Comparative Placentation

Anthony M Carter, University of Southern Denmark, Odense, Denmark

© 2018 Elsevier Inc. All rights reserved.

Glossary
Chorioallantoic placenta Placenta of which the fetal components are trophoblast and allantois.
Choriovitelline placenta Placenta of which the fetal components are trophoblast and yolk sac.
Hemotrophic nutrition Exchange of oxygen and nutrients between maternal and fetal blood.
Histotrophic nutrition Supply of nutrients as uterine secretions, cell debris or red cells taken up to the placenta by pinocytosis
or endocytosis.
Lecithotrophy Nourishment of the embryo by egg yolk.
Matrotrophy Nourishment of the embryo by maternal sources other than egg yolk.
Oophagy Ingestion of eggs by the embryo.
Placentotrophy The supply of oxygen and nutrients through a placenta.
Viviparity Bearing of live young.

Introduction

Viviparity has evolved in many types of animal. The embryos may be retained in the reproductive tract or some form of breeding
chamber, yet rely exclusively on the nutrients provided by the yolk (lecithotrophy). More often viviparity is accompanied by
provision of nutrients to the embryo by one or both parents (matrotrophy) (Blackburn, 2015). Matrotrophy takes many forms,
but supply of oxygen and nutrients through a placenta is the main focus of this article.
A recent survey found evidence of matrotrophy in 21 of 34 animal phyla (Ostrovsky et al., 2016). It is common in flatworms,
arthropods and bryozoans. In arthropods alone, matrotrophy is estimated to have evolved around 30 times. Arrangements for
enhancing nutritional transport from parent to embryo take several forms. In velvet worms and arthropods they include placental
analogs that mimic vertebrate placentation.
Even among chordates there are several variants of placentation, including the incubation chamber of salps described by Thomas
Huxley (Lemaire and Piette, 2015). Salps are tubular animals found near the surface of oceans, where they swim by jet propulsion.
The life cycle of salps involves alternation between asexual and sexual generations. The asexual phase (oozooid) develops within the
jet chamber of the sexual phase (blastozooid). The placenta consists of two layers separating the embryonic and maternal
circulations. Both layers are syncytial and maternal in origin.

Placentation in Anamniotes

Prior to evolution of the cleidoic egg, the yolk sac was the only fetal membrane, but non-amniotes have a long history of
placentation. The males of some placoderms, the earliest jawed fishes, had clasper-like appendages, like those of modern sharks,
suggesting they practiced intromission of sperm. From intromission, it is but a short step to matrotrophy and placentation. A
remarkable fossil from Western Australia shows fetuses one-third of adult body size. This specimen (Materpiscis attenboroughi)
was so well preserved that it was possible to identify a vitelline cord and show by high resolution computer tomography that it
contained blood vessels. Thus viviparity and placentation in vertebrates dates back to the Devonian period, about 380 million years
ago (Long et al., 2008).

Cartilaginous Fish
All chondrichthyans, including the basal holocephalans, employ internal fertilization (Hamlett et al., 1993). Many lay eggs but
around 55% are viviparous; most of these practice some form of matrotrophy. Examples not involving placentation are oophagy
and cannibalism of siblings, which occurs in mackerel sharks. Supplementation of yolk by uterine secretions or histotroph occurs in
several species. Thus in sawfish histotroph is secreted by uterine villi. In stingrays, there are elaborate outgrowths from the uterine
wall called trophonemata. They secrete lipid-rich histotroph and are also considered important for gas exchange.
There are instances where nutrition is essentially lecithotrophic yet maternal-fetal exchange of blood gases occurs across
placenta-like structures. This can be difficult to assess in the absence of functional data. As an example, the embryos of viviparous
dogfish derive their nutrition from yolk, but highly vascularized uterine villi act as a source of oxygen, and late embryos use buccal
pumping to perfuse their gills and take up oxygen from the uterine fluid. However, modelling of gas exchange in dogfish (Squalus

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spp.) has shown that oxygen diffusion across the uterine wall cannot provide sufficient oxygen to late stage embryos. Additional
oxygen may be supplied through periodic flushing of the uterus with seawater (Tomita et al., 2016).
True placentation occurs in requiem and hammerhead sharks (Carcharhiniformes), where gestation lasts 9–10 months. Initially,
the embryo is supported by yolk. When this has been used up, the yolk sac persists and forms a placenta. In the sandbar shark, for
example, there are well vascularized elevations of the uterine attachment site that interdigitate with the distal portion of the yolk sac.
The uterine secretion products may be similar to yolk proteins.

