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Most vertebrates lay eggs. In reptiles and birds, the embryos are surrounded by a layer of albumen, a shell membrane, and a shell. These layers are present in monotreme mammals which lay eggs and some of these layers may be retained in live-bearing mammals as well. Marsupial embryos are surrounded by a zona pellucida, albumen, and a shell membrane. Placental embryos have a zona pellucida and a thin layer of albumen but have no trace of a shell or shell membrane (Mossman, p.31). In marsupials, the keratinous shell membrane is usually lost after the embryo reaches the uterus but may last until birth in some species (Mossman, p. 55).
Most bony fish and amphibians lay eggs before they are fertilized, and thus embryonic development occurs outside the body of the female. In most cartilaginous fish, reptiles, and all birds fertilization occurs inside the body of the female. While most of these groups lay eggs, reproduction through live birth (viviparity) is known in some species. Viviparity seems to have evolved separately about 132 times in amniotes: once in ancestral mammals, once in ichthyosaurs, and about 100 times in lizards in snakes, in 16 of the 27 families. (Thompson, 2002; Blackburn, 1992). Skinks are the largest family of squamates (with about a third of lizard species). Many skinks are viviparous and some have evolved a placenta to nourish the fetuses. The only 5 groups of squamates with complex placentae are skinks, including members in 2 of the 4 subfamilies. Viviparity and oviparity can not only be found in the same family, the can exist in the same subfamily, such as the skink subfamily Lygosominae. Within subfamily Lygosominae, there are 3 species groups. The Eugongylus species group contains both oviparous and viviparous species and the viviparous species have at least 2 types of placenta (Thompson, 2002).
In addition to these amniotes, there are viviparous cartilaginous fish, actinopterygian bony fish, sarcopterygian bony fish (coelocanths), and amphibians (Mossman, p.3). Thus a number of anamniote lineages have evolved vivparity separately as well, given that the mechanisms of live birth in these various groups are so different enough to preclude common ancestry (such as in the mechanisms of live birth in the two bony fish Heterandria and Cymatogaster), (Mossman, p. 13). The lizard genus Scleroporous includes viviparous and oviparous species.
Among live-bearers, the mother can provide
substantial nutrition to the fetuses in addition to what is present in
the yolk. This type of prenatal
investment (matrotrophy) is thought to have arisen
about 24 times occuring in placental mammals,
some bony fish, cartilaginous fish, lizards, and caecilians (
It is interesting that all amniote embryos share the same extraembryonic membranes whether they develop in eggs or inside the body of the female. Amniotes share four extra-embryonic membranes: the yolk sac, allantois, amnion, and chorion. In all amniotes, these extra-embryonic membranes develop much faster than the embryo itself and an early embryo invests more cells into these membranes than into what will later become the embryo’s body. In the illustrations used in this chapter, the amnion will be depicted with a light blue, the chorion with red (and the chorionic cavity with a light red), the yolk sac with yellow, and the allantois with green. In some illustrations, the maternal tissue will be represented with purple.
In the following illustration of a oviparous lizard (egg-laying; the egg shell is not included in the drawing), the primitive amniote condition is seen. Development occurs in the fluid of the amnion. The yolk sac provides the nourishment for the developing embryo and fetus and the allantois collects wastes which develop during development. The chorion performs gas exchange with the outside world through the egg shell. Monotremes (the platypus and echidnas) reproduce by laying eggs and their extra-embryonic membranes perform the same essential functions as observed in their homologs in reptiles.
|The same set of extra-embryonic membranes present in egg-laying lizards are present in lizards which give birth to live young as well. The initial transition to viviparity apparently does not require a significant reorganization of the extraembryonic membranes of egg-laying ancestors.|
The amnion doesn’t vary much in amniotes. It surrounds the embryo and is filled with an amniotic fluid. As a result, amniote embryos can develop in a watery environment as do the embryos of fish and most amphibians. This amnion was critical in the adaptation of amniotes to terrestrial environments. Although humans are terrestrial animals, we spend our first 9 months surrounded by fluid. In some mammals the amnion fuses to the chorion (such as anthropoid primates including humans) while in others it fuses with the allantois (as in carnivores and artiodactyls) (Mossman, p. 59).
