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      Developmental origin underlies evolutionary rate variation across the placental skull

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          Abstract

          The placental skull has evolved into myriad forms, from longirostrine whales to globular primates, and with a diverse array of appendages from antlers to tusks. This disparity has recently been studied from the perspective of the whole skull, but the skull is composed of numerous elements that have distinct developmental origins and varied functions. Here, we assess the evolution of the skull's major skeletal elements, decomposed into 17 individual regions. Using a high-dimensional morphometric approach for a dataset of 322 living and extinct eutherians (placental mammals and their stem relatives), we quantify patterns of variation and estimate phylogenetic, allometric and ecological signal across the skull. We further compare rates of evolution across ecological categories and ordinal-level clades and reconstruct rates of evolution along lineages and through time to assess whether developmental origin or function discriminate the evolutionary trajectories of individual cranial elements. Our results demonstrate distinct macroevolutionary patterns across cranial elements that reflect the ecological adaptations of major clades. Elements derived from neural crest show the fastest rates of evolution, but ecological signal is equally pronounced in bones derived from neural crest and paraxial mesoderm, suggesting that developmental origin may influence evolutionary tempo, but not capacity for specialisation.

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

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          phytools: an R package for phylogenetic comparative biology (and other things)

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            Inferring the mammal tree: Species-level sets of phylogenies for questions in ecology, evolution, and conservation

            Big, time-scaled phylogenies are fundamental to connecting evolutionary processes to modern biodiversity patterns. Yet inferring reliable phylogenetic trees for thousands of species involves numerous trade-offs that have limited their utility to comparative biologists. To establish a robust evolutionary timescale for all approximately 6,000 living species of mammals, we developed credible sets of trees that capture root-to-tip uncertainty in topology and divergence times. Our “backbone-and-patch” approach to tree building applies a newly assembled 31-gene supermatrix to two levels of Bayesian inference: (1) backbone relationships and ages among major lineages, using fossil node or tip dating, and (2) species-level “patch” phylogenies with nonoverlapping in-groups that each correspond to one representative lineage in the backbone. Species unsampled for DNA are either excluded (“DNA-only” trees) or imputed within taxonomic constraints using branch lengths drawn from local birth–death models (“completed” trees). Joining time-scaled patches to backbones results in species-level trees of extant Mammalia with all branches estimated under the same modeling framework, thereby facilitating rate comparisons among lineages as disparate as marsupials and placentals. We compare our phylogenetic trees to previous estimates of mammal-wide phylogeny and divergence times, finding that (1) node ages are broadly concordant among studies, and (2) recent (tip-level) rates of speciation are estimated more accurately in our study than in previous “supertree” approaches, in which unresolved nodes led to branch-length artifacts. Credible sets of mammalian phylogenetic history are now available for download at http://vertlife.org/phylosubsets, enabling investigations of long-standing questions in comparative biology.
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              The “Domestication Syndrome” in Mammals: A Unified Explanation Based on Neural Crest Cell Behavior and Genetics

