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      Ecomorphological diversification in squamates from conserved pattern of cranial integration

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          With >10,000 living species, squamate reptiles (lizards, snakes) exhibit enormous phenotypic variation reflecting their incredible range in ecology and developmental strategies. What drove this exceptional diversity? We analyze high-density surface morphometric data for skulls representing ∼200 modern and extinct species to provide a comprehensive, clade-wide investigation of how ecological and developmental factors contributed to cranial evolution across geologic time, skull regions, and taxa. Although diet and habitat have had an overarching impact on skull evolution (e.g., herbivory, along with aquatic and fossorial habitats, are associated with rapid evolution), lizards and snakes surprisingly share a common pattern of trait correlations (integration). The remarkable ecological and morphological diversity in squamates thus arose from selection acting on a conserved architecture of phenotypic integration.

          Abstract

          Factors intrinsic and extrinsic to organisms dictate the course of morphological evolution but are seldom considered together in comparative analyses. Among vertebrates, squamates (lizards and snakes) exhibit remarkable morphological and developmental variations that parallel their incredible ecological spectrum. However, this exceptional diversity also makes systematic quantification and analysis of their morphological evolution challenging. We present a squamate-wide, high-density morphometric analysis of the skull across 181 modern and extinct species to identify the primary drivers of their cranial evolution within a unified, quantitative framework. Diet and habitat preferences, but not reproductive mode, are major influences on skull-shape evolution across squamates, with fossorial and aquatic taxa exhibiting convergent and rapid changes in skull shape. In lizards, diet is associated with the shape of the rostrum, reflecting its use in grasping prey, whereas snakes show a correlation between diet and the shape of posterior skull bones important for gape widening. Similarly, we observe the highest rates of evolution and greatest disparity in regions associated with jaw musculature in lizards, whereas those forming the jaw articulation evolve faster in snakes. In addition, high-resolution ancestral cranial reconstructions from these data support a terrestrial, nonfossorial origin for snakes. Despite their disparate evolutionary trends, lizards and snakes unexpectedly share a common pattern of trait integration, with the highest correlations in the occiput, jaw articulation, and palate. We thus demonstrate that highly diverse phenotypes, exemplified by lizards and snakes, can and do arise from differential selection acting on conserved patterns of phenotypic integration.

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          geiger v2.0: an expanded suite of methods for fitting macroevolutionary models to phylogenetic trees.

          Phylogenetic comparative methods are essential for addressing evolutionary hypotheses with interspecific data. The scale and scope of such data have increased dramatically in the past few years. Many existing approaches are either computationally infeasible or inappropriate for data of this size. To address both of these problems, we present geiger v2.0, a complete overhaul of the popular R package geiger. We have reimplemented existing methods with more efficient algorithms and have developed several new approaches for accomodating heterogeneous models and data types.
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            PERSPECTIVE: COMPLEX ADAPTATIONS AND THE EVOLUTION OF EVOLVABILITY.

            The problem of complex adaptations is studied in two largely disconnected research traditions: evolutionary biology and evolutionary computer science. This paper summarizes the results from both areas and compares their implications. In evolutionary computer science it was found that the Darwinian process of mutation, recombination and selection is not universally effective in improving complex systems like computer programs or chip designs. For adaptation to occur, these systems must possess "evolvability," i.e., the ability of random variations to sometimes produce improvement. It was found that evolvability critically depends on the way genetic variation maps onto phenotypic variation, an issue known as the representation problem. The genotype-phenotype map determines the variability of characters, which is the propensity to vary. Variability needs to be distinguished from variations, which are the actually realized differences between individuals. The genotype-phenotype map is the common theme underlying such varied biological phenomena as genetic canalization, developmental constraints, biological versatility, developmental dissociability, and morphological integration. For evolutionary biology the representation problem has important implications: how is it that extant species acquired a genotype-phenotype map which allows improvement by mutation and selection? Is the genotype-phenotype map able to change in evolution? What are the selective forces, if any, that shape the genotype-phenotype map? We propose that the genotype-phenotype map can evolve by two main routes: epistatic mutations, or the creation of new genes. A common result for organismic design is modularity. By modularity we mean a genotype-phenotype map in which there are few pleiotropic effects among characters serving different functions, with pleiotropic effects falling mainly among characters that are part of a single functional complex. Such a design is expected to improve evolvability by limiting the interference between the adaptation of different functions. Several population genetic models are reviewed that are intended to explain the evolutionary origin of a modular design. While our current knowledge is insufficient to assess the plausibility of these models, they form the beginning of a framework for understanding the evolution of the genotype-phenotype map.
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              Morphological Integration and Developmental Modularity