Bony Fish
Viviparity has arisen in 13 clades of teleost fish including the coelacanth (Latimeria chalumnae), a relict of the lobe-finned fish.
Studies in viviparous poeciliid and cichlid fish have shown that placentation can evolve quite rapidly.
Teleosts do not possess uteri or oviducts. Ovulation occurs into the ovarian lumen, which is connected to the exterior by a duct
opening at the genital pore. Consequently, the embryos of viviparous fish develop either in the ovarian follicle or in the ovarian
lumen (Schindler and Hamlett, 1993). In intraluminal gestation, the ovarian lining becomes highly vascularized and secretes
histotroph to the lumen where the embryos develop. In goodeid fish appendages called trophotaenia, which protrude from the
cloaca, serve as absorptive surfaces. Otherwise absorption of histotroph is through the embryonic gut. In viviparous brotulas
(Ogilbia) projections from the ovarian lining protrude into the mouth of the embryo (ovarian nipples).
Where development is intrafollicular, the follicular epithelium answers for transfer of nutrients from the maternal circulation to
the follicular fluid. Absorptive surfaces of the embryo may be closely apposed to this epithelium forming placenta-like structures.
The embryonic component may be the yolk sac. However, in the four-eyed fish (Anableps), the pericardial trophoderm develops
bulbs that interdigitate with pit-like depressions in the follicular epithelium (Knight et al., 1985).
Viviparity in seahorses and pipefish involves incubation of the embryos in the brood pouch of the male. Analysis of the
transcriptome of the brood pouch of the pot-bellied seahorse has identified the genes that are upregulated during pregnancy.
Many of the same genes or their homologs are upregulated during pregnancy in mammals (Whittington et al., 2015).

Amphibians
Viviparous species occur in all three orders of amphibians (Wake, 2015). Live-bearing in frogs enables them to abandon their
amphibious lifestyle for a more terrestrial one. In the marsupial frogs from South and Central America (Hemiphractidae), the
embryo develops on the back of the mother in either a mucous-filled depression or a closed pouch (Duellman, 2014). The embryos
may develop into tadpoles and be released to water-filled cavities in plants or skip the tadpole stage and develop directly into
froglets. In embryos of the genus Gastrotheca, 1–2 pairs of external gills serve for respiratory gas exchange with maternal tissues
in the brood pouch. The gills are shed around the time of birth. A similar strategy has been adopted by frogs in the Neotropical
genus Pipa (Pipidae) where the eggs develop to tadpoles within individual chambers in the dorsal skin (Fernandes et al., 2011).
The chambers become highly vascularized suggesting that gas exchange could occur between mother and embryo. Recently, nutrient
transfer from pouch to embryo has been shown to occur in Gastrotheca (Warne and Catenazzi, 2016).
Female frogs of the extinct genus Rheobatrachus ingested the fertilized eggs and incubated them in the stomach. The developing
embryos secreted prostaglandin to inhibit gastric secretion. Male frogs of Rhinoderma darwinii ingest eggs and brood the embryos
within their vocal sacs; there is evidence in support of nutrient transfer from the paternal circulation to the embryos. There are
a few examples of frog larvae developing to froglets within the oviduct, although maternal provision of nutrients other than
yolk has been documented only for the Mount Nimba viviparous toad (Nimbaphrynoides occidentalis).
Caecilians comprise an order of limbless amphibians adapted for a burrowing lifestyle. They embrace both oviparous and
viviparous species. In the former there is extended parental care with the hatchlings feeding on the outer layer of the parent’s
skin. In viviparous caecilians, the fetuses have teeth and feed on the hypertrophied lining of the oviduct (Wilkinson et al.,
2008). A few species of salamander are viviparous. Embryos of the alpine salamander (Salamander atra) ingest unfertilized eggs
and feed on the hypertrophied epithelium of the oviduct. Placental analogs have not been described for caecilians or salamanders.

