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 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, ).  In marsupials the keratinous shell membrane is usually lost after the embryo reaches the uterus but may last until birth in some species (Mossman, ).

    Most bony fish and amphibians lay eggs before they are fertilized, and thus 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.  Viviparity seems to have evolved separately about 100 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).        Skinks are the largest family of squamates (with about a third of lizard species). Many skinks are viviparous and some have evolved placenta. 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, it is evident that a number of anamniote lineages have evolved vivparity separately as well.   These mechanisms of live birth in these various cases are physiologically different and are isolated in separate lineages (such as in the mechanisms of live birth in the two bony fish Heterandria and Cymatogaster) (Mossman, p. 13).

     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 function as observed in reptiles.

LIZARD IN EGG This set of extra-embryonic membranes are seen 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 it 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).

Cat Embryo in adjacent photo



     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 (Mossman, p. 3)

     In some fish, the pericardium may be expanded to the point where it forms a pseudoamnion and a pseudochorion around the neck.  In Heterandria formosa, the urinary bladder expands to surround the neck.  Some fish possess other specialized fetal structures for gas, nutrient, and/or waste exchange such as modified fin folds, large pectoral fins, and anal structures known as trophotaeniae (Mossman, p. 18).  There are a number of maternal membranes as well; some may approach the condition observed in placental mammals, complete with villi.  In the fish family Anablepidae, these maternal villi contact a fetal belly sac.

shark with placenta

     In one frog, extensions to the gills function for materials exchange 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, ).  Most vivparous snakes and lizards possess some sort of placenta, including a chorioallantoic placenta in some lizards (Mossman, ).


Shark embryos vary in their nutrition as is evident in the adjacent drawing.

     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, 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). marsupial with placenta

      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)


     Thus, placental mammals are not the only group of vertebrates which have evolved a placenta.  Mammals (named for the mammary glands which nourish the young after birth) are not the only vertebrates in which parents can produce nutrients for the young.  In pigeons, for example, the hormone prolactin (the same hormone which causes milk production in mammals) causes the formation of “crop milk” which is produced in the crop to nourish the young. 


     The earliest placental mammals are known from the Cretaceous. 

They possessed a number of primitive characteristics such as the large number of teeth (especially the incisors). ukhaatherium teeth
      Many Mesozoic mammals, modern monotremes, and modern marsupials, have small bone extending from the pubis called epipubic bones.  Epipubic bones existed in many primitive mammals (mutlitberculates, eupantotheres, and even some therapsids) of both sexes.  It may have served more for muscle attachment than for a pouch.  Although modern placental mammals lack epipubic bones, at least two early species, Zalambdalestes and Ukhaatherium (and probably Barunlestes as well) had them.  Epipubic bones seem to be homologous to the bones which exist in the penis and, more rarely, the clitoris, of many modern placental mammals.