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      Craniodental anatomy in Permian–Jurassic Cynodontia and Mammaliaformes (Synapsida, Therapsida) as a gateway to defining mammalian soft tissue and behavioural traits

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          Abstract

          Mammals are diagnosed by more than 30 osteological characters (e.g. squamosal-dentary jaw joint, three inner ear ossicles, etc.) that are readily preserved in the fossil record. However, it is the suite of physiological, soft tissue and behavioural characters (e.g. endothermy, hair, lactation, isocortex and parental care), the evolutionary origins of which have eluded scholars for decades, that most prominently distinguishes living mammals from other amniotes. Here, we review recent works that illustrate how evolutionary changes concentrated in the cranial and dental morphology of mammalian ancestors, the Permian–Jurassic Cynodontia and Mammaliaformes, can potentially be used to document the origin of some of the most crucial defining features of mammals. We discuss how these soft tissue and behavioural traits are highly integrated, and how their evolution is intermingled with that of craniodental traits, thus enabling the tracing of their previously out-of-reach phylogenetic history. Most of these osteological and dental proxies, such as the maxillary canal, bony labyrinth and dental replacement only recently became more easily accessible—thanks, in large part, to the widespread use of X-ray microtomography scanning in palaeontology—because they are linked to internal cranial characters.

          This article is part of the theme issue ‘The mammalian skull: development, structure and function’.

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          Most cited references146

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          Evolution of the neocortex: a perspective from developmental biology.

          The enlargement and species-specific elaboration of the cerebral neocortex during evolution holds the secret to the mental abilities of humans; however, the genetic origin and cellular mechanisms that generated the distinct evolutionary advancements are not well understood. This article describes how novelties that make us human may have been introduced during evolution, based on findings in the embryonic cerebral cortex in different mammalian species. The data on the differences in gene expression, new molecular pathways and novel cellular interactions that have led to these evolutionary advances may also provide insight into the pathogenesis and therapies for human-specific neuropsychiatric disorders.
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            Msx2 deficiency in mice causes pleiotropic defects in bone growth and ectodermal organ formation.

            The composite structure of the mammalian skull, which forms predominantly via intramembranous ossification, requires precise pre- and post-natal growth regulation of individual calvarial elements. Disturbances of this process frequently cause severe clinical manifestations in humans. Enhanced DNA binding by a mutant MSX2 homeodomain results in a gain of function and produces craniosynostosis in humans. Here we show that Msx2-deficient mice have defects of skull ossification and persistent calvarial foramen. This phenotype results from defective proliferation of osteoprogenitors at the osteogenic front during calvarial morphogenesis, and closely resembles that associated with human MSX2 haploinsufficiency in parietal foramina (PFM). Msx2-/- mice also have defects in endochondral bone formation. In the axial and appendicular skeleton, post-natal deficits in Pth/Pthrp receptor (Pthr) signalling and in expression of marker genes for bone differentiation indicate that Msx2 is required for both chondrogenesis and osteogenesis. Consistent with phenotypes associated with PFM, Msx2-mutant mice also display defective tooth, hair follicle and mammary gland development, and seizures, the latter accompanied by abnormal development of the cerebellum. Most Msx2-mutant phenotypes, including calvarial defects, are enhanced by genetic combination with Msx1 loss of function, indicating that Msx gene dosage can modify expression of the PFM phenotype. Our results provide a developmental basis for PFM and demonstrate that Msx2 is essential at multiple sites during organogenesis.
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              The skull of Morganucodon

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                Author and article information

                Contributors
                Role: ConceptualizationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Journal
                Philos Trans R Soc Lond B Biol Sci
                Philos Trans R Soc Lond B Biol Sci
                RSTB
                royptb
                Philosophical Transactions of the Royal Society B: Biological Sciences
                The Royal Society
                0962-8436
                1471-2970
                July 3, 2023
                May 15, 2023
                May 15, 2023
                : 378
                : 1880 , Theme issue ‘The mammalian skull: development, structure and function’ compiled and edited by Lucja Fostowicz-Frelik and Jack Tseng
                : 20220084
                Affiliations
                [ 1 ] Evolutionary Studies Institute, University of the Witwatersrand, , Private Bag 3, Wits 2050, Johannesburg, South Africa
                [ 2 ] Unidad Ejecutora Lillo, CONICET-Fundación Miguel Lillo, , Miguel Lillo 251, Tucumán 4000, Argentina
                Author notes

                One contribution of 13 to a theme issue ‘ The mammalian skull: development, structure and function’.

                Author information
                http://orcid.org/0000-0002-9434-9267
                https://orcid.org/0000-0001-9838-2497
                http://orcid.org/0000-0001-5378-3940
                Article
                rstb20220084
                10.1098/rstb.2022.0084
                10184251
                d9dac896-7369-4285-b6e1-a55f5a601a25
                © 2023 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : August 13, 2022
                : November 11, 2022
                Funding
                Funded by: Consejo Nacional de Investigaciones Científicas y Técnicas, http://dx.doi.org/10.13039/501100002923;
                Funded by: National Research Foundation, http://dx.doi.org/10.13039/501100001321;
                Award ID: African Origins Platform
                Funded by: PAST, http://dx.doi.org/10.13039/100016207;
                Funded by: GENUS DSI-NRF Centre of Excellence in Palaeosciences;
                Award ID: UID 86073
                Categories
                1001
                144
                70
                Articles
                Review Articles
                Custom metadata
                July 3, 2023

                Philosophy of science
                mammal evolution,hair,lactation,secondary palate,mastication,parietal foramen
                Philosophy of science
                mammal evolution, hair, lactation, secondary palate, mastication, parietal foramen

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