The Fetal Membranes of Amniotes

Whereas placentation in anamniotes often is based on the yolk sac, the cleidoic egg offers three more membranes that can be
recruited for placentation (Mossman, 1987; Carter, 2016). These are the amnion, allantois and chorion (Fig. 1(A)). The
fluid-filled amnion surrounds the embryo and offers protection from desiccation and mechanical shocks. The allantois is a pathway
for gaseous exchange with the ambient air and its cavity is a receptacle for waste. Outermost is the chorion, which in birds and
reptiles is situated beneath the egg shell.
Various combinations of these membranes form the basis of placentation in reptiles and mammals (Fig. 1(B)). The chorioal-
lantoic placenta is formed by the chorion and allantois. It is the basis for placentation in viviparous lizards, some marsupials and
extant eutherians (known misleadingly as “placental mammals”). The chorionic epithelium constitutes the trophectoderm (in
mammals the trophoblast). The chorionic mesoderm supplies the blood vessels. The choriovitelline placenta is formed by the
chorion and yolk sac. There may be a substantial vasculature. This type of placenta is found in all marsupials. In addition,
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Fig. 1 Fetal membranes that contribute to placentation in reptiles and mammals. (A) The amniote egg as in birds, oviparous reptiles and
monotremes. (B) Embryo and fetal membranes within the uterus of a generic mammal. The chorion (CHOR) is found beneath the egg shell (ES) in
the former and facing the uterine wall (UT) in the latter. In birds and reptiles the other membranes enclose the amniotic sac (AM), allantoic vesicle
(ALL) and yolk sac (YS). In mammals and viviparous reptiles, yolk sac and chorion can form a choriovitelline placenta and the allantois and chorion
can form a chorioallantoic placenta. Reproduced with permission from Carter, A.M., Mess, A.M., 2014. Mammalian placentation: Implications for
animal models. In: McManus, L., Mitchell, R. (Eds.), Pathobiology of Human Disease. San Diego, CA: Elsevier, pp. 2423–2442. © 2014 Elsevier.

non-vascular areas of the yolk sac can play a role in uptake of histotroph in marsupials, viviparous lizards and some eutherians. As
described below, viviparous snakes have a third type of placenta derived from the allantochorion and a derivative of the yolk sac.

Placentation in Reptiles

Like birds, the non-avian dinosaurs generally had calcified eggs and fossil evidence of viviparity is restricted to the aquatic ichthyo-
saurs. Other extinct marine reptiles that were viviparous include archosaurs, mesosaurs and plesiosaurs. Among extant reptiles,
neither crocodilians nor tortoises and turtles are viviparous, but live birth does occur in squamate reptiles, including several families
of lizards and snakes (Blackburn, 2015; Stewart and Thompson, 2000).

Lizards
In oviparous and viviparous lizards the egg comprises two hemispheres with the chorioallantois covering the embryonic
compartment and the yolk sac occupying the abembryonic compartment (Fig. 2). A yolk cleft separates most of the yolk from
a smaller portion associated with the yolk sac ectoderm and endoderm (bilaminar omphalopleure). This membrane is a conduit
for water even in oviparous species. In viviparous ones the oviduct epithelium facing the yolk sac may proliferate and perhaps
secretes histotroph that can be taken up by the yolk sac.
However, in lizards with limited or extensive matrotrophy it is the allantochorion that develops into a placenta. Although four
types of allantochorion are recognized it is by no means certain that Types I and II are true placentas (Stewart and Thompson, 2000).
Type I occurs mainly in lecithotrophic species and the close association between the yolk sac and uterine epithelium may serve
solely for respiratory gas exchange. In Type III, on the other hand, interdigitating folds of maternal and fetal tissues form a placen-
tome. This has been best described for a number of skinks, including the Italian three-toed skink (Chalcides chalcides) and the
southern grass skink (Pseudemoia entrecasteauxii) from Australia. An even more complex placenta, designated Type IV, is found in
a genus of long-tailed skinks (Mabuya) from South America (Fig. 3). Altogether there has been convergent evolution of placentrophy
in six clades of skinks. Ample evidence exists for maternal-fetal transfer of nutrients across Type III and IV placentas. In addition
electron microscopy has indicated specializations for nutrient transfer even in lizards that are mainly lecithotrophic; these have
been characterized as cases of incipient placentotrophy.

