Evolution of Placentation in Primates: Implications of Mammalian Phylogeny

Abstract

Primates are quite unique among placental mammals in that the two extreme types of placentation are present within a single order. Strepsirrhines (lemurs and lorisiforms) have non-invasive epitheliochorial placentation, whereas haplorhines (tarsiers and higher primates) have highly invasive haemochorial placentation. Resemblance in placenta type in fact provided the first evidence that tarsiers are linked to higher primates and distinct from lemurs and lorisiforms. Tree-shrews differ from both primate subgroups in having moderately invasive endotheliochorial placentation, while colugos have invasive haemochorial placentation like haplorhines. All three kinds of placentation have been identified as primitive for placentals by different authors, but until recently the prevailing interpretation has been that non-invasive epitheliochorial placentation is primitive and ''less efficient''. Opposing this interpretation, Martin (Primate origins and evolution: a phylogenetic reconstruction, 1990) proposed that moderately invasive endotheliochorial placentation is primitive. Epitheliochorial placentation is unlikely to be primitive because it is predominantly associated with large body size, relatively long gestation periods and precocial offspring. Furthermore, some strepsirrhines and other placental mammals with epitheliochorial placentation retain indications of former invasiveness of the placenta. The recent availability of comprehensive molecular phylogenies for placental mammals has provided an independent framework to determine the most parsimonious interpretation of the evolution of placenta types and other reproductive features. It has consistently emerged that epitheliochorial placentation is best explained as a derived condition, although opinions differ as to whether the ancestral condition for placental mammals (and hence for primates) was endotheliochorial or haemochorial. It is argued that on balance the most likely ancestral condition is endotheliochorial. Comparative evidence across placentals clearly indicates that epitheliochorial placentation is not less efficient than more invasive forms of placentation, at least with respect to growth in overall fetal body mass. The ratio of neonate mass to gestation period (a simple indicator of average daily maternal investment in fetal growth) shows no difference according to placenta type. Differential evolution of placentation is hence presumably linked to immunological factors, parent/offspring conflict and/or genomic imprinting.

Maternal investment, life histories, and the costs of brain growth in mammals

“…Although it has been suggested that the structure of the placenta might influence nutrient transfer and hence prenatal brain growth (15,27), recent comparative studies find no evidence for a specific relationship between placental structure and brain growth (28,29). Capellini et al found that variation among mammals in placental structure correlated with fetal growth rates and gestation duration, but not with neonate brain size (28).…”

Placentation and Maternal Investment in Mammals

“…Placental gross morphology varies in the number and position of the exchange areas over the placental surface (shape), in how maternal and fetal tissues are spatially arranged with one another (interdigitation), and in the number of maternal tissue layers separating maternal blood from fetal tissues (invasiveness ;Mossman 1987;Leiser and Kaufmann 1994;Wooding and Burton 2008). Placental invasiveness is the trait that has received the most attention regarding a possible impact of placental morphology on offspring prenatal development and maternal investment, particularly in relation to brain growth (Kihlström 1972;Sacher and Staffeldt 1974;Leutenegger 1979;Haig 1993;Crespi and Semeniuk 2004;Elliot and Crespi 2008;Martin 2008). In noninvasive epitheliochorial placentation, three maternal tissue layers (uterine epithelium, connective tissues, and endothelium) constitute a barrier between fetal tissues and maternal blood (Mossman 1987;Leiser and Kaufmann 1994;Wooding and Burton 2008).…”

“…Haig (1993, p. 501) related placental invasiveness to maternal-fetal conflict, arguing that hemochorial placentation "evolved more than once as a means by which the fetus gained greater access to maternal nutrients." However, recent phylogenetic studies suggest that more invasive placentas (either hemochorial or endotheliochorial) are likely to be the ancestral condition for mammals, with the least invasive epitheliochorial placentation being an evolutionarily derived trait that emerged independently in several lineages (Vogel 2005;Mess and Carter 2006;Wildman et al 2006;Carter and Mess 2007;Martin 2008;Elliot and Crespi 2009). In a sense, therefore, it is the repeated evolution of less invasive placentas that is demanding of an explanation.…”

“…In a sense, therefore, it is the repeated evolution of less invasive placentas that is demanding of an explanation. Although suggestions have been made about possible correlates of evolutionary changes in placentation (reviewed in Martin 2008), such associations have not been systematically investigated, and as a result the functional consequences of placental variation remain obscure.…”

Advances in flow cytometry in basic and applied equine andrology

“…That has been confirmed numerous times though there is disagreement about whether the plesiomorphic state is endotheliochorial (Mess and Carter, 2006;Martin, 2008) or haemochorial (Wildman et al, 2006;Elliot and Crespi, 2009). …”