Asher, 2005;Vogel, 2005). Moreover, the parsimony-based method of character analysis in MacClade easily allows handling of missing data.…”

“…Thus yolk sac placentation is more different between Eutheria and Metatheria than indicated by common text books. Interestingly, a phylogenetic analysis of marsupial placentation (Freyer et al, 2003) led to the conclusion that a chorioallantoic placenta was part of the stem species pattern of marsupials but that the yolk sac had evolved to become the principal organ of physiological exchange.…”

Mammalian diversity: gametes, embryos and reproduction

“…However, there are exceptions. A true chorioallantoic placenta has been described in marsupials for four species of bandicoots, as well as a mildly invasive connection of the allantois to the chorion in didelphids, dasyurids and vombatids (Tyndale-Biscoe and Renfree 1987;Freyer et al 2003). A choriovitelline placenta is also important during early gestation for eutherian mammals.…”

Ancient and continuing Darwinian selection on insulin-like growth factor II in placental fishes

“…The strongest evidence of parent-offspring conflict associated with the evolution of matrotrophy (i.e., mother-feeding) is that the growth factor, insulin-like growth factor II (IGF2), and its antagonistic receptor, IGF2r, are oppositely imprinted in eutherian mammals and marsupials (6)(7)(8). Nevertheless, placentation and imprinting likely evolved in the common ancestor to Eutheria and Marsupialia Ͼ100 million years ago (9,10); therefore, evidence that these two genes evolved under positive selection has been difficult to discern. Any evidence for antagonistic coevolution of genes that may have coincided with the evolution of placentas in mammals is likely to have faded into the background of neutral mutation accumulated since the Cretaceous.…”