Heterochrony in somitogenesis rate in a model marsupial, Monodelphis domestica

Abstract

Marsupial newborns are highly altricial and also show a wide array of shifts in the rate or timing of developmental events so that certain neonatal structures are quite mature. One particularly notable feature is the steep gradient in development along the anterior-posterior axis such that anterior structures are generally well developed relative to posterior ones. Here, we study somitogenesis in the marsupial, Monodelphis domestica, and document two heterochronies that may be important in generating the unusual body plan of the newborn marsupial. First, we demonstrate a 4-fold change in somitogenesis rate along the anterior-posterior axis, which appears to be due to somitogenesis slowing posteriorly. Second, we show that somitogenesis, particularly in the cervical region, initiates earlier in Monodelphis relative to other developmental events in the embryo. The early initiation of somitogenesis may contribute to the early development of the cervical region and forelimbs. Other elements of somitogenesis appear to be conserved. When compared to mouse, we see similar expression of genes involved in the clock and wavefront, and genes of the Wnt, Notch, and fibroblast growth factor (FGF) pathways also cycle in Monodelphis. Further, we could not discern differences in somite maturation rate along the anterior-posterior axis in Monodelphis, and thus rate of maturation of the somites does not appear to contribute to the steep anterior-posterior gradient.

Heterochrony and developmental timing mechanisms: Changing ontogenies in evolution

“…Somites give rise to much of the axial skeleton, all postcranial skeletal muscles, including limb muscles, as well as the tongue muscle precursors which migrate from the anterior-most somites. While certain elements of somitogenesis appear to be conserved–gene expression of Clock and Wavefront components and rate of somite maturation along the anterior-posterior axis are consistent with expression reported for other amniotes–two changes in the relative timing of somitogenesis in M. domestica contribute to the characteristic configuration of the marsupial neonate [51]. There exists a four-fold change in the rate of somitogenesis along the anterior-posterior axis (Figure 3).…”

“…Given the demands for elaborated anterior structures and a functional feeding apparatus during the short period from primitive streak to birth (approximately 4.5 days in M. domestica ) it has been proposed that an energy trade-off exists to emphasize structures required at birth and de-emphasize non-necessary structures, such as the hindlimbs and pelvis [62,72,73]. Somitogenesis slows posteriorly in opossum relative to mouse [51]. With somitogenesis occurring more slowly, the maturation of posterior somites is delayed, possibly freeing resources for other structures in the embryo.…”

From sauropsids to mammals and back: New approaches to comparative cortical development

“…M. domestica , like all marsupials, shows altricial development, being born when immature and migrating to the teats and clinging to them for a significant part of their postnatal development (Keyte and Smith, 2012). Marsupial cortices display a hexalaminar arrangement similar to that seen in eutherian mammals (Gray, 1924) leading to a debate whether the presence of an SVZ predates the eutherian–metatherian split.…”

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

“…For developmental comparisons with other marsupials, we used McCrady Jr. () for D . virginiana , Mate et al (), Smith (), and Keyte and Smith () for M . domestica , and Werneburg et al () for both.…”