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      Modularity and heterochrony in the evolution of the ceratopsian dinosaur frill

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          Abstract

          The fossil record provides compelling examples of heterochrony at macroevolutionary scales such as the peramorphic giant antlers of the Irish elk. Heterochrony has also been invoked in the evolution of the distinctive cranial frill of ceratopsian dinosaurs such as Triceratops. Although ceratopsian frills vary in size, shape, and ornamentation, quantitative analyses that would allow for testing hypotheses of heterochrony are lacking. Here, we use geometric morphometrics to examine frill shape variation across ceratopsian diversity and within four species preserving growth series. We then test whether the frill constitutes an evolvable module both across and within species, and compare growth trajectories of taxa with ontogenetic growth series to identify heterochronic processes. Evolution of the ceratopsian frill consisted primarily of progressive expansion of its caudal and caudolateral margins, with morphospace occupation following taxonomic groups. Although taphonomic distortion represents a complicating factor, our data support modularity both across and within species. Peramorphosis played an important role in frill evolution, with acceleration operating early in neoceratopsian evolution followed by progenesis in later diverging cornosaurian ceratopsians. Peramorphic evolution of the ceratopsian frill may have been facilitated by the decoupling of this structure from the jaw musculature, an inference that predicts an expansion of morphospace occupation and higher evolutionary rates among ceratopsids as indeed borne out by our data. However, denser sampling of the meager record of early‐diverging taxa is required to test this further.

          Abstract

          We find support for peramorphic evolution of the frill of ceratopsian dinosaurs, likely facilitated by the decoupling of this structure from jaw musculature.

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          Most cited references 108

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          Size and shape in ontogeny and phylogeny

          We present a quantitative method for describing how heterochronic changes in ontogeny relate to phyletic trends. This is a step towards creating a unified view of developmental biology and evolutionary ecology in the study of morphological evolution. Using this representation, we obtain a greatly simplified and logical scheme of classification. We believe that this scheme will be particularly useful in studying the data of paleontology and comparative morphology and in the analysis of processes leading to adaptive radiation. We illustrate this scheme by examples drawn from the literature and our own work.
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            Size-correction and principal components for interspecific comparative studies.

            Phylogenetic methods for the analysis of species data are widely used in evolutionary studies. However, preliminary data transformations and data reduction procedures (such as a size-correction and principal components analysis, PCA) are often performed without first correcting for nonindependence among the observations for species. In the present short comment and attached R and MATLAB code, I provide an overview of statistically correct procedures for phylogenetic size-correction and PCA. I also show that ignoring phylogeny in preliminary transformations can result in significantly elevated variance and type I error in our statistical estimators, even if subsequent analysis of the transformed data is performed using phylogenetic methods. This means that ignoring phylogeny during preliminary data transformations can possibly lead to spurious results in phylogenetic statistical analyses of species data.
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              Superiority, competition, and opportunism in the evolutionary radiation of dinosaurs.

              The rise and diversification of the dinosaurs in the Late Triassic, from 230 to 200 million years ago, is a classic example of an evolutionary radiation with supposed competitive replacement. A comparison of evolutionary rates and morphological disparity of basal dinosaurs and their chief "competitors," the crurotarsan archosaurs, shows that dinosaurs exhibited lower disparity and an indistinguishable rate of character evolution. The radiation of Triassic archosaurs as a whole is characterized by declining evolutionary rates and increasing disparity, suggesting a decoupling of character evolution from body plan variety. The results strongly suggest that historical contingency, rather than prolonged competition or general "superiority," was the primary factor in the rise of dinosaurs.
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                Author and article information

                Contributors
                redshore@gmail.com
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                22 May 2020
                July 2020
                : 10
                : 13 ( doiID: 10.1002/ece3.v10.13 )
                : 6288-6309
                Affiliations
                [ 1 ] Institut Català de Paleontologia Miquel Crusafont Universitat Autònoma de Barcelona Barcelona Spain
                [ 2 ] Integrative Research Center Field Museum of Natural History Chicago IL USA
                [ 3 ] CREAF Barcelona Spain
                [ 4 ] Department of Biology Washington University St. Louis MO USA
                [ 5 ] Department of Neurology and Ahmanson Lovelace Brain Mapping Center University of California, Los Angeles Los Angeles CA USA
                [ 6 ] Division of Paleontology American Museum of Natural History New York NY USA
                [ 7 ] Department of Earth and Environmental Sciences University of Minnesota Minneapolis MN USA
                Author notes
                [* ] Correspondence

                Albert Prieto‐Márquez, Institut Català de Paleontologia Miquel Crusafont, Universitat Autònoma de Barcelona, Carrer de l’Escola Industrial 23, 08201 Sabadell, Barcelona, Spain.

                Email: redshore@ 123456gmail.com

                Article
                ECE36361
                10.1002/ece3.6361
                7381594
                © 2020 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                Page count
                Figures: 8, Tables: 6, Pages: 22, Words: 15649
                Product
                Funding
                Funded by: Generalitat de Catalunya , open-funder-registry 10.13039/501100002809;
                Funded by: Field Museum of Natural History
                Funded by: National Science Foundation , open-funder-registry 10.13039/100000001;
                Award ID: FRES 1925884
                Award ID: PLR 1341645
                Funded by: Ministry of Economy, Industry and Competitivity of Spain
                Award ID: FJCI‐2014‐20380
                Award ID: RyC‐2015‐17388
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                July 2020
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.8.5 mode:remove_FC converted:25.07.2020

                Evolutionary Biology

                modularity, morphometrics, heterochrony, dinosaur, evolution

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