Evolution of Viviparity
E. C. Amoroso - Reproduction is one of the cardinal attributes of all
living things and although the end result in all instances
is the same, the ways by which it is accomplished may
be quite different. Irrespective of the ordinal rank,
living creatures face much of the same problems in
their efforts to survive as individuals and as species.
Species must adjust according to their environment and seasonal changes.
These changes have been made through the use of the endocrine system.
However, it is the tissues and not really the hormones that have
developed to react.
Viviparity encompasses a broad span of adaptations for the retention of
young in the dam during early embryonic development.
Seen in fish to man
How did the ovary evolve, and how was its evolution connected
to that of eutherian viviparity?
How did oocytes become enclosed in follicles?
Irving Rothchild
Four unique characteristics of the mammalian follicle
1) Mature follicle is vesicular
2) Granulosa cells more differentiated at follicle maturity
3) Contains more total cells compared to other vertebrates
4) In eutherians, oocyte is smallest of all vertebrates and
contains no yolk
Was the loss of vitellogenin gene expression a predecessor to Viviparity?
Follicular Stages of Maturation. Depiction of representative
primordial (pig) (a), primary (pig) (b), preantral (hamster) (c),
incipient antral (mouse) (d), small antral (hamster) (e) and
Graafian (pig) (f) follicles.
How did the mammalian ovary change from the large number
of oocytes released in spawning vertebrates?
Follicular atresia is a common fact
of ovarian development in almost
all mammalian species.
The oocyte and the granulosa cells are both involved with the
survival of the oocyte in development. (Obligatory Symbiosis)
Developing Tertiary Follicle
Tertiary
Follicle
Granulosa
Cells
Primary
Oocyte
Theca
Interna
Antrum
Nucleus
The Corpus Luteum of Eutherians is Unique
1) Granulosa Cells become luteinized and theca interna.
2) A large number of cells form the CL.
3) Cumulus oophorus not part of the CL formation. (except
Marsupials)
4) Endothelial Cells invade and angiogenesis allows
formation of dense capillary network.
Before true viviparity could be attained, the problem of endocrine
adaptation for retention of fertilized eggs had to be solved.
1. A prerequisite to internal gestation - Internal fertilization (also evolution of
intromittent organs for copulation).
2. Suppression of Ovulation during pregnancy.
3. Intrauterine care of young until they attain greater degrees of development. Also,
the need for placental development to absorb nutrients.
4. Adoption of the corpus luteum as an endocrine gland. Development of receptor!
5. Signaling by the conceptus to dam to maintain pregnancy “Maternal Recognition
of Pregnancy”.
6. Participation of biochemical secretions of the conceptus in extending gestation
beyond the length of the normal estrous cycle.
7. Abrogation of the maternal immune response against the conceptus (Fetal Allograft)
8. Involvement of the fetus in the initiation of parturition.
9. Endocrine control of lactation in preparation for nutrient requirements of newborn.
Key Alterations to Progress to Eutherian Viviparity
I. Reptilian form of viviparity to Marsupial viviparity
Marsupial “implantation” to parturition last no longer than 4 to
10 days.
Progesterone is not involved with maintenance of pregnancy.
The marsupial thus lost the ability to hold the embryo in the
uterus for a long period of time. Developed the use of the
pouch and milk secretion to complete development.
II. Marsupial to Eutherian Viviparity
Uterus “regained the ability to hold the embryo in the uterus
Uterus developed the ability to respond to progesterone.
The corpus luteum developed the ability to respond to extrinsic stimuli.
Thus Rothchild theory is that eutherian viviparity actually returned to a reptilian
form with notable exceptions.
Placentation more prolonged and advanced.
Eutherian trophoblast and placentation, may be improvisations from
marsupials that made prolonged intrauterine gestation possible.
Evolution of viviparity must have involved increasingly longer retention
of the conceptus with the body of the mother so that they might develop
to a more mature stage.
Pointed out that when mammals evolved
phenomenon of utero-gestation, the chosen place
for shelter, the uterus was developed form part of
the oviduct which existed as a channel that had for
its purpose, the efficient transportation and
discharge of eggs, not retention and maintenance
Acquirement of a viviparous relationship between parent and offspring
may involve:
Corner (1947) -
Primitive - Simple storage of young for advanced embryo development - embryos
development through yolk reserves (species - molluses, annelids and cockroaches).
Although development occurs in mother, no nutrients provided by her.
Advanced - Through formation of the placenta are nourished by the secretions provided
by the maternal system. Simple type - Teste fly - single egg in uterus with special
structures serve to nourish larva. Milk gland has a nipple similar to marsupial. It also
provides antibodies like colostrum in ungulates. No ovulation until young removed
from uterus.
Examples of adaptations in invertebrates
Peripatus (Worm-like anthropod)
Each egg becomes implanted in a newly formed segment of the oviduct
(similar to yolk sac placenta). As it develops, remains attached and is
displaced distally while new embryos are added proximally.
Adaptations in Fishes
Egg-layers
Without hard shell
Remain in maternal
system for a period
of time
Although most elasmobranches are oviparous, a few are ovoviviparous
and some show advanced conditions of viviparity.
