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      The taming of the neural crest: a developmental perspective on the origins of morphological covariation in domesticated mammals

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          Abstract

          Studies on domestication are blooming, but the developmental bases for the generation of domestication traits and breed diversity remain largely unexplored. Some phenotypic patterns of human neurocristopathies are suggestive of those reported for domesticated mammals and disrupting neural crest developmental programmes have been argued to be the source of traits deemed the ‘domestication syndrome’. These character changes span multiple organ systems and morphological structures. But an in-depth examination within the phylogenetic framework of mammals including domesticated forms reveals that the distribution of such traits is not universal, with canids being the only group showing a large set of predicted features. Modularity of traits tied to phylogeny characterizes domesticated mammals: through selective breeding, individual behavioural and morphological traits can be reordered, truncated, augmented or deleted. Similarly, mammalian evolution on islands has resulted in suites of phenotypic changes like those of some domesticated forms. Many domesticated mammals can serve as valuable models for conducting comparative studies on the evolutionary developmental biology of the neural crest, given that series of their embryos are readily available and that their phylogenetic histories and genomes are well characterized.

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          Most cited references76

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          The placental mammal ancestor and the post-K-Pg radiation of placentals.

          To discover interordinal relationships of living and fossil placental mammals and the time of origin of placentals relative to the Cretaceous-Paleogene (K-Pg) boundary, we scored 4541 phenomic characters de novo for 86 fossil and living species. Combining these data with molecular sequences, we obtained a phylogenetic tree that, when calibrated with fossils, shows that crown clade Placentalia and placental orders originated after the K-Pg boundary. Many nodes discovered using molecular data are upheld, but phenomic signals overturn molecular signals to show Sundatheria (Dermoptera + Scandentia) as the sister taxon of Primates, a close link between Proboscidea (elephants) and Sirenia (sea cows), and the monophyly of echolocating Chiroptera (bats). Our tree suggests that Placentalia first split into Xenarthra and Epitheria; extinct New World species are the oldest members of Afrotheria.
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            The genomic signature of dog domestication reveals adaptation to a starch-rich diet.

            The domestication of dogs was an important episode in the development of human civilization. The precise timing and location of this event is debated and little is known about the genetic changes that accompanied the transformation of ancient wolves into domestic dogs. Here we conduct whole-genome resequencing of dogs and wolves to identify 3.8 million genetic variants used to identify 36 genomic regions that probably represent targets for selection during dog domestication. Nineteen of these regions contain genes important in brain function, eight of which belong to nervous system development pathways and potentially underlie behavioural changes central to dog domestication. Ten genes with key roles in starch digestion and fat metabolism also show signals of selection. We identify candidate mutations in key genes and provide functional support for an increased starch digestion in dogs relative to wolves. Our results indicate that novel adaptations allowing the early ancestors of modern dogs to thrive on a diet rich in starch, relative to the carnivorous diet of wolves, constituted a crucial step in the early domestication of dogs.
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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

                Journal
                R Soc Open Sci
                R Soc Open Sci
                RSOS
                royopensci
                Royal Society Open Science
                The Royal Society
                2054-5703
                June 2016
                1 June 2016
                1 June 2016
                : 3
                : 6
                : 160107
                Affiliations
                [1 ]Palaeontological Institute and Museum, University of Zurich , Karl-Schmid-Street 4, 8006 Zurich, Switzerland
                [2 ]Department of Orthopaedic Surgery, University of California at San Francisco, 513 Parnassus Avenue, S-1161, San Francisco, CA, USA
                Author notes
                Authors for correspondence: Marcelo R. Sánchez-Villagra e-mail: m.sanchez@ 123456pim.uzh.ch
                Authors for correspondence: Richard A. Schneider e-mail: rich.schneider@ 123456ucsf.edu
                Article
                rsos160107
                10.1098/rsos.160107
                4929905
                27429770
                4e294831-f979-4a39-95c1-69610e7bf706

                © 2016 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
                : 15 February 2016
                : 3 May 2016
                Funding
                Funded by: Swiss SNF
                Award ID: SNF 31003A-149605
                Funded by: National Institute for Health Research http://dx.doi.org/10.13039/501100000272
                Award ID: NIH/NIDCR R01 DE016402
                Categories
                1001
                70
                144
                58
                Biology (Whole Organism)
                Review Article
                Custom metadata
                June, 2016

                ontogeny,modularity,dog,pleiotropy,island,evolutionary developmental biology

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