Snakes
Some 20% of snakes are viviparous, but since there is no net increase in dry weight from egg to neonate, placental transfer of
nutrients may play a limited role in growth of the embryo. So far placentation has been described in just a handful of species.
As in lizards there are two distinct regions of placentation. The chorioallantois is similar to that of lizards. Recent work in water
snakes (Nerodia) has established that it is specialized for respiratory gas exchange since both the chorioallantois and the apposing
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Fig. 2 Extraembryonic membranes of a viviparous lizard, the southern grass skink (Pseudemoia entrecasteauxii). The embryonic compartment is
enclosed by the chorioallantois, which is apposed to hypertrophied uterine epithelium and the site of nutrient exchange. The bilaminar omphalopleure
encloses the yolk. It also faces hypertrophied uterine epithelium and constitutes a yolk sac placenta. Putative sites of placental function are based on
functional analysis of differentially expressed genes. Reproduced from Griffith, O,W., Brandley, M.C., Beloiv, K., Thompson, M.B., 2016. Reptile
pregnancy is underpinned by complex changes in uterine gene expression: A comparative analysis of the uterine transcriptome in viviparous and
oviparous lizards, Genome Biology and Evolution 8, 3226–3239. © The Author 2016.

Fig. 3 Placentation in a South American long-tailed skink (Mabuya sp.). (a) Uterus with placentome (chorioallantoic placenta), paraplacentome,
areolae and absorptive plaques. (b) Interface between the chorionic epithelium and syncytial uterine epithelium within the placentome. (c) Interface
within the paraplacentomal area and plaques. Reproduced with permission from Wooding, F.B.P., Ramirez-Pinilla, M.P., Forhead, A.S., 2010.
Functional studies of the placenta of the lizard Mabuya sp. (Scincidae) using immunocytochemistry. Placenta 31, 675–685. © 2010 Elsevier Ltd.
 Development and Anatomy of Reproductive Organs j Comparative Placentation 133

uterine epithelium are well vascularized (Blackburn et al., 2017). The yolk sac placenta of snakes is unique in that the allantois enters
the yolk sac cleft and expands to line the inner face of the omphalopleure. The resultant structure is known as an omphalallantoic
placenta. It has some ultrastructural features consistent with a role in nutrient transfer.

Placentation in Monotremes and Marsupials

Monotremes are egg-laying mammals, yet two-thirds of embryonic development takes place in the uterus. The embryo is nourished
partly by yolk and partly by endometrial secretions taken up through the egg shell membrane. This is porous and able to stretch so
the embryo and its membranes increase in size before the egg is laid.
Marsupials are poorly developed at birth and most of their growth occurs as pouch young. The intrauterine phase of develop-
ment is supported in all marsupials by a choriovitelline placenta and in some by an additional chorioallantoic one (Freyer and
Renfree, 2003; Renfree, 2010). A shell membrane persists through the first two-thirds of gestation and the principal source of
nutrition is uterine gland secretion. There are vascular and non-vascular parts to the yolk sac and both are able to absorb these
secretions. Although exchange of blood gases occurs between maternal capillaries and those of the yolk sac, there is scant evidence
of nutrient exchange by that route. A chorioallantoic placenta is found in the koala (Phascolarctos cinereus) and in bandicoots (e.g.,
Perameles nasuta). It is supplied by allantoic blood vessels and thought to function primarily as a respiratory organ. Interestingly,
chorioallantoic placentation is not associated with greater maturity of the neonate; in bandicoots it may rather contribute to
shortening of pregnancy duration. The marsupial placenta generally is considered to be epitheliochorial. However, invasive
trophoblast has been described in several opossums (e.g., Philander opossum) and in the fat-tailed dunnart (Sminthopsis crassicaudata).
The marsupial placenta secretes hormones, as evidenced by expression of growth hormone, prolactin and luteinizing hormone
genes in the placenta of the tammar wallaby (Macropus eugenii) (Menzies et al., 2011).

