Review
Evolution and development of fetal membranes and placentation in amniote vertebrates

https://doi.org/10.1016/j.resp.2011.03.029Get rights and content

Abstract

We review aspects of fetal membrane evolution and patterns of placentation within amniotes, the most successful land vertebrates. Special reference is given to embryonic gas supply. The evolution of fetal membranes is a prerequisite for reproduction independent from aquatic environments. Starting from a basically similar repertoire of fetal membranes – the amnion, chorion, allantois and yolk sac, which form the cleidoic egg – different structural solutions for embryonic development have evolved. In oviparous amniotes the chorioallantoic membrane is the major site for the exchange of respiratory gases between fetus and outer environment. The richly vascularised yolk sac and allantois in concert with the chorion play an important role in the evolution of placentation in various viviparous amniotes. Highly complex placentas have evolved independently among squamate sauropsids and in marsupial and placental mammals. In conclusion, there seems to be a natural force to improve gas exchange processes in intrauterine environments by reducing the barrier between the blood systems and optimising the exchange areas.

Introduction

The evolution and establishment of additional fetal membranes such as the amnion, the allantois and the chorion, enclosed in a calcified eggshell, allowed the vertebrates to live and reproduce independent of aquatic environments and led to the successful evolution of terrestrial vertebrates (amniotes) (Westheide and Rieger, 2010). Fetal membranes are essential to embryonic development, providing functions for embryonic respiration, nutrition, protection and excretion. In amniotes a new type of egg evolved, the amniotic or cleidoic (“enclosed”) egg, in which the embryos are contained independent of aquatic surroundings. These innovations contributed to the striking evolutionary and ecological diversity of amniotes from early Paleozoic times onwards, helping to make them the most successful group of tetrapods (Mess et al., 2003). Major evolutionary radiations have led to renowned taxa such as the mammals as well as the birds and other sauropsids (Fig. 1, Appendix A; Mess et al., 2003, Westheide and Rieger, 2010). In addition, diverse reproductive strategies have evolved, many of them associated with specialized feto-maternal structures to nourish the embryo (Mess et al., 2003). Starting from a basically similar repertoire of fetal membrane structure, a remarkably wide variety of placental types established (Mossman, 1937, Mossman, 1987). Among the adaptations that occurred during amniote evolution there are several important characteristics that meet respiratory requirements of the developing embryo. Here we review aspects of fetal membrane evolution and patterns of placentation within amniotes with special reference to embryonic gas supply.

In the beginning, we would like to clarify some terminological aspects. The evolution of placentation in vertebrates is linked to the evolution of viviparity, a reproductive pattern in which the females retain their eggs to term and give birth to their young. Such “live-bearing” species (e.g. lizards, snakes, eutherians, marsupials) are termed “viviparous” to distinguish them from “oviparous” animals (birds, monotremes), in which females deposit eggs (Blackburn, 1993). In viviparous amniotes, the fetal membranes have taken on specialized functions for embryonic nutrition and respiration inside the maternal reproductive tract. This leads to another aspect of classifying reproductive patterns in vertebrates – independent from the product deposited by the female, but characterized by the source of nutrients for embryonic development (Blackburn, 1993, Mess et al., 2003). In lecithotrophic animals – either oviparous or viviparous – nutrients are derived mainly from the yolk of the ovulated egg. This is especially the case in amniotes, which usually have macrolecithal eggs, e.g. birds, turtles, crocodiles, snakes, and monotremes. In such animals respiration is usually facilitated by the fusion of two extraembryonic membranes, the chorion and the allantois, which build the chorioallantoic membrane (CAM). In contrast, many viviparous species rely on “matrotrophy” or “placentotrophy,” in which substantial quantities of nutrients following ovulation are supplied by the maternal organism. This is the case in squamates, eutherians and marsupials. Placental tissues connect the fetal and maternal organisms in order to nourish the developing young. Placentas are found in several taxa among the amniotes, i.e. in various squamate sauropsids and in mammals.

The placenta developed as a multi-functional organ of physiological exchange between mother and conceptus (Starck, 1975, Mossman, 1987). The initially small area of fetomaternal apposition is usually enormously increased by folding and refolding as it proliferates in parallel with the growth of the developing embryo or fetus (Wooding and Flint, 1994). The main functions of the placenta are to act as a surrogate fetal lung, gut, and kidney and to camouflage the usually allogeneic fetus from the maternal immune system (Lala et al., 1983, Gill and Wegmann, 1987, Wooding and Flint, 1994, Cross et al., 2003, Blackburn and Flemming, 2009, Carter, 2009, Banet et al., 2010, Chuong et al., 2010). The main principles of placentation lead to contradictory effects.