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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
                16 July 2019
                1 July 2019
                1 July 2019
                : 116
                : 29
                : 14688-14697
                Affiliations
                [1] aDepartment of Anatomy, New York Institute of Technology College of Osteopathic Medicine , Old Westbury, NY 11568;
                [2] bLife Sciences Department, Vertebrates Division, Natural History Museum , London SW7 5BD, United Kingdom;
                [3] cDivision of Paleontology, American Museum of Natural History , New York, NY 10024;
                [4] dCentre for Integrative Anatomy, Department of Cell and Developmental Biology, University College London , London WC1E 6BT, United Kingdom;
                [5] eJackson School of Geosciences, University of Texas at Austin , Austin, TX 78712;
                [6] fMuseum für Naturkunde, Leibniz Institute for Evolution and Biodiversity Science , Berlin 10115, Germany;
                [7] gDépartement Adaptations du Vivant, Centre National de la Recherche Scientifique, Muséum National d’Histoire Naturelle , Paris 75005, France;
                [8] hDepartment of Genetics, Evolution and Environment, University College London , London WC1E 6BT, United Kingdom
                Author notes
                1To whom correspondence may be addressed. Email: awatanab@ 123456nyit.edu .

                Edited by David M. Hillis, The University of Texas at Austin, Austin, TX, and approved June 4, 2019 (received for review December 8, 2018)

                Author contributions: A.W., R.N.F., and A.G. designed research; A.W., A.-C.F., and R.N.F. performed research; A.W., R.N.F., and A.G. contributed new reagents/analytic tools; A.W., A.-C.F., J.A.M., J.M., and A.H. performed data collection; A.W. and A.-C.F. analyzed data; and A.W., A.-C.F., J.A.M., J.M., A.H., and A.G. wrote the paper.

                Author information
                http://orcid.org/0000-0001-5057-4772
                http://orcid.org/0000-0002-9201-9213
                http://orcid.org/0000-0003-0991-4434
                Article
                201820967
                10.1073/pnas.1820967116
                6642379
                31262818
                1fbd29f1-a561-4878-85b1-6e0ec998ae25
                Copyright © 2019 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).

                History
                Page count
                Pages: 10
                Funding
                Funded by: EC | H2020 | H2020 Priority Excellent Science | H2020 European Research Council (ERC) 100010663
                Award ID: STG-2014-637171
                Award Recipient : Anjali Goswami
                Funded by: National Science Foundation (NSF) 100000001
                Award ID: EF-0334961
                Award Recipient : Jessica A. Maisano
                Funded by: Deutsche Forschungsgemeinschaft (DFG) 501100001659
                Award ID: DFG Mu 1760/7-1
                Award Recipient : Johannes Müller
                Funded by: European Council
                Award ID: SYNTHESIS DE-TAF-6532
                Award Recipient : Akinobu Watanabe
                Funded by: Paleontological Society 100010841
                Award ID: Newell Grant
                Award Recipient : Akinobu Watanabe
                Categories
                PNAS Plus
                Biological Sciences
                Evolution
                PNAS Plus

                geometric morphometrics,integration and modularity,macroevolution,skull,squamata

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