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      Evolution of hyperossification expands skull diversity in frogs

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          Significance

          The vertebrate head is an integrated system essential for sensory functions, capturing prey, and defense mechanisms. Head anatomy has long attracted the attention of biologists, yet identifying the factors responsible for the evolution of deviant morphological forms has remained a long-standing challenge. Frogs are one of the most diverse vertebrate orders but have not been thoroughly studied with respect to cranial morphological variation. We use extensive sampling of all major lineages to quantify skull diversity, reconstruct the evolution of increased mineralization (hyperossification), and test for relationships between ecology, skull shape, and hyperossification. We find that several extreme skull shapes have repeatedly evolved in frogs, hyperossification has arisen independently many times, and deviant skulls often cooccur with hyperossification and specialized functions.

          Abstract

          Frogs (Anura) are one of the most diverse vertebrate orders, comprising more than 7,000 species with a worldwide distribution and extensive ecological diversity. In contrast to other tetrapods, frogs have a highly derived body plan and simplified skull. In many lineages of anurans, increased mineralization has led to hyperossified skulls, but the function of this trait and its relationship with other aspects of head morphology are largely unexplored. Using three-dimensional morphological data from 158 species representing all frog families, we assessed wide-scale patterns of shape variation across all major lineages, reconstructed the evolutionary history of cranial hyperossification across the anuran phylogeny, and tested for relationships between ecology, skull shape, and hyperossification. Although many frogs share a conserved skull shape, several extreme forms have repeatedly evolved that commonly are associated with hyperossification, which has evolved independently more than 25 times. Variation in cranial shape is not explained by phylogenetic relatedness but is correlated with shifts in body size and ecology. The species with highly divergent, hyperossified skulls often have a specialized diet or a unique predator defense mechanism. Thus, the evolution of hyperossification has repeatedly facilitated the expansion of the head into multiple new shapes and functions.

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          Most cited references 56

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          The Ecology and Behavior of Amphibians

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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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              Novelty in Evolution: Restructuring the Concept

               G Muller,  G P Wagner (1991)
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                14 April 2020
                27 March 2020
                27 March 2020
                : 117
                : 15
                : 8554-8562
                Affiliations
                aDepartment of Natural History, Florida Museum of Natural History, University of Florida , Gainesville, FL 32611;
                bDepartment of Biology, University of Florida , Gainesville, FL 32611
                Author notes
                1To whom correspondence may be addressed. Email: dpaluh@ 123456ufl.edu .

                Edited by Neil H. Shubin, University of Chicago, Chicago, IL, and approved February 28, 2020 (received for review January 16, 2020)

                Author contributions: D.J.P., E.L.S., and D.C.B. designed research; D.J.P. performed research; D.J.P. analyzed data; D.J.P., E.L.S., and D.C.B. wrote the paper; and D.J.P. and E.L.S. generated CT data.

                Article
                202000872
                10.1073/pnas.2000872117
                7165440
                32220958
                Copyright © 2020 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                Page count
                Pages: 9
                Product
                Funding
                Funded by: NSF | EHR | Division of Graduate Education (DGE) 100000082
                Award ID: 1315138 and 1842473
                Award Recipient : Daniel J Paluh
                Funded by: NSF | BIO | Division of Biological Infrastructure (DBI) 100000153
                Award ID: 1701714
                Award Recipient : Edward L Stanley Award Recipient : David C. Blackburn
                Categories
                Biological Sciences
                Evolution

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