Conservation of placentation during the tertiary radiation of mammals in South America

Abstract

The eutherian placenta is considered to possess great plasticity, but it is not clear how this variation reflects adaptation to different ecological niches. Because South America was isolated for most of the Tertiary, it represents a natural laboratory to examine this question. We here describe placentation in three South American groups: Xenarthra have been part of the fauna from at least the mid-Paleocene whereas caviomorph rodents and Neotropical primates are each derived from a single founder that reached South America in the Eocene and Oligocene, respectively. The common ancestor of Xenarthra had a villous, haemochorial placenta, from which the labyrinthine, endotheliochorial placenta of sloths later evolved. Placentation in Caviomorpha follows an extraordinary stable pattern, characterized by a haemomonochorial, labyrinthine and highly lobed structure with specialized growing areas. This pattern was present before arrival of these rodents in South America and enabled a successful radiation especially during the spread of grasslands. Neotropical primates have haemochorial, trabecular placentas with a specialized maternal blood supply; a pattern that contrasts with that of Old World monkeys and may have been present in the founder generation on arrival in South America. In conclusion, there is a dichotomy within Xenarthra but otherwise the ancient South American mammals do not show much variation in principal placental characters. Thus, the successful radiation of these three groups, and their adaptation to diverse ecological niches, did not require substantial alterations in placentation.

Placental Evolution within the Supraordinal Clades of Eutheria with the Perspective of Alternative Animal Models for Human Placentation

“…Most of these features exhibit parallels to humans [119]. In humans the syncytiotrophoblast is formed from proliferative cytotrophoblast cells and we have suggested that the cytotrophoblast cells in xenarthran species have a similar function [52]. However, the villous pattern in anteaters (giant anteater Myrmecophaga tridactyla, lesser anteater Tamandua tetradactyla, and two-toed anteater Cyclopes didactyla) is much simpler in terms of developmental differentiation and more similar to humans than the condition in armadillos.…”

“…Among 2 Advances in Biology them are nonmurine rodents native to South America and Africa [26][27][28][29][30][31][32][33][34][35][36][37][38][39][40], as was shown by Figure 2, bats [41][42][43], anteaters and armadillos [44,45], and some other taxa [46][47][48][49][50][51]. Also, there were several promising attempts to reinvestigate historical histological material from museum collections such as neotropical primates [52] or great apes [53][54][55][56] in order to answer open questions.…”

“…Also, villous placentation occurs in Old World monkeys and great apes that has been convergently evolved in armadillos and anteaters [45,71]. In some taxa, neotropical primates for instance, the villi are connected by bridges of trophoblast (usually syncytial trophoblast), resulting in a trabecular condition [52,71]. A peculiar type in most placentas with a diffuse shape and some of the zonary type is that the villous trees interdigitate with corresponding areas in the uterine wall, forming, for instance, the placentomes of ruminants.…”

“…They are known from the fossil record from the mid Paleocene onward, but their origin may be older [52,76,90,[111][112][113]. There are three morphologically distinct subgroups that contain relatively few species.…”

“…Besides their systematic position, armadillos and anteaters are more similar to each other in sharing a villous and hemochorial type of placentation [44,45,[115][116][117], in contrast to the sloths that are characterised by lobulated, labyrinthine, and endotheliochorial placentas [24,118]. The similarity between the two former taxa suggests that their condition occurred in the ancestral condition or last common ancestor of Xenarthra, whereas the endotheliochorial placenta of sloths likely is a derived state that evolved after the dichotomy of sloths and anteaters [52]. From the standpoint of animal models for human placentation, xenarthrans are usually not much taken into consideration [68,71].…”