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

Abstract

Analysis of molecular data sets has provided new insights into higher-level relationships of living Eutheria, including the recognition of Afrotheria as a novel taxon. This offers an opportunity to take a fresh look at the evolution of organ systems, including some that are little used in traditional systematics. In the present study, we attempted a reconstruction of the evolution of characters associated with placentation, the fetal membranes and the female reproductive tract. The evolutionary history of 21 characters has been traced, based on a current hypothesis of eutherian relationships, by applying the computer program MacClade. Accordingly, the analysis provides a first comprehensive interpretation of the stem species pattern of Eutheria. Of particular note, this pattern includes an endotheliochorial chorioallantoic placenta. The reconstructed pattern of Eutheria does not change in the basal nodes of the group. Thus, no character transformations occur on the stem lineages of Laurasiatheria or Euarchontoglires, and even Afrotheria has mostly plesiomorphic character conditions. However, two character transformations occur on the common stem lineage of Afrotheria and its sister taxon Xenarthra, i.e., amniogenesis by cavitation instead of folding and the precocial state of the newborn. In addition, we recognized one character transformation on the stem lineage of Afrotheria, i.e., the occurrence of a four-lobed allantoic sac. Thus, contrary to previous assertions, it is possible to identify morphological characters that could be synapomorphic for this novel taxon.

Evolution of the placenta and associated reproductive characters in bats

“…To reconstruct the evolution of characters associated with placentation, early ontogeny, the female reproductive tract and the neonate in Chiroptera, we followed an approach that had been successful in several earlier studies (see Mess and Carter, 2006). Respecting available information as far as possible (Tables 1 and 2), we first defined a set of characters and character states.…”

“…Thus, the distribution of each character was mapped on a pre-existing phylogeny, using the most recent tree of molecular phylogenetics (Miller-Butterworth et al, 2007) that is in broad agreement with other, similar studies. A major advantage of presumed character optimization by MacClade is that it allows one to cope with large data sets, both of characters and taxa, and to handle missing data (see Mess and Carter, 2006). Characters were coded as unordered to avoid a priori assumptions about character evolution.…”

“…These species have been regarded as providing ancestral conditions of Placentalia (e.g. Luckett, '76;Mossman, '87;Mess and Carter, 2006). This approach was chosen because of the basal position of Chiroptera within Laurasiatheria (Murphy et al, 2001) and the derived form of placentation in other orders (Vogel, 2005;Mess and Carter, 2006;Wildman et al, 2006), which makes most members of Laurasiatheria of limited value for analyzing the course of placental evolution in bats.…”

“…This approach was chosen because of the basal position of Chiroptera within Laurasiatheria (Murphy et al, 2001) and the derived form of placentation in other orders (Vogel, 2005;Mess and Carter, 2006;Wildman et al, 2006), which makes most members of Laurasiatheria of limited value for analyzing the course of placental evolution in bats. Finally, we compared the results of the current analysis with reconstructions on placental and fetal membrane characters in the stem species pattern of Placentalia (Vogel, 2005;Mess and Carter, 2006;Wildman et al, 2006) and Chiroptera (Simmons and Geisler, '98;Gunnell and Simmons, 2005).…”

“…However, the placenta and other fetal membranes exhibit a high degree of diversity (Mossman,'37;Amoroso,'52;Starck,'59). Scenarios for the evolution of these systems have been published for several placental groups (Mess, 2003;Mess and Carter, 2006;Klisch and Mess, 2007). Although there has been considerable progress in understanding reproductive traits in Chiroptera (e.g.…”