In birds and reptiles, the chorion is the extraembryonic membrane which lies just deep to the eggshell and performs gas exchange between the developing embryo and the outside world. In viviparous animals, the chorion performs gas exchange between the embryo and the environment of the uterus, inside the body of the female. In placental mammals, the chorion composes the fetal portion of the placenta.
What is a placenta? Placental mammals possess a chorioallantoic placenta, in which the placenta is composed of maternal uterine tissue and fetal chorionic tissue with blood vessels derived from the allantois. This is not the only type of placenta, however. In some placental mammals, the yolk sac may contribute blood vessels to the placenta at an early stage, creating a transient choriovitelline placenta. If the definition of placenta is widened to refer to maternal and fetal tissues which interact and allow for the exchange of substances, then placentas are not confined to placental mammals. In fact, at least a few members of all vertebrate groups except for birds, jawless fish (represented by two modern kinds), and monotremes possess placentas, using that definition (Mossman, p. 3)
In some embryonic fish, the pericardium may
be expanded to the point where it forms a pseudoamnion
and a pseudochorion around the neck. In Heterandria
In one frog, extensions to the gills function for the exchange of materials with maternal tissue while the larvae develop in pouches on the back of the parent. In the viviparous salamander Proteus, larval gill filaments contact the uterine mucosa. Of course, there are other ways to provide nutrients for the young in utero. In the genus Salamandra, 40-60 eggs are produced of which only one or two are born alive. The young feed on the remaining eggs and even some maternal blood once their yolk is exhausted (Mossman, p. 22-4). In amphibians, the gills and tailfin may serve as placental structures (Mossman, p. 142). Most vivparous snakes and lizards possess some sort of placenta, including a chorioallantoic placenta in some lizards (Mossman, p. 35).
The following list illustrates the variety structures that can exist to provide nutrients and/or gas exchange for a developing fetus:
1) the yolk sac provides nutrients
2) a primitive placenta is formed between folds of the yolk sac and the maternal endometrium
3) a primitive placenta is formed from folds of the yolk sac, filaments from the yolk stalk, and the maternal endometrium
4) uterine villi contact expanded gill filaments
5) uterine villi grow into the fetal spiracles and secrete materials into the pharynx
6) the continual ovulation of under-developed eggs provides fetuses with a food source they can eat
7) the yolk sac contents are supplemented with additional yolk around the fetus which it can ingest
(Mossman, p. 29-31)
The different types of placentas have been
classified as to whether the embryonic/fetal cells of the trophoblast
contact the maternal uterine epithelia (epitheliochorial
placentas), invade the maternal tissue and contact the endothelia of maternal
blood vessels (endotheliochorial placentas),
or whether the maternal blood directly contacts the fetal trophoblast
cells (hemochorial placentas). Of the four superorders
of mammals, the members of the two most primitive groups (Xenarthra
and Afrotheria) all possess either endotheliochorial or hemochorial
placentas. In the group Euarchontoglires, flying lemurs, higher primates, and most
rodents possess hemochorial placentas (lemurs
and lorises possess epitheliochorial
placentas and tree shrews possess endotheliochorial
placentas). Among the Laurasiatheria, carnivores typically have endotheliochorial placentas, bats possess either endotheliochorial or hemochorial placentas, and epitheliochorial
placentas are found in whales, horses, and many artiodactyls (Carter,
.Ancestral placental mammals possessed a discoid hemochorial placental interface with interdigitating structures joining maternal and fetal tissues (Wildman, 2006).
The placentas of rodents are known to vary in being endotheliochorial/hemochorial, the folding which can produce a lobed placenta, the presence of giant trophoblastic cells, and the structure of the interhemal area (Carter, 2004). The endotheliochorial placentas of microbats can vary considerably and variations of the hemochorial placentas of megabats are also known (Carter, 2004). All marsupials except bandicoots possess a choriovitelline placenta and all eutherians pass through this temporary stage (Carter, 2001).
4 groups of mammals and placentas (Carter, 2001). Two genera of skinks (Pseudemoia and Niveoscincus) have developed chorioallantoic placenta. N. ocellatus and N. metallicus both possess chorioallantoic placenta but N. ocellatus transfers more embryonic nutrition across this placenta (Thompson, 2001).