(1) On one hand, the provision of the fetus requires efficient exchange of a wide range of metabolites and hormones, which is favored by a reduction in the separation of fetal and maternal blood flows (Moll, 1985, Munro, 1986). Among the various functions, it facilitates gas exchange for the fetus (e.g. Bartels, 1970, Schröder, 1995, Mess and Carter, 2007, Carter, 2009, Enders, 2009, Mess and Ferner, 2010). Gas exchange in the placenta is regarded to be less efficient than in other organs such as the lung, because the minimum diffusion distance is larger and the permeability of the blood–blood barrier is lower than the permeability of the blood–gas barrier in the lung (Brandis, 2002, Mess and Ferner, 2010).

(2) In contrast, the immunological camouflage is vital to avoid recognition by cellular and hormonal mechanisms mediating sensitization and immune rejection and is best served by the provision of a barrier between the two circulations (Amoroso and Perry, 1975, Mess and Carter, 2007). Finally, since the requirements for fetal supply and camouflage are so complex and mutually antagonistic (Zeh and Zeh, 2000), a wide variety of structures has evolved to harmonize the contradictory effects. Further constraints of gross size, habitat (e.g. arboreal or aquatic) and lifestyle (e.g. altricial versus precocial offspring) modify the requirements defining a successful placenta (Elliot and Crespi, 2009). Perhaps because of these various conflicting pressures, there is no straightforward progression to a unique ‘best’, most efficient placenta. Different groups have developed different structural solutions (Wooding and Flint, 1994, Mess et al., 2003).

Section snippets

Starting point: fetal membranes in (amniote) vertebrates

The remarkably wide variety of structures in the mature placenta developed from a basically similar repertoire of membranes typical for the amniotic egg: the amnion surrounding the embryo, the chorion, the yolk sac and the allantois. The latter could serve as a placenta in association with the chorion (Fig. 2A; Steven, 1975, Mossman, 1987, Mess et al., 2003). We prefer the term fetal membranes because of common acceptance (instead of extraembryonic membranes or other terms; see Mess et al., 2003

Sauropsida in general

The majority of sauropsid amniotes (turtles, crocodiles, most lizards, birds, see Appendix A) are egg-laying amniotes with a full complement of fetal membranes (Mess et al., 2003, Westheide and Rieger, 2010). The adoption of viviparity, associated with the evolution of placentation, may be an adaptation to extreme habitats and has occurred many times among squamate sauropsids, especially in lizards and snakes (Weekes, 1935, Shine and Bull, 1979, Blackburn, 1993, Blackburn, 1998, Stewart and

Aves

Birds – a subgroup of Sauropsida (Fig. 1, Appendix A) – are the only amniotes without viviparous forms. They have the full complement of embryonic membranes in the egg with very little variation despite enormous differences of habitat and size. The four membranes, the yolk sac, amnion (or amnios), chorion, and allantois develop very early from the ventral portion of the embryo (Romanoff, 1960). Of these, the chorion–allantois and to a minor extent the yolk sac are concerned with gas exchange (

Monotremata

Among mammals Monotremes, including the aquatic platypus and the echidnas or spiny anteaters, are of great interest because of their combination of basal and derived reproductive characters. One characteristic is that females are oviparous. It sets monotremes apart from other mammals (Fig. 1, Appendix A). This is interpreted as “reptile feature” or ancient condition among amniotes. However, oviparity of the Monotremata is in many aspects different from the recent sauropsids: their eggs are

Marsupialia

Although Marsupialia are viviparous, their ontogenesis resembles in many ways that of monotremes (Zeller, 1999). Both groups share similarities that most likely represent basal or plesiomorphic characteristics of mammals: The development of newborn marsupials corresponds to that of monotremes at hatching (Griffith, 1978, Renfree, 1991). Even though marsupials do not have an eggshell, a shell membrane is present throughout major parts of pregnancy. It is permeable for small molecules and

Eutheria

Eutheria form by far the largest group of mammals and one of the most successful groups among terrestrial vertebrates (Westheide and Rieger, 2010). Their viviparous mode of reproduction is associated by an exceptional structural and functional diversity of placentation (Mossman, 1987, Mess and Carter, 2006, Mess and Carter, 2007). Recently a revolution took place in eutherian systematics in that molecular phylogenetics led to a completely new higher-level relationship, including the

Conclusion

A primary distinction with respect to reproduction occurs between the two major groups of animals that are adapted to live on land. Frogs, salamanders and other amphibians are classed as Lissamphibia or An-Amniota, because of their bi-phase lifestyle with adult life on land and reproduction in aquatic environments. Although they are fascinating animals, their evolutionary success measured for instance by species richness is limited.

In contrast, Amniota as the dominating land vertebrates form an

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