              Charles Darwin, while trying to devise a general theory of heredity from the observations of animal and plant breeders, discovered that domesticated mammals possess a distinctive and unusual suite of heritable traits not seen in their wild progenitors. Some of these traits also appear in domesticated birds and fish. The origin of Darwin’s “domestication syndrome” has remained a conundrum for more than 140 years. Most explanations focus on particular traits, while neglecting others, or on the possible selective factors involved in domestication rather than the underlying developmental and genetic causes of these traits. Here, we propose that the domestication syndrome results predominantly from mild neural crest cell deficits during embryonic development. Most of the modified traits, both morphological and physiological, can be readily explained as direct consequences of such deficiencies, while other traits are explicable as indirect consequences. We first show how the hypothesis can account for the multiple, apparently unrelated traits of the syndrome and then explore its genetic dimensions and predictions, reviewing the available genetic evidence. The article concludes with a brief discussion of some genetic and developmental questions raised by the idea, along with specific predictions and experimental tests.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Investigation
                Role: Data curationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: ResourcesRole: Writing – review & editing
                Role: Funding acquisitionRole: MethodologyRole: SoftwareRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: MethodologyRole: ResourcesRole: Writing – review & editing
                Role: MethodologyRole: Resources
                Role: Data curationRole: InvestigationRole: Resources
                Role: Data curationRole: Funding acquisitionRole: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: MethodologyRole: SoftwareRole: Writing – review & editing
                Role: Data curationRole: Funding acquisitionRole: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: Data curationRole: Funding acquisitionRole: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: Data curationRole: Funding acquisitionRole: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: Data curationRole: Funding acquisitionRole: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: VisualizationRole: 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
                : 20220083
                Affiliations
                [ 1 ] Department of Life Sciences, Natural History Museum, , London SW7 5BD, UK
                [ 2 ] Department of Genetics, Evolution, and Environment, University College London, , London WC1E 6BT, UK
                [ 3 ] Centre for Integrative Anatomy, Department of Cell and Developmental Biology, University College London, , London WC1E 6BT, UK
                [ 4 ] Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, , Washington, DC 20013, USA
                [ 5 ] Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, , Washington, DC 20013, USA
                [ 6 ] Université Lyon, Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023 LEHNA, , 69622 Villeurbanne, France
                [ 7 ] Naturhistorisches Museum Bern, , 3005 Bern, Switzerland
                [ 8 ] Institute of Ecology and Evolution, University of Bern, , 3012 Bern, Switzerland
                [ 9 ] School of Geography, Earth and Environmental Sciences, University of Birmingham, , Birmingham B15 2TT, UK
                [ 10 ] Department of Biology, University of Wisconsin Oshkosh, , Oshkosh, WI 54901, USA
                [ 11 ] Department of Biology, University of Washington, , Seattle, WA 98195, USA
                [ 12 ] Department of Anatomy, College of Osteopathic Medicine, New York Institute of Technology, , Old Westbury, NY 11568, USA
                [ 13 ] Division of Paleontology, American Museum of Natural History, , New York, NY 10024, USA
                [ 14 ] Department of Mammalogy, Division of Vertebrate Zoology, American Museum of Natural History, , New York, NY 10024, USA
                [ 15 ] Department of Earth and Environmental Sciences, University of Minnesota, , Minneapolis, MN 55455, USA
                Author notes

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

                Electronic supplementary material is available online at https://doi.org/10.6084/m9.figshare.c.6602949.

                Author information
                http://orcid.org/0000-0001-9465-810X
                http://orcid.org/0000-0001-7310-1775
                http://orcid.org/0000-0002-4077-732X
                http://orcid.org/0000-0001-5057-4772
                http://orcid.org/0000-0002-5464-0041
                http://orcid.org/0000-0002-4880-1152
                Article
                rstb20220083
                10.1098/rstb.2022.0083
                10184245
                37183904
                22694204-b8d1-499e-a4a0-c805b16431cc
                © 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
                : December 13, 2022
                : April 4, 2023
                Funding
                Funded by: Horizon 2020 Framework Programme, http://dx.doi.org/10.13039/100010661;
                Award ID: MCSA Fellowship IF 797373-EVOTOOLS
                Funded by: H2020 European Research Council, http://dx.doi.org/10.13039/100010663;
                Award ID: STG-2014-637171
                Funded by: National Science Foundation, http://dx.doi.org/10.13039/100000001;
                Award ID: EAR 1338262
                Award ID: EAR 1349607
                Funded by: Natural Environment Research Council, http://dx.doi.org/10.13039/501100000270;
                Award ID: Doctoral Training Partnership training grant NE/L0
                Funded by: Gertner Scholar;
                Award ID: Postdoctoral Research Fellowship
                Funded by: Labex, http://dx.doi.org/10.13039/501100004100;
                Award ID: BCDiv 10-LABX-0003
                Categories
                1001
                70
                144
                60
                58
                Articles
                Research Articles
                Custom metadata
                July 3, 2023

                Philosophy of science
                skull evolution,morphometrics,cranial neural crest,development,ecology
                Philosophy of science
                skull evolution, morphometrics, cranial neural crest, development, ecology

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