Adaptations of the Marsupial Newborn: Birth as an Extreme Environment

Abstract

At birth a mammalian neonate enters an extreme environment compared to the intrauterine environment in which it has grown. This transition may be particularly extreme in marsupials because they are born at an exceedingly altricial state, after an exceptionally short gestation. Their stage of development must be considered embryonic by almost any criteria. Yet at this very early stage of development marsupials must travel to the teat, attach and suckle, and have basic functioning of all major physiological systems. In this article, we review the adaptations of the marsupial neonate for survival at an embryonic state, showing that the neonate exhibits a mosaic of accelerations and delays of various tissues and organs as well as several special adaptations to produce the functioning newborn. We then discuss the development of the craniofacial region, the body axis and limbs in order to detail some of the major changes to development leading to this uniquely configured neonate. We show that marsupial development arises out of a variety of heterochronies (changes in relative timing of events) and heterotopies (changes in location of specific developmental events) at the genetic, cellular and organ level. We argue that these data support hypotheses that many of the specific patterns seen in marsupial development arise from the basic constraint of embryonic energetic and tissue resources. Finally ideas on the evolutionary context of the marsupial developmental strategy are briefly reviewed.

J. P. Hill and Katherine Watson's studies of the neural crest in marsupials

“…Currently, the term ectomesenchyme is generally used for these neural crest cells. Keyte and Smith (2012) and Smith and Keyte (2020). Embryos pass through these stages quite rapidly; the number of hours given is generally the mean of many individual litters.…”

“… Note : Major events in Monodelphis domestica in each of the stages examined here. For more details and comparisons of relative timing with Mus musculus , see Keyte and Smith (2012) and Smith and Keyte (2020). Embryos pass through these stages quite rapidly; the number of hours given is generally the mean of many individual litters. …”

“…In later stages, the issue of neural crest contribution to the mesenchyme of the facial and branchial arch regions is more difficult to observe, and in fact, neural crest migration to the arches may have essentially ceased (Vaglia & Smith, 2003). These observations suggest a timing gradient in the differentiation of neural crest that corresponds with the overall gradient in the relative altriciality of marsupial neonates (e.g., Hall & Hughes, 1987, 1988Smith & Keyte, 2020;Tyndale-Biscoe & Renfree, 1987). Hughes and Hall (1988) and Grade 3 (diprotodonts) neonates are increasingly more advanced at birth and have longer periods between primitive streak formation and birth.…”

The embryo of the silky shrew opossum, Caenolestes fuliginosus (Tomes, 1863): First description of the embryo of Paucituberculata

“…G2 species are in an intermediate state with evidence of rhythmic respiration at birth. Finally, G3 species present an enlarged and subdivided lung with rich vascularization and most of the respiration is pulmonary (Smith & Keyte, ). For example, American marsupials such as D .…”

Comparative skeletal anatomy of neonatal ursids and the extreme altriciality of the giant panda

“…Given the small sample size of Starck (), we cannot affirm if his observations on nervous system development represent only a pathological case, which may be unlikely, nor can we determine if his observations apply to other bears or reflect differences in adult morphology. Currently, we have no data on newborn ursids’ nervous system or other organ systems such as the lungs, which exhibit different trajectories in marsupial mammals relative to placentals (Smith & Keyte, ).…”