Placentation in Eutherian Mammals

Unlike in marsupials, the yolk sac plays a subsidiary role in eutherians, while all have a chorioallantoic placenta that supports the
fetus to term (Carter and Enders, 2004; Mossman, 1987; Wooding and Burton, 2008). Moreover the trophoblast is invasive except
in lower primates and three other orders (Carter et al., 2015). Gestation generally is much longer in eutherians (although shorter in
the mouse than the Eastern gray kangaroo). The newborn is better developed than in marsupials, but there is a striking difference
between species like the mouse, which give birth to altricial young, and those like the guinea pig that have precocial young. As a rule
mammals with precocial young have long gestations and small litters, sometimes just a single newborn, whilst the reverse applies to
species with altricial young. There is a remarkable variation in the shape, structure and vascular arrangements of the placenta, but no
consistent pattern in relation to gestation length or maturity of the young at birth. Humans are a special case in having a long preg-
nancy that results in a baby advanced in organ development yet entirely dependent on extended parental care. Portmann coined the
term “secondary altriciality” to describe this unique state of affairs.
The remarkable variation in the shape and structure of the placenta is summarized by order in Table 1. As to shape, human
placenta resembles a flattened cake; this type of discoid placenta is also found in rodents and several other orders. At the opposite
extreme, the diffuse placenta of swine occupies most of the uterine horn and resembles a large sac. In between are the placentas of
pecoran ruminants, with a variable number of small discs or placentomes, and the zonary placentas of carnivores.
The arrangement of fetal and maternal tissues in the placenta varies considerably. The most common pattern is a labyrinth.
Broadly speaking, fetal capillaries run in one direction and maternal capillaries (or blood channels) in the other, an arrangement
that promotes countercurrent exchange. An alternative design has interdigitation of fetal villi with maternal trabeculae that succeeds
in minimizing the distance between fetal and maternal capillaries but without countercurrent flow. This is common in the diffuse
type of placenta, as in dolphins, and in the placentomes of ruminants. In a small number of species, including catarrhine primates
and armadillos, there is a villous tree with fetal capillaries that is suspended in an intervillous space perfused by maternal blood.
Traditionally most attention has been directed to the fine structure of the interhemal barrier and the number of tissue layers
separating maternal and fetal blood (Fig. 4). In the epitheliochorial placenta, the uterine epithelium is intact and interdigitates
with the trophoblast (Fig. 4(a)). In pecoran ruminants the overall pattern is similar, but a remarkable feature is fusion of binucleate
trophoblast cells with uterine epithelial ones to form either a hybrid trinucleate cell (Fig. 4(b)) or syncytium. Some authors refer to
this as synepitheliochorial placentation. In endotheliochorial placentas, the only maternal tissue remaining is the capillary epithe-
lium, which frequently is hypertrophied (Fig. 4(c)). Finally, in hemochorial placentas, the trophoblast is directly in contact with
maternal blood. The latter may flow in small channels in a labyrinth (Fig. 4(d) and (e)) or perfuse an intervillous space (Fig. 4(f)).
While exchange between maternal and fetal vessels is the principal function of the mammalian placenta, there may be additional
supply of nutrients as uterine gland secretions, tissue debris or maternal red cells (Carter, 2012). This is particularly important where
the interhemal barrier is epitheliochorial. Thus artiodactyls and perissodactyls have prominent areolae and strepsirrhine primates
have chorionic vesicles. These structures contain columnar trophoblast cells arranged in proximity of the mouths of uterine glands
and with the ability to phagocytose and process glandular secretions. There are also structures with a more specialized function that
take up maternal red cells (hemophagous areas). Such modifications are not confined to epitheliochorial placentas; thus areolae are
found in moles and hemophagous areas in tenrecs, both of which have hemochorial placentation.
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Development and Anatomy of Reproductive Organs j Comparative Placentation
Table 1 The orders of mammals and the principle characteristics of their placentation including the yolk sac at term

Superordinal clade and

order Common names Placental shape Internal structure Interhemal barrier Yolk sac

Afrotheria
Hyracoidea Hyraxes Zonary Labyrinth Hemochorial Absent
Proboscidea Elephants Zonary Labyrinth Endotheliochorial Absent
Sirenia Manatees, dugong Zonary Labyrinth Endotheliochorial Missing data
Macroscelidae Elephant shrews Discoid Labyrinth Hemochorial Free
Afrosoricida Tenrecs, golden moles Discoid Labyrinth Hemochorial or endotheliochorial Free (large in golden moles)
Tubulidentata Aardvark Zonary Labyrinth Endotheliochorial Rudimentary
Xenarthra
Cingulata Armadillos Discoid Intervillous space Hemochorial Completely inverted visceral yolk
sac
Pilosa Sloths, anteaters Discoid or double discoid Intervillous space (anteaters) Hemochorial (anteaters) or Absent
or labyrinth (sloths) endotheliochorial (sloths)
Euarchontoglires
Primates: Strepsirhini Lemurs and lorises Diffuse Labyrinth Epitheliochorial Absent
Primates: Haplorhini Tarsiers, monkeys and apes Discoid or double discoid Labyrinth in tarsiers; Hemochorial Absent
intervillous space
Dermoptera Colugos Discoid Labyrinth Hemochorial Free
Scandentia Tree shrews Discoid Labyrinth Endotheliochorial Persistent choriovitelline placenta
Rodentia Rodents Discoid Labyrinth Hemochorial or endotheliochorial Inverted visceral yolk sac
Lagomorpha Rabbits, hares, pikas Discoid Labyrinth Hemochorial Inverted visceral yolk sac
Laurasiatheria
Cetartiodactyla Whales, dolphins, even-toed Diffuse; cotyledonary in Interdigitating villi Epitheliochorial Absent or free
ungulates pecoran ruminants
Perissodactyla Horses, tapirs Diffuse Interdigitating villi Epitheliochorial Absent or rudimentary
Chiroptera Bats Discoid or double discoid Labyrinth Hemochorial or endotheliochorial Free or with inverted visceral yolk
sac
Carnivora Carnivores Zonary Labyrinth Endotheliochorial or hemochorial Persistent T-shaped visceral yolk
(hyenas) sac
Pholidota Pangolins Diffuse Interdigitating villi Epitheliochorial Smallvisceral yolk sac
Soricomorpha Shrews, moles, solenodons Discoid; zonary in some Labyrinth Hemochorial or endotheliochorial Inverted visceral yolk sac
moles
Erinaceomorpha Hedgehogs, gymnures Discoid Labyrinth Hemochorial Inverted visceral yolk sac
 Development and Anatomy of Reproductive Organs j Comparative Placentation 135

