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Postnatal development in a marsupial model, the fat-tailed dunnart (Sminthopsis crassicaudata; Dasyuromorphia: Dasyuridae).

ABSTRACT: Marsupials exhibit unique biological features that provide fascinating insights into many aspects of mammalian development. These include their distinctive mode of reproduction, altricial stage at birth, and the associated heterochrony that is required for their crawl to the pouch and teat attachment. Marsupials are also an invaluable resource for mammalian comparative biology, forming a distinct lineage from the extant placental and egg-laying monotreme mammals. Despite their unique biology, marsupial resources are lagging behind those available for placentals. The fat-tailed dunnart (Sminthopsis crassicaudata) is a laboratory based marsupial model, with simple and robust husbandry requirements and a short reproductive cycle making it amenable to experimental manipulations. Here we present a detailed staging series for the fat-tailed dunnart, focusing on their accelerated development of the forelimbs and jaws. This study provides the first skeletal developmental series on S. crassicaudata and provides a fundamental resource for future studies exploring mammalian diversification, development and evolution.

SUBMITTER: Cook LE

PROVIDER: S-EPMC8413461 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundAfter a short gestation, marsupials give birth to immature neonates with lungs that are not fully developed and in early life the neonate partially relies on gas exchange through the skin. Therefore, significant lung development occurs after birth in marsupials in contrast to eutherian mammals such as humans and mice where lung development occurs predominantly in the embryo. To explore the mechanisms of marsupial lung development in comparison to eutherians, morphological and gene expression analysis were conducted in the gray short-tailed opossum (Monodelphis domestica).ResultsPostnatal lung development of Monodelphis involves three key stages of development: (i) transition from late canalicular to early saccular stages, (ii) saccular and (iii) alveolar stages, similar to developmental stages overlapping the embryonic and perinatal period in eutherians. Differentially expressed genes were identified and correlated with developmental stages. Functional categories included growth factors, extracellular matrix protein (ECMs), transcriptional factors and signalling pathways related to branching morphogenesis, alveologenesis and vascularisation. Comparison with published data on mice highlighted the conserved importance of extracellular matrix remodelling and signalling pathways such as Wnt, Notch, IGF, TGFβ, retinoic acid and angiopoietin. The comparison also revealed changes in the mammalian gene expression program associated with the initiation of alveologenesis and birth, pointing to subtle differences between the non-functional embryonic lung of the eutherian mouse and the partially functional developing lung of the marsupial Monodelphis neonates. The data also highlighted a subset of contractile proteins specifically expressed in Monodelphis during and after alveologenesis.ConclusionThe results provide insights into marsupial lung development and support the potential of the marsupial model of postnatal development towards better understanding of the evolution of the mammalian bronchioalveolar lung.

Project description:Global biodiversity loss continues unabated, and in Australia, the rate of recent mammal extinctions is among the worst in the world. Meanwhile, the diversity among and within many endemic mammal species remains undescribed. This information is crucial to delineate species boundaries and thus inform decision-making for conservation. Sminthopsis virginiae (the red-cheeked dunnart) is a small, dasyurid marsupial found in four disjunct populations around the northern coast of Australia and New Guinea. There are three currently recognized subspecies, each occupying a distinct geographic location. Sminthopsis v. virginiae occurs in Queensland, S. v. rufigenis is distributed across New Guinea and the Aru Islands, and S. v. nitela has populations in the Top End of the Northern Territory and the Kimberley region of Western Australia. Previous molecular work has suggested the current subspecies definitions are not aligned with DNA sequence data, though the sampling was limited. We undertook a comprehensive genetic and morphological review of S. virginiae to clarify relationships within the species. This included mitochondrial (CR, 12S, and cytb) and nuclear (omega-globin, IRBP, and bfib7) loci, and morphometric analysis of skulls and whole wet-preserved specimens held in museums. Maximum Likelihood and Bayesian phylogenetic analyses resolved samples into two distinct clades, demarcated by the Gulf of Carpentaria in Australia's north. Sminthopsis. v. nitela was consistently separated from S. v. virginiae and S. v. rufigenis, based on the overall body and skull size and craniodental features, while S. v. virginiae and S. v. rufigenis were more difficult to distinguish from each other. Thus, we redescribed S. virginiae, recognizing two species, S. nitela (raised from subspecies) and S. virginiae (now comprising the subspecies S. v. virginiae and S. v. rufigenis). This study highlights the importance of recognizing cryptic mammal fauna to help address the gap in our knowledge about diagnosing diversity during a time of conservation crisis.

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Postnatal development in a marsupial model, the fat-tailed dunnart (Sminthopsis crassicaudata; Dasyuromorphia: Dasyuridae).

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