Evolution of Viviparity E. C. Amoroso - Reproduction is one of the cardinal attributes of all

1. 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. Viviparity encompasses a broad span of adaptations for the retention of young in the dam during early embryonic development. 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. Seen in fish to man

3. 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

4. Was the loss of vitellogenin gene expression a predecessor to Viviparity?

7. 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.

8. 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)

9. Developing Tertiary Follicle Tertiary Follicle Granulosa Cells Antrum Nucleus Primary Oocyte Theca Interna

10. The Corpus Luteum of Eutherians is Unique • Granulosa Cells become luteinized and theca interna. • A large number of cells form the CL. • Cumulus oophorus not part of the CL formation. (except Marsupials) • Endothelial Cells invade and angiogenesis allows formation of dense capillary network.

11. Before true viviparity could be attained, the problem of endocrine adaptation for retention of fertilized eggs had to be solved. A prerequisite to internal gestation - Internal fertilization (also evolution of intromittent organs for copulation). Suppression of Ovulation during pregnancy. Intrauterine care of young until they attain greater degrees of development. Also, the need for placental development to absorb nutrients. Adoption of the corpus luteum as an endocrine gland. Development of receptor! Signaling by the conceptus to dam to maintain pregnancy “Maternal Recognition of Pregnancy”. Participation of biochemical secretions of the conceptus in extending gestation beyond the length of the normal estrous cycle. Abrogation of the maternal immune response against the conceptus (Fetal Allograft) Involvement of the fetus in the initiation of parturition. Endocrine control of lactation in preparation for nutrient requirements of newborn. 1. 2. 3. 4. 5. 6. 7. 8. 9.

12. Key Alterations to Progress to Eutherian Viviparity • 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.

13. 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 eutherianviviparity actually returned to a reptilian form with notable exceptions. Placentation more prolonged and advanced. Eutheriantrophoblast and placentation, may be improvisations from marsupials that made prolonged intrauterine gestation possible.

19. 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 Corner (1947) - Acquirement of a viviparous relationship between parent and offspring may involve: 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.

20. 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.

21. Without hard shell Remain in maternal system for a period of time Adaptations in Fishes Although most elasmobranches are oviparous, a few are ovoviviparous and some show advanced conditions of viviparity. Chief adaptations: 1. 2. 3. 4. 5. 6. Egg-layers 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 ovulating- gonadotropins or estrogen. In some fish corticosteroids involved (Stress?) Internal Fertilization Development of Mullerian Duct as an organ for development of young 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. Development of corpora lutea on ovaries. Involvement of progesterone?? Amphibian - CL produce progesterone Involvement of pituitary gonadotropins? Pituitary-Gonadal interactions. Control of parturition - Sharks - Relaxin

22. 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. Chief adaptation: 1. 2. 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. Is progesterone involved with inhibiting parturition and slowing embryo growth which occurs at a more accelerated rate without it? Estrogen stimulates vascularity. 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. Development of Chorioallantoic membrane. Pituitary control of stimulating progesterone. Stress - increase ACTH--increase P4. Parturition - arginine vasotocin, PGF2a, oxytocin

23. 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

24. 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!

25. 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

26. 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. 2. 3. 4. 5. Corpus luteum - Progesterone Hypothalamus - Hypophysis - LH and Prolactin Placenta - PL, Steroids, hCG, eCG Uterine endometrium - Secretions, PGF2a Immunoglogical Protection

27. 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.

29. "Facts don't make a theory; it's the theory that makes factsvisible" (source unknown). In other words, how we look at afact can be more important than the fact itself. Irving Rothchild