If a placenta is defined as the fusion of maternal and fetal tissue, then all marsupials are placental mammals. Although typical marsupials involve the yolk sac in the placenta rather than the allantois in forming the placenta, there are 3 marsupials in which the allantois fuses with the chorion to produce a chorioallantoic placenta (as observed in “placental” mammals): Perameles, Isoodon, and Echymipera (Mossman, p. 54).
|Placental (eutherian) mammals typically develop a transient choriovitelline placenta before the development of a chorioallantoic placenta as is illustrated in the image below.|
The yolk sac is the only fetal membrane which all vertebrates possess. In its primitive condition, the yolk sac is not an extraembryonic membrane, it is simply a distended portion of the digestive tract. Even in amniotes where it appears as an extra-embryonic membrane, it may make some contribution to the midgut of the newborn, as in reptiles and birds (Mossman, p. 5). As the amount of yolk increased in evolution (as in amniotes and cartilaginous fish), this portion of the digestive tract developed into an extra-embryonic structure (Mossman, p. 117). In some cartilaginous fish the yolk sac is an appendage to the embryonic body which does not compose any part of the adult (Mossman, p. 16).
There is considerable variation in the blood vessels which service the yolk sac. In amniotes, the vitelline arteries supply the yolk sac while veins supply the yolk sac in fish and amphibians (Mossman, p. 59).
In placental mammals, the yolk sac performs nutrient transfer with maternal tissue until the chorioallantoic placenta has formed. The first blood cells are synthesized in the yolk sac and the primordial germ cells originate there. The yolk sac does contribute to some of the fetal gut but most of it will deteriorate. In some fetuses, the yolk sac persists throughout pregnancy and is located under the amnion (Mossman, p.154). A fish embryo is depicted below developing around a prominent yolk sac.
|Two fish and a salamander are depicted with their yolk sacs below.|
In viviparous animals, the yolk sac may be reduced. The viviparous teleost fish Heterandria produces so little yolk that its yolk sac approaches the condition found in placental mammals (Mossman, p. 12).
Some placental mammals, such as rodents and some edentates, bats, and insectivores, have a persistent yolk sac (Mossman, p. 59). Some mammals such as rodents, rabbits, moles, shrews, armadillos and some bats develop an early choriovitelline placenta and the yolk sac may invert towards the uterine tissue (Mossman, p. 84). In carnivores, rodents, and some insectivores (soricoids), the yolk sac is large and has a significant vascular supply (Mossman, p. 126).
Note the prominent yolk sac (yellow) in the following embryos.
In 2-4% of people, part of the vitelline duct persists. If it is complete, it may discharge fecal material into the umbilical area. It some cases, it contains pancreatic tissue (Sadler, p. 251).
In birds and oviparous reptiles, the allantois is an extension of the bladder which collects the wastes produced in development. The allantois of the chick is evident in the following photos.
|The placenta in placental mammals is a chorioallantoic placenta. Although the endodermal portion of the allantois may be rudimentary and eventually degenerates, the blood vessels of the allantois supply the chorion. One type of lizard and three marsupials are also known to possess chorioallantoic placentas (Mossman, p.40, 54). The allantois seems to be a precocious urinary bladder which grows rapidly (Mossman, p.118). Without the allantois to collect embryonic wastes, amniote embryos would not have been able to grow larger than tiny marsupial infants (Mossman, p. 118). The allantois persists as a separate sac in some marsupials, especially those which are born very young. In carnivores and perissodactyls, there is a large allantoic cavity while in anthropoids the allantoic cavity and duct are only rudimentary. Some eutherian mammals may still use the allantois to collect waste (Mossman, p. 119). True moles (insectivores) possess the most primitive eutherian fetal membrane system which includes a large allantois (Mossman, p.168-9). A prominent allantois (in green) is evident in a number of mammalian embryos depicted in the following illustrations.|
|Since the allantois and the yolk sac are no longer essential to store wastes and nutrients in placental mammals, they have undergone reduction in some groups such as the primates. The following series of illustrates depicts a gradual reduction of the yolk sac and allantois in the lineage leading to humans.|
|The allantois also performs some early blood formation. Portions of the allantois may persist in some pregnancies to form allantoic cysts or cause some herniation of the viscera (Mossman, p. 154). Part of the allantois may persist as an urachal fistula, cyst, or sinus (Sadler, p. 270).|