Fig. 4 Interhemal barrier of representative mammals. (a) Epitheliochorial placenta of the bush baby (Otolemur crassicaudatus). (b) Synepitheliocho-
rial placenta of the cow (Bos taurus); note the binucleate trophoblast cells (asterisks) and trinucleate cells (arrows). (c) Endotheliochorial placenta of
a bat (Natalus sp.); note the enlarged endothelial cells of the maternal capillary in contact with the trophoblast. (d) Hemotrichorial labyrinthine
placenta of the mouse (Mus musculus). (e) Hemomonochorial labyrinthine placenta of the guinea pig (Cavia porcellus). (f) Hemomonochorial villous
placenta of an armadillo (Dasypus novemcinctus). CYTO TR, cytotrophoblast; ENDO, Endothelium; FC, fetal capillary; MC, maternal capillary; MBS,
maternal blood space; MES, enlarged mesenchymal cell; SYN TR, syncytial trophoblast; T1, trophoblast layer 1 (cellular); T2, trophoblast layer 2
(syncytial); T3, trophoblast layer 3 (syncytial); UT EP, uterine epithelium. Based on material kindly supplied by Dr. Allen C. Enders, University of
California at Davis, United States. Reproduced with permission from Carter, A.M., Mess, A.M., 2014. Mammalian placentation: Implications for animal
models. In: McManus, L., Mitchell, R. (Eds.), Pathobiology of Human Disease. San Diego, CA: Elsevier, pp. 2423–2442. © 2014 Elsevier.
136 Development and Anatomy of Reproductive Organs j Comparative Placentation

There are no consistent patterns that can explain the variation of the chorioallantoic placenta in terms of parameters such as
gestation length or developmental stage at birth. For example, the highly invasive nature of human placentation and the dilated
vessels that supply the maternal side of the placenta seem designed to maximize the oxygen supply to the fetus and the fetal brain.
But newborn whales and dolphins also have large brains, yet their development is supported by a non-invasive epitheliochorial
placenta. It is striking that even-toed and odd-toed ungulates have small litters, long gestations and epitheliochorial placentation.
A case can be made that evolution of this placental type conveyed an immunological advantage. On the other hand the African
elephant gives birth to a single calf after 22 months, but has an endotheliochorial placenta.
There is further variation in the part played by other fetal membranes in various orders of eutherians. In particular, the visceral
yolk sac may persist until term (Carter, 2016). As a rule there has been inversion of the germ layers at an early stage so that the yolk
sac presents an absorptive epithelium, the yolk sac endoderm, to the uterine wall as in rodents, lagomorphs and some bats (inverted
visceral yolk sac; Table 1). This may be a conduit for the transfer of maternal antibodies that confer passive immunity on the fetus.
In many orders, however, the yolk sac is absent at term or is a small sac floating free in the exocoelom (Table 1). Passive immunity
may then be conferred by antibodies crossing the chorioallantoic placenta. In orders with epitheliochorial placentation, on the
other hand, passive immunity is conferred after birth by antibodies secreted to the colostrum. Finally, in many bats, the yolk sac
assumes the morphological characteristics of a gland of unknown function.

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