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Polarities in Mammalian Evolution Seen Through Homologs of the Inner Cell Mass

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Abstract

Embryogenetic pathways differ markedly among monotremes, marsupials, and placentals, and their analysis provides information of fundamental importance to recognition of mammalian evolutionary directions. The cap of cuboidal cells of the marsupial late unilaminar blastocyst, generally known as the “embryonic area,” probably is induced to form (prior to origin of Hensen's node) by signals from earliest hypoblastic cells (“anterior visceral endoderm”). The thickened cap is a “medullary plate” of sauropsid terminology because it includes epiblastic cells presumptive to neurectoderm (including neural crest), Hensen's node, primitive streak, and gut endoderm. The remainder of the definitive embryo (i.e., parts of epidermal origin, including ectodermal placodes) derives from squamous ectoderm (surrounding the medullary plate) of the blastocyst's ill-named “trophoblastic area.” Amniotic ectoderm develops farther distally within the “trophoblastic area.” The autapomorphic inner cell mass (ICM) of placental mammals is homologous to medullary plate of the marsupial blastocyst plus morphologically undefined, proximal parts of surrounding ectoderm (of the “trophoblastic area”). Considerations of early cell lineages in marsupials are greatly affected by recognition that the boundary between future embryonic and extra-embryonic tissues does not match the margin of the medullary plate (i.e., “embryonic area”). Marsupials and monotremes largely conform to sauropsid early embryogenesis, but placentals express, at earliest developmental stages, innovations unique within Amniota that are linked to early establishment of the brain. Neonatal marsupials and hatchling monotremes are extremely altricial and closely comparable anatomically/physiologically; they share a temporal pattern in combining early morphogenesis of craniofacial features (related to suckling) with deferral of telencephalic completion into postnatal/posthatching life. Placentals contrast greatly in establishing the central nervous system prior to rudiments of the cranial skeleton and associated musculature, and they complete essentials of forebrain development before birth. Comparative evidence from transitory periderm suggests that primordial eutherians had extremely altricial hatchlings or newborns, whichever was the mode of early development. Details remain unknown about the origin of the unique specialization of ICM plus encapsulating trophoblast from the more generalized blastula of ancestral synapsids.

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  1. Departments of Geology/Geophysics and Zoology/Physiology, The University of Wyoming, Laramie, Wyoming, 82071-3006, USA

    Jason A. Lillegraven

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Lillegraven, J.A. Polarities in Mammalian Evolution Seen Through Homologs of the Inner Cell Mass. Journal of Mammalian Evolution 11, 143–202 (2004). https://doi.org/10.1023/B:JOMM.0000041193.29946.fe

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