In some live-bearing fish, the ovary provides housing and nourishment of young.
Caused by lack of ovulation stimulation? At later stages become sensitive to ovulatinggonadotropins or estrogen. In some fish corticosteroids involved (Stress?)
Chief adaptations:
1. Internal Fertilization
2. Development of Mullerian Duct as an organ for development of young
3. Development of fetal Yolk Sac as a Placenta - Degree of uterine secretions
and liver is negatively correlated. Loss of Shell - Need for respiration and water
uptake - need to increase vascular supply.
4. Development of corpora lutea on ovaries. Involvement of progesterone??
Amphibian - CL produce progesterone
5. Involvement of pituitary gonadotropins? Pituitary-Gonadal interactions.
6. Control of parturition - Sharks - Relaxin
Adaptations in Reptiles:
Various reptiles have developed rudimentary placentas that may be the
fore-runner to that inherited by mammals. Reptiles have a chorion,
allantois and a yolk sac.Is progesterone involved with inhibiting parturition and
slowing embryo growth which occurs at a more accelerated
Chief adaptation: rate without it? Estrogen stimulates vascularity.
1. Corpora lutea form and function to produce progesterone (both in oviparous
and viviparous species). CL function throughout gestation unlike birds in
which they are short-lived.
2. Development of Chorioallantoic membrane. Pituitary control of stimulating
progesterone. Stress - increase ACTH--increase P4. Parturition - arginine
vasotocin, PGF2a, oxytocin
The involvement of progesterone is reptilian pregnancy remains
equivocal. It should be clearly indicated that although observations
seem to deny ovarian participation in maintenance of gestation in
reptiles, evidence demonstrated that the ovaries are capable of
producing steroid hormones.
Hisaw (1959) suggested that the next stage in evolution of viviparity
leading to conditions found in mammals was the adaptation of the corpus
luteum into the family of endocrine glands.
He suggested that synthesis of progesterone, on a small scale, was the
first step in specialization. This is probably the most important
contributing factor to viviparity in mammals. It added a luteal phase
with follicular phase that terminated at ovulation, thus forming the
stages of the estrous cycle.
Adaptations in Mammals:
The unique feature in mammals was the establishment of a trophic and
respiratory placental connection between the dam and conceptus.
Through evolution, the placenta of mammals also developed into an
endocrine organ
Examples:
Monotremes: (Only species that lay eggs) - Egg is small and yolk
insufficient to support development. Evidence that endometrial gland
secretions are absorbed by the egg until shell is deposited. Egg is layed
with involution of the corpora lutea. Egg transport controlled by CL as
well as suppressing ovulation and stimulating endometrial development.
Involved in development of mammary gland (much like pig).
Luteinizing Hormone involved with ovulation.
Marsupials: Progesterone stimulates uterine endometrial development.
Duration of pregnancy does not exceed the length of the estrous cycle.
Placenta does secrete progesterone. Kangaroos and Wallabies have
developed the ability to hold the embryo dormant for a period of time
known as “Embryonic Diapause”. Lactation inhibition of cyclicity.
Oxytocin can inhibit progesterone from CL - May function to inhibit
embryo growth during embryonic lactational diapause. Ovx delays
parturition!
Eutherian: The previous species the development of viviparity has
evolved the interaction between pituitary gland, gonad, and very little
from the conceptus. However, in majority of mammals above
marsupials, gestation is longer than the estrous cycle. Therefore, there
was a need to extend the length of embryo storage.
Lengthening of gestation was accomplished by either prolonging the
functional life-span of the CL or by the placenta acquiring endocrine
capability.
Example:
Human, monkeys, mare, sheep and guinea pigs
Hypophysectomy does not interrupt pregnancy in mice and rats
This coincides with the time that chorioallantoic placental circulation
is established to secrete mouse placental lactogen (mPL).
In rat CL (cycle 4 days) maintained by prolactin after breeding then mPL
Apart from structural modification in the arrangement of the female
genital ducts, mammals have uniformly adopted endocrine mechanisms
to solve many problems posed by viviparity.
Five components are involved:
1. Corpus luteum - Progesterone
2. Hypothalamus - Hypophysis - LH and Prolactin
3. Placenta - PL, Steroids, hCG, eCG
4. Uterine endometrium - Secretions, PGF2a
5. Immunoglogical Protection
Mammals needed to develop signal for:
“Maternal Recognition of Pregnancy”
Embryonic Signals vary from species to species
- Regression of CL in majority of species is achieved through release
of a uterine luteolysin (PGF2a)
Cow, Ewe - Interferon t
Gilt - Estrogen
Mare - Protein?
Women - hCG
Mouse, Rat - Placental Lactogen
Attachment, or fusion, between the placenta and uterine surface
constitutes a naturally occurring instance of tissue transplantation, which
with prolonged gestation period, represents an allograft that breaks one
of the fundamental laws of transplantation immunology.
"Facts don't make a theory; it's the theory that makes facts
visible" (source unknown). In other words, how we look at a
fact can be more important than the fact itself.
Irving Rothchild