Abstract
BackgroundIn contrast to placental neonates, in which all cranial bones are ossified, marsupial young have only the bones of the oral region and the exoccipital ossified at birth, in order to facilitate suckling at an early stage of development. In this study, we investigated whether this heterochronic shift in the timing of cranial ossification constrains cranial disparity in marsupials relative to placentals.MethodsWe collected three-dimensional (3D) landmark data about the crania of a wide range of extant placentals and marsupials, and from six fossil metatherians (the clade including extant marsupials and their stem relatives), using a laser scanner and a 3D digitizer. Principal components analysis and delta variance tests were used to investigate the distribution and disparity of cranial morphology between different landmark sets (optimizing either number of landmarks or number of taxa) of the whole skull and of individual developmental or functional regions (neurocranium, viscerocranium, oral region) for extant placentals and marsupials. Marsupial and placental data was also compared based on shared ecological aspects including diet, habitat, and time of peak activity.ResultsWe found that the extant marsupial taxa investigated here occupy a much smaller area of morphospace than the placental taxa, with a significantly (P<0.01) smaller overall variance. Inclusion of fossil taxa did not significantly increase the variance of metatherian cranial shape. Fossil forms generally plotted close to or within the realm of their extant marsupial relatives. When the disparities of cranial regions were investigated separately, significant differences between placentals and marsupials were seen for the viscerocranial and oral regions, but not for the neurocranial region.ConclusionThese results support the hypothesis of developmental constraint limiting the evolution of the marsupial skull, and further suggest that the marsupial viscerocranium as a whole, rather than just the early-ossifying oral region, is developmentally constrained.
Highlights
In The Beginning of the Age of Mammals
Despite the exclusion of several placental taxa with unusual cranial morphologies, and the limited fossil taxa included, we found in the current study that marsupial crania are, on the whole, significantly less disparate compared with placentals
Developmental timing, integration, and lability relative cranial ossification sequence is largely conserved across mammals [23,24], there is a delay in raw timing between the development of bones in the oral region and those in the neurocranium of marsupials compared with placentals [25,26,27]
Summary
In The Beginning of the Age of Mammals. Baltimore: The Johns Hopkins University Press; 2006:1–21. 59. Fossil and molecular estimates generally agree that the lineages leading to marsupial and placental mammals diverged over 160 million years ago (Ma), in the Late Jurassic period [1,2] Despite this shared time of origin as sister clades, recent marsupials and placentals differ markedly in taxonomic diversity and geographical range. In peramelimorphians (bandicoots) and some diprotodontians (such as wombats), which have backwardsfacing pouches, and in dasyuromorphians (marsupial carnivores and mice), which have open pouches, the journey to the pouch is a downwards, sinusoidal slither, aided by the positioning of the mother (Wilson and Reeder [3] and references therein) These mechanical demands do not end with arrival in the pouch, as once the neonate is attached to the teat, it must satisfy the mechanical demands of suckling to survive. Even the most altricial neonates of their placental sister group are born at a much later stage of development, with all or most cranial bones at least partially ossified prior to the commencement of suckling
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