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Biological Considerations of the Marsupial-Placental Dichotomy
Jason A. Lillegraven
Vol. 29, No. 4 (Dec., 1975), pp. 707-722
Published by: Society for the Study of Evolution
Stable URL: http://www.jstor.org/stable/2407079
Page Count: 16
You can always find the topics here!Topics: Marsupials, Evolution, Mammals, Gestation period, Species, Pregnancy, Fetus, Jaw, Immunology, Nipples
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The phylogenetic divergence of marsupial and placental mammals probably occurred in the Early Cretaceous. In sharp contrast to the Late Jurassic, this was a time of exceptional restriction of intercontinental migration of land vertebrates due to marine barriers and probably was a time of development of 'island continent' centers of distinct endemism. Paleontological and anatomical evidences do not suggest the derivation of marsupials and placentals from different pantotherian ancestors, but on the contrary, point to a common source. Living marsupials are born following a short period of internal gestation at a remarkably immature stage of organogenesis. As described by Dr. Fabiola Muller, they have a series of temporary closures for the mouth, eyes, and ears that develop shortly before birth and are functionally significant after birth in attachment to the nipple, development of the secondary jaw joint, and in protecting the eyes and ears against desiccation in the new atmospheric environment. Living eutherians generally have longer periods of internal gestation than do marsupials, and some have greatly lengthened intrauterine development times. Even eutherians that may be born in precocial states, however, intrauterinely form transitory mouth, eye, and ear closures at early stages of development that may be lost well before birth. These closures are today without function in eutherian nidifuges and seem only to be conservative features retained from eutherian ancestors that were born, as are marsupials today, in an extreme nidicolous state following a short period of internal gestation. Although the duration of internal gestation of living marsupial species is highly variable (11-38 days), all are born at similar stages of organogenesis. Thus those with longer pregnancy times, in contrast to eutherians, seem not to 'take advantage' of the full duration of intrauterine life for rapid development; they have marked standstills or retardations in rates of organogenesis and the degree of anatomical refinement does not necessarily correlate with the length of pregnancy as it generally does in eutherians. Early developmental stages of therian mammals in general are characterized by the near absence of self-contained energy reserves (yolk, albumen) and postblastocystic embryos depend almost entirely upon the mother for nutrients. Embryonic energy needs are comparatively low up to the stage of embryogenesis characteristic of marsupials at birth (and the correlative anatomical stage in eutherians) but increase sharply thereafter. Rising embryonic energy demands necessitate a close physical intimacy of fetal and maternal tissues of exchange (i.e., placentation). Marsupials can make apposition of their yolk sac placenta with the uterine wall only following intrauterine 'hatching' from their porous eggshell, a process that occurs only within the last one-third of pregnancy in all species yet investigated. Eutherians, on the other hand, lack eggshells and effect intimacy of placentation (first yolk sac then chorioallantoic) in very early stages of embryogenesis. This intimacy is possible in eutherians only because of the as yet poorly understood properties of the trophoblast that allow blocking of a maternal immune response against the paternal antigens held in the fetal tissues. The inert eggshell (of maternal origin) apparently does this task until late in the pregnancy of marsupials and they are probably born before a full-fledged immunological attack against the embryo by the mother can be completed. Marsupial intrauterine development is a study in the compromise that becomes necessary when feto-maternal intimacy in placentation required for advanced morphological development conflicts with the threat of immunological rejection in the absence of protective layers. The 'invention' of trophoblastic tissues by primaeval eutherians was probably the single most important evolutionary event in the history of the infraclass. The ability of the trophoblast to protect the embryo from immunological attack and to coordinate endocrinological events, nutritional sources, and waste removal requirements were key features in the evolution of prolonged internal gestation combined with sustained high rates of organogenesis; the birth of anatomically advanced offspring was thus allowed. Marsupial embryogenesis is rigidly channeled by natural selection in that the newborn must be capable of independent travel to and attachment onto the teat. Eutherians, on the other hand, are allowed greater flexibility of embryological heterochrony and anatomical 'experimentation.' This is seen especially clearly in adaptations of forelimbs (with flippers, non-opposable claws, single hooves, etc.), parts of the body critically adapted to specific ways of life in all species. A case is made for the possibility that the immediate common ancestor to marsupials and placentals was viviparous and nidicolous as are the marsupials today.
Evolution © 1975 Society for the Study of Evolution